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Ann Thorac Surg 2004;77:1926-1930
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Evolution of surgical outcomes for nonsmall cell lung cancer: time trends in 1,465 consecutive patients undergoing complete resection

Morihito Okada, MD, PhDa*, Wataru Nishio, MD, PhDa, Toshihiko Sakamoto, MD, PhDa, Kazuya Uchino, MDa, Tsuyoshi Yuki, MDa, Akio Nakagawa, MDa, Noriaki Tsubota, MD, PhDa

a Department of Thoracic Surgery, Hyogo Medical Center for Adults, Akashi City, Hyogo, Japan

Accepted for publication December 10, 2003.

* Address reprint requests to Dr Okada, Department of Thoracic Surgery, Hyogo Medical Center for Adults, Kitaohji-cho 13-70, Akashi City 673-5885, Hyogo, Japan
e-mail: morihito1217jp{at}aol.com


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: Lung cancer is still the most common cause of death due to cancer. Although the 5-year survival rate of patients with lung cancer is reported to be increasing, whether the surgical results have actually been improving or not is controversial. We reviewed our experience to evaluate time trends of surgical outcomes in patients with nonsmall cell lung cancer.

METHODS: We reviewed the clinical records of 1,465 consecutive patients with proven primary nonsmall cell carcinoma who underwent complete removal of the primary tumor together with hilar and mediastinal lymph nodes from 1985 to 1995 (early era) and from 1996 to 2002 (late era). The clinical characteristics, surgical outcome, and overall survival of the patients were analyzed, and data from the two eras were compared.

RESULTS: There were 694 patients in the early era and 771 in the late era. As for their characteristics, elder age, female sex, adenocarcinoma, earlier stage of disease and smaller size of tumor were more frequently encountered in the late era. Lobectomy was the most common procedure performed during both periods, and in the late era, the rate of segmentectomy was doubled (11% to 25%) whereas that of pneumonectomy was much less (6% to 1%). Although the frequency of operative deaths in the two eras did not differ (0.3%), that of in-hospital deaths and of postoperative complications decreased significantly in the late era (2% to 0.5% and 28% to 12%, respectively). A significant improvement in survival probability was observed in patients with pathologic stage IA (p < 0.0001), IB (p = 0.0477), and III disease (p = 0.00120) but not in those with pathologic stage II disease (p = 0.5353). Also, the multivariate analysis of patients with pathologic stage I or III demonstrated that age, sex, and size of the tumor were significant prognostic determinants, and confirmed that the recent prolonged survivals remained significant even after simultaneous adjustment for other factors.

CONCLUSIONS: These data indicate a significant recent improvement in surgical outcomes after stratification of various prognostic variables although careful consideration should be given to the retrospective nature of this study.


   Introduction
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 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Recent progress in the therapy for cancer is one of the best examples of the successful evolution of clinical medicine. Cancer has been the leading cause of death since 1981 in Japan, where the average life expectancy is one of the highest in the world. Likewise, in the United States, it is estimated that 1,334,100 new cases of cancer will be diagnosed and 556,500 people will die of cancer in 2003 [1]. In the United States, lung cancer continues to be the most common cause of cancer death in both men and women; the 5-year survival has significantly increased from 12% in the 1970s to 15% in the 1990s, while the estimated number of deaths from lung cancer remains relatively stable at 157,200 patients per year [1].

Among patients with primary lung cancer, approximately 80% have nonsmall cell lung cancer. Although pulmonary resection is the most effective treatment of choice whenever possible for patients with nonsmall cell lung cancer who are presumed to have no disseminated disease, the assessment of surgical results is still hampered by insufficient follow-up and the small number of patients studied. The actual impact of advances in surgical treatment on the outcome of patients with nonsmall cell lung cancer is of great interest to us but it remains unclear. There have been few reports on time trends in surgical outcomes for nonsmall cell lung cancer [2]. Even meta-analyses based on reports from many institutions or literatures have seldom been published. The limitation of such analyses is that pooled data collected from multiple institutions over many years lack uniformity with regard to diagnosis and treatment, and in reporting outcomes. Therefore, we reviewed our data on surgical treatment provided by a single team to evaluate the changes with the times regarding the survival of patients with nonsmall cell lung cancer.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Between January 1985 and December 2002, 1,465 consecutive patients with proven primary nonsmall cell lung carcinoma underwent complete removal of the tumor together with ipsilateral hilar and mediastinal lymph nodes. Patients who had evidence of residual tumor at the surgical margin, malignant effusion, or N3 disease verified by intraoperative findings or postoperative pathologic examination, were defined as having undergone incomplete surgery and were excluded from this study. Patients whose tumors were subsequently classified as small cell carcinoma or low-grade malignant tumor were also excluded. The criteria, based on and modified from those of Martini and Melamed [3] have been used for the designation of multiple primary lung cancers [4]. Tumors with minute satellite nodules that were found incidentally within the same lobe of the resected specimen were not excluded from this study, because we were not certain whether these lesions should be considered local tumor spread or not. Tumors with satellite lesions in another lobe were excluded. One hundred sixty-four patients who received induction chemoradiotherapy were included.

