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Ann Thorac Surg 2000;69:913-918
© 2000 The Society of Thoracic Surgeons

Original Articles

Age does not influence early and late tumor-related outcome for bronchogenic carcinoma

Franziska Bernet, MDa, Rudolf Brodbeck, MDa, Marie-Olivier Guenin, MDa, Guido Schüpfer, MDa, James M. Habicht, MDa, Peter M. Stulz, MDa, Thierry P. Carrel, MDa

a Division of Cardiothoracic Surgery and Institute for Anesthesiology, University Hospital Basel, Basel, Switzerland

Address reprint requests to Dr Bernet, Division of Cardiothoracic Surgery, University Hospital Basel, CH-4001 Basel, Switzerland


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The influence of age on early and late outcome after surgical resection of bronchogenic carcinoma is unknown. In an attempt to clarify this issue, we reviewed the outcome of 212 consecutive patients with primary lung cancer who had surgical treatment for bronchogenic carcinoma.

Methods. Ninety-two patients were younger than 50 years (group 1), and 120 patients were older than 70 years of age (group 2). Squamous cell carcinoma and adenocarcinoma were the most common histologic types in both groups. According to the new international staging classification, a similar proportion of stage I, II, and III were observed in both groups.

Results. Only the rate of pneumonectomy was significantly higher in younger patients (41% versus 22%, p = 0.002). The overall operative mortality rate in group 1 was 2.2% and 2.6% after pneumonectomy. In group 2 the overall mortality rate was 2.5% and 3.8% after pneumonectomy. Advanced age did not affect operative mortality. The adjusted (tumor-related) survival rate at 5 years was 56% in group 1 and 53% in group 2 (p = 0.93). The adjusted survival rate for patients with stage I was 61% in group 1 and 65% in group 2 (p = 0.21), and for stage IIIa 39% in group 1 and 48% in group 2 (p = 0.43). The adjusted 5-year survival rate was 56% in group 1 and 59% in group 2 for squamous cell carcinoma (p = 0.53) and 49% in group 1 and 42% in group 2 for adenocarcinoma (p = 0.76).

Conclusions. Perioperative risk and midterm survival were similar in younger and older patients after surgical resection of bronchogenic carcinoma. We believe that this result is because surgical candidates constitute already a highly selected group of patients. From these data it is not possible to conclude that biologic behavior of lung cancer is more aggressive in younger patients.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Lung cancer is generally considered a disease that predominantly affects men in middle age who smoke. It is uncommon in younger patients (< 50 years), but a substantial increase has also been observed among women [1–11]. The biologic and clinical behavior of bronchogenic carcinoma is not always predictable in younger patients: although some authors have described a rather aggressive biologic course with a poor outcome, others have shown that there might be no difference in terms of perioperative and long-term survival between younger and older patients [5–12]. Because most bronchogenic carcinomas occur between 50 and 70 years of age, it seemed interesting and appropriate to investigate two groups of patients, those younger than 50 years and those older than 70 years, who had surgically resectable lung cancer.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
We reviewed hospital charts of 212 consecutive patients who had surgical treatment of bronchogenic carcinoma at our institution (92 patients younger than 50 years and 120 patients older than 70 years). All patients had been operated on between 1972 and 1994 and had received a macroscopically complete and potentially curative resection. Exploratory thoracotomies (in clinically and radiographically unsuspected more advanced disease and patients with adenoid cystic carcinoma or carcinoid tumors) were excluded from this study. All patients had undergone preoperative staging, and from the available information cancer stage was expressed according to the new international TNM staging system for lung cancer [13]. Information about tumor recurrence or late death was obtained from hospital charts or general practitioners. Any death within 30 days postoperatively was considered perioperative early death. In each group, 5 patients were lost to follow-up. Survival rates were calculated by the Kaplan-Meier method. Non-tumor–related deaths were excluded and age correction was done. We used Cox regression analysis to evaluate the effect of age after adjusting for covariates such as stage, histology, and gender. Statistical significance was achieved when the p value was less than 0.05. Differences in surgical therapy between the two groups were evaluated by the log rank test.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Demographics and clinical presentation
Group 1 consisted of 92 patients between 29 and 50 years of age (mean age, 45 years), and group 2 included 120 patients between 70 and 85 years of age (mean age, 74 years). The male:female ratio was 2.8:1 in group 1 and 5.6:1 in group 2. Eighty percent of all patients were habitual smokers (Table 1).


