0
Special Features |

Radiation Risks in Lung Cancer Screening ProgramsRadiation Risks in Lung Cancer Screening Programs: A Comparison With Nuclear Industry Workers and Atomic Bomb Survivors FREE TO VIEW

Robert J. McCunney, MD, MPH; Jessica Li, BS
Author and Funding Information

From the Department of Biological Engineering (Dr McCunney and Ms Li), Massachusetts Institute of Technology, Cambridge, MA; and Brigham and Women’s Hospital (Dr McCunney), Harvard Medical School, Boston, MA.

Correspondence to: Robert J. McCunney, MD, MPH, Department of Biological Engineering, Massachusetts Institute of Technology, 77 Massachusetts Ave, Room 16-771, Cambridge, MA 02139; e-mail: mccunney@mit.edu


For editorial comment see page 439

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;145(3):618-624. doi:10.1378/chest.13-1420
Text Size: A A A
Published online

The National Lung Cancer Screening Trial (NLST) demonstrated that screening with low-dose CT (LDCT) scan reduced lung cancer and overall mortality by 20% and 7%, respectively. The LDCT scanning involves an approximate 2-mSv dose, whereas full-chest CT scanning, the major diagnostic study used to follow up nodules, may involve a dose of 8 mSv. Radiation associated with CT scanning and other diagnostic studies to follow up nodules may present an independent risk of lung cancer. On the basis of the NLST, we estimated the incidence and prevalence of nodules detected in screening programs. We followed the Fleischner guidelines for follow-up of nodules to assess cumulative radiation exposure over 20- and 30-year periods. We then evaluated nuclear worker cohort studies and atomic bomb survivor studies to assess the risk of lung cancer from radiation associated with long-term lung cancer screening programs. The findings indicate that a 55-year-old lung screening participant may experience a cumulative radiation exposure of up to 280 mSv over a 20-year period and 420 mSv over 30 years. These exposures exceed those of nuclear workers and atomic bomb survivors. This assessment suggests that long-term (20-30 years) LDCT screening programs are associated with nontrivial cumulative radiation doses. Current lung cancer screening protocols, if conducted over 20- to 30-year periods, can independently increase the risk of lung cancer beyond cigarette smoking as a result of cumulative radiation exposure. Radiation exposures from LDCT screening and follow-up diagnostic procedures exceed lifetime radiation exposures among nuclear power workers and atomic bomb survivors.

Lung cancer is the leading cause of cancer death worldwide. Despite treatment advances, 5-year survival rates from 1995 to 2001 were about 15.7%. Major risks of lung cancer include cigarette smoking and exposure to asbestos and other occupational agents, such as crystalline silica, hexavalent chromium, and arsenic.1

In the late 1990s, screening programs using low-dose CT (LDCT) scanning offered the promise of detecting early stage lung cancer. These early observational studies were limited, however, by the absence of control groups.

In 2011, a prospective assessment of 50,000 individuals that compared annual LDCT scan with annual chest film screening noted a decrease in mortality from lung cancer (20%) and all-cause mortality (7%) among those in the LDCT scan group.2 The results led the American College of Chest Physicians and the American Society of Clinical Oncology to recommend annual screening with LDCT scan “for smokers and former smokers aged 55 to 74 years who have smoked for 30 pack-years or more and either continue to smoke or have quit within the past 15 years.”3 These are the first organizational recommendations advocating lung cancer screening; however, the recommendations are specific to the same entry criteria for participation in the National Lung Screening Trial (NLST).

What remains unclear, however, is how to evaluate potential benefits and risks of screening associated with other entry criteria. For example, will reduced lung cancer mortality be associated with younger ages at entry to screening or for lower pack-years of smoking than the 30-pack-year criteria of the NLST? In addition, articles have raised concern about ionizing radiation exposure risks associated with long-term lung cancer screening programs and the corresponding follow-up diagnostic studies.4,5 The high percentage of nodules detected during prevalence and incidence screening and the need to evaluate these nodules with full-chest CT scanning (and corresponding higher radiation exposure than LDCT scanning) and diagnostic interventions, such as fine-needle aspiration biopsy (FNAB), may increase cumulative radiation exposure. The rate of nodules that prove to be false positive has ranged from 96% to 98%.69 In the NLST, 96.4% of nodules detected were false positives not reflective of lung cancer.2

The need to follow up nodules detected on LDCT screening has raised the issue of the cumulative radiation dose that screening participants may encounter in both the screening and the diagnostic follow-up studies. In combination with periodic LDCT scans, these additional sources of radiation exposure could present an independent risk of lung cancer.

We determined ranges of cumulative radiation exposure a person may experience over 20- and 30-year periods by including both the screening LDCT scan and the follow-up diagnostic studies. We then contrasted the cumulative radiation exposures in screening programs with results of nuclear power plant workers and atomic bomb survivors.