Surgical-pathologic staging was carried out according to the New International Staging System for Lung Cancer [5]. Routine systematic dissection of all the hilar and mediastinal lymph nodes was performed in every case, even if the preoperative evaluation was N0 or N1 [6]. Every node dissected was examined by more than one pathologist to be diagnosed as microscopically positive or negative during and after the operation. In general, the patients were examined after surgery at 3-month intervals for 5 years and thereafter at 1-year intervals. The evaluation included physical examination, chest roentgenography, and tumor markers. Moreover, chest, abdominal and brain computed tomographic (CT) scans and a bone scinti scan were carried out each year. Whenever any symptoms or signs of recurrence were detected, further examinations to detect the disease were performed. Minor complications as well as major ones were taken into account for the analyses of data in this study.

In this study we evaluated our institutional experience in the surgical treatment of nonsmall lung cancer from 1985 to 1995 (early era) and from 1996 to 2002 (late era). These historical periods selected were determined as the number of patients surgically treated was roughly equal on the two groups. The clinicopathologic characteristics, surgical outcomes, and overall survival of the patients were analyzed, and data from the two eras were compared.

The survival probabilities were calculated by the Kaplan-Meier method, and differences in survival were determined by the log-rank analysis. A multivariable analysis of several independent prognostic factors was carried out using Cox's proportional hazards regression model. Zero time was the date of surgery, and the terminal event was death attributable to cancer, noncancer or unknown causes. Patients with operative or in-hospital mortality, defined as death occurring within 30 days after the operation or during hospitalization, respectively, were included in this study. Factors potentially influencing the prognosis for a proportion of the patients' population were analyzed by the Mann-Whitney U test. A value of p less than 0.05 was considered to indicate statistical significance, and all resulting p values were two-tailed.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
There were 694 patients in the early era and 771 in the late era. Median follow-up periods for the early and late eras (for patients still alive) were 103 and 41 months, respectively. The clinicopathologic characteristics, types of procedure, and surgical outcomes are presented in Table 1. Elder age, female sex, adenocarcinoma, earlier stage of disease and smaller size of the tumor were encountered more frequently in the late era. On the basis of the international staging system, there was a remarkable increase in the number of patients with stage IA disease in the late era (42%) compared with the early era (31%). Lobectomy was by far the most common procedure performed during both periods, and the frequency of segmentectomy was doubled in the late era (11% to 25%). Because we always kept in mind the possibility of lung-saving procedures [7, 8], the ratio of broncoplasties was relatively high (12% to 13%) through both periods while that of pneumonectomies was much less in the late era (6% to 1%). Although the frequency of operative deaths in the two eras did not differ (0.3%), that of in-hospital deaths and of postoperative complications decreased significantly in the late era (2% to 0.5% and 28% to 12%, respectively).


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  		Table 1. Clinicopathologic Characteristics

 
Next, we analyzed overall survival probability in all patients according to pathologic stages (Fig 1). There were marked differences between stage I versus stage II and between stage II versus stage III (p < 0.0001). Survivals by age, sex, size of the tumor, histologic type, surgical procedure, pathologic stage, and era were summarized (Table 2). Statistical differences were found in the probability of survival in favor of the late era as well as younger, female, smaller tumor, adenocarcinoma, lesser resection, and early stage. In the late era, there were significant increases in the probability of survival of patients with pathologic stage IA disease (89.6% versus 70.9% at 5 years, p < 0.0001; Fig 2) as well as in that of patients with pathologic stage IB disease (74.9% versus 62.8% at 5 years, p = 0.0477; Fig 3). However, no significant difference was found in the survival of patients with pathologic stage II disease between the two eras (p = 0.5353; Fig 4). The survival of patients with pathologic stage III disease was 44.3% at 5 years in the late era and significantly better than that of patients in the early era (26.2% at 5 years, p = 0.0120; Fig 5). Thus, the improvement in overall survival probability was observed in patients with pathologic stage I or III disease.



