Occupational lung cancer screening: A Collegium Ramazzini statement

Lung cancer is the most common cause of death from cancer in the world. It is also the most common lethal work-related cancer. After tobacco smoking, occupational exposures present the most frequent specific cause of lung cancer that is amenable to intervention. Early detection and treatment can identify and cure primary lung cancer. Randomized controlled trials have demonstrated the efficacy of low dose computed tomography (LDCT) screening among persons at high risk of lung cancer. Guidelines for determining eligibility for LDCT screening have been established for the general population but have largely neglected those for whom occupational exposure to lung carcinogens is a risk factor. The Collegium recommends that persons at risk for lung cancer from occupational exposures be offered annual LDCT if their cumulative risk of lung cancer approximates the level of risk endorsed by the guidelines promulgated by the United States Preventive Services Task Force (USPSTF) in 2021 and the National Comprehensive Cancer Network (NCCN) in the United States in 2021. At present, these agencies recommend screening for people aged 50 and over who have smoked at least 20 pack-years of cigarettes. The Collegium recommends that additional lung cancer risk factors, including exposure to known or suspected occupational and environmental lung carcinogens; family history of lung cancer (especially among first degree relatives and relatives <60 years of age); a personal history of chronic obstructive lung disease, pneumoconiosis, or pulmonary fibrosis; or a personal history of cancer (excluding skin cancer) be considered as part of the risk assessment for eligibility determination for lung cancer screening. Latency, or the period of time since initial occupational exposure (e.g., >15 years) is another factor that should be considered. If the presence of these additional risk factors, in combination with age and smoking history, is associated with a level of risk that meets or exceeds the level of risk identified by the USPSTF and NCCN, then an annual low dose chest CT for lung cancer screening should be offered. We do not favor a specific age cut-off at which to end screening, but we recognize that only persons who are sufficiently healthy and have sufficient life expectancy to undergo diagnostic work-up and potentially curative treatment should be offered screening for lung cancer. In view of the rising risk of occupational lung cancer over time and the potential or actual interaction between occupational lung carcinogens and cigarette smoking even after quitting, screening programs may choose to screen workers with occupational lung cancer risk for prolonged periods after they have quit smoking cigarettes. The Collegium acknowledges that there are uncertainties and assumptions entailed in this approach and that risk assessment for individual workers necessitates application of significant professional judgement. We encourage the implementation of well-organized screening programs that can further our knowledge about optimal occupation-inclusive lung cancer screening strategies. Workers with a history of exposure to known or suspected lung carcinogens or working in occupations/trades or work tasks that are known to elevate the risk for lung cancer form the target population for lung cancer screening. Important examples of lung carcinogens include asbestos, silica, diesel exhaust, welding fumes, selected metals, and radiation. Screening participants should be provided with complete and comprehensible information about risks and benefits. Screening should be offered annually and continuously. Screening should be achieved through the application of low dose computed tomography (LDCT) to minimize the radiation dose delivered. Proper CT scan interpretation should be performed by experienced radiologists or other well-trained readers. Prompt, appropriate follow-up of abnormal CT scans involving relevant medical expertise is mandatory. Patients who are current smokers should be offered smoking cessation programs. The Collegium calls upon occupational health and medical professionals and stakeholders (governments, employers, insurance companies, and labor unions) to identify worker populations that have excess lung cancer risk, to promote lung cancer screening, and to develop and support well-organized programs to conduct such screening in these populations. While elimination or minimization of exposure to lung carcinogens in the workplace through environmental controls is critical for lung cancer prevention, lung cancer screening is an essential secondary intervention for reducing deaths and disabling disease from exposure to workplace lung carcinogens. Lung cancer is the most common cause of death from cancer in the world, causing one in five (20.4%) cancer deaths in 2019.1 It is the most common cause of cancer death for males in most countries, including low-, middle-, and high-income nations, and the most frequent cause of cancer death among women in China, the United States, Australia, Scandinavia, and Canada. Tobacco