Nuclear worker studies allow for an assessment of chronic low-dose radiation exposure, whereas atomic bomb survivor studies address acute high-dose exposure in people now followed over many decades. Nuclear worker studies offer advantages in this assessment because (1) the exposure pattern is generally chronic and low dose, (2) exposure data among nuclear workers have been closely documented, and (3) prospective studies have evaluated large cohorts (> 400,000 participants) over long periods of time and from many countries.10 Atomic bomb survivor studies address health consequences of acute high-dose radiation exposure among people followed over 50 years. We considered the range in prevalence of nodules detected in LDCT screening and radiation doses associated with LDCT scan, chest CT scan, and FNAB in light of recommended Fleischner guidelines for follow-up of pulmonary nodules.11 The purpose of the present report is to assess potential chronic radiation exposure in long-term (20-30 years) lung cancer screening programs and to assess the corresponding independent risk of lung cancer from radiation.

The NLST was used as the primary lung cancer screening reference because recommendations for screening by the American College of Chest Physicians and the American Society of Clinical Oncology have been based on this study.2,3 Participants were aged 55 to 74 years, had a ≥ 30-pack-year smoking history, and were current smokers or former smokers who quit in the past 15 years.

Screenings yielding noncalcified nodules > 4 mm necessitated diagnostic follow-up, with full CT scan initially. The size of the nodule is the primary factor affecting the type of diagnostic follow-up.12 According to the Fleischner guidelines, full CT scan is recommended for noncalcified nodules ranging in diameter from 4 to 8 mm, whereas FNAB is used for nodules > 8 mm11 (Table 1).

Table Graphic Jump Location
Table 1 —Fleischner Guidelines for Follow-up of Pulmonary Nodules

From MacMahon et al.11

To assess radiation exposure among LDCT scan screening participants, we approximated the range of nodules detected in both prevalence and incidence screening as 25% to 50% on the basis of a review of longitudinal studies of lung cancer screening with low-dose CT scanning. We used the follow-up of nodules as recommended by the Fleischner Society and considered lung cancer screening participants in the high-risk category.

Assumptions on the Prevalence and Incidence of Nodules Detected in Lung Cancer Screening

Up to 50% of smokers aged > 50 years have pulmonary nodules.11,13 A significant heterogeneity has been noted in the percentage of nodules detected at incidence and prevalence in lung cancer screening programs. We chose to use the range of 25% to 50% for both incidence and prevalence of nodules detected on LDCT scan on the basis of several studies.2,3,6,8,9 Incidence of nonpulmonary conditions warranting follow-up averaged about 5% in lung cancer screening programs.9

Radiation Doses From LDCT Scanning and CT Scanning

Radiation exposure is measured by a number of units, including sieverts and grays. The sievert reflects the effective dose and represents the stochastic biologic effects of ionizing radiation. One sievert equals 100 rem (roentgen equivalent man), an older radiation metric. The gray is the radiation measure used to reflect the absorbed dose.

In the NLST, the estimated effective doses of LDCT and CT scans were 2 mSv and 7 to 8 mSv, respectively; about 10% of the LDCT scans were associated with radiation exposures between 2 and 4 mSv.14 Brenner15 estimated the LDCT scan dose to be 5.2 mGy, which is based on an earlier study that indicated that lung doses vary from 2.5 to 9.0 mGy. In a study of 31,642 patients who underwent CT scanning examinations in 2007, the effective dose was 8 mSv.16 These dose estimates for LDCT scanning, however, are higher than those estimated from the NLST, which estimated doses for LDCT scans to be about 2 mSv.14 Values reported in the scientific literature have ranged from 4 to 18 mSv.17 A CT image-guided FNAB has an estimated effective dose of 1.5 mSv.18 Natural background radiation ranges from 2.4 to 3 mSv per year.17 In the NLST, any nodule > 4 mm was evaluated as follows: chest CT scan (73%), fluorodeoxyglucose PET-CT scan (10%), and FNAB (2.2%). In the first round of NLST, 7,191 positive tests (ie, a nodule > 4 mm) were noted. Among those with positive test results, lung cancer was noted in 3.8%. Thus, 96.2% of the nodules were false positive. Of the 693 people with lung cancer detected, 649 (93.6%) had a positive LDCT scan. Forty-four people (6.4%) with lung cancer had a negative LDCT scan, reflecting false-negative test results. Among these 44 people with lung cancer who had a normal LDCT scan, 15 (35%) had small cell carcinoma.

To determine cumulative radiation exposure, we used the following assumptions:

  • • Average radiation dose of an LDCT scan is 2 mSv.

  • • Average radiation dose of a full CT scan is 8 mSv.

  • • Follow-up of nodules will be conducted according to the Fleischner guidelines, which suggest three follow-up CT scans over a 2-year period for nodules > 4 mm as detected on CT scan.

Assessing Risk of Occupational Radiation Exposure

We addressed chronic low-dose radiation risks by reviewing nuclear worker cohort studies in which the risk of lung cancer was evaluated in light of total ionizing radiation exposure. We also used atomic bomb survivor data to assess acute high-dose radiation exposure risk.

