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Kaplan-Meier curve for incident cases of lung cancer among 3348 current and former smokers, stratified by degree of lung function impairment. From the National Health and Nutrition Examination Survey, 1971 through 1975, and follow-up through 1992. COPD indicates chronic obstructive pulmonary disease.

Kaplan-Meier curve for incident cases of lung cancer among 3348 current and former smokers, stratified by degree of lung function impairment. From the National Health and Nutrition Examination Survey, 1971 through 1975, and follow-up through 1992. COPD indicates chronic obstructive pulmonary disease.

Table 1. 
Participants Included in the Analysis*
Participants Included in the Analysis*
Table 2. 
Participants Included in Analysis Stratified by Smoking Status and Degree of Pulmonary Function Impairment*
Participants Included in Analysis Stratified by Smoking Status and Degree of Pulmonary Function Impairment*
Table 3. 
Proportional Hazards Model for Incident Lung Cancer*
Proportional Hazards Model for Incident Lung Cancer*
1.
Greenlee  RTMurray  TBolden  SWingo  PA Cancer statistics, 2000. CA Cancer J Clin. 2000;507- 33Article
2.
Steenland  KLoomis  DShy  CSimonsen  N Review of occupational lung carcinogens. Am J Ind Med. 1996;29474- 490Article
3.
Skillrud  DMOfford  KPMiller  RD Higher risk of lung cancer in chronic obstructive pulmonary disease: a prospective, matched, controlled study. Ann Intern Med. 1986;105503- 507Article
4.
Tockman  MSAnthonisen  NRWright  ECDonithan  MG Airways obstruction and the risk for lung cancer. Ann Intern Med. 1987;106512- 518Article
5.
Lange  PNyboe  JAppleyard  MJensen  GSchnohr  P Ventilatory function and chronic mucus hypersecretion as predictors of death from lung cancer. Am Rev Respir Dis. 1990;141613- 617Article
6.
American Thoracic Society, Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;152 (5, pt 2) S77- S121
7.
Pauwels  RABuist  ASCalverley  PMJenkins  CRHurd  SS Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) workshop summary. Am J Respir Crit Care Med. 2001;1631256- 1276Article
8.
National Center for Health Statistics, Plan and Operation of the HANES I Augmentation Survey of Adults 25-74 Years, United States, 1974-75.  Washington, DC National Center for Health Statistics1978;
9.
National Center for Health Statistics, Plan and Operation of the Health and Nutrition Examination Survey, United States, 1971-73.  Washington, DC National Center for Health Statistics1973;
10.
Cohen  BBBarbano  HECox  CS  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study: 1982-84. Vital Health Stat 1. 1987;221- 142
11.
Cox  CSMussolino  MERothwell  ST  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study, 1992. Vital Health Stat 1. 1997;351- 231
12.
Cox  CSRothwell  STMadans  JH  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study, 1987. Vital Health Stat 1. 1992;271- 190
13.
Finucane  FFFreid  VMMadans  JH  et al.  Plan and operation of the NHANES I epidemiologic followup study, 1986. Vital Health Stat 1. 1990;251- 154
14.
American Thoracic Society, Lung function testing: selection of reference values and interpretive strategies. Am J Respir Crit Care Med. 1991;1441202- 1218
15.
