This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kaufman, E. L. Articles by Neugut, A. I. Search for Related Content PubMed PubMed Citation Articles by Kaufman, E. L. Articles by Neugut, A. I. Related Articles Related Correspondence Social Bookmarking                            What's this?

Effect of Breast Cancer Radiotherapy and Cigarette Smoking on Risk of Second Primary Lung Cancer

Elizabeth L. Kaufman, Judith S. Jacobson, Dawn L. Hershman, Manisha Desai, Alfred I. Neugut

From the Departments of Epidemiology and Biostatistics, Mailman School of Public Health; Department of Medicine and Herbert Irving Comprehensive Cancer Center, College of Physicians and Surgeons, Columbia University; and the Division of Medical Oncology, New York Presbyterian Hospital, New York, NY

Corresponding author: Alfred I. Neugut, MD, PhD, Division of Medical Oncology, Columbia University Medical Center, 722 W 168th St, MSPH 725, New York, NY 10032; e-mail: ain1{at}columbia.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Purpose Prior studies have found that postmastectomy radiotherapy (PMRT) for breast cancer (BC) increases the risk of lung cancer (LC). We explored the joint effects of cigarette smoking and PMRT on LC risk.

Methods We conducted a population-based nested case-control study among women registered in the Connecticut Tumor Registry diagnosed with nonmetastatic BC between January 1, 1965 and December 31, 1989. Patient cases developed a LC 10 years after BC diagnosis. Controls were matched to patient cases on age, year of BC diagnosis, and length of survival. Medical records were reviewed for pathology, BC therapy, and smoking history. We used conditional logistic regression to estimate odds ratios for the independent and joint effects of smoking and PMRT on risk of overall, ipsilateral, and contralateral LC.

Results Among 113 second primary LC patient cases and 364 controls, compared with nonsmoking women who did not receive PMRT, nonsmoking women who received PMRT had no higher risk of LC; adjusted odds ratios were 5.9 (95% CI, 2.7 to 12.8) for ever-smokers who did not receive PMRT and 18.9 (95% CI, 7.9 to 45.4) for ever-smokers who received PMRT. Adjusted odds ratios for the joint effects of smoking and PMRT were 10.5 (95% CI, 2.9 to 37.8) for the contralateral lung and 37.6 (95% CI, 10.2 to 139.0) for the ipsilateral lung. Smoking and PMRT were associated with increased risk for all histologic types of LC.

Conclusion PMRT after a diagnosis of BC sharply increased the risk of second primary LC, especially in the ipsilateral lung, among ever-smokers. Clinicians should consider including smoking history in their discussions with patients about the risks and benefits of PMRT.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
During the last three decades, advances in screening and treatment have resulted in significantly improved survival among breast cancer (BC) patients.^1-5 As a result, the more than two million BC survivors in the United States are at increased risk for a number of health problems, most notably second primary cancers.⁶

For select high-risk subgroups of women who have undergone mastectomy for surgical resection of the tumor, postmastectomy radiation therapy (PMRT) reduces the risk of locoregional recurrence and improves survival.^7-10 Both the American Society of Clinical Oncology and National Comprehensive Cancer Network have issued evidence-based guidelines for PMRT,^11,12 and population-based studies indicate that its use is increasingly prevalent.¹³

However, studies have also suggested that women with BC are at increased risk of developing long-term complications from PMRT, including lymphedema, brachial plexopathy, pneumonitis, and late cardiac complications.¹¹ In addition, radiation increases the risk of second primary cancers.^11,14 Prior studies from our group have shown that secondary lung cancer in BC patients is more frequent in the lung that is ipsilateral to the irradiated breast than in the contralateral lung.¹⁵ The increased risk associated with PMRT generally has a latency period of at least 10 years.^15,16

Smoking is a known risk factor for lung cancer (LC). The carcinogenic effects of radiation on the lung may be synergistic with the carcinogenic effects of cigarette smoking. A small pilot study by our group, based on data from the Connecticut Tumor Registry (CTR), suggested that women who smoked were at a higher risk of PMRT-induced LC than those who did not smoke.¹⁷ However, that study had a small sample size and a poorly matched control group, which may have resulted in bias.

In this study, we evaluated the LC risk associated with PMRT exposure among women with and without a history of cigarette smoking.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
The study was approved by the institutional review boards of Columbia University and the participating hospitals, and the Connecticut Department of Public Health Human Investigations Committee.