Determining Cumulative Dose of Ionizing Radiation in Lung Cancer Screening Programs

Different scenarios were used to estimate the cumulative radiation exposure from screening over 20- to 30-year periods. The primary variables were (1) percentage of nodules detected on LDCT scan requiring follow-up, (2) radiation doses associated with screening and diagnostic studies, and (3) length of the screening program (20 vs 30 years). We considered 30 years as reflective of starting screening at age 50 and stopping at age 80. These assumptions were made to simplify the estimation of possible total radiation experienced given the number of years of screening and the prevalence of nodules requiring follow-up diagnostic procedures.

Estimating Cumulative Radiation Exposure From Lung Cancer Screening Programs

If a 4-mm nodule is detected per LDCT scan, an additional three CT scans are recommended before concluding that the nodule is benign. These additional full CT scans per 4-mm nodule detected add another 24 mSv of radiation exposure. If a 4-mm nodule is detected every 2 years, the cumulative radiation exposure would be 2 mSv per year over 20 years (40 mSv) for the LDCT scans and 24 mSv per follow-up for each 4-mm nodule detected. Thus, over a 20-year period (ages 55-75 years), the cumulative exposure would be 280 mSv. Over a 30-year program (ages 50-80 years), the cumulative radiation exposure would be 420 mSv among participants who show a 4-mm nodule every 2 years (Table 2).

Table Graphic Jump Location
Table 2 —Estimation of Radiation Exposure From LDCT Scanning and Follow-up Tests

LDCT = low-dose CT.

Occupational Radiation Exposure

Epidemiologic studies of workers exposed to radiation have been conducted among medical personnel, Chernobyl clean-up workers, and nuclear power industry workers.19 Studies were evaluated to determine the excess relative risk (ERR) of lung cancer associated with radiation dose (ERR/Sv).

In a pooled analysis of > 400,000 nuclear power industry workers from 15 countries, the average cumulative radiation dose was 19.4 mSv, a level markedly lower than the dose that lung cancer screening participants can experience in only a few years.10 Among the cohort, 5,233 cancer deaths occurred, indicating an ERR/Sv of 0.97 (90% CI, 0.28-1.77), and 1,457 lung cancer deaths occurred, indicating an ERR/Sv of 1.86 (90% CI, 0.49-3.63). ERR of lung cancer at 100 mSv was 1.19. The ERR/Sv for lung cancer among workers aged > 50 years was 3.87 (90% CI, 0.92-7.93). The “risks [of cancer in this international cohort] were quantitatively consistent with those reported for atomic bomb survivors.”20

Subsequently, nuclear worker studies from Germany, the United States, the United Kingdom, Korea, and Japan have been published.2126 What follows is a summary of studies published since the international pooled analysis described previously.10

In a German cohort of 4,844 employees, no increase in total cancer mortality was noted.21 In a study of US shipyard workers employed between 1957 and 1982 and who were involved in overhauls of nuclear powered ships, workers with exposures > 50 mSv compared with those with exposures between 5.0 and 9.9 mSv had a higher relative risk of lung cancer (1.26; 95% CI, 0.9-1.9). In a study of British atomic energy workers, estimates of risk associated with radiation exposure were similar to atomic bomb survivors.23 Of the 118,766 workers for whom radiation measurements were available, just < 10% (10,505) had exposures of > 100 mSv. The mean dose of the cohort was 24.9 mSv. These results, consistent with the 15-country nuclear worker study, showed a statistically significant increase between radiation exposure and mortality from all malignancies. Results for lung cancer were not separately reported.

A study of Korean nuclear power industry workers employed between 1992 and 2005 assessed 8,429 radiation workers and 7,807 nonradiation workers.24 Estimated mean dose was 0.82 ± 3.98 mSv. Follow-ups were conducted for 7.53 years for radiation workers and 6.19 years for nonradiation workers. A statistically significant relative risk for lung cancer was reported at 3.48 (95% CI, 1.19-11.48) for radiation workers compared with nonradiation workers. The ERR/Sv for lung cancer was estimated to be 1.69 (95% CI, −2.07 to 8.21).

Among 5,801 US radiation workers and 41,169 nonradiation workers employed from 1948 to 1999 for at least 6 months, a mean dose of 13.5 mSv from external radiation exposure was noted.25 Workers were compared with both the general public (standardized mortality ratio, 0.88 [95% CI, 0.81-0.95] vs 0.87 [95% CI, 0.76-1.00] for all cancer and lung cancer deaths, respectively) and to nonradiation workers employed for at least 6 months at the same facility during the same calendar year. No significant dose-response relationship was found for exposures > 200 mSv; however, only seven cases were noted in the ≥ 200 mSv exposure category. Among 200,583 Japanese nuclear workers, the average cumulative radiation dose was 12.2 mSv.26 The ERR/Sv for all cancers, excluding leukemia and alcohol-related malignancies, was 0.20 (95% CI, −1.42 to 2.09).