smoking is the dominant cause of lung cancer, and the maturity of the cigarette smoking epidemic and variable uptake and adoption of smoking cessation determines much of the geographic and gender variation in lung cancer incidence and mortality.2 Lung cancer is also the dominant cause of occupational cancer (excluding nonmelanoma skin cancers), causing more than 50% of all workplace-related cancers.3 A recent analysis associated with the Global Burden of Disease Study 2016 estimated that 300,000 lung cancer deaths occurred as a result of exposure to 10 IARC Group 1 lung carcinogens in 2016, representing 86% of all occupational cancer deaths.4 Work-related lung cancer deaths increased 55% from 1990 to 2016, from an estimated 193,000–300,000 deaths per year (GBD 2016 Occupational Carcinogens Collaborators 2020). Excellent reviews of occupational cancer in general are readily available.5-7 Occupational lung cancer remains grossly neglected by public health surveillance, clinical medicine, and worker compensation systems, despite its enormous burden of illness and death. Studies in diverse populations and industries across three continents (Asia, Europe, and North America) have demonstrated that a very small fraction—less than 3%—of the total number of estimated occupational lung cancers have been attributed to occupation. In Korea, where an estimated 630 to 1181 occupational lung cancers occur annually, only 179 work-related lung cancers, or 10 per year on average, were compensated by the Korean national worker compensation system over a nearly two-decade period.8, 9 In Great Britain, where 5442 occupational lung cancer cases are estimated to occur each year,10 only 21 cases per year (or 392 cases over a 19 year period, 1996–2014) were recorded in Surveillance of Work-Related and Occupational Respiratory Disease (SWORD), a national voluntary reporting system.11 Similarly, in Canada, of the estimated 4150 annual occupational lung cancer cases, only 120 occupational lung cancers were compensated each year between 2005 and 2009.7, 12 Over the past five decades, the International Agency for Research on Cancer (IARC) has identified 20 IARC Group 1 occupational lung carcinogens (substances or mixtures) and an additional 7 occupations, industries or work processes in which occupational epidemiology studies were instrumental in establishing specific lung carcinogenicity.5 These agents, occupations and industries are listed in Table 1, adapted from IARC sources.5, 13 Four in ten of all agent-specific IARC Group 1 carcinogens cause lung cancer. In addition, two-thirds of all occupations, industries, or processes that cause occupational cancer cause lung cancer (Table 1). Arsenic and inorganic arsenic compounds Asbestos (all forms) Beryllium and beryllium compounds Bis(chloromethy)ether; chloromethyl methyl either (technical grade) Cadmium and cadmium compounds Chromium (VI) compounds Coal, indoor emissions from household combustion Coal tar pitch Engine exhaust, diesel Nickel compounds Outdoor air pollution Particulate matter in outdoor air pollution Plutonium Radon-222 and its decay products Silica dust, crystalline, in the form of quartz or cristobalite Soot Tobacco smoke, secondhand Welding fumes X-, and Gamma-radiation Acid mists, strong organic Benzene Biomass fuel (primarily wood), indoor emissions from household combustion of Bitumens, occupational exposure to hard bitumens and their emissions during mastic asphalt work alpha-Chlorinated toluenes (benzyl chloride, benzotrichloride, benzyl chloride) and benzoyl chloride (combined exposures) Cobalt metal with tungsten carbide Creosotes Diazinon Hydrazine Nonarsenical insecticides (occupational exposures in spraying and application of) Silicon carbide, fibrous 2,3,7,8 Tetrachlorordibenzo-para-dioxin Trivalent antimony Uranium, mixture of isotopes Acheson process, occupational exposures associated with Aluminum production Coal gasification Coke production Hematite mining (underground) Iron and steel founding Painter (occupational exposure) Rubber manufacturing industry Art glass, glass containers and pressed ware (manufacture of) Carbon electrode manufacture Frying, emissions from high-temperature Printing processes (occupational exposures in) Further, there is limited evidence for an association with lung cancer of numerous other exposures, though less broadly recognized within the occupational health community. They include cobalt,2, 3, 7, 8 tetrachlorordibenzo-para-dioxin (dioxin), and high temperature frying emissions and total eight agents or mixtures and four occupations, industries or processes (Table 1).13 The number of occupational lung carcinogens are increasing. In the past decade alone, IARC has added common exposures such as diesel engine exhaust (2013), outdoor air pollution (2016), and welding fumes (2017) to its Group 1 list of carcinogens (Table 1).5, 13 For additional carcinogens, there is limited evidence for an association with lung cancer: emissions from combustion of biomass fuel (2010); bitumens from roofing (2013); diazinon (2017); and hydrazine (2018). The occupational lung cancer burden is likely