Study Population
The CTR, established in 1935, is the oldest population-based tumor registry in the United States.¹⁸ It collects data on all cancer cases diagnosed at all the acute-care hospitals that serve Connecticut’s 3.4 million residents, and captures at least 94% of cancer cases in the state. Since 1973, the CTR has been part of the Surveillance, Epidemiology, and End-Results program (SEER). As of July 2001, when data collection for this study ended, the CTR’s incidence data were updated through 1998.

Patient Cases
Patient cases were women registered in the CTR with a first diagnosis of BC from January 1, 1965, through December 31, 1989, who were diagnosed with LC more than 10 years after the BC diagnosis.

Controls
Controls were women who were newly diagnosed in the CTR with BC after January 1, 1965, and who survived as long as the patient case to whom they were matched without developing another cancer. The controls were matched to the patient cases on age (± 5 years) and year of BC diagnosis (± 1 year), in a ratio up to 4:1.

Data Collection
On the basis of our pilot studies, cigarette smoking information was less commonly available before 1965 (when the Surgeon General’s report on the association between smoking and LC was released) than subsequently; we therefore included patients diagnosed with BC in 1965 or later. We worked with the Rapid Case Ascertainment Shared Resource of the Yale Cancer Center (New Haven, CT) to facilitate the identification of patient cases and controls.

Our study team reviewed and abstracted data from the patient records on site in the participating hospitals; the data to be abstracted included demographics, details regarding BC diagnosis, stage, treatment (chemotherapy/radiation therapy [RT]), medical history, reproductive history, smoking history, and, for patient cases, data on the second primary LC diagnosed more than 10 years after the BC diagnosis, including disease site, hospital of diagnosis, and clinical characteristics of the tumor. The pathology reports for the BC and/or LC were reviewed, when available, in accordance with institutional review board standards.

Cigarette smoking history was obtained from records for periods before LC diagnosis; that is, smoking history taken only in connection with a LC diagnosis was excluded to reduce bias. Information was obtained regarding whether the participant ever smoked cigarettes (never smoked, current smoker, ex-smoker, or smoking history unknown). Where available, quantitative data were obtained, including the number or packs of cigarettes smoked per day, the age at which the participant started/stopped smoking, and whether other tobacco products were used by the participant.

Statistical Methods
Patient cases and controls were compared with respect to demographic factors (age, year of BC diagnosis, race/ethnicity), medical history, lifestyle factors (consumption of alcohol), BC tumor characteristics (stage, laterality, histology), treatment (surgery, RT, chemotherapy), and menstrual history. Covariates were evaluated for inclusion in the logistic regression models.

Conditional logistic regression was used to estimate odds ratios (ORs) and 95% CIs for second primary LC, given RT and smoking exposure, with adjustment for potential confounders.

In analyses of categoric variables, for which a significant number of medical records were missing data, we made decisions regarding the most likely categoric code for that particular variable. Participants missing ethnicity information were coded as white. Those missing oophorectomy and/or menopause-inducing surgery information were coded as not having had the procedure. Among participants whose menstrual status at the time of their BC diagnosis was missing, we coded those younger than 45 years as premenopausal, those 45 to 55 years as perimenopausal, and those older than 55 years as postmenopausal. A substantial proportion of medical records reviewed for our study lacked information about smoking status and alcohol use. We categorized participants whose medical records lacked this information as discrete risk groups.

All covariates that qualified as confounders by causing a change in the smoking exposure regression coefficient of 10% were included in the final multivariate models. Polytomous logistic regression was used to analyze the relative strengths of the association of smoking with subsequent cancer in the ipsilateral lung versus the contralateral lung. We also conducted an unmatched analysis in which the case group included only those with adenocarcinoma of the lung; we compared that group with all of the controls.

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Among participants who met eligibility criteria, 119 developed LC. These patient cases were matched with 380 controls. All but 22 patient cases had had mastectomy; we therefore excluded from the analyses the six patient cases and 16 controls who had lumpectomy.

Table 1 shows the distribution of demographic, clinical, and lifestyle factors between patient cases and controls. At least 95% of both patient cases and controls were non-Hispanic and white. Not surprisingly, nearly 50% of patient cases but only 18% of controls were current smokers. Patient cases were also more likely to drink alcohol and to have a history of nonmalignant lung disease than controls. Patient cases were only slightly more likely than controls to have undergone PMRT, but nearly five times as likely to have both undergone RT and smoked (P < .0001).

