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(Chest. 2001;119:1635-1640.)
© 2001 American College of Chest Physicians

Cigarette Smoking and the Risk of Pulmonary Metastasis From Breast Cancer*

Susan Murin, MD, FCCP and John Inciardi, PharmD, MS

* From the University of California-Davis Medical Center.

Correspondence to: Susan Murin, MD, FCCP, 4150 V St, Suite 3400, Sacramento, CA 95817; e-mail: sxmurin{at}ucdavis.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To determine whether there is an association between cigarette smoking and the development of pulmonary metastatic disease among women with breast cancer.

Design: A case-control study.

Setting: The University of California, Davis Medical Center.

Participants: Eighty-seven women patients with unilateral, invasive breast cancer and pulmonary metastatic disease were identified as cases, and each patient was matched with two control patients who did not have pulmonary metastatic disease. Case patients and control patients were matched for year of diagnosis, age at diagnosis, size of primary tumor, and nodal status.

Data analysis: Multivariate analysis using conditional logistic regression was used to determine the odds of smoking among women with pulmonary metastatic disease compared to matched control patients without pulmonary metastatic disease, after correction for potential confounding factors.

Results: Thirty-eight percent of the case patients vs 29% of the control patients were classified as ever-smokers; 24.1% of case patients were actively smoking at the time of breast cancer diagnosis vs 15.3% of the control patients. The unadjusted odds ratio for active smoking was 1.76 for women with pulmonary metastatic disease compared to women without pulmonary metastatic disease (p = 0.06). In the final multivariate model, the odds ratio for active smoking among women with pulmonary metastatic disease was 1.96 (p = 0.06).

Conclusions: There appears to be an association between cigarette smoking and the development of pulmonary metastatic disease among women with breast cancer. This may explain the previously noted higher breast cancer fatality rate among smokers. The relationship between smoking behavior and pulmonary metastasis from breast and other cancers warrants further investigation.

Key Words: breast cancer • metastasis • smoking


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Carcinoma of the breast is the most common cancer and the number two cause of cancer death, overall, among women.1 After definitive treatment of primary breast cancer, the overall rate of disease recurrence is disappointingly high.2 Relapse, in the form of distant metastases, is common, with lung, bone, liver, and brain being the sites most often involved.3 The development of metastases, for this and many other tumors, is almost universally indicative of incurable disease. A number of clinical and pathologic factors, such as tumor size, nodal involvement, and degree of tumor differentiation, are predictors of disease course.4 5 However, much of the apparent heterogeneity in the risk of disease progression, and in the sites of disease progression, remains unexplained.

Smokers have been found to have an increased rate of death from breast cancer in several epidemiologic studies,6 7 although they do not have an increased incidence of the disease.8 9 10 One potential explanation for this is that smoking, through its pulmonary or systemic effects, adversely affects the natural history of breast cancer. Since the lung is a common site of metastasis from breast cancer, and smoking is a cause of numerous changes in the lung that could affect the likelihood of metastatic spread to this organ, it is plausible that smoking might alter the course of breast cancer by increasing the frequency with which breast cancer metastasizes to the lung. Cigarette smoking and breast cancer are both sufficiently common that an effect of smoking on the natural history of breast cancer may have important implications for the health of women. We examined the relationship between cigarette smoking and pulmonary metastatic disease from unilateral, invasive breast cancer in a case-control study.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Identification of Cases and Control Subjects
Cases were identified from hospital discharge records and from the records of the University of California-Davis Tumor Registry. This American College of Surgeons-certified tumor registry has a cancer case reporting rate of 100% and a > 90% rate of case follow-up until death. Cases were defined as women patients with unilateral, invasive breast cancer who had at diagnosis, or had developed during follow-up, radiologic or pathologic evidence of pulmonary metastatic disease (see definition below). Patients with bilateral breast cancer or with a potentially confounding second primary malignancy were excluded. Each case patient was matched with two control patients who were identified by a computer query of the Tumor Registry database. Control patients were defined as women with unilateral, invasive breast cancer who did not have pulmonary metastatic disease, per information contained in the Tumor Registry and confirmed by a detailed review of medical records including radiologic reports. Control patients were matched to each case patient according to age at diagnosis, year of diagnosis, size of the primary tumor, and number of positive lymph nodes, if applicable. The sample size was chosen based on a power analysis that demonstrated that a sample size of 81 patients in each group would be sufficient to detect an odds ratio for smoking of 3 ({alpha} = 0.05; ß = 0.20), assuming 0.2 as the proportion of smokers in the control group. The study was approved by the University of California-Davis Human Subjects Committee, and patient consent for medical records review was not required.