to grow. Only a small fraction of the tens of thousands of chemical agents in commercial use have been evaluated for toxicity. In five decades, IARC has evaluated more than 1000 agents, occupations and industries, but found that available scientific studies are inadequate or lacking in approximately one-half of the evaluations.5, 14 For context, there are an estimated 86,000 chemicals in the United States Environmental Protection Agency's Toxic Substances Control Act Inventory.15 Given the frequency of exposure of the respiratory system to inhaled toxicants and the demonstrated carcinogenicity of many chemical agents, it is likely that only a fraction of occupational lung carcinogens has been identified and the total burden of occupational lung cancer remains undefined. Exposure to occupational lung carcinogens has been and remains reasonably common. National and cross-national surveys of workplace exposures have been conducted in high income countries for 4 decades, including the US National Occupational Hazard and Exposure Surveys (1972–1974 and 1981–1983); CAREX (carcinogen exposure) project in the European Union (1990–1993)16; FINJEM (Finnish job-exposure matrix) system in Finland17; and the Canadian version of FINJEM.18 The most prevalent occupational lung carcinogens in high income countries over the past 30 years have been diesel exhaust, welding fumes, and silica. Based on data from Europe, Finland, and Canada, more than 2% of the employed population has been exposed to each of these three mixtures or agents. This proportion has not changed in the past three decades. Exposure to asbestos had been a dominant exposure in these countries, but its use declined markedly in recent decades due to widely accepted bans and restrictions. Asbestos exposure continues in these countries, however, due to large quantities of asbestos-containing materials still in place. For middle- and low-income countries, national estimates of the prevalence of exposure to occupational lung carcinogens have not been identified. Given the extent and lack of adequate regulation of manufacturing, mining, and construction, exposures to said agents is likely to be more common and at higher levels than in high income countries. For the purpose of lung cancer screening, workplace exposures that were prominent 20–40 years ago are highly relevant today due to the latency of asbestos-related lung cancer. Asbestos exposure was common in worksites in many high-income countries before the 1980s, though exposure in recent decades has declined. The prior and continuing high use of asbestos in China, Russia, India, and selected other countries is almost certainly associated with elevated risk of asbestos-related lung cancer for large populations of workers at, both at present and well into the future.19, 20 Other highly relevant exposures, such as silica, diesel exhaust, and welding fumes, were prevalent in the past and remain prevalent in countries of all national income levels. Salient industries and examples of occupations with current exposure to occupational lung carcinogens are provided in Table 2.21 Many construction workers are exposed to the most common lung carcinogens: asbestos, diesel exhaust, silica, and welding. Diesel engine exhaust exposure is highly prevalent among workers who drive or maintain diesel vehicles, including buses, trucks, trains, ships, and heavy equipment. Many workers in mining are exposed to diesel exhaust from mining equipment. Miners and workers in many manufacturing industries continue to have exposure to carcinogenic metals and silica. Metal fabricators, assemblers Metal processors, shaping workers Clay, stone, glass processors Forging workers Boilermakers, platers Silica, diesel exhaust, painting, welding, coal-tar pitch, asbestos Outdoor air pollution Excavators Welders Painters Plumbers Other construction Bus drivers Truck drivers Mechanical maintenance Drillers, blasters Miners, quarry workers Mineral ore treaters Occupation and, more generally, social class, are closely associated with cigarette smoking. In the United States, one-quarter or more of workers in construction, manufacturing, mining, and transportation smoke cigarettes compared to 10% of workers in professional or managerial positions.22 In China, for example, the prevalence of smoking among male machine operators (67%) was nearly twice that of male medical/health personnel or teaching staff (36%–38%).23 It is well-established that occupational lung carcinogens and cigarette smoke act in concert in some circumstances to increase the risk of lung cancer. They share mechanistic pathways and have been repeatedly shown in epidemiologic studies to increase lung cancer risk above that expected by the presence of each risk factor alone. Asbestos is the best-known example of this phenomenon. Asbestos frequently shows at least a supra-additive interaction with smoking in determining lung cancer risk.24-28 Several large studies addressing the lung cancer risk among silica-exposed workers have been completed in the past decade, generally suggesting a supra-additive effect with cigarette smoke.29-33 Other