Journal of Clinical Oncology, Vol 24, No 28 (October 1), 2006: pp. 4539-4544
© 2006 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2005.04.4859
Changing Epidemiology of Small-Cell Lung Cancer in the United States Over the Last 30 Years: Analysis of the Surveillance, Epidemiologic, and End Results Database
Ramaswamy Govindan,
Nathan Page,
Daniel Morgensztern,
William Read,
Ryan Tierney,
Anna Vlahiotis,
Edward L. Spitznagel,
Jay Piccirillo
From the Departments of Internal Medicine, Otolaryngology-Head and Neck Surgery, Psychiatry, and Mathematics, Washington University School of Medicine, St Louis, MO; and the University of California-San Diego, San Diego, CA
Address reprint requests to Ramaswamy Govindan, MD, Division of Oncology, Washington University School of Medicine, 4960 Children's Place, Suite 108, St Louis, MO 63110; e-mail: rgovinda{at}im.wustl.edu
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ABSTRACT
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PURPOSE: Small-cell lung cancer (SCLC) is a histologic subtype of lung cancer with a distinct biology and clinical course. It has been observed that the incidence of SCLC has been decreasing over the last several years.
METHODS: We used the Surveillance, Epidemiologic, and End Results (SEER) database to determine the incidence of SCLC over the last 30 years. In addition, we sought to determine sex- and stage-based differences in the incidence and survival of SCLC among a proportion of reported cases of lung cancer over the last 30 years (1973 to 2002). Joinpoint analyses were applied to test the trends in annual percentage change for statistical significance.
RESULTS: The proportion of SCLC (among all lung cancer histologic types) decreased from 17.26% in 1986 to 12.95% in 2002. Of all patients with SCLC, the proportion of women with SCLC increased from 28% in 1973% to 50% in 2002. A modest but statistically significant improvement in 2- and 5-year survival was noted among both limited-stage SCLC and extensive-stage SCLC cohorts during the study period.
CONCLUSION: Our analysis indicates that the incidence of SCLC is decreasing in the United States, and only modest improvements have been seen in survival over the last 30 years. Possible explanations for the decreasing incidence include the decrease in the percentage of smokers and the change to low-tar filter cigarettes. Despite trends toward modest improvement in survival, the outcome remains very poor.
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INTRODUCTION
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Small-cell lung cancer (SCLC) is distinct from the more common non–small-cell lung cancer by its rapid doubling time, high growth fraction, early development of widespread metastases, and dramatic initial response to chemotherapy and radiation.1 However, despite high initial responses to therapy, most patients die from recurrent disease.2
The distribution of histologic lung cancer subtypes has been changing over the last few decades. Although squamous cell carcinoma (SCC) and SCLC were the most frequent histologic subtypes of lung cancer in the initial period of the smoking-related cancer epidemic, more recent studies have consistently reported the predominance of adenocarcinoma, which is now recognized as the most common histologic type of lung cancer.3-7
The American Cancer Society estimated that SCLC represented 25% of the 170,000 new cases of lung cancer in the United States in 1993.8 Recent studies however have shown a decrease in the total number of lung cancer cases, particularly in men with SCLC and SCC.9,10 We analyzed the Surveillance, Epidemiologic, and End Results (SEER) program of the National Cancer Institute (Bethesda, MD) to determine the changes in incidence, proportion of SCLC among new cases of lung cancer, and survival rates for patients with SCLC during the period from 1973 to 2002.
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METHODS
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Database
We used the SEER Cancer Incidence Public Use Database 1973 to 2002 that was submitted in November 2004 and issued in April 2005 (http://seer.cancer.gov). SEER cancer registries collect data from 13 geographic samples: the states of Connecticut, Iowa, New Mexico, Utah, and Hawaii, and the metropolitan areas of Detroit, MI; Atlanta, GA; San Francisco, CA; Seattle, WA; San Jose, CA; and Los Angeles, CA; plus 10 counties in rural Georgia and a sample of Alaskan natives. Together these 13 groups represent approximately 14% of the total US population. Data from nine of these registries were used. Lung tumors (site codes, C34.0-C34.9) were extracted from the SEER database for the years 1973 through 2002. Histologic codes 8041 to 8045 were designated as SCLC. The ICD-O-3 histology code for non–small-cell carcinoma (8046) is distinct. The SEER database uses its own staging system, local, regional, and distant, to describe the extent of tumor. In the SEER database system, local and regional disease describes limited-stage SCLC and distant disease indicates extensive-stage SCLC. Approximately 10% of SCLC patients each year are not staged.