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  		Table 1. Demographics and Clinical Data of Patients With Primary Lung Cancer

 
Cough, hemoptysis, chest pain, and dyspnea were the most common symptoms, but 38% of the younger group and 53% of the older group were asymptomatic. Bronchogenic carcinoma presented as an incidental finding on a routine chest X-ray in 38% of all patients (Table 2). Definitive diagnosis and histologic differentiation were established preoperatively in all patients by using transbronchial biopsy, sputum cytology, or bronchial lavage, alone or more often in combination. There was no hint of an age effect in this multivariate analysis.


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  		Table 2. Symptoms at Diagnosis

 
Histology and staging
Histologic examination revealed a high proportion of squamous cell carcinoma and adenocarcinoma in both groups. Squamous cell carcinoma was predominantly found in the older group of patients (65%, n = 77), whereas adenocarcinoma was found in 22% (n = 26). In the younger group the same percentage (44%) had squamous cell carcinoma and adenocarcinoma. Therefore, the histologic distribution shows a highly significant difference between both groups (Table 1). Regarding gender preference, adenocarcinoma was the most common histologic type in younger women (63% in group 1) and squamous cell carcinoma was the most common histologic type in men (49% in group 1 and 68% in group 2). The histologic data are summarized in Table 3.


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  		Table 3. Gender Distribution in Patients With Primary Lung Cancera

 
According to the TNM staging classification for lung cancer [13], 52% (n = 48) of group 1 had stage I, 17% (n = 16) had stage II, and 31% (n = 28) had stage IIIa disease at the time of the operation. In group 2, 60% (n = 72) had stage I, 21% (n = 25) had stage II, and 19% (n = 23) had stage IIIa disease. These data show no statistically significant difference in the distribution of the three stages among the two groups of patients.

Surgical procedure and adjuvant therapy
The following surgical interventions were done in group 1: 47 lobectomies (51%), seven bilobectomies (8%), and 38 pneumonectomies (42%). In group 2, there were 85 lobectomies (71%), nine bilobectomies (7%), and 26 pneumonectomies (22%) (Table 4). Of 29 patients in group 1 with stage IIIa lung cancer, 20 received postoperative radiotherapy and 9 refused this adjuvant treatment. In group 2 only 10 of 23 patients with a stage IIIa received a postoperative radiotherapy, 7 patients denied the treatment, 2 patients had an additional life-limiting disease, and 4 were too weak physically to receive radiotherapy.


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  		Table 4. Operative Procedures According to Stage of Primary Lung Cancera

 
Operative mortality and morbidity
The overall operative mortality rate in group 1 was 2.2%. Causes of death were myocardial infarction in 1 and septicemia with respiratory distress syndrome in another patient. One death occurred after pneumonectomy (mortality rate 2.6%). In group 2, the operative mortality rate was 2.5% (myocardial infarction in 1 and severe pulmonary embolism in 2 patients). In this group there was also only one death after pneumonectomy (mortality rate 3.8%).

The overall postoperative complication rate (cardiac arrythmia, prolonged intubation time, partial respiratory failure, renal failure) was significantly lower in group 1 (14 of 90 patients; 15.5%) than in group 2: (75 of 120 patients; 63%, p < 0.01) (Table 5). Pulmonary complications with a therapeutic intervention (bronchoscopy, prolonged pleural drainage, antimicrobial treatment) occurred in 17 cases.