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  		Fig 1. Survival of patients who underwent complete resection for nonsmall cell lung cancer by pathologic stage. Significant differences in survival among pathologic stages were found (pathologic stage I versus II, and II versus III; p < 0.0001).

 

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  		Table 2. Univariate Analysis of Prognostic Factors

 


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  		Fig 2. Survival of patients who underwent complete resection for pathologic stage IA nonsmall cell lung cancer. The survival in the late era (1996 to 2002) was significantly higher than that in the early era (1985 to 1995; p < 0.0001).

 


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  		Fig 3. Survival of patients who underwent complete resection for pathologic stage IB nonsmall cell lung cancer. The survival in the late era (1996 to 2002) was significantly higher than that in the early era (1985 to 1995; p = 0.0477).

 


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  		Fig 4. Survival of patients who underwent complete resection for pathologic stage II nonsmall cell lung cancer. There was no significant difference in the survival between the early (1985 to 1995) and the late era (1996 to 2002; p = 0.5353).

 


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  		Fig 5. Survival of patients who underwent complete resection for pathologic stage III nonsmall cell lung cancer. The survival in the late era (1996 to 2002) was significantly higher than that in the early era (1985 to 1995) (p = 0.0120).

 
Finally, we performed Cox proportional hazards regression analysis not only to determine independent prognostic variables but also to remove any bias as much as possible because of the retrospective nature of the study. The results of multivariate analyses were same as those of univariate analyses except for surgical mode (Table 3). Interestingly, after stratified by various possible variables, no difference was found in survival between standard and lesser resections. The analysis of patients with pathologic stage I (n = 859) or stage III (n = 336) demonstrated that age, sex, and size of the tumor were the factors with stronger influence on the postoperative prognosis, and confirmed that the improvement in survival in the late era remained significant even after simultaneous adjustment for age, sex, size, and histology of the tumor (Table 4). It is interesting to note that in terms of histology adenocarcinoma was a significantly independent worse determinant among patients with pathologic stage III disease although it was associated with a relatively better prognostic tendency in patients with pathologic stage I disease.


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  		Table 3. Multivariate Analysis of Prognostic Factors

 

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  		Table 4. Multivariate Analysis of Prognostic Factors in Patients With Pathologic Stage I or III Disease

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
One of the most important findings in the present series was a significant improvement in postoperative survival from the early to the late period. Univariate comparisons of the prognosis according to pathologic stage revealed an improvement in all patients except those with pathologic stage II disease. In particular, the overall survival rate of patients with pathologic stage IA disease in the late era was extremely high (89.6%). Multivariate analyses performed after adjustment for age, sex, size of the tumor, and histology also showed a significant increase in the survival of patients with pathologic stage I or III disease. In both periods, lobectomy was the most common procedure, but the rate of sublobar resection including segmentectomy significantly increased in the late era. The ratio of patients who underwent pneumonectomy markedly decreased from 6% to 1%, which was in part the reason the incidence of in-hospital deaths and postoperative complications decreased significantly in the late era [8]. In recent times, more patients prefer a lesser resection to preserve as much lung function as possible [7, 9, 10]. Additional reasons for the decrease in occurrence of postoperative complications and operation-related deaths were not entirely clear in the present series.

There were differences in the distribution of patients between the two eras concerning age, sex, histology, stage of the disease, and size of the tumor. Elder age, female sex, adenocarcinoma, and early stage of the disease were more frequent in the late era; and these were independent prognostic determinants as shown by the multivariate analyses. It is of interest to note the marked increase in the proportion of patients with stage I disease, particularly of stage IA disease, which was a strong factor for the better prognosis of patients treated surgically because of an increase in the rate of early detected lung tumors as a result of our extended screening system and improved diagnostic techniques. Besides, advances in diagnostic ability such as speed and high resolution of computed tomographic images have allowed the detection of patients with inoperable disease and those who could undergo complete resection of the tumor. Preoperative care for patients with other morbidities has improved, and patients have routinely been transferred to the intensive care unit postoperatively. In addition, surgeons in the department might have become more experienced. Thus, the improvement may be attributable to many factors, including comprehensive screening and evolution of diagnostic methods, but there is little doubt that meaningful advances have also taken place in surgical techniques and supportive care. Surgical results depend on two major factors, which are oncologic radicality to prevent recurrences and quality of postoperative status, that is, preservation of lung function and preclusion of perioperative complications. The surgeons should advocate less invasive surgery because we have reached the limit of pursuing radicality of the disease by extensive surgical procedures.

