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(Chest. 2000;117:104S-109S.)
© 2000 American College of Chest Physicians

Surgical Therapy of Early Non-Small Cell Lung Cancer*

Jean Deslauriers, MD and Jocelyn Grégoire, MD

* From the Centre de pneumologie de l’Hôpital Laval, Sainte-Foy, Quebec, Canada.

Correspondence to: Jean Deslauriers, MD, Centre de pneumologie de l’Hôpital Laval, 2725 chemin Sainte-Foy, Sainte-Foy, Quebec, Canada G1V 4G5


   Abstract
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 Abstract
Introduction
 Surgical Management of T1n0M0...
 Surgical Management of T1n1M0...
 Conclusion
 References
 
Approximately 45% of all lung carcinomas are limited to the chest, where surgical resection is not only an important therapeutic modality, but in many cases, the most effective method of controlling the disease. Patients with T1N0 and T2N0 tumors have early lung cancer, and most are curable by resection, with 5-year survival rates in the range of 75 to 80% for patients with T1N0 status. Patients with smaller tumors do better than patients with larger ones, while visceral pleural invasion does not seem to influence survival. Histologic type is also a significant prognostic variable, with squamous tumors having a better prognosis than tumors of nonsquamous histology. Other known prognostic factors are age and gender of the patient and completeness of resection. The "gold standard" of surgery remains lobectomy, regardless of tumor size at presentation. Stage T1N1 and T2N1 carcinomas represent a group of patients where the disease involves hilar and bronchopulmonary nodes. This group is best treated by complete resection with mediastinal lymphadenectomy. Tumor size and histology are significant prognostic variables, and 5-year survival after complete resection is in the range of 40 to 50%. Postoperative radiation therapy may improve local control, while chemotherapy results in a slightly reduced risk of death.

Key Words: early-stage non-small cell lung cancer • stage I non-small cell lung cancer • surgery


   Introduction
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 Abstract
 Introduction
Surgical Management of T1n0M0...
 Surgical Management of T1n1M0...
 Conclusion
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Lung cancer is a significant health problem, with approximately 170,000 new cases being diagnosed annually in the United States. Of these, about 45% are limited to the thorax, where surgery is not only an important therapeutic modality, but in many cases, the most effective method of controlling the disease. Of all resectable tumors, 28% are T1N0 lesions, which have a high cure rate, and 37% are T1N1, T2N0, and T2N1 lesions, which have a somewhat lower cure rate.

In the revised stage grouping of TNM subsets, stage I patients have been subclassified into two subsets (I-a and I-b) because end-results reports consistently show a better outcome for patients with T1N0M0 disease (stage I-a) than for those with T2N0 disease (stage I-b; p < 0.01; Table 1 ).1 Similarly, patients with T2N1M0 tumors and those with T3N0M0 disease have been regrouped in stage II-b, because little difference was observed in their cumulative 5-year survival rates.1


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  		Table 1.. Cancer Stages and Survival*

 
The reported survival after resection of early stage non-small cell lung cancer (NSCLC) varies a great deal in the literature, and factors such as characteristics of the study population, sophistication of the staging process, or length of follow-up have a significant bearing on the end result.2 The extent of intraoperative staging and the nodal map used by surgeons reporting end results are particularly relevant, even if the two series that compared mediastinal lymphadenectomy to systematic node sampling failed to show a difference in pathologic stage TNM.3 4 Level 10 node, for instance, is an N1 node in the American Joint Committee of Cancer staging map5 but an N2 node in the American Thoracic Society map.6 These differences are recognized, and a unified nodal mapping system has recently been proposed by Mountain and Dresler.7

The length of follow-up available in end-results reports may also influence survival figures, because early stage NSCLC includes notoriously slow-growing neoplasms, and longer follow-up intervals may be necessary before final assessment of survival differences.8

This review will summarize the survival information available for the various TNM subsets of early stage NSCLC. It is acknowledged that nearly all of these data come from surgical series where resection of the primary tumor was the mainstay of treatment.


