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(Chest. 2006;129:1305-1312.)
© 2006 American College of Chest Physicians

Prevalence of COPD in Women Compared to Men Around the Time of Diagnosis of Primary Lung Cancer*

Raghu S. Loganathan, MD, FCCP; Diane E. Stover, MD, FCCP; Weiji Shi, MS and Ennapadam Venkatraman, PhD

* From Lincoln Medical and Mental Health Center (Dr. Loganathan), Pomona, NY; and Memorial Sloan-Kettering Cancer Center (Drs. Stover and Venkatraman, and Ms. Shi), New York, NY.

Correspondence to: Raghu S. Loganathan, MD, FCCP, Lincoln Medical and Mental Health Center, Department of Medicine, 234 E 149th St, Bronx, NY 10451; e-mail: raglogan{at}hotmail.com

Abstract

Purpose: COPD is a well-known independent risk factor that is associated with primary lung cancer. There is, however, a striking paucity of women in studies demonstrating this association. The purpose of this study was to compare the prevalence of COPD as determined by pulmonary function tests (PFTs) between women and men at around the time of lung cancer diagnosis.

Methods: We retrospectively reviewed patients with newly diagnosed primary lung cancer who had undergone PFTs prior to their treatment. The diagnosis of airflow obstruction was made according to American Thoracic Society guidelines. Comparisons of the prevalence of COPD between men and women were performed using univariate and multivariate logistic regression analysis.

Results: Of the 294 patients in the study, 151 patients (51.4%) were men and 143 patient (48.6%) were women. Of the men, 110 patients (72.8%) had COPD compared with 75 patients (52.5%) among the women. This represented a significantly lower prevalence of COPD in women than in men (odds ratio [OR], 0.41; 95% confidence interval [CI], 0.25 to 0.67; p = 0.0003). When adjusted for age and smoking status, a sustained lower prevalence of COPD was noted in women compared to men (OR, 0.44; 95% CI, 0.26 to 0.74; p = 0.002). In a subset of 256 smokers, there remained a lower prevalence of COPD in women compared to men (OR, 0.45; 95% CI, 0.27 to 0.77; p = 0.003). Adjusted analysis to control for age and number of pack-years of smoking in this subset again showed a sustained reduction in the OR for women presenting with COPD (OR, 0.48; 95% CI, 0.28 to 0.83; p = 0.009).

Conclusions: When COPD was examined as an end point among patients who had newly diagnosed lung cancer, a significantly higher proportion of women had normal PFT results. Gender-based differences on PFT results should be considered during the screening of lung cancer, because the stratification of high-risk patients based on the presence of COPD may miss a significant proportion of women with lung cancer.

Key Words: airways obstruction • COPD • lung cancer • pulmonary function tests • gender • women

Over the past decade, there has been an exponential rise in the incidence of and death rates due to lung cancer in women. Mortality trends between 1990 and 1998 show a 1.1% annual increase in death rates among women compared to a 1.8% annual decline in men during the same period.1 Among women, lung cancer surpassed breast cancer as the leading cause of cancer death in 1987, and in 2003 lung cancer accounted for 25% of all cancer deaths among women. The rise in death rates in women due to lung cancer exceeds that expected from a slower decline in smoking rates among women compared to men. This growing epidemic has generated enormous interest in studies23456 related to the pathobiology and risk factors related to lung cancer in women.

The close association between lung cancer and diseases characterized by airflow obstruction such as COPD is well-recognized.78910 Although a large body of evidence exists on this association, most studies have been based mainly on men. This has been attributed to the historically high smoking rates in men. A review of these studies also reveals that the presence of COPD in study participants was seen inconsistently. A diagnosis of COPD was included from either the clinical history alone (ie, a questionnaire based on the presence of chronic sputum production) or from variable spirometric criteria on pulmonary function tests (PFTs) that did not conform to the revised standard guidelines.1112

This investigation was motivated by the paucity of women in prior studies that have evaluated COPD as an independent risk factor for lung cancer. A retrospective study was performed to compare the prevalence of COPD from PFT results in a population of men and women from around the time of the diagnosis of primary lung cancer.

Materials and Methods

All patients in whom primary lung cancer was diagnosed at Memorial Sloan-Kettering Cancer Center (MSKCC) between March 1995 and January 1997 and who had undergone PFTs prior to their treatment were included in the study. The interpretation of the PFT results was based on the guidelines of the American Thoracic Society (ATS).11 Patients were considered to have COPD when the FEV1/FVC ratio was < 70%.