Not Available, International Classification of Diseases, Ninth Revision, Clinical Modification. 3rd ed. Washington, DC Public Health Service, US Dept of Health and Human Services1989;
16.
Islam  SSSchottenfeld  D Declining FEV1 and chronic productive cough in cigarette smokers: a 25-year prospective study of lung cancer incidence in Tecumseh, Michigan. Cancer Epidemiol Biomarkers Prev. 1994;3289- 298
17.
Van den Eeden  SKFriedman  GD Forced expiratory volume (1 second) and lung cancer incidence and mortality. Epidemiology. 1992;3253- 257Article
18.
Hole  DJWatt  GCDavey-Smith  GHart  CLGillis  CRHawthorne  VM Impaired lung function and mortality risk in men and women: findings from the Renfrew and Paisley prospective population study. BMJ. 1996;313711- 715Article
19.
Mannino  DMGagnon  RCPetty  TLLydick  E Obstructive lung disease and low lung function in adults in the United States: data from the National Health and Nutrition Examination Survey, 1988-1994. Arch Intern Med. 2000;1601683- 1689Article
20.
Mannino  DMEtzel  RAFlanders  WD Do the medical history and physical examination predict low lung function? Arch Intern Med. 1993;1531892- 1897Article
21.
Badgett  RGTanaka  DJHunt  DK  et al.  Can moderate chronic obstructive pulmonary disease be diagnosed by historical and physical findings alone? Am J Med. 1993;94188- 196Article
22.
Ferguson  GTEnright  PLBuist  ASHiggins  MW Office spirometry for lung health assessment in adults: a consensus statement from the National Lung Health Education Program. Chest. 2000;1171146- 1161Article
23.
Burns  DMShanks  TGChoi  W The American Cancer Society Cancer Prevention Study 1: 12-Year Follow-up of 1 Million Men and Women: Changes in Cigarette-Related Disease: Risk and Their Implications for Prevention and Control.  Washington, DC US Dept Health and Human Services2001;113- 304NIH publication 97-1213.
24.
Tong  LSpitz  MRFueger  JJAmos  CA Lung carcinoma in former smokers. Cancer. 1996;781004- 1010Article
25.
Not Available, US Department of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. The Health Benefits of Smoking Cessation: A Report of the Surgeon General.  Rockville, Md US Dept of Health and Human Services1990;DHHS publication 90-8416.
26.
Enstrom  JE Smoking cessation and mortality trends among two United States populations. J Clin Epidemiol. 1999;52813- 825Article
27.
Eddy  DM Screening for lung. Ann Intern Med. 1989;111232- 237Article
28.
Manser  RLIrving  LBStone  CByrnes  GAbramson  MCampbell  D Screening for lung cancer [Cochrane Review on CD-ROM].  Oxford, England Cochrane Library, Update Software2003; (issue 1)
29.
Henschke  CI Early lung cancer action project: overall design and findings from baseline screening. Cancer. 2000;89 (11 suppl) 2474- 2482Article
30.
Henschke  CINaidich  DPYankelevitz  DF  et al.  Early lung cancer action project: initial findings on repeat screenings. Cancer. 2001;92153- 159Article
31.
Petty  TL Lung cancer screening. Compr Ther. 1995;21432- 437
32.
Petty  TL Screening strategies for early detection of lung cancer: the time is now. JAMA. 2000;2841977- 1980Article
33.
Wolpaw  DR Early detection in lung cancer: case finding and screening. Med Clin North Am. 1996;8063- 82Article
34.
Jett  JR Spiral computed tomography screening for lung cancer is ready for prime time. Am J Respir Crit Care Med. 2001;163812- 815Article
Original Investigation
June 23, 2003