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  		Table 5. Early Mortality Rate and Complications After Surgical Resection

 
Follow-up and long-term survival
Median follow-up interval was 2.4 years (range, 4 months to 7 years). During long-term follow-up, 85 patients from group 1 could be evaluated and 7 were lost. Thirty-six patients were still alive, 33 (91.6%) had no evidence of recurrent tumor, and 3 had local recurrence. Of the 49 patients (56.3%) who died during the follow-up interval, 41 deaths (83%) were tumor related. In group 2, 112 patients could be evaluated and 8 were lost to follow-up. Only 29 (24.2%) patients were still alive, 26 (23.2%) without tumor recurrence and 3 with local recurrence. Of the 83 patients (74.1%) who died during follow-up, 44 (53.0%) deaths were tumor related.

The tumor-free median survival time was 18.4 months in group 1 and 17.2 months in group 2. The adjusted 5-year survival rate of the patients younger than 50 years and of those older than 70 years was 56% and 53%, respectively (p = 0.93) (Fig 1). The adjusted survival rates for the two most common histologic types are shown in Figure 2; as expected, squamous cell carcinoma had the better outcome (p = 0.53) than adenocarcinoma (p = 0.76) in both age groups. Survival according to the stage of the disease is shown in Figure 3; stage IIIa (p = 0.43) disease was associated with a significantly poorer outcome (p < 0.055) than stage I (p = 0.21).



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  		Fig 1. Adjusted 5-year overall survival, comparing group 1 (squares) and group 2 (diamonds).

 


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  		Fig 2. (A) Adjusted 5-year overall survival for patients with squamous cell tumor. (B) Same representation for patients with adenocarcinoma. (Squares = group 1; diamonds = group 2.)

 


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  		Fig 3. Adjusted 5-year survival for patients in groups 1 (squares) and 2 (diamonds) with tumor stage I (A) and stage IIIa (B).

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
In this study we tried to clarify the hypothesis that there might be a difference in early and late outcome between younger and older patients after surgical resection of bronchogenic cancer. This issue has only been addressed occasionally in the literature. The age group between 50 and 70 years was excluded as part of the aim of the study itself. The fact that a more aggressive approach was probably chosen in younger patients and that only optimal candidates older than 70 years were operated on represents a limitation of the study. However, we were unable to demonstrate that age affects early outcome after surgical resection of lung cancer. Unlike other series [9, 10], the male-to-female ratio was high in our sample.

Concerning the histology of the tumor, several authors found that adenocarcinoma is the most common histologic type in younger patients (varying from 32% to 54%) and that squamous cell carcinoma has a higher prevalence in elderly patients (35% to 42%) [2, 6, 7, 10, 14]. We found that mainly younger women are affected by adenocarcinoma. The results of El-Torky and coworkers [15] support the hypothesis that the frequency of adenocarcinoma is continuously increasing and that additional risk factors to smoking, eg, environment and occupational exposure, might explain that observation [16–18].

In our series, 38% of the young patients were asymptomatic at the time of the diagnosis; this corresponds closely to the observation of Icard and associates [19]. The high proportion (53%) of asymptomatic patients in the older group might benefit from more regular routine physical and radiologic examinations, especially those with a history of smoking.

A high proportion of younger patients presented initially with advanced disease in this series; this is a common observation that has been previously reported [2, 3, 6–12, 14]. Icard and associates [19] reported that, of 69 patients treated surgically for bronchogenic cancer, 34% were stage I, 14% were stage II, and 52% were stage IIIa/IIIb. This contrasts with the fact that in the older patients group, only 18% were in stage IIIa. These observations must be interpreted with caution, because the indication for medical treatment and the degree of suspicion might have been different in the younger and older groups. Similarly, younger patients might often ignore or misinterpret nonspecific changes in their health status. Conversely, the good physical condition of young patients and a more aggressive approach to their disease have certainly led to a higher incidence of more extensive surgery, as indicated by the incidence of pneumonectomy being significantly higher than in the older population (41% versus 22%, p < 0.05). This finding might be the result of selection bias because surgeons understandably are reluctant to undertake pneumonectomy in older patients. However, the stage distribution in both groups was similar. The fact that pneumonectomy did not confer any survival benefit in patients of advanced age is probably due to the small number of patients. Although the highest proportion of pneumonectomy (71%) was done in younger patients with stage IIIa disease, 23% were done in patients with stage I lung cancer. Regarding the 5-year survival rate of 56% versus 53% in group 1 and group 2, respectively, and the low perioperative risk, this approach seems to be justified. Table 6 summarizes some clinical data and results obtained in similar patients in recent years [4, 5, 20, 21].