Data Analysis
We used the SAS system for Windows version 8.02 (SAS Institute, Cary, NC) to analyze the data for the following: (1) incidence of SCLC each year as a percentage of all reported lung cancer; (2) incidence of SCLC as a percentage of all reported lung cancers for each sex; (3) incidence of limited-stage and extensive-stage SCLC each year as a percentage of all reported lung cancers; and (4) all-cause survival rates over time for limited- and extensive-stage SCLC. Joinpoint regression analyses were used to identify significant changes and trends in the data. This method uses a statistical algorithm to define a best-fitting regression line through incidence data across time, determining how many, if any, joinpoints should be used to determine where significant changes take place. In the final models, the most significant numbers of joinpoints are used, and an annual percentage change is calculated for each slope. Joinpoint trends were calculated using age-adjusted rates weighted by the proportion of persons in corresponding age groups of a standard million population (2000 US standard population). We used Joinpoint Software version 3.0 (distributed by the Statistical Applications and Research Branch of the National Cancer Institute, Bethesda, MD; http://srab/cancer.giv/joinpoint/) to calculate annual percentage change and to analyze these trends for statistical significance.
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RESULTS
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Incidence
Table 1 outlines the characteristics of patients with small-cell lung cancer as identified in the SEER data set from 1973-2002. The percentage of SCLC among all cases of lung cancer rose to a peak of 17.26% in 1986 in our analysis (Fig 1). As of 2002, SCLC comprised only 12.95% of all lung cancers. Joinpoint regression analyses confirm these changes. Figure 2 reveals that the absolute incidence of SCLC increased at an annual rate of 6.5% until 1982 (P < .0001). It increased modestly between 1982 and 1989 at an annual percentage change rate of 1.2% that was not statistically significant. Since then, the incidence of SCLC has decreased at a statistically significant annual rate of 2.4%. This downward trend is statistically significant (P < .0001), suggesting that this decrease is a real trend rather than random fluctuation.
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Fig 2. Joinpoint regression of diagnosis of small-cell lung cancer, by year. (*) P  .05. APC, annual percentage change.
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Sex and Stage
Figure 3 shows that the initial strong male predominance among SCLC patients in 1973 (72.37% of all patients with SCLC) has steadily decreased over the subsequent 20 years. In 2002, the male-to-female ratio of patients with SCLC was 1 to 1. In addition, we analyzed the incidence of all lung cancers represented by SCLC, stratified by sex. The average annual age-adjusted incidence rate of SCLC during the early decades of the monitoring period was higher among men, compared with women. Figures 1 and 3 illustrate the changes in the proportion of women with SCLC from 1973 to 2002. Joinpoint analyses confirm that these changes are statistically significant (Fig 4).
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Fig 4. Joinpoint analyses of the distribution of sex in the diagnosis of small-cell lung cancer over 30 years. (*) P .05. APC, annual percentage change.
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The percentages of SCLC represented by limited- and extensive-stage subtypes in relation to each other have not changed significantly during the last 30 years, although the absolute numbers do appear to increase (Fig 5). The increase in overall percentages is a reflection of the increased number of patients who were staged in 2002 compared with in 1973. In 1973, 32.5% of SCLC patients had limited-stage disease, 49.5% of patients had extensive-stage disease, and 17.9% of patients were unstaged. In 2002, a similar pattern emerged: 39.6% of patients were staged with limited-stage disease and 56.6% of patients were staged with extensive-stage disease, and only 3.8% of patients were left unstaged. Joinpoint analyses of the changes in distribution of stages over time are illustrated in Figure 6.
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Fig 6. Joinpoint analyses of the distribution of stage in the diagnosis of small-cell lung cancer over 30 years. (*) P .05. APC, annual percentage change.
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Survival
Figure 7 depicts the 2-year all-cause survival of patients with extensive-stage (ES) SCLC. Although there are fluctuations from year to year, there is an overall trend toward increased survival. In 1973, 1.5% of all patients with ES-SCLC survived 2 years. This number increased to 4.6% by 2000. Joinpoint analyses confirm this trend of a subtle but steady increase in the 2-year survival rate for these patients; the 2-year survival rate for all patients with ES-SCLC increased at an annual percentage change of 2.96% (P < .0001) throughout the monitoring period (Fig 8). Stratification by sex revealed that 2-year survival among men with ES-SCLC increased at an annual rate of 3.45% (P < .0001) and 2-year survival rates among similar women increased by 1.74% annually (P = .015; Fig 9). In each year represented, the 2-year survival rate among women with ES-SCLC is greater than that of men. Survival rates among women in this cohort increased from 1.96% in 1973 to 5.94% in 2000. The 2-year survival rate among men with ES-SCLC increased from 1.32% in 1973 to 3.57% in 2000.