Low Lung Function and Incident Lung Cancer in the United StatesData From the First National Health and Nutrition Examination Survey Follow-up

Author Affiliations

From the Air Pollution and Respiratory Health Branch, Division of Environmental Hazards and Health Effects, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Ga (Drs Mannino and Redd); the Veterans Administration Medical Center, Decatur, Ga (Dr Aguayo); and Division of Pulmonary Sciences and Critical Care Medicine, University of Colorado Health Sciences Center, Denver, Colo (Dr Petty). The authors have no relevant financial interest in this article.

Arch Intern Med. 2003;163(12):1475-1480. doi:10.1001/archinte.163.12.1475
Abstract

Background  Obstructive lung disease and lung cancer are tobacco-related diseases that can remain clinically silent until late in the disease process. We sought to define the risk for incident lung cancer among a national cohort of US adults with and without obstructive lung disease.

Methods  We studied participants in the First National Health and Nutrition Examination Survey, who had up to 22 years of follow-up. We classified subjects as having moderate or severe obstructive lung disease at baseline if the ratio of forced expiratory volume in 1 second (FEV1) to forced vital capacity (FVC) was less than 70% and the FEV1 was less than 80% of the predicted value. We also determined incident cases of lung cancer during the follow-up period.

Results  A total of 113 lung cancers occurred in the 5402 adults in the cohort. In the proportional hazards model adjusted for covariates of age, sex, race, education, smoking status, and duration and intensity of smoking, the presence of moderate or severe obstructive lung disease was associated with a higher risk for incident lung cancer (hazard ratio, 2.8; 95% confidence interval, 1.8-4.4).

Conclusions  The presence of moderate or severe obstructive lung disease is a significant predictor of incident lung cancer in long-term follow-up. This finding may be useful clinically and in studies evaluating the utility of new tools for the early detection of lung cancer.

LUNG CANCER is the leading cause of cancer-related mortality in the United States. In 2000, an estimated 156 900 deaths were attributed to lung cancer.1 Tobacco smoking is the most important risk factor for lung cancer, although exposures to other agents, such as radon and asbestos, are also important factors.2 A diagnosis of obstructive lung disease has been found to be associated with a higher rate of lung cancer in several studies,35 although none of these have been representative of the US adult population.

The diagnosis of obstructive lung disease has traditionally depended on the presence of symptoms such as chronic cough or sputum production.6 New international guidelines for the diagnosis of obstructive lung disease depend almost exclusively on measured lung function to diagnose and classify disease.7

We applied spirometric criteria for the diagnosis of obstructive lung disease to the cohort of 5402 subjects who had pulmonary function measurements obtained as part of the First National Health and Nutrition Examination Survey (NHANES I).8,9 We searched the NHANES I follow-up database for incident cases of lung cancer in the up to 22 years of follow-up and determined the significant predictors of lung cancer in this cohort.

METHODS

The NHANES I was conducted by the National Center for Health Statistics from 1971 to 1975.8,9 This was a survey of a probability sample of the civilian, noninstitutionalized population of the United States. Follow-up surveys of the adult participants (aged 25-74 years old) in the NHANES I occurred in 1982 to 1984, 1986, 1987, and 1992.1013 Data collected on participants included hospitalization records, vital status, and, for decedents, death certificates. Through 1992, 96% of the original cohort had been successfully traced, and death certificates were available for 98% of the 4604 documented decedents.11

QUESTIONNAIRE DATA

Participants in the NHANES I completed an extensive questionnaire that included the demographic data of age, race, sex, and education level. We classified subjects as having no greater than 12 or at least 13 years of education. A nationally representative subset of participants completed a cardiorespiratory module that included a series of questions about the presence of respiratory symptoms and the diagnosis of respiratory disease. The pulmonary symptoms included in the analysis (to define an asymptomatic subset of the population to calculate equations for lung function) were cough (defined as a positive response to "Have you ever had a cough first thing in the morning in the winter?" or "Have you ever had a cough first thing in the morning in the summer?"), sputum (defined as a positive response to "Have you ever had any phlegm from your chest first thing in the morning in the winter?" or "Have you ever had any phlegm from your chest first thing in the morning in the summer?"), and wheeze (defined as a positive response to "Have you ever had wheezy or whistling sounds in your chest?"). Participants were also asked if they had physician-diagnosed chronic bronchitis (nonallergic), emphysema, or asthma.

Complete smoking histories were obtained on all participants. We considered participants to be current smokers if they reported the use of cigarettes, cigars, or pipes at the time of the survey. We considered participants to be former smokers if they reported any previous use of cigarettes (≥100), cigars (≥50), or pipes (≥3 packages of tobacco), but no current use. Long-term intensity of use data were available only for cigarettes. We calculated pack-years of cigarette use by multiplying the average number of cigarettes smoked daily by the number of years smoked and dividing the product by 20. Former cigarette smokers reported how long it had been since they smoked cigarettes fairly regularly.

PULMONARY FUNCTION DATA

Subjects who participated in the cardiorespiratory module performed spirometry using a spirometer (Model 800; Ohio Medical Instrument Company, Inc, Cincinnati, Ohio). The procedures used have been documented previously.9 Subjects were excluded from this analysis if they did not perform spirometry or had results that were not reliable. Values used in this analysis included forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1), and the FEV1/FVC ratio. We determined predicted values of FEV1 and FVC by performing linear regression (stratified by sex and using age and height as predictors) on a subgroup of participants who were white, had never smoked, and did not report respiratory symptoms or physician-diagnosed lung disease. The results from these regression models were applied to the data from all participants to obtain predicted values of FEV1 and FVC. We used an adjustment factor of 0.88 to estimate predicted values for African American participants.14 We classified the subjects as having moderate or severe obstructive lung disease if the FEV1/FVC ratio was less than 70% and the FEV1 was less than 80% of the predicted value7; as having mild obstructive lung disease if the FEV1/FVC ratio was less than 70% and the FEV1 was at least 80% of the predicted value; and as having restrictive disease if the FEV1/FVC ratio was at least 70% and the FVC was less than 80% of the predicted value.