In summary, nuclear worker studies, with rare exceptions, did not show mean radiation exposures as high as those projected for some lung cancer screening participants (Table 3). In fact, only a small percentage of nuclear workers had exposures > 100 mSv, a dose readily reached by participants in lung cancer screening programs conducted over 20- to 30-year periods. Small numbers in the highest exposure categories of the nuclear worker studies, however, limit reliable analysis of risk of cancer at doses > 100 mSv (Table 427).

Table Graphic Jump Location
Table 3 —Nuclear Worker Studies and Cancer Risk

ERR = excess relative risk (per sievert); SMR = standardized mortality ratio.

a 

95% CI not available.

b 

Standardized incidence ratio.

c 

For ≥ 5 mSv.

d 

For < 5 mSv.

Table Graphic Jump Location
Table 4 —Nuclear Worker Studies and Cancer Risk at Highest Exposures

N/A = not available.

a 

No lag.

b 

Five-year lag.

Atomic Bomb Survivor Studies

Atomic bomb survivor studies offer another perspective for evaluating potential radiation risks from lung cancer screening programs.28 The International Commission on Radiation Protection, the United Nations Scientific Commission on the Effects of Atomic Radiation, and the Biologic Effects of Ionizing Radiation of the US National Academy of Sciences have used studies of atomic bomb survivors for cancer risk estimates.

In the most recent update, the incidence of solid cancers, including lung cancer, was analyzed for a 40-year period.28 In a cohort of 105,427 people, 17,448 cancers were diagnosed from 1958 through 1998. Among 80,000 atomic bomb survivors who were within 10 km of the epicenter of the bomb and were alive and free of cancer in 1958, a statistically significant dose-response relationship was noted for risk of cancer at radiation doses ≤ 150 mGy. About 35,000 people received doses between 5 and 200 mGy, which would easily be experienced by lung cancer screening participants (Table 2). Risk of lung cancer based on radiation doses among atomic bomb survivors was 0.28 per gray for men and 1.33 per gray for women. The combined rate for lung cancer was 0.81 per gray. Risk of cancer was based on radiation dose, attained age, and age at exposure. The mean radiation dose of atomic bomb survivors was 40 mSv.29

Of the 90 million current and former smokers in the United States, about 8 to 8.7 million adults meet the NLST criteria for lung cancer screening with LDCT scan.3,3032 Thus, lung cancer screening may involve a substantial number of people, which makes clarifying the risks and benefits of screening of paramount importance.

We evaluated cumulative radiation doses for lung cancer screening participants from the LDCT scan to follow-up full CT scan and FNAB according to the incidence and prevalence of nodules consistent with the Fleischner guidelines. An earlier study assessed the potential radiation-induced cancer risks among lung cancer screening participants by comparing the dose from LDCT scans over a 25-year period with dose estimates from an earlier study of atomic bomb survivors.15 The author estimated a radiation-related lung cancer risk to be 0.85%, in addition to the approximate 17% expected lung cancer risk caused by cigarette smoking.15 It was estimated that if 50% of all current and former smokers participated in annual LDCT screening, about 36,000 cancers would develop from the screening itself.

An excess risk of cancer due to high-dose diagnostic procedures, such as CT scanning, interventional radiology, and barium enemas, has also been suggested.33,34 According to risk models in the National Research Council Biologic Effects of Ionizing Radiation report, about 4,100 cases of lung cancer per year could be related to CT scans.35

Limited data are available regarding high cumulative dose radiation exposure in nuclear worker studies, such as > 100 mSv, that could reliably be contrasted to the cumulative dose exposure in some long-term screening participants. Because radiation exposure is carefully controlled and routinely monitored at nuclear power plants, there are rare instances where cumulative radiation doses exceed 100 to 200 mSv. Nonetheless, some authors have suggested that radiation cancer risks of nuclear workers may be larger than expected,36 concluding that the cancer risk for low-dose radiation exposure is not lower than that in atomic bomb survivors, an assumption that has been incorporated into risk estimates and radiation exposure limits. Further complicating the assessment of radiation risk from lung cancer screening programs is the potential synergistic link between cigarette smoking and radiation exposure.37

Radiation doses associated with LDCT scanning and CT scanning vary among clinical settings. We used the radiation doses from the NLST, which arguably were under ideal conditions, even though radiation doses associated with CT scanning have ranged from 4 to 18 mSv.38 The challenge with the use of LDCT scans in screening is to provide sufficient radiation to differentiate between noise and artifact at a low dose and too much radiation at a high dose.39 The role of MRI of the lung in diagnosing a variety of pulmonary disorders has been reviewed.40 The authors drew attention to the potential for MRI to detect lung nodules and, thus, reduce ionizing radiation exposure. The sensitivity for MRI to detect lung nodules measuring 3 to ≥ 4 mm was described as 80% to 90%, whereas the MRI reaches 100% sensitivity in detecting nodules > 8 mm.40

Cancer risks associated with low levels of radiation have attracted attention for many years and have consistently shown a linear dose-response relationship, with radiation effects being cumulative.29 Epidemiologic evidence has linked some cancers with radiation doses of 50 to 100 mSv.29 According to Mascalchi et al,18 77% of the radiation dose in a screening program occurs as a result of annual screening and 23% as a result of follow-up of LDCT scan abnormalities. These authors estimated 0.33 radiation-induced cancers per 1,000 people screened.