When PFTs were performed at MSKCC, measurements were made from spirometry (GS Pulmonary Module spirometer; Collins Medical; Braintree, MA). FEV1 and FVC were recorded for at least three FVC maneuvers using flow-volume loops. The best FEV1 and FVC test results were used for analysis, after conversion to percentages of predicted normal values by using the formulas of Crapo and coworkers.13 Estimation of lung volumes was done by helium dilution method.13

Patient demographics, clinical history, and smoking history were obtained from computerized medical records maintained by pulmonologists, thoracic surgeons, and oncologists at our institution. Based on their smoking status, patients were grouped as current smokers, former smokers, or nonsmokers. Histologic or cytologic proof of primary lung cancer for all patients was confirmed at our institution. Histology was categorized as non-small cell lung cancer (NSCLC) and small cell lung cancer (SCLC). NSCLC was further classified into adenocarcinoma, bronchoalveolar carcinoma (BAC), squamous cell carcinoma, large cell carcinoma, and other types of cancer (ie, poorly differentiated, undifferentiated carcinoma and carcinoid tumors). The pathologic stage of lung cancer at the time of presentation was classified according to revised standard guidelines.14 NSCLC was grouped as stage I, stage II, stage IIIa (all surgically resectable), stage IIIb, and stage IV (surgically unresectable). SCLC was staged as "limited" and "extensive" according to standard guidelines. The MSKCC institutional review board reviewed the study and deemed it exempt from its oversight and the requirement for patient consent.

Statistical Analysis
A comparison of the distributions of patient and clinical characteristics between men and women was performed using t tests, {chi}2 test, or the Fisher exact test. The relationship between the presence of COPD around the time of diagnosis of lung cancer and potential prognostic factors such as age, gender, smoking status, tumor histology, and pathologic stage at presentation was assessed using univariate and multivariate logistic regression. All variables for which the univariate test results yielded p values of ≤ 0.1 were included in the multivariate model. Since smoking is a risk factor that is common to both COPD and lung cancer, similar analyses, including the number of pack-years smoked, were performed in the subset of smokers. Logarithmic transformation (to base 2) was applied to the number of pack-years of smoking to normalize the data. All test results with a p value of < 0.05 were considered to indicate significance. A statistical software package (SAS, release 8.2; SAS Institute; Cary, NC) was used for all analyses.

Results

During the study period, primary lung cancer was diagnosed in 436 patients. Of these, 294 patients (67%) had undergone PFTs prior to receiving treatment and were included in the study. The median time from the date of the PFTs to the diagnosis of lung cancer in the study was 0.1 month (range, –3.8 to 10.7 months). In 78%, 18%, 3%, and 1% of patients, respectively, PFTs were performed 1 month, 1 to 3 months, 3 to 6 months, and > 6 months from the date of lung cancer diagnosis. There was no difference in the time interval from the date of PFTs to the date of the diagnosis of lung cancer between women and men (p = 0.89 [Wilcoxon rank sum test]). Figure 1 shows the distribution of the FEV1 percent predicted among men and women in the study population.


Figure 1
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  		Figure 1. Distributions of FEV1 (percent predicted) by gender. Black bars = women; gray bars = men.

 
Patient demographics and clinical characteristics in the study population are shown in Table 1. Of the 294 patients in the study, 151 (51.4%) were men and 143 (48.6%) were women. Smoking history was available in 275 of the 294 patients (93.5%), and was unavailable for 8 men (5.3%) and 11 women (7.7%). The only statistical difference between men and women when considering age and smoking status was that more men were smokers compared to women (p = 0.002 [smokers vs nonsmokers]).


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  		Table 1. Characteristics of the Study Population According to Gender*

 
Although there was an almost identical proportion of women (95.1%) and men (95.4%) in whom NSCLC (men, 95.4%; women, 95.1%) and SCLC (men, 4.6%; women, 4.9%) was diagnosed, there was a small number of patients with SCLC in our entire study cohort (n = 14; 4.7%). This may be due to the fact that patients with SCLC were less likely to undergo PFTs at the time of their initial presentation. There were no significant differences in the distribution of histology between men and women (p = 0.13), but a higher proportion of men had squamous cell carcinoma (men, 31.8%; women, 22.4%), while a higher proportion of women had BAC (women, 10.5%; men, 4.0%). The distribution of men and women was similar when patients with NSCLC were analyzed based on resectability of the disease (ie, stage I/ II/ IIIa vs stage IIIb/IV disease). Among men, 60.9% presented with surgically resectable disease and 34.5% presented with unresectable disease. Similar numbers were noted among women, with 63.7% presenting with surgically resectable disease and 31.5% with an unresectable stage at presentation.