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Fig 8. Joinpoint regression of all-cause 2-year survival trends in extensive-stage small-cell lung cancer. (*) P .05. APC, annual percentage change.
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Fig 9. Joinpoint regression of the distribution of sex in all-cause 2-year survival trends in extensive-stage small-cell lung cancer. (*) P .05. APC, annual percentage change.
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Figure 10 illustrates the 5-year all-cause survival data of patients with limited stage (LS) SCLC. The 5-year survival rate for patients with limited-stage disease increased from 4.9% in 1973 to 10% in 1998. The survival rates for men in this cohort increased from 3.95% in 1973 to 7.51% in 1997 (the last year for which 5-year survival data was available). The survival rate for women with LS-SCLC increased from 6.74% in 1973 to 12.25% in 1997. Joinpoint analyses support this trend, and suggest that the relative survival for patients with LS-SCLC increased moderately throughout the study period (annual percentage change, 2.62%; P < .0001; Fig 11). For men, an initial decline in survival (19.31%; P = .57) was followed by a statistically significant increase in survival with an annual percent change of 3.34% (P < .0001). The female patient model was not fit with any joinpoints, and the annual percentage change across the range of study was not statistically significant (0.3%; P = .225; Fig 12).
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Fig 11. Joinpoint regression of all-cause 5-year survival trends in limited-stage small-cell lung cancer. (*) P .05. APC, annual percentage change.
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Fig 12. Joinpoint regression of the distribution of sex in all-cause 5-year survival trends in limited-stage small-cell lung cancer. (*) P .05. APC, annual percentage change.
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DISCUSSION
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Our analysis of the SEER database indicates that the incidence of SCLC has been steadily decreasing in the United States over the last several years. The use of joinpoint regression analyses support that this decrease is a real trend, as opposed to fluctuations within a normal distribution.
The decrease in the incidence of SCLC may be explained by the decreased percentage of smokers and by the change in cigarette composition. It is estimated that there were 55 million smokers (36%) in a US total population of 151.3 million in 1950 and 50.1 million cigarette smokers (20%) among 248.8 million US residents in 1990.11 Although the annual consumption of cigarettes increased from 248.8 billion in 1964 to 511.2 billion in 1981, it declined to 465 billion in 1998.11 In addition, the yearly consumption of cigarettes per adults older than 18 years decreased from 3,800 in 1965 to 2,800 in 1993.12 Cigarette smoking is a very strong risk factor for the development of SCLC. More than 90% of patients with SCLC are current or past smokers and the risk is related to the duration and intensity of the smoking.13 Barbone et al14 reported an increased odds ratio (OR) for the development of SCLC based on the number of cigarettes consumed daily and the age of starting smoking. Furthermore, the OR decreased from 14.5 in current smokers to 10.9 in patients who had quit smoking for fewer than 4 years to 2.2 in patients with more than 25 years of abstinence.14 A case-control series evaluating the characteristics of patients with lung cancer showed that none of the 117 men and only six (2.9%) of the 207 women who never smoked had SCLC.15 A recent meta-analysis evaluating the effects of cigarette smoking on the histologic subtypes of lung cancer showed a stronger association with SCLC and SCC than large cell lung cancer and adenocarcinoma, for both current and former smokers.16 The highest OR, 72.5, was seen in current smokers with SCLC. The OR was higher for current female smokers than for men (79.9 v 20.3).16 Therefore, the decrease in the percentage of smokers may account for the proportionally higher decrease in the incidence of SCLC and SCC, the histologic subtypes more strongly associated with cigarette smoking, and the increase in the proportion of adenocarcinoma, the most common subtype in nonsmokers.