   Surgical Management of T1N0M0 AND T2N0M0 LUNG CANCER
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 Abstract
 Introduction
 Surgical Management of T1n0M0...
Surgical Management of T1n1M0...
 Conclusion
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According to the TNM staging system (Table 2 ), stage I tumors are defined as those without lymph node metastasis (N0) that are completely surrounded by lung parenchyma or that do not extend beyond the visceral pleura or within 2 cm of the carina.1 9 The prognosis for surgically treated patients with T1N0M0 NSCLC is generally good, and 5-year survival figures approximate 80%. In a series from the Mayo Clinic, the survival of 225 patients who had T1N0 lesions was 91% at 2 years and 80% at 5 years.10 In that series, TNM subset (T1 vs T2), age at operation (< 70 years vs > 70 years), gender (women vs men), and extent of operation (limited resection and lobectomy vs pneumonectomy or bilobectomy) were important determinants of survival. There were no differences in survival on the basis of cell type, although the 5-year survival rate was slightly better in patients with bronchioloalveolar carcinoma (81%). In 1990, Thomas and Rubinstein8 reviewed the sites of cancer recurrences in 907 patients with T1N0 disease enrolled in Lung Cancer Study Group (LCSG) protocols. The median survival was approximately 8 years, and the median time to recurrence of malignancy, including new primaries, was 7.5 years. Brain, bone, and mediastinum were the most common sites of recurrences in decreasing order of frequency. That study and a follow-up article11 also showed that the recurrence rate decreases with time after resection, whereas the rate of new primary lung cancer increases with time, and can be as high as 1 to 2%/yr. Thus, early detection techniques12 and continued patient surveillance are particularly applicable to this cohort of patients.


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  		Table 2.. Definitions of Primary Tumor and Nodal Status in Early Stage Lung Cancer

 
A summary of prognostic factors in resected stage I lung cancer is listed in Table 3 . Tumor size does make a difference in the survival of patients with T1N0M0 and T2N0M0 lung carcinomas.13 14 15 16 In 1995, Martini et al14 showed that patients with T1 lesions do better than those with T2 lesions, and that patients with small tumors (< 1 to 2 cm) do better than patients who have tumors >= 5 cm in diameter. Survival in patients with T1N0 tumors was 82% at 5 years and 74% at 10 years, compared with 68% at 5 years and 60% at 10 years for patients with T2 tumors (p < 0.0004). In that series, nearly 60% of all recurrences occurred within the first 2 years of follow-up, and second primary cancers in the lung or at other sites developed in 34% of patients.14 In a group of 221 patients with a primary lung cancer <= 3.0 cm (T1 tumors), Ishida et al15 also showed that 5-year survival rates decrease with increase in tumor size. This was attributed to an increase in the incidence of occult lymph node metastasis in larger tumors (N1, 5%, and N2, 12% in tumors from 1.1 to 2.0 cm; N1, 12%, and N2, 25% in tumors from 2.1 to 3.0 cm) not detected preoperatively or even by intraoperative lymph node sampling.


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  		Table 3.. Summary of Prognostic Factors in Resected Stage I Lung Cancer

 
Visceral pleura involvement does not seem to influence the survival of patients with stage I disease,14 although Ichinose et al17 were able to document by univariate analysis of survival curves that pleural involvement was a significant prognostic factor. These investigators observed a survival difference between patients having tumors not extending beyond the elastic layer of the visceral pleura (p0), tumors extending beyond the elastic layer but not exposed on the pleural surface (p1), and tumors exposed to the pleural surface (p2). These investigators also identified other significant prognostic factors, including tumor size (T1 vs T2), tumor differentiation (well differentiated vs moderately or poorly differentiated), artery invasion, lymphatic vessel invasion, and degree of DNA ploidy pattern (diploid vs aneuploid).17 18

Histologic type of the tumor is a fairly consistent determinant of time to recurrence and survival in patients with resected stage I carcinoma.19 20 21 In a LCSG analysis, cancer recurrences were more frequent and recurrence rates were higher in patients with tumors of nonsquamous histology (Table 4 ).19 However, this advantage disappeared after 5 years.11 In other LCSG data, 5-year survival following surgery in patients with T1N0 tumors was 83% for squamous carcinomas and 69% for adenocarcinomas (p = 0.02); for patients with T2N0 tumors, these rates were 64% and 57%, respectively.21 22 In some series, the survival advantage for patients with tumors of squamous histology was only seen in smaller-size tumors.23 24


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  		Table 4.. Recurrences: Squamous vs Nonsquamous*

 
The level of bronchial invasion often determines the tumor (T) status, because a tumor < 3 cm in diameter is considered T1 if there is no proximal invasion to a lobar bronchus, and T2 when the lesion involves the main bronchus.1 9 Several articles have now shown that survival is excellent after surgery in superficial tumors confined to the bronchial mucosa and without nodal involvement (N0).15 25 26 These tumors are now classified as T1 tumors even if they are located within 2 cm of the carina.1

The presence of satellite nodules within the primary lobe has also been identified as a poor prognostic factor,27 and in the revised TNM classification, these are considered T4 tumors.1 Blood vessel invasion has been inconsistently shown to have prognostic significance in early stage lung cancer, although two recent studies from Europe28 29 have provided data supporting the concept that the absence of blood vessel invasion identifies a group of patients with very low probability of distant metastases.