Table 2 shows the results from univariate and multivariate logistic regressions for all patients for the presence or absence of COPD (n = 294). Around the time of the diagnosis of lung cancer, 75 of 143 women (52.4%) and 110 of 151 men (72.8%) had COPD. This represented a significantly lower prevalence of COPD among women compared to men (odds ratio [OR], 0.41; 95% confidence interval [CI], 0.25 to 0.67; p = 0.0003). Older age was associated with the occurrence of COPD (OR, 1.33 per 10-year increment; 95% CI, 1.06 to 1.68; p = 0.02). Smoking status was strongly associated with COPD (p = 0.003). Both former smokers (OR, 10.31; 95% CI, 2.88 to 36.91; p = 0.001) and current smokers (OR, 9.52; 95% CI, 2.48 to 36.64; p = 0.02) were about 10 times more likely to have COPD than were nonsmokers. Neither histology nor pathologic stage was associated with the presence of COPD in the study (p = 0.29 and p = 0.64, respectively).


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  		Table 2. Univariate and Multivariate Logistic Regression in All Patients for the Presence and Absence of COPD*

 
In multivariate analysis, age, gender, and smoking status were significantly associated with the presence of COPD. There was a significantly lower prevalence of COPD among women compared to men (OR, 0.44; 95% CI, 0.26 to 0.74; p = 0.002), and this was sustained after adjusting for age and smoking status (Table 2).

As the majority of the study population were smokers (257 of 294 patients; 87%), we performed a similar regression analysis restricted to smokers only (Table 3 ). One smoker for whom the number of pack-years was unavailable was excluded from the analyses. Between male and female smokers, there were no significant differences in the distribution of age (p = 0.57), histology (p = 0.15), and pathologic stage (p = 0.09). Men had significantly more pack-years of cigarette smoking compared to women (Table 3).


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  		Table 3. Univariate and Multivariate Logistic Regression in Smokers for the Presence and Absence of COPD*

 
COPD occurred in 57.3% of female smokers (67 of 117 women) and 74.8% of male smokers (104 of 139 men) around the time of the diagnosis of lung cancer (Table 3). In the univariate analysis, male gender, older age, and increasing number of pack-years of cigarette smoking were significantly associated with COPD. The presence of COPD was significantly lower among women compared to men (OR, 0.45; 95% CI, 0.27 to 0.77; p = 0.003) and was similar to the results based on the overall patient population. Similarly, neither histology nor pathologic stage was significantly associated with the presence of COPD (p = 0.30 and p = 0.48, respectively) in smokers (Table 3).

In multivariate analysis, female smokers continued to demonstrate a significantly lower prevalence of COPD compared to male smokers around the time of the diagnosis of primary lung cancer (OR, 0.48; 95% CI, 0.28 to 0.83; p = 0.009). After controlling for age and gender, as the number of pack-years of smoking doubled, the likelihood of having COPD almost increased by nearly 50% (Table 3). Older age was not a significant prognostic factor for having COPD when adjusted for gender and the number of pack-years of smoking.

Discussion

The results of this study show that at or around the time of lung cancer diagnosis, fewer women were noted to have spirometric evidence of airflow obstruction compared to men. When adjusted for age and smoking history, there remained a significantly lower proportion of women with COPD. These data suggest (although they do not prove) that the prevalence of COPD in lung cancer patients may be different in women compared to men. The findings from this study supplement results from the literature,234516 which highlights the fact that there may be gender-based differences in various risk factors associated with primary neoplastic disease of the lung.

The historical perception that smoking-related illnesses, like COPD and lung cancer, are male diseases is fast diminishing. A review of data from the US Surgeon General1718 and the Centers for Disease Control and Prevention (CDC)1 shows a very disturbing reversal of mortality trends due to COPD, with death rates among women surpassing those in men. There has been a 550% increase in lung cancer mortality among women from 1950 to 1991, and, as a result of the rapid increase in lung cancer, it is now the most common cause of death from cancer in US women.115161718 It is unclear whether these dramatic changes in epidemiologic trends are solely reflective of prior high smoking rates in women in the 1960s and 1970s or whether there are certain innate factors that make women more vulnerable to carcinogenesis.619

Fewer than 20% of people who smoke develop lung cancer, with a similar percentage of smokers reported to develop COPD. However, when patients presenting with lung cancer are considered, > 85% are smokers and up to 75% have COPD according to spirometric criteria.2021 Although cigarette smoking is a common etiologic factor for both COPD and lung cancer, it is an established fact that airflow obstruction, measured by simple spirometry, is an independent risk factor for the development of lung cancer. Some studies791022 have reported an increased risk of four to six times that of patients without airflow obstruction. The exact mechanism of the impact of COPD on the development of lung cancer is unknown.2324