Most of the carcinogens in the tobacco smoke are present in the tar, a complex mixture including several chemicals capable of cancer initiation or promotion. Since 1954, the sales-weighted average tar and nicotine yields of American cigarettes, defined as the yield of tar and nicotine in each cigarette available in the United States weighted by the number of packages of each brand sold annually in the United States, decreased from about 38 mg and 2.7 mg to 12 mg and 0.95 mg, respectively.12 The lower tar emissions have been achieved with the use of efficient filter tips, highly porous cigarette paper, and changes in the composition of the tobacco blend with an increased use of expanded and reconstituted tobacco. Smokers of cigarettes with low-nicotine delivery tend to smoke more intensely, with greater frequency of puff drawing, increased puff volume, and deeper inhalation, in an adaptation to achieve a desired physiologic response to nicotine.11 Furthermore, the size use of filtered cigarettes led to the decrease in the size of aerosols, since filters appear to be less effective in the elimination of smaller particles. Whereas long-term smokers of cigarettes with high nicotine and no filter have the highest deposition of particles in the bifurcation zone of the tracheobronchial tree, the deeper inhalation of smaller particles leads to an increased deposition of smoke particles in the smaller airways and alveoli. This distal distribution is typical of adenocarcinomas but not of SCLC or SCC.17,18 Recent changes in the composition of smoke may also be implicated in the increased incidence of adenocarcinoma. Over the last few decades, there has been a decrease in the amount of benzo(a)pyrene, a surrogate for the carcinogenic polynuclear aromatic hydrocarbon (PAH), and an increase in the amount of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone, a surrogate measure of the total tobacco specific nitrosamines (TSNAs). In several animal models, NKK has induced mainly adenoma and adenocarcinoma.19,20
The narrowing of the sex gap in the incidence of SCLC could be at least partially explained by the increased number of women diagnosed with lung cancer over the last 20 years. This increase in the number of women diagnosed with lung cancer is directly related with the increased prevalence of smoking in this population, which though lags behind prevalence among men, reached the peak of 55% in the cohort of women born between 1935 and 1944.9 The estimated prevalence of smokers in the United States for the year 1997 was 25.7% among men and 20.7% among women.9 Although there has been a significant decline in the incidence of lung cancer in men after peaking in 1984, the incidence in women has only slowed in recent years and appeared to plateau in 1994.9,21 Although smoking has shown to increase the risk of all major histologic subtypes of lung cancer in both men and women, the OR for smokers compared with nonsmokers is highest for SCLC in women.22 Therefore, the increased proportion of women smokers combined with the increased risk among women smokers of developing SCLC perhaps accounts for the narrowing of the sex gap in the incidence of SCLC, particularly in face of decreased smoking with consequently decreased incidence of SCLC in men.
Several studies of patients with SCLC have shown improved survival rates in women compared with men. In a study comparing the survival of women and men treated from 1973 to 1986 at the National Cancer Institute, both the rates of median survival (13 months v 10 months) and of survival beyond 2.5 years (15% v 6%) favored women.23 Similar findings were reported in a large retrospective analysis of five studies conducted by the Cancer and Leukemia Study Group B (CALGB) between 1972 and 1986, in which women had improved response rates and long-term survival.24 A retrospective review by the Southwest Oncology Group (SWOG) reported that the improved survival rates in women was restricted to patients with limited-stage disease.25
In summary, we confirmed the decreased incidence of SCLC over the last 30 years based on the analysis of the SEER database. The proportion represented by SCLC now constitutes only 12.95% of all newly diagnosed lung cancers. Such a decrease could be explained by the decrease in the prevalence of smokers, particularly among men, and by the change of cigarette composition, including decreased tar and nicotine. With the continued increase in the incidence of lung cancer in women, mostly related to cigarette smoking, the number of SCLC cases in women now equals the number seen in men. Improved outcomes for women have been previously suggested by large retrospective studies but the overall improvement in survival for both men and women over the last 30 years is very modest. SCLC is strongly associated with cigarette smoking and consequently it is a highly preventable disease.
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Authors' Disclosures of Potential Conflicts of Interest
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The authors indicated no potential conflicts of interest.
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Author Contributions
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| Conception and design: Ramaswamy Govindan, Jay Piccirillo
Collection and assembly of data: Nathan Page, Ryan Tierney, Anna Vlahiotis
Data analysis and interpretation: Ramaswamy Govindan, Daniel Morgensztern, William Read, Ryan Tierney, Anna Vlahiotis, Edward L. Spitznagel, Jay Piccirillo
Manuscript writing: Ramaswamy Govindan, Daniel Morgensztern, William Read, Anna Vlahiotis, Jay Piccirillo
Final approval of manuscript: Ramaswamy Govindan, Nathan Page, Daniel Morgensztern, William Read, Ryan Tierney, Anna Vlahiotis, Edward L. Spitznagel, Jay Piccirillo
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ACKNOWLEDGMENTS
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We thank the anonymous statistical reviewer for helpful suggestions.