The present work suggests that cumulative exposure to ionizing radiation over 20- to 30-year lung cancer screening programs can exceed lifetime doses experienced by nuclear power workers and atomic bomb survivors. The corresponding risks for cancer among radiation workers, atomic bomb survivors, and lung cancer screening participants will vary on the basis of numerous factors, including age and type of radiation exposure. In fact, direct comparisons of risks among the cohorts does not appear to be reliable for drawing definitive conclusions. Nonetheless, although individual risk of lung cancer from radiation in lung cancer screening programs appears relatively low (0.2%-1%) compared with the risks of lung cancer from smoking (about 16%), significant numbers of cancer can develop when considering population risks. Further efforts in controlling radiation and refining who will benefit from lung cancer screening are warranted.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

ERR

excess relative risk

ERR/Sv

excess relative risk of lung cancer associated with radiation dose

FNAB

fine-needle aspiration biopsy

LDCT

low-dose CT

NLST

National Lung Cancer Screening Trial

Collins LG, Haines C, Perkel R, Enck RE. Lung cancer: diagnosis and management. Am Fam Physician. 2007;75(1):56-63. [PubMed]
 
Aberle DR, Adams AM, Berg CD, et al; National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409. [CrossRef] [PubMed]
 
Bach PB, Mirkin JN, Oliver TK, et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA. 2012;307(22):2418-2429. [CrossRef] [PubMed]
 
Sarma A, Heilbrun ME, Conner KE, Stevens SM, Woller SC, Elliott CG. Radiation and chest CT scan examinations: what do we know? Chest. 2012;142(3):750-760. [CrossRef] [PubMed]
 
Brenner DJ. Radiation and chest CT scans: are there problems? What should we do? Chest. 2012;142(3):549-550. [CrossRef] [PubMed]
 
Neugut AI, Accordino MK. ACP Journal Club. Review: CT screening for lung cancer reduced mortality in 1 large trial but not in 2 smaller trials. Ann Intern Med. 2012;157(6):JC3-JC6. [CrossRef] [PubMed]
 
Bach PB, Gould MK. When the average applies to no one: personalized decision making about potential benefits of lung cancer screening. Ann Intern Med. 2012;157(8):571-573. [CrossRef] [PubMed]
 
Greenberg AK, Lu F, Goldberg JD, et al. CT scan screening for lung cancer: risk factors for nodules and malignancy in a high-risk urban cohort. PLoS ONE. 2012;7(7):e39403 10.1371/journal.pone.0039403. [CrossRef] [PubMed]
 
Priola AM, Priola SM, Cataldi A, et al. Diagnostic accuracy and complication rate of CT-guided fine needle aspiration biopsy of lung lesions: a study based on the experience of the cytopathologist. Acta Radiol. 2010;51(5):527-533. [CrossRef] [PubMed]
 
Cardis E, Vrijheid M, Blettner M, et al. The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat Res. 2007;167(4):396-416. [CrossRef] [PubMed]
 
MacMahon H, Austin JH, Gamsu G, et al; Fleischner Society. Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society. Radiology. 2005;237(2):395-400. [CrossRef] [PubMed]
 
Tan BB, Flaherty KR, Kazerooni EA, Iannettoni MD; American College of Chest Physicians. The solitary pulmonary nodule. Chest. 2003;123(1_suppl):89S-96S. [CrossRef] [PubMed]
 
Meyer JD, Islam SS, Ducatman AM, McCunney RJ. Prevalence of small lung opacities in populations unexposed to dusts. A literature analysis. Chest. 1997;111(2):404-410. [CrossRef] [PubMed]
 
Larke FJ, Kruger RL, Cagnon CH, et al. Estimated radiation dose associated with low-dose chest CT of average-size participants in the National Lung Screening Trial. AJR Am J Roentgenol. 2011;197(5):1165-1169. [CrossRef] [PubMed]
 
Brenner DJ. Radiation risks potentially associated with low-dose CT screening of adult smokers for lung cancer. Radiology. 2004;231(2):440-445. [CrossRef] [PubMed]
 
Sodickson A, Baeyens PF, Andriole KP, et al. Recurrent CT, cumulative radiation exposure, and associated radiation-induced cancer risks from CT of adults. Radiology. 2009;251(1):175-184. [CrossRef] [PubMed]
 
Mettler FA Jr, Huda W, Yoshizumi TT, Mahesh M. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology. 2008;248(1):254-263. [CrossRef] [PubMed]
 