Survival data could be biased due to selection bias, lead-time bias, and length bias [11, 12]. Selection bias is a major determinant of participation in surgical intervention. Although in a nonrandomized study it is impossible to avoid selection bias, the surgical procedures in this study had been performed by the same team, so that the criteria to select patients for surgery were the same throughout the periods of this study. On the other hand, the phenomena called lead-time bias and length bias more recently occurs when a suitable diagnostic practice or a screening test leads to exposure of a disease before symptoms have developed. The advance in the time of diagnosis without moving back the time of death creates lead-time bias in survival comparison. Moreover, the attempt to discover a tumor results in detection of more biologically indolent tumors, which is named length bias. Even if therapy is ineffectual, the period of survival will increase because of the increment provided by presymptomatic detection of the disease.

Both the lead-time and length problems are pertinent, but we were concerned about another problem regarding the comparison of survival in each of the constituent stages [13, 14]. If innovative systems of diagnostic imaging routinely found silent or early metastases, the stages for the more recent patients would not be assigned to the same data as in the older era. The new data would allow patients with silent metastases to migrate from lower stages into higher ones, which would improve survival both in the lower and higher stages, although the total survival rate would be unaffected. Therefore, we must always pay careful attention to the extent to which known biases may have influenced the observed results.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Jemal A., Murray T., Samuels A., Ghafoor A., Ward E., Thun M.J. Cancer statistics, 2003. CA Cancer J Clin 2003;53:5-26.[Abstract/Free Full Text]
  2. Jie C., Wever A.M., Huysmans H.A., Franken H.C., Wever-Hess J., Hermans J. Time trends and survival in patients presented for surgery with non-small-cell lung cancer 1969–1985. Eur J Cardiothorac Surg 1990;4:653-657.[Abstract]
  3. Martini N., Melamed M.R. Multiple primary lung cancers. J Thorac Cardiovasc Surg 1975;70:606-612.[Abstract]
  4. Okada M., Tsubota N., Yoshimura M., Miyamoto Y. Operative approach for multiple primary lung carcinomas. J Thorac Cardiovasc Surg 1998;115:836-840.[Abstract/Free Full Text]
  5. Mountain C.F. Revisions in the International System for Staging Lung Cancer. Chest 1997;111:1710-1717.[Abstract/Free Full Text]
  6. Okada M., Tsubota N., Yoshimura M., Miyamoto Y. Proposal for reasonable mediastinal lymphadenectomy in bronchogenic carcinomas: role of subcarinal nodes in selective dissection. J Thorac Cardiovasc Surg 1998;116:949-953.[Abstract/Free Full Text]
  7. Okada M., Tsubota N., Yoshimura M., et al. Extended sleeve lobectomy for lung cancer: the avoidance of pneumonectomy. J Thorac Cardiovasc Surg 1999;118:710-713.[Abstract/Free Full Text]
  8. Okada M., Yamagishi H., Satake S., et al. Survival related to lymph node involvement in lung cancer after sleeve lobectomy compared with pneumonectomy. J Thorac Cardiovasc Surg 2002;119:814-819.
  9. Okada M., Yoshikawa K., Hatta T., Tsubota N. Is segmentectomy with lymph node assessment an alternative to lobectomy for non-small cell lung cancer of 2 cm or smaller?. Ann Thorac Surg 2002;71:956-960.
  10. Tsubota N., Ayabe K., Doi O., et al. Ongoing prospective study of segmentectomy for small lung tumors. Study Group of Extended Segmentectomy for Small Lung Tumor. Ann Thorac Surg 1998;66:1787-1790.[Abstract/Free Full Text]
  11. Strauss GM, Gleason RE, Sugarbaker DJ. Chest X-ray screening improves outcome in lung cancer. A reappraisal of randomized trials on lung cancer screening. Chest 1995;107(6 Suppl):270S-9S
  12. Cole P., Morrison A.S. Basic issues in population screening for cancer. J Natl Cancer Inst 1980;64:1263-1272.
  13. Feinstein A.R. Symptoms as an index of biological behaviour and prognosis in human cancer. Nature 1966;209:241-245.[Medline]
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