INCIDENT CASES OF LUNG CANCER

Participants who reported cancer at the baseline interview were excluded from the analysis. Lung cancer cases were defined as any hospital discharge diagnosis coded 162 using the International Classification of Diseases, Ninth Revision, Clinical Modification,15 or a death certificate containing this code.

DATA ANALYSIS

Our primary outcome of interest was incident lung cancer, and the main predictor of interest in our analysis was baseline lung function. We used logistic regression models to predict incident cases of lung cancer in the follow-up group using baseline lung function, stratified into 4 categories, as the main predictor and controlling for age, smoking status, race, sex, education level, years since last smoked (for former smokers), and pack-years of cigarettes (for current and former smokers). These analyses were performed using the statistical package SUDAAN (RTI, Research Triangle Park, NC) and SPSS (SPSS Inc, Chicago, Ill). Results were similar in analyses performed with and without the NHANES I sampling weights and complex design incorporated. Only the unweighted data are presented.

Cox proportional hazard regression models were developed using the SUDAAN procedure SURVIVAL to take into account the potential of differential follow-up in NHANES I participants. We used time of follow-up as the underlying time metric. For lung cancer cases, the exit date was the date of the first hospitalization with a discharge diagnosis of lung cancer or, if this was unavailable, the date of death reported on the death certificate. For those without a diagnosis of lung cancer (noncases), the exit date was the date of death or the date the subject was last known to be alive. We included age, sex, race, smoking status, pulmonary function level, pack-years of cigarette smoking, and years since last smoked in the regression models.

RESULTS

A total of 14 407 adults aged 25 to 74 years participated in the NHANES I. From this sample, 6913 participated in the cardiorespiratory survey and examination. We excluded 1371 subjects who did not undergo pulmonary function testing or had results that were not reliable, and 140 subjects who admitted to a history of cancer at the baseline evaluation, resulting in 5402 subjects in the final analytic cohort. Subjects excluded because of missing pulmonary function data were more likely to be older than 60 years (37.8% vs 22.8%; P<.001) and to be of nonwhite race (21.8% vs 11.8%; P<.001) than subjects included in the final cohort. Current smokers had a mean smoke exposure of 33.1 pack-years (SE, 0.7 pack-years) and 27.9 cigarettes per day (SE, 0.4 cigarette per day), whereas former smokers had a mean smoke exposure of 33.3 pack-years (SE, 1.0 pack-years) and 25.4 cigarettes per day (SE, 0.6 cigarette per day) and had quit smoking 8.6 years (SE, 0.3 years) before the initial survey.

Median duration of follow-up of the cohort was 17.9 years (interquartile range [IQR], 15.4-19.9 years). During the follow-up period, 113 cases of lung cancer (2.1% of cohort) (Table 1) were identified, including 82 identified from hospitalization records and 31 from death certificates. Lung cancer developed during follow-up in a similar proportion of subjects who did not participate in the cardiorespiratory survey (2.0%), but it developed in a higher proportion of subjects without pulmonary function testing (3.8%). Of the 113 lung cancer cases, 85 occurred in current smokers, 18 in former smokers, and 10 in never smokers. Among current smokers, lung cancer developed in 3.7% in the follow-up period, compared with 1.7% of former smokers and 0.5% of those who never smoked (Table 2). Mild and moderate obstructive disease and restrictive disease at the baseline evaluation were associated with a higher proportion of lung cancer development among current and former smokers (Table 2).