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NOTES
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Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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REFERENCES
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1. Elias AD: Small cell lung cancer: State-of-the-art therapy in 1996. Chest 112:251S-258S, 1997[Abstract/Free Full Text]2. Stupp R, Monnerat C, Turrisi AT 3rd, et al: Small cell lung cancer: State of the art and future perspectives. Lung Cancer 45:105-117, 2004[CrossRef][Medline] 3. Alberg AJ, Samet JM: Epidemiology of lung cancer. Chest 123:21S-49S, 2003[Abstract/Free Full Text] 4. Valaitis J, Warren S, Gamble D: Increasing incidence of adenocarcinoma of the lung. Cancer 47:1042-1046, 1981[CrossRef][Medline] 5. Vincent RG, Pickren JW, Lane WW, et al: The changing histopathology of lung cancer: A review of 1682 cases. Cancer 39:1647-1655, 1977[CrossRef][Medline] 6. Charloux A, Quoix E, Wolkove N, et al: The increasing incidence of lung adenocarcinoma: Reality or artefact? A review of the epidemiology of lung adenocarcinoma. Int J Epidemiol 26:14-23, 1997[Abstract/Free Full Text] 7. Travis WD, Travis LB, Devesa SS: Lung cancer. Cancer 75:191-202, 1995[CrossRef][Medline] 8. Hinson JA Jr, Perry MC: Small cell lung cancer. CA Cancer J Clin 43:216-225, 1993[Abstract/Free Full Text] 9. Wingo PA, Ries LA, Giovino GA, et al: Annual report to the nation on the status of cancer, 1973-1996, with a special section on lung cancer and tobacco smoking. J Natl Cancer Inst 91:675-690, 1999[Abstract/Free Full Text] 10. Janssen-Heijnen ML, Coebergh JW: Trends in incidence and prognosis of the histological subtypes of lung cancer in North America, Australia, New Zealand and Europe. Lung Cancer 31:123-137, 2001[CrossRef][Medline] 11. Hoffmann D, Hoffmann I, El-Bayoumy K: The less harmful cigarette: A controversial issue—A tribute to Ernst L. Wynder. Chem Res Toxicol 14:767-790, 2001[CrossRef][Medline] 12. Wynder EL, Muscat JE: The changing epidemiology of smoking and lung cancer histology. Environ Health Perspect 103:143-148, 1995 (suppl 8) 13. Brownson RC, Chang JC, Davis JR: Gender and histologic type variations in smoking-related risk of lung cancer. Epidemiology (Cambridge, MA) 3:61-64, 1992 14. Barbone F, Bovenzi M, Cavallieri F, et al: Cigarette smoking and histologic type of lung cancer in men. Chest 112:1474-1479, 1997[Abstract/Free Full Text] 15. Muscat JE, Wynder EL: Lung cancer pathology in smokers, ex-smokers and never smokers. Cancer Lett 88:1-5, 1995[CrossRef][Medline] 16. Khuder SA: Effect of cigarette smoking on major histological types of lung cancer: A meta-analysis. Lung Cancer 31:139-148, 2001[CrossRef][Medline] 17. Stellman SD, Muscat JE, Thompson S, et al: Risk of squamous cell carcinoma and adenocarcinoma of the lung in relation to lifetime filter cigarette smoking. Cancer 80:382-388, 1997[CrossRef][Medline] 18. Janssen-Heijnen ML, Coebergh JW: The changing epidemiology of lung cancer in Europe. Lung Cancer 41:245-258, 2003[CrossRef][Medline] 19. Hoffmann D, Brunnemann KD, Prokopczyk B, et al: Tobacco-specific N-nitrosamines and Areca-derived N-nitrosamines: Chemistry, biochemistry, carcinogenicity, and relevance to humans. J Toxicol Environ Health 41:1-52, 1994[Medline] 20. Hoffmann D, Djordjevic MV, Hoffmann I: The changing cigarette. Prev Med 26:427-434, 1997[CrossRef][Medline] 21. Bilello KS, Murin S, Matthay RA: Epidemiology, etiology, and prevention of lung cancer. Clin Chest Med 23:1-25, 2002[CrossRef][Medline] 22. Osann KE, Anton-Culver H, Kurosaki T, et al: Sex differences in lung-cancer risk associated with cigarette smoking. Int J Cancer 54:44-48, 1993[Medline] 23. Johnson BE, Steinberg SM, Phelps R, et al: Female patients with small cell lung cancer live longer than male patients. Am J Med 85:194-196, 1988[Medline] 24. Spiegelman D, Maurer LH, Ware JH, et al: Prognostic factors in small-cell carcinoma of the lung: An analysis of 1,521 patients. J Clin Oncol 7:344-354, 1989[Abstract] 25. Albain KS, Crowley JJ, LeBlanc M, et al: Determinants of improved outcome in small-cell lung cancer: An analysis of the 2,580-patient Southwest Oncology Group data base. J Clin Oncol 8:1563-1574, 1990[Abstract]
Submitted October 4, 2005;
accepted May 16, 2006.