occupational lung carcinogens that have been studied for interaction include diesel exhaust34, 35; and radon.36-38 Occupational exposures also indirectly increase lung cancer risk by causing chronic lung diseases, namely, chronic obstructive lung disease (COPD) and pneumoconioses, such as silicosis and asbestosis.21, 39 In fact, since occupational exposures to vapors, gases, dusts, or fumes raise the risk of COPD,40 for example, the occupational contribution to lung cancer should be considered more broadly than simply the role of the occupational agents causing lung cancer. Smoking works similarly as a major cause of COPD and as an established risk factor for idiopathic pulmonary fibrosis.41, 42 Figure 1 illustrates the complexity of these relationships. Key aspects of these relationships have been well-studied (e.g., the smoking and asbestos interaction noted above and the contribution of asbestosis and silicosis to risk of lung cancer). Other relationships, such as the interaction between work-related COPD and lung cancer, have received relatively less attention. Three decades of research provide strong evidence that periodic low dose chest CT scans can identify lung cancers at an early stage and can reduce lung cancer mortality. In Japan and the United States, Sone et al.43 and Henschke et al.44 separately demonstrated that low dose chest CT scanning in high risk populations detected ~85% of lung cancers at Stage I. In 2006, Henschke and colleagues further showed that treated early CT-detected lung cancers had excellent survival: a group of 412 Stage 1 lung cancers detected by CT screening had an estimated 88% 10-year survival.45 Of those who underwent surgical resection within 1 month of diagnosis, 10-year survival was 92%, 95% CI 88–95%. These remarkable results of nonrandomized studies stimulated intense interest and the initiation of randomized controlled trials of the impact of low dose CT scans on lung cancer mortality. Two large complementary randomized clinical trials of populations at high risk of lung cancer—the US National Lung Screening Trial (NLST) and the Dutch–Belgian Nederlands–Leuvens Longkanker Screenings Onderzoek (NELSON)—conclusively demonstrated that periodic low dose chest CT scanning reduces lung cancer mortality.46, 47 The NLST, conducted by the United States National Cancer Institute, included 53,454 enrollees aged 55–74 who had smoked at least 30 pack-years and, for former smokers, had quit within the past 15 years. The CT versus chest X-ray (CXR) study arms were screened annually for 5 years and followed for a median of 6.5 years. The CT scan screening arm showed a 20% reduction in lung cancer mortality versus the CXR screening arm.46 The NELSON trial included 13,195 men and 2594 women aged 50–74 years who had smoked at least 15–20 pack-years and, if former smokers, had quit 10 or fewer years before the entry date into the study. NELSON compared an intervention group who underwent four rounds of CT screening (baseline, year 1, year 3, and year 5.5) with a reference group who had no screening; all were followed for at least 10 years. NELSON observed a 24% and 33% lung cancer mortality reduction among men and women, respectively, in the trial.47 Neither the NLST nor the NELSON trials were designed to evaluate the efficacy of lung cancer among screenees defined other than by age and smoking. Other factors would include occupational exposures, chronic lung disease, family history of lung cancer, personal history of cancer, or environmental exposure to radon, air pollution, or other to the use of age and smoking history to lung cancer risk and to screening eligibility is the of a of lung cancer risk factors in lung cancer risk than 20 lung cancer risk on large lung cancer data (e.g., and cancer screening trial in North lung project in have been and many are of a and more of lung cancer risk factors than the NLST and NELSON These additional risk factors include and of smoking, number of years since smoking chronic lung disease, chronic obstructive pulmonary disease personal history of cancer, family history of lung cancer, and asbestos the the only occupational included is asbestos, which is part of the Lung and other occupational or environmental exposures have been included in the risk Lung cancer risk from these use no or information about in determining In a of the risk factor versus risk to the use of ten established lung cancer risk to the large data of the NLST and the and compared results to the risk factor eligibility in the NLST, and lung cancer incidence and mortality as The of the risk versus the NLST were very but four had higher levels of compared to that of the NLST with to lung cancer The in for lung cancer mortality between the NLST and the was even for the NLST versus for the and for the and In a US National Cancer study of this compared the lung cancer mortality of a risk versus a USPSTF to age and and that the former which family history, and a of smoking history as eligibility a number of lung cancer deaths than a on USPSTF screening guidelines Based on the results of the NLST, the United States Preventive Task Force (USPSTF) in that annual low dose CT scanning be offered to at high risk of lung cancer, who were defined as people aged 55–74 years who had smoked at least 30 pack-years of cigarettes and smoke or quit less than 15 years In after of the NELSON trial the USPSTF its for annual LDCT eligibility to include people aged years who have at least a 20 smoking history and smoke or have quit within the past 15 These were by the US and insurance for use in health insurance and clinical in to date have a more In a by for by European a of European and lung cancer screening with LDCT is either a combination of age and smoking or the group of European and who are in lung cancer screening in have a of on lung cancer screening, which were in They the use of lung cancer risk (e.g., over a to results of risk to who should be for lung cancer screening. Of the numerous risk that have been the group those from the Lung and the and Cancer Screening Trial In China, a lung cancer early detection and treatment group by the National and established the National Lung Cancer Screening annual lung cancer screening with LDCT for people aged 50–74 years who have at least a 20 smoking history and who smoke or have quit within the past 5 The guidelines by the National Cancer of recommends lung cancer screening eligibility current smokers with pack-years or former smokers with pack-years who have quit within 15 secondhand smokers who have or with smokers for at least 20 people with participants who have exposure year to asbestos, radon, silica, or people with first degree relatives have lung The guidelines for lung cancer screening. They recommend that annual LDCT should be offered to people between and years of age who are current or former smokers quit less than 15 years with a history of years of smoking. should have no history of lung cancer and be in health and and to be treated for lung cancer. They that the high prevalence of in that only lung Occupation is generally in current screening they are on selected risk factors and or on risk in the US include guidelines by the National Comprehensive Cancer Network (NCCN) and the of guidelines include additional risk factors to screening that family history, history of chronic lung disease and occupational Group eligibility first in screening people aged years with a 20 smoking history if they have an additional risk factor for lung cancer, such as exposure to occupational lung carcinogens, chronic lung disease, or a family history of lung cancer and had an year risk of lung cancer a 20 screening for aged 50 years and over but and other risk factors can be considered in determining eligibility for Occupational lung carcinogens include silica, asbestos, diesel exhaust, smoke, and In a group of in asbestos-related in and that the lung cancer risk level associated with the NLST study population be as the risk level in low dose CT scan programs for screening workers for lung The was before of the NELSON clinical numerous and of the USPSTF eligibility guidelines in 2021. In an working group in for the application of LDCT for lung cancer screening for workers who have a history of exposure to Group 1 IARC occupational lung carcinogens, including They conducted a scientific and an on to identify the of lung cancer risks associated with these Group 1 carcinogens, and in combination with cigarette smoking, and identified the that or the lung cancer risk associated with NLST eligibility They a not a supra-additive or effect between the occupational carcinogenic and tobacco in the They estimated that the risk of lung cancer associated with the NLST study eligibility history of cigarette was the target risk level of exposure to each of the IARC Group 1 lung carcinogens in combination with years of smoking or the target risk smokers who were exposed to lung carcinogens at level not a risk sufficient to lung cancer screening with the of and the of this of in the results of the NELSON trial and studies the USPSTF to the age and smoking levels for eligibility for lung cancer screening 50 years and The associated estimated risk level of lung cancer in the analysis would be these workers with asbestos exposure years and workers with years of high asbestos exposure would be for lung cancer screening even among smokers with a smoking history of less than 20 Studies of lung cancer screening among occupational populations at high risk of lung cancer are limited to Two of occupational have been and US nonrandomized studies of populations with participants results of LDCT screening for lung cancer between and smoking history, and asbestos exposure were or eligibility with frequent use of age and smoking than those in NLST or These studies were included in a and by et and et of these studies risk NLST, or NELSON eligibility to with NLST or the NELSON results is by the of the study populations and the lack of sufficient on smoking history and age in the the screening results of these studies lung cancers detected among smokers and lung cancers detected among smokers of asbestos exposure widely among the studies by of

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