The median time to lung cancer diagnosis (for the 82 cases detected on the basis of hospitalization records) was 9.8 years (IQR, 5.3-15.5 years). The median time to lung cancer diagnosis varied by level of lung function. Among subjects with no obstructive lung disease, this time was 12.4 years (IQR, 8.5-16.6 years); among subjects with restrictive lung disease, 10.0 years (IQR, 6.3-15.3 years); among subjects with mild obstructive lung disease, 9.5 years (IQR, 6.7-17.8 years); and among subjects with moderate or severe obstructive lung disease, 5.3 years (IQR, 2.6-9.8 years). Similar results were obtained when the end point was lung cancer diagnosis or death due to lung cancer among current and former smokers (Figure 1).

The median age at lung cancer diagnosis (for the 82 cases detected on the basis of hospitalization records) was 69.6 years (IQR, 63.1-74.4 years). The median age of lung cancer diagnosis varied by level of lung function. Among subjects with no obstructive lung disease, this age was 68.2 years (IQR, 63.1-74.4 years); among subjects with moderate or severe obstructive lung disease, 71.1 years (IQR, 67.1-74.4 years).

Moderate or severe obstructive lung disease was a significant predictor of incident lung cancer in logistic regression models that controlled for age, smoking status, sex, education level, pack-years of cigarette smoking, and years since quitting smoking (odds ratio [OR], 2.4; 95% confidence interval [CI], 1.5-3.8). Similar results were obtained in a model restricted to current and former smokers (OR, 2.6; 95% CI, 1.6-4.2).

In the multivariate proportional hazards analysis (Table 3), moderate or severe obstructive lung disease was a significant hazard for incident lung cancer in the follow-up period among the entire cohort (hazard ratio [HR], 2.8; 95% CI, 1.8-4.4) and when limited to current or former smokers (OR, 3.0; 95% CI, 1.9-4.8).

COMMENT

In this analysis of a nationally representative cohort of the US population with up to 22 years of follow-up, we found that the presence of moderate or severe obstructive lung disease was associated with an increased risk for development of incident lung cancer during the follow-up period. Lung cancer is predominantly a disease of current and former smokers, and in our analyses limited to this group, the presence of moderate or severe obstructive lung disease remained a predictor of incident lung cancer. A somewhat surprising finding was that lung cancer developed in 6.7% of former smokers with obstructive lung disease during the follow-up period (Table 2). Another interesting finding was that subjects with restrictive lung disease had a slightly increased risk for development of lung cancer during the follow-up period.

Most previous studies of the association of obstructive lung disease and lung cancer in the United States have been performed in smaller populations not necessarily representative of the US population.3,4 One prospective study of 226 subjects, including 113 case subjects with an FEV1 of no greater than 70% and 113 matched control subjects with an FEV1 of at least 85%, found that lung cancer developed in 8.8% of the cases and 2.0% of the controls (all among current smokers) during the 10-year follow-up period.3 Another US study that included people with moderate to severe obstructive lung disease and current smokers found that the risk for lung cancer increased with increasing levels of airway obstruction, although subjects were only followed up for 1 to 3 years.4 A larger study of 3956 subjects from Tecumseh, Mich, followed up from 1962 through 1987, identified 60 incident lung cancers (1.5%) and found that a lower baseline FEV1 and a more rapid decline in FEV1 were associated with a higher risk for lung cancer.16 Another US study found that a lower FEV1 was associated with higher lung cancer mortality rates among currently smoking men, but not among women.17

International studies have shown similar results. A Danish study of 13 946 participants followed up for 10 years found increased mortality risks due to lung cancer in subjects with an FEV1 of less than 40% (HR, 3.9 [95% CI, 2.2-7.2]) or of 40% to 79% (HR, 2.1 [95% CI, 1.3-5.4]) when compared with subjects with an FEV1 of at least 80%.5 In a Scottish study of 15 411 subjects followed up for 15 years, men and women with low lung function (FEV1 of <73% and <75%, respectively) had a higher risk for lung cancer mortality (HR, 2.5 and 4.4, respectively) compared with subjects in the highest quintile of lung function.18

One difference between our study and the previous studies was our separate evaluations of mild obstructive lung disease and restrictive lung disease. There was a suggestion in the univariate models that lung cancer is more likely to develop in both of these groups (Table 3), although these findings did not remain significant in the multivariate models.