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|
P. Ceppi, S. Novello, A. Cambieri, M. Longo, V. Monica, M. Lo Iacono, M. Giaj-Levra, S. Saviozzi, M. Volante, M. Papotti, et al.
Polymerase {eta} mRNA Expression Predicts Survival of Non-Small Cell Lung Cancer Patients Treated with Platinum-Based Chemotherapy
Clin. Cancer Res.,
February 1, 2009;
15(3):
1039 - 1045.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. J. Slotman, M. E. Mauer, A. Bottomley, C. Faivre-Finn, G. W.P.M. Kramer, E. M. Rankin, M. Snee, M. Hatton, P. E. Postmus, L. Collette, et al.
Prophylactic Cranial Irradiation in Extensive Disease Small-Cell Lung Cancer: Short-Term Health-Related Quality of Life and Patient Reported Symptoms--Results of an International Phase III Randomized Controlled Trial by the EORTC Radiation Oncology and Lung Cancer Groups
J. Clin. Oncol.,
January 1, 2009;
27(1):
78 - 84.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. L. Hann and D. S. Ettinger
The Change in Pattern and Pathology of Small Cell Lung Cancer
ASCO Educational Book,
January 1, 2009;
2009(1):
451 - 454.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Krug and M. C. Pietanza
Emerging Therapies in Small Cell Lung Cancer
ASCO Educational Book,
January 1, 2009;
2009(1):
455 - 460.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Inoue, S. Sugawara, K. Yamazaki, M. Maemondo, T. Suzuki, K. Gomi, S. Takanashi, C. Inoue, M. Inage, H. Yokouchi, et al.
Randomized Phase II Trial Comparing Amrubicin With Topotecan in Patients With Previously Treated Small-Cell Lung Cancer: North Japan Lung Cancer Study Group Trial 0402
J. Clin. Oncol.,
November 20, 2008;
26(33):
5401 - 5406.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. P. Sculier, J. J. Lafitte, A. Efremidis, M. C. Florin, J. Lecomte, M. C. Berchier, M. Richez, T. Berghmans, A. Scherpereel, A. P. Meert, et al.
A phase III randomised study of concomitant induction radiochemotherapy testing two modalities of radiosensitisation by cisplatin (standard versus daily) for limited small-cell lung cancer
Ann. Onc.,
October 1, 2008;
19(10):
1691 - 1697.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Titulaer, P. W. Wirtz, L. N.A. Willems, K. W. van Kralingen, P. A.E. S. Smitt, and J. J.G.M. Verschuuren
Screening for Small-Cell Lung Cancer: A Follow-Up Study of Patients With Lambert-Eaton Myasthenic Syndrome
J. Clin. Oncol.,
September 10, 2008;
26(26):
4276 - 4281.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. E. Stinchcombe and M. A. Socinski
Gefitinib in Advanced Non-Small Cell Lung Cancer: Does It Deserve a Second Chance?
Oncologist,
September 1, 2008;
13(9):
933 - 944.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. D. Peacock and D. N. Watkins
Cancer Stem Cells and the Ontogeny of Lung Cancer
J. Clin. Oncol.,
June 10, 2008;
26(17):
2883 - 2889.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. J. Weiss, L. T. Bemis, E. Nakajima, M. Sugita, D. K. Birks, W. A. Robinson, M. Varella-Garcia, P. A. Bunn Jr, J. Haney, B. A. Helfrich, et al.