Mascalchi M, Mazzoni LN, Falchini M, et al. Dose exposure in the ITALUNG trial of lung cancer screening with low-dose CT. Br J Radiol. 2012;85(1016):1134-1139. [CrossRef] [PubMed]
 
Wakeford R. Radiation in the workplace-a review of studies of the risks of occupational exposure to radiation. J Radiol Prot. 2009;29(2A):A61-A79. [CrossRef] [PubMed]
 
Brenner DJ, Hall EJ. Computed tomography—an increasing source of radiation exposure. N Engl J Med. 2007;357(22):2277-2284. [CrossRef] [PubMed]
 
Hammer GP, Fehringer F, Seitz G, et al. Exposure and mortality in a cohort of German nuclear power workers. Radiat Environ Biophys. 2008;47(1):95-99. [CrossRef] [PubMed]
 
Matanoski GM, Tonascia JA, Correa-Villaseñor A, et al. Cancer risks and low-level radiation in US shipyard workers. J Radiat Res (Tokyo). 2008;49(1):83-91. [CrossRef]
 
Muirhead CR, O’Hagan JA, Haylock RG, et al. Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer. 2009;100(1):206-212. [CrossRef] [PubMed]
 
Jeong M, Jin Y-W, Yang KH, Ahn YO, Cha CY. Radiation exposure and cancer incidence in a cohort of nuclear power industry workers in the Republic of Korea, 1992-2005. Radiat Environ Biophys. 2010;49(1):47-55. [CrossRef] [PubMed]
 
Boice JD Jr, Cohen SS, Mumma MT, et al. Updated mortality analysis of radiation workers at Rocketdyne (Atomics International), 1948-2008. Radiat Res. 2011;176(2):244-258. [CrossRef] [PubMed]
 
Akiba S, Mizuno S. The third analysis of cancer mortality among Japanese nuclear workers, 1991-2002: estimation of excess relative risk per radiation dose. J Radiol Prot. 2012;32(1):73-83. [CrossRef] [PubMed]
 
Howe GR, Zablotska LB, Fix JJ, Egel J, Buchanan J. Analysis of the mortality experience amongst US nuclear power industry workers after chronic low dose exposure to ionizing radiation. Radiat Res. 2004;162(5):517-526. [CrossRef] [PubMed]
 
Little MP. Cancer and non-cancer effects in Japanese bomb survivors. J Radiol Prot. 2009;29(2A):A43-A59. [CrossRef] [PubMed]
 
Preston DL, Pierce DA, Shimizu Y, et al. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat Res. 2004;162(4):377-389. [CrossRef] [PubMed]
 
Brenner DJ, Doll R, Goodhead DT, et al. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci U S A. 2003;100(24):13761-13766. [CrossRef] [PubMed]
 
Zurawska JH, Jen R, Lam S, Coxson HO, Leipsic J, Sin DD. What to do when a smoker’s CT scan is “normal”? Implications for lung cancer screening. Chest. 2012;141(5):1147-1152. [CrossRef] [PubMed]
 
Doria-Rose VP, White MC, Klabunde CN, et al. Use of lung cancer screening tests in the United States: results from the 2010 National Health Interview Survey. Cancer Epidemiol Biomarkers Prev. 2012;21(7):1049-1059. [CrossRef] [PubMed]
 
Jones DG, Shrimpton PC. Survey of CT Practice in the UK: Normalised Organ Doses for X-ray Computed Tomography Calculated Using Monte Carlo Techniques. Harwell, England: National Radiological Protection Board; 1991.
 
Hall EJ, Brenner DJ. Cancer risks from diagnostic radiology. Br J Radiol. 2008;81(965):362-378. [CrossRef] [PubMed]
 
Berrington de González A, Mahesh M, Kim KP, et al. Projected cancer risks from computed tomographic scans performed in the United States in 2007. Arch Intern Med. 2009;169(22):2071-2077. [CrossRef] [PubMed]
 
Jacob P, Rühm W, Walsh L, Blettner M, Hammer G, Zeeb H. Is cancer risk of radiation workers larger than expected? Occup Environ Med. 2009;66(12):789-796. [CrossRef] [PubMed]
 
Pierce DA, Sharp GB, Mabuchi K. Joint effects of radiation and smoking on lung cancer risk among atomic bomb survivors. Radiat Res. 2003;159(4):511-520. [CrossRef] [PubMed]
 
Mettler FA Jr, Bhargavan M, Faulkner K, et al. Radiological and nuclear medicine studies in the United States and worldwide: frequency, radiation dose, and comparison with radiation sources—1950-2007. Radiology. 2009;253(2):520-531. [CrossRef] [PubMed]
 
Donnelly EF. Technical parameters and interpretive issues in screening computed tomography scans for lung cancer. J Thorac Imaging. 2012;27(4):224-229. [CrossRef] [PubMed]
 
Wielpütz M, Kauczor HU. MRI of the lung: state of the art. Diagn Interv Radiol. 2012;18(4):344-353. [PubMed]
 

Figures

Tables

Table Graphic Jump Location
Table 1 —Fleischner Guidelines for Follow-up of Pulmonary Nodules

From MacMahon et al.11

Table Graphic Jump Location
Table 2 —Estimation of Radiation Exposure From LDCT Scanning and Follow-up Tests

LDCT = low-dose CT.