Data Collection
The medical records of case patients and control patients were reviewed, and the data were abstracted by a single trained abstractor. Information on date of diagnosis, age at diagnosis, race, menopausal status, tumor size and histology, tumor hormone receptor status, number of positive lymph nodes, body mass, breast cancer treatment, and smoking status was recorded on a standardized data collection instrument.

Definition of Metastatic Disease
Patients were considered to have pulmonary metastatic disease if their conditions met the following criteria: (1) pleural effusion with cytologic evidence of malignancy; (2) pleural effusion, exudative in character, without alternative explanation and attributed, in the medical record, to metastatic disease; (3) multiple pulmonary nodules on chest radiograph or CT scan, which were interpreted by the clinician and radiologist to be metastatic in etiology, whether or not a biopsy was performed; and (4) a radiographic pattern on plain film or CT scan that was interpreted by the radiologist to be consistent with lymphangitic carcinomatosis. Patients with single-mass lesions of the lung were excluded because of the potential for misidentification of a lung cancer lesion as a metastatic lesion. Other sites of metastatic involvement were identified by a review of all radiologic and pathologic reports in the chart and in the computerized databases of the University of California-Davis Radiology and Pathology Departments. A bone scan, head CT scan, MRI scan, or other scan that was read as consistent with metastatic disease was considered to be evidence of metastasis, even in the absence of pathologic confirmation.

Smoking Status
Information on smoking history was obtained from a review of all potential sources contained in the medical record, including hospital admission histories, clinic notes, and consultations. Patients were classified as ever-smokers or never smokers. Ever-smokers were further classified according to smoking status at the time of diagnosis as active smokers or former smokers.

Statistical Analysis
Univariate analyses were performed using t tests for continuous variables and {chi}2 or Fisher’s Exact Tests for the comparison of proportions. Age was calculated in years. Body mass index was recorded in kilograms per square meter and was regarded as a continuous variable. Tumor size was coded as a categoric variable, with categories of < 2 cm, 2 to 5 cm, and > 5 cm. Positive lymph nodes were considered to be a categoric variable, with categories of 0, 1 to 3, 4 to 10, and > 10 positive nodes. Race was coded as a categoric variable, with categories of white, black, and other. Family history of breast cancer, menopausal status, radiation therapy, chemotherapy, and hormonal therapy (ie, tamoxifen therapy or oophorectomy) were coded as dichotomous variables. The number of pack-years was coded as a categoric variable by dividing the data into quartiles (nonsmokers, 1 to 19 pack-years, 20 to 39 pack-years, and >= 40 pack-years). Multivariate analysis was performed using conditional logistic regression and a forward selection variable selection algorithm (SAS statistical software, version 6; SAS Institute; Cary, NC).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
A total of 87 case patients were identified, and those patients were matched with 174 control patients. Table 1 shows the characteristics of the case and control patients. The mean (± SD) age of the case patients at diagnosis was 48.1 ± 12.5 years, compared with 48.4 ± 12.6 years for the control patients. In multivariable analysis, there were no significant differences between case patients and control patients in racial distribution, distribution of tumor size or nodal status, tumor estrogen receptor status, or percentage of patients undergoing surgery or receiving chemotherapy. The percentage of patients receiving hormonal therapy (23.3%) was significantly lower for case patients than for control patients (42.8%) (p < 0.05). Case patients were significantly more likely than control subjects also to have metastatic disease involving other sites as well as the lung.