EGFR regulation by microRNA in lung cancer: correlation with clinical response and survival to gefitinib and EGFR expression in cell lines
Ann. Onc.,
June 1, 2008;
19(6):
1053 - 1059.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Leyvraz, S. Pampallona, G. Martinelli, F. Ploner, L. Perey, S. Aversa, S. Peters, P. Brunsvig, A. Montes, A. Lange, et al.
A Threefold Dose Intensity Treatment With Ifosfamide, Carboplatin, and Etoposide for Patients With Small Cell Lung Cancer: A Randomized Trial
J Natl Cancer Inst,
April 16, 2008;
100(8):
533 - 541.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Sher, G. K. Dy, and A. A. Adjei
Small Cell Lung Cancer
Mayo Clin. Proc.,
March 1, 2008;
83(3):
355 - 367.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. P. Belani, S. Ramalingam, M. C. Perry, R. V. LaRocca, D. Rinaldi, P. S. Gable, and W. J. Tester
Randomized, Phase III Study of Weekly Paclitaxel in Combination With Carboplatin Versus Standard Every-3-Weeks Administration of Carboplatin and Paclitaxel for Patients With Previously Untreated Advanced Non-Small-Cell Lung Cancer
J. Clin. Oncol.,
January 20, 2008;
26(3):
468 - 473.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. S. Ramalingam, S. E. Dahlberg, C. J. Langer, R. Gray, C. P. Belani, J. R. Brahmer, A. B. Sandler, J. H. Schiller, and D. H. Johnson
Outcomes for Elderly, Advanced-Stage Non Small-Cell Lung Cancer Patients Treated With Bevacizumab in Combination With Carboplatin and Paclitaxel: Analysis of Eastern Cooperative Oncology Group Trial 4599
J. Clin. Oncol.,
January 1, 2008;
26(1):
60 - 65.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. M. Arnold, L. Seymour, M. Smylie, K. Ding, Y. Ung, B. Findlay, C. W. Lee, M. Djurfeldt, M. Whitehead, P. Ellis, et al.
Phase II Study of Vandetanib or Placebo in Small-Cell Lung Cancer Patients After Complete or Partial Response to Induction Chemotherapy With or Without Radiation Therapy: National Cancer Institute of Canada Clinical Trials Group Study BR.20
J. Clin. Oncol.,
September 20, 2007;
25(27):
4278 - 4284.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Socinski and J. A. Bogart
Limited-Stage Small-Cell Lung Cancer: The Current Status of Combined-Modality Therapy
J. Clin. Oncol.,
September 10, 2007;
25(26):
4137 - 4145.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. E. Lally, J. J. Urbanic, A. W. Blackstock, A. A. Miller, and M. C. Perry
Small Cell Lung Cancer: Have We Made Any Progress Over the Last 25 Years?
Oncologist,
September 1, 2007;
12(9):
1096 - 1104.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Slotman, C. Faivre-Finn, G. Kramer, E. Rankin, M. Snee, M. Hatton, P. Postmus, L. Collette, E. Musat, S. Senan, et al.
Prophylactic Cranial Irradiation in Extensive Small-Cell Lung Cancer
N. Engl. J. Med.,
August 16, 2007;
357(7):
664 - 672.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Schairer, M. Hisada, B. E. Chen, L. M. Brown, R. Howard, S. D. Fossa, M. Gail, and L. B. Travis
Comparative Mortality for 621 Second Cancers in 29356 Testicular Cancer Survivors and 12420 Matched First Cancers
J Natl Cancer Inst,
August 15, 2007;
99(16):
1248 - 1256.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. R. Eckardt, J. von Pawel, J.-L. Pujol, Z. Papai, E. Quoix, A. Ardizzoni, R. Poulin, A. J. Preston, G. Dane, and G. Ross
Phase III Study of Oral Compared With Intravenous Topotecan As Second-Line Therapy in Small-Cell Lung Cancer
J. Clin. Oncol.,
May 20, 2007;
25(15):
2086 - 2092.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Garcia and B. I. Rini
Recent Progress in the Management of Advanced Renal Cell Carcinoma
CA Cancer J Clin,
March 1, 2007;
57(2):
112 - 125.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. S. Ettinger and J. Aisner
Changing Face of Small-Cell Lung Cancer: Real and Artifact
J. Clin. Oncol.,
October 1, 2006;
24(28):
4526 - 4527.
[Full Text]
[PDF]
|
|
|
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TOP
ABSTRACT
INTRODUCTION