We used objective criteria for obstructive lung disease to define the population with moderate or severe airway obstruction.7 We know from other studies that 63% of the adult US population with this degree of airway obstruction has never received a diagnosis of any lung disease,19 and that dependence on clinical signs or symptoms will not detect most of these individuals.20,21 To address this gap, a new national health care initiative, the National Lung Health Education Program, recommends spirometric testing for all smokers (current and former) aged 45 years or older and anyone with respiratory symptoms.22

A surprising finding in our analysis was that the proportion of former smokers with moderate obstructive disease in whom lung cancer developed was almost as high as the proportion of current smokers (6.7% vs 10.8%). Many lung cancers are being diagnosed in former smokers because of the increasing numbers of former smokers in the population and their greater age (relative to current smokers).23,24 Most studies suggest that even after 3 to 5 years of smoking abstinence, the risk for cancer is similar to that of current smokers.23,25 In our univariate models, former smokers who stopped smoking at least 10 years before the survey had an HR of 3.7 for development of lung cancer, compared with those who never smoked (Table 3). In our analysis, we only determined smoking status at baseline, although a proportion of these subjects likely stopped smoking during the follow-up period, which would result in an even higher proportion of lung cancer in former smokers.26

Another finding in our analysis was that although subjects without obstructive lung disease had a longer interval from the time of the survey to the time of lung cancer diagnosis (12.4 vs 5.3 years for subjects with obstructive lung disease), they received a diagnosis of lung cancer at a slightly younger age (68.2 vs 71.1 years). This difference raises the possibility that the factors related to lung cancer in the presence of obstructive lung disease differ from those in its absence.

Lung cancer remains one of the most deadly malignancies in the United States, with an estimated 164 100 new cases and 156 900 deaths in 2000.1 Screening for lung cancer is currently not recommended, although the basis for this policy consists of studies performed more than 20 years ago.1,27,28 Modern imaging techniques involving computed tomography scanning with low-dosage radiation may be able to alter this recommendation.29,30 The findings of our study point to the potential utility of pulmonary function testing among current and former smokers to identify a subgroup of patients in whom lung cancer is more likely to develop and who are more likely to benefit from screening or case detection.3134

There are certain limitations to our analysis. Pulmonary function data were obtained only at the baseline evaluation, so we could not determine in which subjects obstructive lung disease may have developed in the follow-up period. Hospitalizations and deaths associated with lung cancer had no independent confirmation of the malignancy. Some subjects may have died with occult lung cancer present. Despite these potential limitations, our overall findings of risk factors for lung cancer are consistent with what is known about the epidemiology of lung cancer, suggesting any misclassification did not significantly alter our results.

CONCLUSIONS

In this nationally representative cohort of US adults, the presence of moderate or severe obstructive lung disease was independently associated with an increased risk for incident lung cancer during up to 22 years of follow-up. This finding may be useful in better defining populations that could be targeted for efforts to detect early-stage lung cancer.

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Article Information

Corresponding author: David M. Mannino, MD, National Center for Environmental Health, Centers for Disease Control and Prevention, 1600 Clifton Rd, Mail Stop E-17, Atlanta, GA 30333 (e-mail: dmannino@cdc.gov).

Accepted for publication September 16, 2002.