Although COPD is a known risk factor for the development of lung cancer, its prevalence among lung cancer patients is not well-characterized. We conducted a systematic literature search of the PubMed database to identify relevant studies published between 1965 and 2003 that examined the relationship between COPD and lung cancer. Applying the Boolean logic system, we found 214 studies using the terms "COPD or chronic bronchitis" and "risk of lung cancer." We manually scanned the articles for their relevance and also searched the references of the retrieved articles that demonstrated this relationship after controlling for smoking status. After excluding non-English language studies, we found 17 studies that demonstrated a relationship between COPD and lung cancer (Table 4 ). Most of these studies were several decades old and reflect the higher smoking rates that were prevalent in men the 1960s. However, they no longer reflect the current epidemiologic trends noted among women with lung cancer. The studies also show considerable variation in the prevalence rates of COPD in cancer patients, and this is probably due to the marked variation in the methods and definitions used to measure disease. Studies performed in the early 1960s used clinical symptoms alone to reach prevalence estimates of COPD. Symptoms either were self-reported or were based on physician assessment, and were subject not only to recall bias but also were physiologically inaccurate.25 Among the 17 studies that demonstrated a relationship between COPD and lung cancer, only 6 had sufficient information to calculate the rates of COPD.102627282930 Figure 2 shows the rates of COPD with 95% CIs for the six studies, compared to our study. The figure again displays the poor representation of women in studies demonstrating the relationship between COPD and lung cancer. Aside from our current investigation, only one other study published in 1966 included women in its analysis.27 Although this study27 has a wide CI, the rates of COPD among patients with lung cancer were lower in women compared to men and were similar to the results noted in our study (Fig 2).


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  		Table 4. Epidemiologic Studies Demonstrating the Association Between COPD and Primary Lung Cancer

 

Figure 2
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  		Figure 2. Prevalence of COPD with 95% CIs among patients in whom lung cancer was diagnosed (comparing prior studies with the current study). Cumulative percentages are not shown because the definitions used to include COPD in these studies were variable.

 
Although subsequent studies31 used a combination of symptoms and spirometry, the diagnosis of COPD was variable because different spirometric criteria were used to define it. Some authors used an absolute reduction in FEV1 percent predicted, while others used FEV1/FVC ratios. The criteria used in the United States were not standardized until the early 1990s, and even then they differed in the cutoff points used to define COPD. Viegi et al25 examined the prevalence of COPD as defined by two different criteria in a cohort of 1,727 patients and found that the European Respiratory Society criteria detected lower prevalence rates compared to ATS criteria. The prevalence of COPD in a given population thus depends very much of the criteria used for the definition of airways obstruction. In this study, we used an FEV1/FVC ratio of < 70% to define COPD on spirometry. The ATS guidelines11 and the more recent Global Initiative for Obstructive Lung disease guidelines12 have suggested this ratio to define the presence of COPD.

The Lung Health Study32 is one of the more recent studies that have demonstrated the association of COPD and lung cancer. The major objective of that study was to trace the course and prognosis of patients with mild-to-moderate stages of COPD and the effect of smoking cessation on the rate of change of ventilatory function. Although the study included a large number of women (37%), it was not designed to provide actual prevalence rates of COPD in women or men who develop lung cancer.

More recently, a study by Lam et al33 looked at changes in the bronchial epithelium that were related to sex and smoking status. Spirometry was performed on 401 patients (212 men and 189 women). They found that airflow obstruction (as defined by the ATS criteria) had a stronger association with high-grade preinvasive bronchial lesions in men compared to women. Overall, women had lower smoking intensity (ie, pack-years) and normal lung function compared to men (p = 0.008). With the exception of the above data, there have not been any more recent studies exploring the prevalence of COPD as an end point in a gender-matched population presenting with lung cancer.

Our finding that the prevalence of COPD among lung cancer patients differs across gender has a number of implications. These data provide further evidence that there are gender-based differences among various risk factors associated with the development of lung cancer.2345619 Second, it should be kept in mind that the presence of COPD as a criterion for "high risk" might miss women who are at risk for the development of lung cancer.

The limitations of this study include its retrospective nature, small sample size, and a possible selection criterion bias, since only patients with lung cancer who had undergone spirometry were included in the study. Although 67% of lung cancer patients seen at our hospital during the study period were studied, a selection bias cannot be excluded. The study had few patients with SCLC. However, it is doubtful whether this would have had any effect on our results and conclusions.

Conclusion

Around the time of the lung cancer diagnosis, a significantly lower proportion of women showed evidence of airways obstruction on spirometry compared to men. Based on this information, gender-based differences in spirometry should be considered when constructing strategies for the screening for lung cancer. Future studies should prospectively examine the prevalence of airflow obstruction in a gender-matched population with and without lung cancer. The understanding of gender-based risk factors for lung cancer will better pave the way to innovative screening and preventive approaches for both men and women.

Footnotes

Abbreviations: ATS = American Thoracic Society; BAC = bronchoalveolar carcinoma; CI = confidence interval; MSKCC = Memorial Sloan-Kettering Cancer Center; NSCLC = non-small cell lung cancer; OR = odds ratio; PFT = pulmonary function test; SCLC = small cell lung cancer

Received for publication January 23, 2005. Accepted for publication November 4, 2005.

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Chronic obstructive pulmonary disease may adversely affect prognosis in lung cancer
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