In an unmatched logistic regression analysis that compared women who developed adenocarcinoma of the lung with the entire control group, smokers had nearly 15 times the risk of nonsmokers (95% CI, 5.0 to 43.7), whereas PMRT alone was associated with less than a doubling of risk, which was not statistically significant (Table 4).

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

PMRT has been shown to reduce the risk of locoregional recurrence and improve survival in selected high-risk patient subgroups. Two Danish studies have shown a 9% survival benefit for premenopausal women⁹ and postmenopausal women⁸ with high-risk stage II/III BC. However, other studies have not found such clear survival benefits.¹¹ In 2001, the American Society of Clinical Oncology published guidelines on the indications for the use of PMRT along with a review of the evidence, and definitively recommended treatment only for patients with tumors 5 cm in size or four affected lymph nodes.¹¹ Similarly, the National Comprehensive Clinical Network guidelines recommend PMRT for patients with tumors 5 cm in size, with positive margins, or four positive lymph nodes, and consideration of PMRT for patients with one to three positive lymph nodes or close margins.¹² For certain subgroups, the uncertainty of benefit should be weighed against the long-term risks.

Ionizing radiation has long been known to have carcinogenic effects on the lung. Prior studies in atomic bomb survivors have found an elevation in risk for LC more than 10 years after exposure.^19,20 Therapeutic radiation to the thorax, in both Hodgkin’s disease²¹ and ankylosing spondylitis,²² has also been shown to increase the risk of lung cancer.

An increased risk of second primary LC has been observed consistently among women with a prior history of BC. We previously used population-based data from SEER to compare women who received PMRT versus women who did not.¹⁶ For BC patients diagnosed between 1973 and 1986, of whom 13,750 (24.4%) underwent PMRT, the relative risk (RR) for LC associated with PMRT was 2.0 (95% CI, 1.0 to 4.3); this increased risk was limited to patients who had survived more than 10 years after the BC diagnosis. The increased risk in these patients was limited to the lung that was ipsilateral to the BC radiation field. The study did not have data on the patients’ history of cigarette smoking. We subsequently confirmed these findings in a follow-up study using SEER data, and found an elevated risk for LC after PMRT, but not after postlumpectomy RT.¹⁵ Several other studies have confirmed this elevation of LC risk after BC RT.^23-26

None of the above-described studies explored the impact of prior cigarette smoking on secondary LC risk. We first conducted a pilot study to explore the joint effects of cigarette smoking and PMRT on LC risk.¹⁷ This study used the CTR to identify 121 women diagnosed with second primary LC. These women were compared with 143 BC patients who developed other non–tobacco-related second primary cancers during the same time period. Cigarette smoking status was known for 78% of the patient cases and 57% of the controls. The study found a risk of LC among nonsmokers who received PMRT of 3.2 (95% CI, 0.6 to 17.4), whereas cigarette smokers who did not receive PMRT had a risk for LC of 14.0 (95% CI, 4.0 to 53.0), and those who were both smokers and were irradiated had an odds ratio of 33 (95% CI, 6.9 to 154.0), all compared with those who were exposed to neither PMRT nor smoking. The effect of PMRT in that study was also limited to the ipsilateral lung, with little or no increased risk to the contralateral lung, as is shown in the current study. The pilot study was limited by its small sample size, the suboptimal control group, and limited smoking information.

Two other studies are of importance with regard to this issue. Inskip et al²⁷ also used CTR data to look at BC patients who survived 10 or more years after their BC diagnosis, and found that PMRT was associated with an increased risk of LC (RR, 1.8; 95% CI, 0.8 to 3.8) which increased with additional follow-up time and became statistically significant after 15 years (RR, 2.8; 95% CI, 1.0 to 8.2). This study had smoking information on only a small fraction of the participants. In contrast, a recent hospital-based case-control study evaluated 280 LC patient cases with previous BC from M.D. Anderson Cancer Center (Houston, TX) and compared them with 300 randomly selected controls.²⁸ They compared cigarette smoking history at the time of the BC diagnosis (current, former, or never) and information on RT. The investigators reported adjusted ORs of 5.6 (95% CI, 2.9 to 10.5) for smokers compared with nonsmokers, and 8.6 (P = .076) for the combined effect of smoking and RT. They concluded that there was no interactive effect between smoking and RT. However, they did not find an increased risk for RT alone for either smokers or nonsmokers. As we did, the investigators obtained their data from medical records; the use of such data may have led to some degree of misclassification and/or bias. They also included as cases patients whose LC was diagnosed as early as 6 months after the BC diagnosis; such cancers could not have been related to treatment.