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  		Table 1.. Features of Case and Control Groups

 
Seventy case patients had multiple pulmonary nodules as their manifestation of pulmonary metastatic disease, 40 patients had pleural effusions, and 2 patients had lymphangitic carcinomatosis (Table 2 ). The categories were not mutually exclusive, and 31 case patients had more than one manifestation of pulmonary metastatic disease. Both of the case patients with lymphangitic carcinomatosis also had pleural effusions. The number of case patients and control patients with evidence of metastatic involvement of other organs was higher among the case patients than the control patients (72.4% vs 31.0%, respectively). Sixty-one percent of case patients with other metastases had metastatic disease involving a single extrapulmonary organ, and 39% of case patients had involvement of two or more extrapulmonary sites. Bone was the most common site of extrapulmonary metastatic disease, followed by the liver.


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  		Table 2.. Types and Frequency of Pulmonary Metastatic Involvement

 
Thirty-eight percent of the case patients vs 29% of the control patients were classified as ever-smokers; 24.1% of the patients were actively smoking at the time of breast cancer diagnosis vs 15.3% of the control subjects. The unadjusted odds ratio for active cigarette smoking was 1.76 for women with pulmonary metastatic disease compared to women without pulmonary metastatic disease (p = 0.06). After adjusting for the variable use of hormonal therapy between the two groups, the odds ratio for smoking among the women with pulmonary metastatic disease was slightly lower (1.65; p = 0.12). In the final multivariate model (Table 3 ), which included variables for the use of hormonal therapy as well as for the presence of other sites of metastatic disease, the odds ratio for smoking among women with pulmonary metastatic disease was 1.96 (p = 0.06). Forcing tumor size and nodal status into the model resulted in an odds ratio for smoking of 2.26 (p = 0.055).


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  		Table 3.. Conditional Logistic Regression: Risk for Pulmonary Metastases*

 
Information on the smoking "dose" was incomplete in many patient records. An analysis of a dose-response relationship for smoking and pulmonary metastatic disease was not feasible given this limitation.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
This case-control study demonstrated a consistent trend toward a higher likelihood of cigarette smoking among women with unilateral, invasive breast cancer who developed pulmonary metastatic disease compared with women, matched for age, year of diagnosis, and disease stage, who did not develop pulmonary metastases. This study supports the earlier work of Scanlon and colleagues,11 which suggested that cigarette smoking is a risk factor for the development of metastatic pulmonary involvement among women with breast cancer. A link between smoking and pulmonary metastatic disease may explain the higher rate of fatal breast cancer found among smokers in epidemiologic studies.6 7

The susceptibility of an organ to invasion by malignant cells is a dynamic variable. Smoking causes a host of changes in the lung, including increased permeability12 13 and altered local immune function,14 15 16 17 18 and is associated with changes in the incidence and/or natural history of a broad variety of lung diseases.19 Smoking causes mild lung injury, and lung injury from a variety of causes, such as hyperoxia, radiation, and bleomycin exposure, has been shown to increase the likelihood of developing pulmonary metastatic disease in animal models of cancer.20 21 22 23 24 In our study, the association between pulmonary metastatic disease and cigarette smoking was strongest for active smoking. This is not unexpected given that many of the biological effects of smoking that might plausibly affect the susceptibility of the lung to pulmonary metastatic disease, such as changes in permeability or immune function, are transient and reversible.