Table Graphic Jump Location
Table 3 —Nuclear Worker Studies and Cancer Risk

ERR = excess relative risk (per sievert); SMR = standardized mortality ratio.

a 

95% CI not available.

b 

Standardized incidence ratio.

c 

For ≥ 5 mSv.

d 

For < 5 mSv.

Table Graphic Jump Location
Table 4 —Nuclear Worker Studies and Cancer Risk at Highest Exposures

N/A = not available.

a 

No lag.

b 

Five-year lag.

References

Collins LG, Haines C, Perkel R, Enck RE. Lung cancer: diagnosis and management. Am Fam Physician. 2007;75(1):56-63. [PubMed]
 
Aberle DR, Adams AM, Berg CD, et al; National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409. [CrossRef] [PubMed]
 
Bach PB, Mirkin JN, Oliver TK, et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA. 2012;307(22):2418-2429. [CrossRef] [PubMed]
 
Sarma A, Heilbrun ME, Conner KE, Stevens SM, Woller SC, Elliott CG. Radiation and chest CT scan examinations: what do we know? Chest. 2012;142(3):750-760. [CrossRef] [PubMed]
 
Brenner DJ. Radiation and chest CT scans: are there problems? What should we do? Chest. 2012;142(3):549-550. [CrossRef] [PubMed]
 
Neugut AI, Accordino MK. ACP Journal Club. Review: CT screening for lung cancer reduced mortality in 1 large trial but not in 2 smaller trials. Ann Intern Med. 2012;157(6):JC3-JC6. [CrossRef] [PubMed]
 
Bach PB, Gould MK. When the average applies to no one: personalized decision making about potential benefits of lung cancer screening. Ann Intern Med. 2012;157(8):571-573. [CrossRef] [PubMed]
 
Greenberg AK, Lu F, Goldberg JD, et al. CT scan screening for lung cancer: risk factors for nodules and malignancy in a high-risk urban cohort. PLoS ONE. 2012;7(7):e39403 10.1371/journal.pone.0039403. [CrossRef] [PubMed]
 
Priola AM, Priola SM, Cataldi A, et al. Diagnostic accuracy and complication rate of CT-guided fine needle aspiration biopsy of lung lesions: a study based on the experience of the cytopathologist. Acta Radiol. 2010;51(5):527-533. [CrossRef] [PubMed]
 
Cardis E, Vrijheid M, Blettner M, et al. The 15-country collaborative study of cancer risk among radiation workers in the nuclear industry: estimates of radiation-related cancer risks. Radiat Res. 2007;167(4):396-416. [CrossRef] [PubMed]
 
MacMahon H, Austin JH, Gamsu G, et al; Fleischner Society. Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society. Radiology. 2005;237(2):395-400. [CrossRef] [PubMed]
 
Tan BB, Flaherty KR, Kazerooni EA, Iannettoni MD; American College of Chest Physicians. The solitary pulmonary nodule. Chest. 2003;123(1_suppl):89S-96S. [CrossRef] [PubMed]
 
Meyer JD, Islam SS, Ducatman AM, McCunney RJ. Prevalence of small lung opacities in populations unexposed to dusts. A literature analysis. Chest. 1997;111(2):404-410. [CrossRef] [PubMed]
 
Larke FJ, Kruger RL, Cagnon CH, et al. Estimated radiation dose associated with low-dose chest CT of average-size participants in the National Lung Screening Trial. AJR Am J Roentgenol. 2011;197(5):1165-1169. [CrossRef] [PubMed]
 
Brenner DJ. Radiation risks potentially associated with low-dose CT screening of adult smokers for lung cancer. Radiology. 2004;231(2):440-445. [CrossRef] [PubMed]
 
Sodickson A, Baeyens PF, Andriole KP, et al. Recurrent CT, cumulative radiation exposure, and associated radiation-induced cancer risks from CT of adults. Radiology. 2009;251(1):175-184. [CrossRef] [PubMed]
 
Mettler FA Jr, Huda W, Yoshizumi TT, Mahesh M. Effective doses in radiology and diagnostic nuclear medicine: a catalog. Radiology. 2008;248(1):254-263. [CrossRef] [PubMed]
 
Mascalchi M, Mazzoni LN, Falchini M, et al. Dose exposure in the ITALUNG trial of lung cancer screening with low-dose CT. Br J Radiol. 2012;85(1016):1134-1139. [CrossRef] [PubMed]
 
Wakeford R. Radiation in the workplace-a review of studies of the risks of occupational exposure to radiation. J Radiol Prot. 2009;29(2A):A61-A79. [CrossRef] [PubMed]
 
Brenner DJ, Hall EJ. Computed tomography—an increasing source of radiation exposure. N Engl J Med. 2007;357(22):2277-2284. [CrossRef] [PubMed]
 