The results of the current study should be interpreted in light of certain limitations. Due to the difficulty of accessing older records, our sample was smaller than expected. All of the data were collected from hospital medical records, 24% of which (19% for patient cases and 25% for controls) lacked smoking data; smoking data were least likely to be available for those participants who were diagnosed in the earliest pentad (1965 to 1969). The records also rarely included data on the quantitative aspects of smoking (eg, pack-years). Although cigarette smoking history was usually recorded at the time of or after the LC diagnosis of the patient cases, we did not use that information to classify participants by smoking status because it would have seriously biased our analyses.

The National Health Interview Surveys have tracked smoking prevalence among women in the United States during a time interval that includes the years 1965 to 1989, when our participants were diagnosed with BC. During those years, 58% of women reported never having smoked.²⁹ Among the controls in our study, only 49% were never-smokers, perhaps because Connecticut is an affluent state, in which smoking prevalence may have been relatively high before the Surgeon General’s report in 1965. The BC patients in our sample were more than 95% white, and white women are more likely than Hispanics and Asians and as likely as non-Hispanic black women to have smoked, but also are more likely to have stopped.

Another possible limitation of the study was misclassification of the LC diagnosis; patients with lung metastases from their BC might have been misclassified as having a second primary LC. Because adenocarcinoma is the common histopathology among primary BC, LCs of this histopathologic type would be of particular concern. Indeed, adenocarcinomas made up the largest histologic group of LC cases in our study (38.9%); however, there was no significant difference in smoking history between this group and the other histopathologic types of LC, and subgroup analyses showed that the risk for adenocarcinoma of the lung was comparable to the risk of the other histologic types of LC for those with available smoking data (Table 4).

Our study was not able to evaluate the impact of smoking history after the BC diagnosis. We assume that patients diagnosed with BC who were never-smokers were unlikely to start smoking after diagnosis. If patients who were smokers stopped after the diagnosis, this might serve to bias our results toward the null hypothesis.

Even among patients who did not receive PMRT, smoking-related risks were higher for the ipsilateral than for the contralateral lung, and alcohol-related risks were higher for the contralateral lung. We have no explanation for these observations but hope that future studies will shed light on them.

To our knowledge, this is the first study in a population-based setting to use individual information on radiotherapy and individual information on cigarette smoking status at the time of BC diagnosis. We were unable to obtain detailed information regarding the radiotherapy (eg, portals and dosimetry). To our knowledge, only two prior studies have attempted to investigate the interactions among BC, RT, and cigarette smoking, and both of these studies also had limited details about RT dosing.

In summary, we found that women who received PMRT and had smoked cigarettes had nearly a 40-fold elevated risk of subsequent ipsilateral LC, compared with women who did not receive PMRT and never smoked. Given those findings, BC survivors who are or have been smokers and have received RT may be appropriate candidates for LC screening with spiral computed tomography. Physicians of patients newly diagnosed with BC, especially those for whom the survival benefits of PMRT are marginal, should consider smoking history when discussing treatment options. Research is needed to determine whether or not smoking cessation after RT may reduce its late effects.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Conception and design: Judith S. Jacobson, Alfred I. Neugut

Financial support: Alfred I. Neugut

Collection and assembly of data: Elizabeth L. Kaufman, Judith S. Jacobson, Dawn L. Hershman, Alfred I. Neugut

Data analysis and interpretation: Elizabeth L. Kaufman, Judith S. Jacobson, Dawn L. Hershman, Manisha Desai, Alfred I. Neugut

Manuscript writing: Elizabeth L. Kaufman, Judith S. Jacobson, Dawn L. Hershman, Alfred I. Neugut

Final approval of manuscript: Elizabeth L. Kaufman, Judith S. Jacobson, Dawn L. Hershman, Manisha Desai, Alfred I. Neugut