A weakness of this study was our inability to control for other lifestyle factors that might confound the relationship between smoking and metastatic disease. For example, smokers are known to have less healthful diets and to be less physically active than their nonsmoking counterparts.25 It is possible that smoking is not itself the cause of a change in the natural history of breast cancer but, instead, is associated with an unidentified confounding factor. With the matching of patients and control subjects for tumor size and nodal status, our study design has accounted for any possible difference between smokers and nonsmokers in disease stage at diagnosis, a factor that has been suggested as a possible explanation for the higher rate of fatal breast cancer among smokers.6

In our study population, women who had pulmonary metastatic disease were significantly less likely to have been treated with hormonal therapy (ie, tamoxifen therapy or oophorectomy), which is of demonstrated efficacy in improving breast cancer survival,26 than were women without pulmonary metastatic disease. The association between the failure to receive hormonal therapy and the development of metastatic disease is not surprising. The reasons that some women did not receive such therapy are not clear. It is possible that such therapy was not offered to, or was refused by, women who smoked because of the increased risk of thrombosis associated with both smoking and the use of tamoxifen, but this is purely speculative. The relationship between pulmonary metastatic disease and smoking status persisted after we corrected for hormonal therapy in our multivariable model.

The possibility of ascertainment bias must be considered as a potential contributing factor to the results of this study. Smokers might be more likely to have chest radiographs performed, with an increased chance of detecting pulmonary metastatic disease. While this might lead to an earlier diagnosis of pulmonary metastatic disease, one would not expect it to significantly alter the overall rate of detection of that disease. Chest radiographs are performed frequently in the care of patients with cancer, and pulmonary metastatic disease is frequently symptomatic. One would not expect there to be a significant number of patients for whom there was a sustained failure to diagnose metastatic disease of the lung.

Our study, as well as the prior work of Scanlon et al,11 focused specifically on the association between smoking and pulmonary metastatic disease. It is possible, however, that an effect of smoking on metastatic propensity is not limited to the lung. Smoking has systemic effects that could affect tumor defense mechanisms external to the lung. For example, the number of circulating natural killer cells is reversibly decreased in active smokers.27 28 Smoking also affects platelet function and coagulability,29 30 factors that are believed to play a role in the body’s defense against tumor cells lodged within capillary beds. In addition, oxidant constituents of cigarette smoke affect signal transduction mechanisms involved in the metastatic process.31 Cigarette smoking is associated with an antiestrogenic effect, and smokers undergo menopause at an earlier age,32 which could affect the biological behavior or therapeutic response of hormone-sensitive tumors such as those in breast cancer. The effect of smoking on metastasis to organs other than the lung has not, to our knowledge, been examined. Our patients were significantly more likely than control subjects also to have metastatic disease at sites other than the lung, which is not surprising in view of the natural history of metastatic cancer. Our study design does not allow for conclusions about the temporal pattern of the metastases or about the assessment of the effect of smoking on other organ metastases.

The phenomenon of an adverse impact of cigarette smoking on the course and outcome of cancer may not be limited to breast cancer, in that smoking has been suggested as a predictor of a more lethal course for other cancers as well.33 34 35 36 The relationship between cigarette smoking and cancer outcome deserves further study. A prospective study, with the ability to control for other potentially confounding lifestyle factors, should be performed. If the relationship between smoking and an adverse effect on the natural history of this and/or other cancers is confirmed, we will need to explore whether the effect is remediable by smoking cessation at the time of cancer diagnosis.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
This case-control study suggests a relationship between active cigarette smoking and the development of pulmonary metastatic disease among women with breast cancer. An effect of smoking on the development of metastatic disease from breast cancer provides an intriguing and biologically plausible explanation for the higher rate of fatal breast cancer among smokers. Given that lung injury is known to increase the incidence of pulmonary metastasis, that smoking is known to cause lung injury, and that the inflammatory changes caused by smoking alter the history of a diversity of lung diseases, it is possible that cigarette smoking makes the lung a more fertile environment for the establishment of metastases. However, systemic effects of smoking, rather than localized pulmonary effects, may also play a role in adversely influencing the course of this and other cancers, and confounding by unrecognized smoking-associated factors cannot be excluded. The effect of smoking on the natural history of breast cancer and other nonpulmonary malignancies warrants further investigation.


   Footnotes
 
Supported by the American Cancer Society-University of California-Davis Institutional Research Grant Program.

Received for publication July 17, 2000. Accepted for publication January 5, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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