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  		Table 6. Summary of Patients Data After Surgical Resection of Primary Lung Cancer

 
The most frequent postoperative complication in the elderly population was atrial fibrillation, with an overall incidence of 22%; consequently digoxine was administered prophylactically in patients scheduled for pneumonectomy. Pulmonary complications were the major perioperative risk and included retained bronchial secretions, atelectasis, and pneumonia. The long history of smoking and the high incidence of chronic obstructive pulmonary disease in the elderly patients contributed to the rate of pulmonary complications. However, Gebitekin and coworkers [20] found more pulmonary complications in their younger patients. The 5-year survival rate for stage IIIa patients was 39% in group 1 versus 48% in group 2. Because these results do not reach a statistically significant difference, we believe that this result might be due to reluctance to undertake radical resection in more advanced cases.

In the literature, there is general agreement that the stage of the disease is the major determinant of long-term survival after pulmonary resection for bronchogenic carcinoma [3, 8, 10–12, 14, 19–25]. Although more patients younger than 50 years were in stage IIIa, the adjusted (tumor-related, age corrected) 5-year survival rate was slightly better than in the elderly population. Despite the higher incidence of tumor-related death in the younger group (83% compared with 53%) it is suprising that the median survival time in both groups was similar (18.4 compared with 17.2 months). From this observation it may be postulated that the extent of the operation did not influence survival. Deneffe and colleagues [14] reported significantly better 5-year survival for squamous cell carcinoma than for adenocarcinoma in any stage, except for stage III. Our observation confirms those data, but the prognostic significance of histology itself after surgical resection is still not completely elucidated.