	ACKNOWLEDGMENTS

 
The authors thank the following Connecticut hospitals, which allowed access to medical records and pathology reports: Bradley Memorial Hospital, Bridgeport Hospital, Bristol Hospital, Charlotte Hungerford Hospital, Danbury Hospital, Day-Kimball Hospital, Greenwich Hospital, Griffin Hospital, Hartford Hospital, Hospital of St Raphael, Johnson Memorial Hospital, Lawrence and Memorial Hospital, Manchester Memorial Hospital, Middlesex Hospital, Milford Hospital, Midstate Medical Center, New Britain General Hospital, Norwalk Hospital, Rockville General Hospital, St Francis Hospital and Medical Center, St Mary’s Hospital, St Vincent’s Medical Center, Stamford Hospital, UConn Health Center, Waterbury Hospital, William W. Backus Hospital, Windham Hospital, and Yale-New Haven Hospital. Certain data used in this study were obtained from the Connecticut Tumor Registry located in the Connecticut Department of Public Health. The authors assume full responsibility for analyses and interpretation of these data.

	NOTES

 
Supported by a supplement to National Cancer Institute (NCI) Grant No. P30 CA13696 and in part by a K07 award from NCI (Grant No. CA95597; to D.L.H.).

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
1. Surveillance, Epidemiology, and End-Results program: SEER, 2004. http://www.seer.cancer.gov

2. Coburn NG, Chung MA, Fulton J, et al: Decreased breast cancer tumor size, stage, and mortality in Rhode Island: An example of a well-screened population. Cancer Control 11:222-230, 2004[Medline]

3. Tamoxifen for early breast cancer: An overview of the randomised trials—Early Breast Cancer Trialists’ Collaborative Group. Lancet 351:1451-1467, 1998[CrossRef][Medline]

4. Polychemotherapy for early breast cancer: An overview of the randomised trials—Early Breast Cancer Trialists’ Collaborative Group. Lancet 352:930-942, 1998[CrossRef][Medline]

5. Punglia RS, Morrow M, Winer EP, et al: Local therapy and survival in breast cancer. N Engl J Med 356:2399-2405, 2007[Free Full Text]

6. Mariotto AB, Rowland JH, Ries LA, et al: Multiple cancer prevalence: A growing challenge in long-term survivorship. Cancer Epidemiol Biomarkers Prev 16:566-571, 2007[Abstract/Free Full Text]

7. Overgaard M: Overview of randomized trials in high risk breast cancer patients treated with adjuvant systemic therapy with or without postmastectomy irradiation. Semin Radiat Oncol 9:292-299, 1999[CrossRef][Medline]

8. Overgaard M, Jensen MB, Overgaard J, et al: Postoperative radiotherapy in high-risk postmenopausal breast-cancer patients given adjuvant tamoxifen: Danish Breast Cancer Cooperative Group DBCG 82c randomised trial. Lancet 353:1641-1648, 1999[CrossRef][Medline]

9. Overgaard M, Hansen PS, Overgaard J, et al: Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy: Danish Breast Cancer Cooperative Group 82b Trial. N Engl J Med 337:949-955, 1997[Abstract/Free Full Text]

10. Poortmans P, Overgaard M, Overgaard J: Postmastectomy radiotherapy should be the standard of care for all women with involved axillary nodes. Radiother Oncol (in press)

11. Recht A, Edge SB, Solin LJ, et al: Postmastectomy radiotherapy: Clinical practice guidelines of the American Society of Clinical Oncology. J Clin Oncol 19:1539-1569, 2001[Abstract/Free Full Text]

12. Punglia R, Hughes M, Edge S: Factors associated with appropriate use of radiation therapy after mastectomy in women with stage I-II breast cancer treated within the National Comprehensive Cancer Network (NCCN). J Clin Oncol 22:527s, 2004 (suppl; abstr 6032)

13. Punglia RS, Weeks JC, Neville BA, et al: Radiation therapy after mastectomy between 1991 and 1999 in elderly women: Response to clinical trial information. J Clin Oncol 24:3474-3482, 2006[Abstract/Free Full Text]

14. Neugut AI, Weinberg MD, Ahsan H, et al: Carcinogenic effects of radiotherapy for breast cancer. Oncology (Huntingt) 13:1245-1256, 1999; discussion 1257, 1261-1265[Medline]

15. Zablotska LB, Neugut AI: Lung carcinoma after radiation therapy in women treated with lumpectomy or mastectomy for primary breast carcinoma. Cancer 97:1404-1411, 2003[CrossRef][Medline]

16. Neugut AI, Robinson E, Lee WC, et al: Lung cancer after radiation therapy for breast cancer. Cancer 71:3054-3057, 1993[CrossRef][Medline]