References
1.
Greenlee  RTMurray  TBolden  SWingo  PA Cancer statistics, 2000. CA Cancer J Clin. 2000;507- 33Article
2.
Steenland  KLoomis  DShy  CSimonsen  N Review of occupational lung carcinogens. Am J Ind Med. 1996;29474- 490Article
3.
Skillrud  DMOfford  KPMiller  RD Higher risk of lung cancer in chronic obstructive pulmonary disease: a prospective, matched, controlled study. Ann Intern Med. 1986;105503- 507Article
4.
Tockman  MSAnthonisen  NRWright  ECDonithan  MG Airways obstruction and the risk for lung cancer. Ann Intern Med. 1987;106512- 518Article
5.
Lange  PNyboe  JAppleyard  MJensen  GSchnohr  P Ventilatory function and chronic mucus hypersecretion as predictors of death from lung cancer. Am Rev Respir Dis. 1990;141613- 617Article
6.
American Thoracic Society, Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;152 (5, pt 2) S77- S121
7.
Pauwels  RABuist  ASCalverley  PMJenkins  CRHurd  SS Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) workshop summary. Am J Respir Crit Care Med. 2001;1631256- 1276Article
8.
National Center for Health Statistics, Plan and Operation of the HANES I Augmentation Survey of Adults 25-74 Years, United States, 1974-75.  Washington, DC National Center for Health Statistics1978;
9.
National Center for Health Statistics, Plan and Operation of the Health and Nutrition Examination Survey, United States, 1971-73.  Washington, DC National Center for Health Statistics1973;
10.
Cohen  BBBarbano  HECox  CS  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study: 1982-84. Vital Health Stat 1. 1987;221- 142
11.
Cox  CSMussolino  MERothwell  ST  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study, 1992. Vital Health Stat 1. 1997;351- 231
12.
Cox  CSRothwell  STMadans  JH  et al.  Plan and operation of the NHANES I Epidemiologic Followup Study, 1987. Vital Health Stat 1. 1992;271- 190
13.
Finucane  FFFreid  VMMadans  JH  et al.  Plan and operation of the NHANES I epidemiologic followup study, 1986. Vital Health Stat 1. 1990;251- 154
14.
American Thoracic Society, Lung function testing: selection of reference values and interpretive strategies. Am J Respir Crit Care Med. 1991;1441202- 1218
15.
Not Available, International Classification of Diseases, Ninth Revision, Clinical Modification. 3rd ed. Washington, DC Public Health Service, US Dept of Health and Human Services1989;
16.
Islam  SSSchottenfeld  D Declining FEV1 and chronic productive cough in cigarette smokers: a 25-year prospective study of lung cancer incidence in Tecumseh, Michigan. Cancer Epidemiol Biomarkers Prev. 1994;3289- 298
17.
Van den Eeden  SKFriedman  GD Forced expiratory volume (1 second) and lung cancer incidence and mortality. Epidemiology. 1992;3253- 257Article
18.
Hole  DJWatt  GCDavey-Smith  GHart  CLGillis  CRHawthorne  VM Impaired lung function and mortality risk in men and women: findings from the Renfrew and Paisley prospective population study. BMJ. 1996;313711- 715Article
19.
Mannino  DMGagnon  RCPetty  TLLydick  E Obstructive lung disease and low lung function in adults in the United States: data from the National Health and Nutrition Examination Survey, 1988-1994. Arch Intern Med. 2000;1601683- 1689Article
20.
Mannino  DMEtzel  RAFlanders  WD Do the medical history and physical examination predict low lung function? Arch Intern Med. 1993;1531892- 1897Article
21.
Badgett  RGTanaka  DJHunt  DK  et al.  Can moderate chronic obstructive pulmonary disease be diagnosed by historical and physical findings alone? Am J Med. 1993;94188- 196Article
22.
Ferguson  GTEnright  PLBuist  ASHiggins  MW Office spirometry for lung health assessment in adults: a consensus statement from the National Lung Health Education Program. Chest. 2000;1171146- 1161Article
23.
Burns  DMShanks  TGChoi  W The American Cancer Society Cancer Prevention Study 1: 12-Year Follow-up of 1 Million Men and Women: Changes in Cigarette-Related Disease: Risk and Their Implications for Prevention and Control.  Washington, DC US Dept Health and Human Services2001;113- 304NIH publication 97-1213.
24.
Tong  LSpitz  MRFueger  JJAmos  CA Lung carcinoma in former smokers. Cancer. 1996;781004- 1010Article
25.
Not Available, US Department of Health and Human Services, Public Health Service, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health. The Health Benefits of Smoking Cessation: A Report of the Surgeon General.  Rockville, Md US Dept of Health and Human Services1990;DHHS publication 90-8416.
26.
Enstrom  JE Smoking cessation and mortality trends among two United States populations. J Clin Epidemiol. 1999;52813- 825Article
27.
Eddy  DM Screening for lung. Ann Intern Med. 1989;111232- 237Article
28.
Manser  RLIrving  LBStone  CByrnes  GAbramson  MCampbell  D Screening for lung cancer [Cochrane Review on CD-ROM].  Oxford, England Cochrane Library, Update Software2003; (issue 1)
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