Conclusions
The results obtained in this series are very acceptable and probably can be attributed to careful preoperative selection, meticulous technique with sophisticated anesthesia, and improved postoperative management in the intensive care unit [22]. Despite new acquisitions in preoperative diagnostic tools and recent developments in surgical technique, the 5-year survival rate of patients with bronchogenic carcinoma treated surgically has not improved recently [23]; however, age alone should not be a contraindication. From our data we are not able to conclude that biologic behavior of bronchogenic carcinoma differs significantly between younger and older patients. This finding might be because patients who have surgical treatment are a highly selected group anyway, regardless of age. However, any preoperative comorbidity can be prohibitive in older patients.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Capewell S., Sankaran R., Lamb D., McIntyre M., Sudlow M.F. Lung cancer in lifelong non-smokers. Thorax 1991;46:565-568.[Abstract/Free Full Text]
  2. McDuffie H.H., Klaassen D.J., Dosman J.A. Female-male differences in patients with primary lung cancer. Cancer 1987;59:1825-1830.[Medline]
  3. Sugio K., Ishida T., Keneko S., Yokoyama H., Sugimachi K. Surgically resected lung cancer in young adults. Ann Thorac Surg 1992;53:127-131.[Abstract]
  4. Ishida T., Yokoyama H., Kaneko S., Sugio K., Sugimachi K. Long-term results of operation for non-small cell lung cancer in the elderly. Ann Thorac Surg 1990;50:919-922.[Abstract]
  5. Roxburgh J.C., Thompson J., Goldstraw P. Hospital mortality and long-term survival after pulmonary resection in the elderly. Ann Thorac Surg 1991;51:800-803.[Abstract]
  6. Green L.S., Fortoul T.I., Ponciano G., Robles C., Rivero O. Bronchogenic cancer in patients under 40 years old. Chest 1993;104:1477-1481.[Abstract/Free Full Text]
  7. Rocha M.P., Fraire A.E., Guntupalli K.K., Greenberg S.D. Lung cancer in the young. Cancer Detect Prev 1994;18:349-355.[Medline]
  8. Bourke W., Milstein D., Giura R., et al. Lung cancer in young adults. Chest 1992;102:1723-1729.[Abstract/Free Full Text]
  9. Antkowiak J.G., Regal A.M., Takita H. Bronchogenic carcinoma in patients under age 40. Ann Thorac Surg 1989;47:391-393.[Abstract]
  10. DeCaro L., Benfield J.R. Lung cancer in young persons. J Thorac Cardiovasc Surg 1982;83:372-376.[Abstract]
  11. Jubelirer S.J., Wilson R.A. Lung cancer in patients younger than 40 years of age. Cancer 1991;67:1436-1438.[Medline]
  12. Pemberton J.H., Nagorney D.M., Gilmore J.C., Taylor W.F., Bernatz P.E. Bronchogenic carcinoma in patients younger than 40 years. Ann Thorac Surg 1983;36:509-515.[Abstract]
  13. Mountain C.F. A new international staging system for lung cancer. Chest 1986;89:225S-233S.[Free Full Text]
  14. Deneffe G., Lacquet L.M., Verbeken E., Vermaut G. Surgical treatment of bronchogenic carcinoma. Ann Thorac Surg 1988;45:380-383.[Abstract]
  15. El-Torky M., El-Zeky F., Hall J.C. Significant changes in the distribution of histologic types of lung cancer. Cancer 1990;65:2361-2367.[Medline]
  16. Brownson R.C., Reif J.S., Keefe T.J., Ferguson S.W., Pritzl J.A. Risk factors for adenocarcinoma of the lung. Am J Epidemiol 1987;125:25-34.[Abstract/Free Full Text]
  17. McKneally M.F. Lung cancer in young patients. Ann Thorac Surg 1983;36:505-507.[Medline]
  18. Fraire A.E., Cooper S., Buffler P.A., Greenberg S.D. Carcinoma of lung. Prog Surg Pathol 1992;12:129-149.
  19. Icard P., Regnard J.F., de Napoli S., Rojas-Miranda A., Dartevelle P., Levasseur P. Primary lung cancer in young patients. Ann Thorac Surg 1992;54:99-103.[Abstract]
  20. Gebitekin C., Gupta N.K., Martin P.G., Saunders N.R., Walker D.R. Long-term results in the elderly following pulmonary resection for non-small cell lung carcinoma. Eur J Cardiothorac Surg 1993;7:653-656.[Abstract]
  21. Morandi U., Stefani A., Golinelli M., et al. Results of surgical resection in patients over the age of 70 years with non-small lung cancer. Eur J Cardiothorac Surg 1997;11:432-439.[Abstract]
  22. Jie C., Wever A.M.J., Huysmans H.A., Franken H.C.M., 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]
  23. Kadri M.A., Dussek J.E. Survival and prognosis following resection for primary non-small cell bronchogenic carcinoma. Eur J Cardiothorac Surg 1991;5:132-136.[Abstract]
  24. Sobue T., Suzuki T., Matsuda M., Kuroishi T., Ikeda S., Naruke T., Japanese Lung Cancer Screening Research Group. Survival for clinical stage I lung cancer not surgically treated. Cancer 1992;69:685-692.[Medline]
  25. Haffty B.G., Goldberg N.B., Gerstley J., Fischer D.B., Peschel R.E. Results of radical radiation therapy in clinical stage I, technically operable non-small cell lung cancer. Int J Radiat Oncol Biol Phys 1988;15:69-73.[Medline]
Accepted for publication August 30, 1999.




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