17. Neugut AI, Murray T, Santos J, et al: Increased risk of lung cancer after breast cancer radiation therapy in cigarette smokers. Cancer 73:1615-1620, 1994[CrossRef][Medline]

18. Connelly RR, Campbell PC, Eisenberg H: Central registry of cancer cases in Connecticut. Public Health Rep 83:386-390, 1968

19. Thompson DE, Mabuchi K, Ron E, et al: Cancer incidence in atomic bomb survivors: Part II. Solid tumors, 1958-1987. Radiat Res 137:S17-S67, 1994[Medline]

20. Pierce DA, Shimizu Y, Preston DL, et al: Studies of the mortality of atomic bomb survivors: Report 12, Part I. Cancer: 1950-1990. Radiat Res 146:1-27, 1996[Medline]

21. van Leeuwen FE, Klokman WJ, Stovall M, et al: Roles of radiotherapy and smoking in lung cancer following Hodgkin’s disease. J Natl Cancer Inst 87:1530-1537, 1995[Abstract/Free Full Text]

22. Weiss HA, Darby SC, Doll R: Cancer mortality following X-ray treatment for ankylosing spondylitis. Int J Cancer 59:327-338, 1994[Medline]

23. Raymond JS, Hogue CJ: Multiple primary tumours in women following breast cancer, 1973-2000. Br J Cancer 94:1745-1750, 2006[Medline]

24. Rutqvist LE, Johansson H: Long-term follow-up of the Stockholm randomized trials of postoperative radiation therapy versus adjuvant chemotherapy among ‘high risk’ pre- and postmenopausal breast cancer patients. Acta Oncol 45:517-527, 2006[CrossRef][Medline]

25. Deutsch M, Land SR, Begovic M, et al: The incidence of lung carcinoma after surgery for breast carcinoma with and without postoperative radiotherapy: Results of National Surgical Adjuvant Breast and Bowel Project (NSABP) clinical trials B-04 and B-06. Cancer 98:1362-1368, 2003[CrossRef][Medline]

26. Fowble B, Hanlon A, Freedman G, et al: Second cancers after conservative surgery and radiation for stages I-II breast cancer: Identifying a subset of women at increased risk. Int J Radiat Oncol Biol Phys 51:679-690, 2001[CrossRef][Medline]

27. Inskip PD, Boice JD Jr: Radiotherapy-induced lung cancer among women who smoke. Cancer 73:1541-1543, 1994[CrossRef][Medline]

28. Ford MB, Sigurdson AJ, Petrulis ES, et al: Effects of smoking and radiotherapy on lung carcinoma in breast carcinoma survivors. Cancer 98:1457-1464, 2003[CrossRef][Medline]

29. Giovino GA: Epidemiology of tobacco use in the United States. Oncogene 21:7326-7340, 2002[CrossRef][Medline]

Submitted June 29, 2007; accepted October 22, 2007.

CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

Related Correspondence

• Risk of Ipsilateral Lung Cancer After Postmastectomy Radiotherapy and Smoking: Does the Possible Triumph Over the Actual?
  Ugo De Giorgi, George H. Perkins, and Massimo Cristofanilli
  JCO 2008 26: 4044-4045 [Full Text]

This article has been cited by other articles:

				A. Berrington de Gonzalez, K. P. Kim, and C. D Berg Low-dose lung computed tomography screening before age 55: estimates of the mortality reduction required to outweigh the radiation-induced cancer risk J Med Screen, September 1, 2008; 15(3): 153 - 158. [Abstract] [Full Text] [PDF]

				U. De Giorgi, G. H. Perkins, and M. Cristofanilli Risk of Ipsilateral Lung Cancer After Postmastectomy Radiotherapy and Smoking: Does the Possible Triumph Over the Actual? J. Clin. Oncol., August 20, 2008; 26(24): 4044 - 4045. [Full Text] [PDF]

				A. I. Neugut, J. S. Jacobson, and D. Hershman In Reply J. Clin. Oncol., August 20, 2008; 26(24): 4045 - 4045. [Full Text] [PDF]

				E J HALL and D J BRENNER Cancer risks from diagnostic radiology Br. J. Radiol., May 1, 2008; 81(965): 362 - 378. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kaufman, E. L. Articles by Neugut, A. I. Search for Related Content PubMed PubMed Citation Articles by Kaufman, E. L. Articles by Neugut, A. I. Related Articles Related Correspondence Social Bookmarking                            What's this?