Hammer GP, Fehringer F, Seitz G, et al. Exposure and mortality in a cohort of German nuclear power workers. Radiat Environ Biophys. 2008;47(1):95-99. [CrossRef] [PubMed]
 
Matanoski GM, Tonascia JA, Correa-Villaseñor A, et al. Cancer risks and low-level radiation in US shipyard workers. J Radiat Res (Tokyo). 2008;49(1):83-91. [CrossRef]
 
Muirhead CR, O’Hagan JA, Haylock RG, et al. Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer. 2009;100(1):206-212. [CrossRef] [PubMed]
 
Jeong M, Jin Y-W, Yang KH, Ahn YO, Cha CY. Radiation exposure and cancer incidence in a cohort of nuclear power industry workers in the Republic of Korea, 1992-2005. Radiat Environ Biophys. 2010;49(1):47-55. [CrossRef] [PubMed]
 
Boice JD Jr, Cohen SS, Mumma MT, et al. Updated mortality analysis of radiation workers at Rocketdyne (Atomics International), 1948-2008. Radiat Res. 2011;176(2):244-258. [CrossRef] [PubMed]
 
Akiba S, Mizuno S. The third analysis of cancer mortality among Japanese nuclear workers, 1991-2002: estimation of excess relative risk per radiation dose. J Radiol Prot. 2012;32(1):73-83. [CrossRef] [PubMed]
 
Howe GR, Zablotska LB, Fix JJ, Egel J, Buchanan J. Analysis of the mortality experience amongst US nuclear power industry workers after chronic low dose exposure to ionizing radiation. Radiat Res. 2004;162(5):517-526. [CrossRef] [PubMed]
 
Little MP. Cancer and non-cancer effects in Japanese bomb survivors. J Radiol Prot. 2009;29(2A):A43-A59. [CrossRef] [PubMed]
 
Preston DL, Pierce DA, Shimizu Y, et al. Effect of recent changes in atomic bomb survivor dosimetry on cancer mortality risk estimates. Radiat Res. 2004;162(4):377-389. [CrossRef] [PubMed]
 
Brenner DJ, Doll R, Goodhead DT, et al. Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci U S A. 2003;100(24):13761-13766. [CrossRef] [PubMed]
 
Zurawska JH, Jen R, Lam S, Coxson HO, Leipsic J, Sin DD. What to do when a smoker’s CT scan is “normal”? Implications for lung cancer screening. Chest. 2012;141(5):1147-1152. [CrossRef] [PubMed]
 
Doria-Rose VP, White MC, Klabunde CN, et al. Use of lung cancer screening tests in the United States: results from the 2010 National Health Interview Survey. Cancer Epidemiol Biomarkers Prev. 2012;21(7):1049-1059. [CrossRef] [PubMed]
 
Jones DG, Shrimpton PC. Survey of CT Practice in the UK: Normalised Organ Doses for X-ray Computed Tomography Calculated Using Monte Carlo Techniques. Harwell, England: National Radiological Protection Board; 1991.
 
Hall EJ, Brenner DJ. Cancer risks from diagnostic radiology. Br J Radiol. 2008;81(965):362-378. [CrossRef] [PubMed]
 
Berrington de González A, Mahesh M, Kim KP, et al. Projected cancer risks from computed tomographic scans performed in the United States in 2007. Arch Intern Med. 2009;169(22):2071-2077. [CrossRef] [PubMed]
 
Jacob P, Rühm W, Walsh L, Blettner M, Hammer G, Zeeb H. Is cancer risk of radiation workers larger than expected? Occup Environ Med. 2009;66(12):789-796. [CrossRef] [PubMed]
 
Pierce DA, Sharp GB, Mabuchi K. Joint effects of radiation and smoking on lung cancer risk among atomic bomb survivors. Radiat Res. 2003;159(4):511-520. [CrossRef] [PubMed]
 
Mettler FA Jr, Bhargavan M, Faulkner K, et al. Radiological and nuclear medicine studies in the United States and worldwide: frequency, radiation dose, and comparison with radiation sources—1950-2007. Radiology. 2009;253(2):520-531. [CrossRef] [PubMed]
 
Donnelly EF. Technical parameters and interpretive issues in screening computed tomography scans for lung cancer. J Thorac Imaging. 2012;27(4):224-229. [CrossRef] [PubMed]
 
Wielpütz M, Kauczor HU. MRI of the lung: state of the art. Diagn Interv Radiol. 2012;18(4):344-353. [PubMed]
 
NOTE:
Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s "Cited By" API will populate this tab (http://www.crossref.org/citedby.html).

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging & repositioning the boxes below.

Find Similar Articles
CHEST Journal Articles
The Cost-Effectiveness of Low-Dose CT Screening for Lung Cancer*: Preliminary Results of Baseline Screening
PubMed Articles
  • CHEST Journal
    Print ISSN: 0012-3692
    Online ISSN: 1931-3543