Role of Limited Resection in Surgical Management of T1N0 and T2N0 Lung Cancer
The current "gold standard" of surgical treatment for patients with T1N0 and T2N0 tumors limited to a lobe is an anatomic lobectomy, regardless of the size of tumor at presentation. Limited resections, which are defined as procedures that are less than lobectomy (generally a wide wedge for peripheral tumors or an anatomic segmentectomy), were introduced by Jensik et al,30 who suggested that more limited operations could be adequate for early stage bronchogenic carcinoma. In this series, 69 patients underwent intentional segmental resection for peripheral tumors. Survival rates of 56.4% at 5 years and 26.8% at 15 years were reported, and the investigators concluded that these figures supported the validity of segmental resection in selected cases of lung cancer. Since then, many authors have adopted this approach as a compromise to lobectomy for high-risk patients with limited function (Table 5 ).31 32 33 34 35 Other possible indications for limited resections include patients with synchronous bilateral tumors and selected patients with very peripheral T3 tumors (ie, superior sulcus tumors), where the majority of the malignancy involves the chest wall rather than the pulmonary parenchyma. The theoretic advantages of limited resection are listed in Table 6 . Possible disadvantages include the potential for increased local recurrence and mortality and an increased operative morbidity, consisting primarily of prolonged air leaks.


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  		Table 5.. Limited Resection as a Compromise Operation

 

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  		Table 6.. Theoretical Advantages and Disadvantages of Lesser Resections

 
More recently, some centers have advocated lesser resections as appropriate treatment for uncompromised patients with peripheral T1N0 tumors not transgressing a segmental plane (Table 7 ).24 36 37 In 1994, the Rush-Presbyterian-St. Luke’s Medical Center group presented the results of a retrospective study concerning 173 patients who had undergone segmental resection (n = 68) or lobectomy (n = 105) for stage I NSCLC over an 8-year interval (from 1980 to 1998).38 While a survival advantage was noted for patients with tumors >= 3 cm undergoing lobectomy (p = 0.006), no survival advantage was apparent for patients undergoing lobectomy for tumors < 2 cm in diameter (p = 0.24). The overall local recurrence rate was higher after segmental resection (22.7%) than after lobectomy (4.9%). In another study, Landreneau et al39 compared the results of open wedge resection, video-assisted wedge resection, and lobectomy in a nonrandomized trial involving 219 patients with pT1N0M0 lung cancer. They concluded that anatomic lobectomy should remain the surgical treatment of choice because of increased risk for local recurrence and death after limited resection.


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  		Table 7.. Limited Resection as an Intentional Operation

 
In 1995, the LCSG published the results of a prospective randomized trial comparing limited resection (wedge or segmental) to lobectomy for patients with peripheral T1N0 NSCLC.40 Of the 276 randomized patients, 247 were eligible for analysis. In the limited-resection group, there was a threefold increase in the incidence of local recurrences, especially high among patients with adenocarcinoma, and an observed 30% increase in overall mortality rate (p = 0.08) when compared to patients undergoing lobectomy. In that study, there were no observed late (12 to 18 months) functional advantages or decreased operative mortality in the limited-resection group. The analysis also showed a significantly higher local recurrence rate after wedge resection vs segmentectomy, presumably because of inadequate margins around the tumor or failure to identify microscopic N1 disease. Thus, the appropriate application of video-assisted thoracic surgery procedures, whether they are wedges or lobectomies for the treatment of early stage NSCLC, remains to be clarified.41 42


   Surgical Management of T1N1M0 AND T2N1M0 LUNG CANCER
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 Abstract
 Introduction
 Surgical Management of T1n0M0...
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Conclusion
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T1N1M0 and T2N1M0 lung cancers include those where the disease involves bronchopulmonary and hilar nodes but without metastases to mediastinal nodes. The T1N1M0 subset is infrequent, and the 5-year survival rate after complete resection is 55% (Table 1) .1 Survival is in the range of 40% for patients within the T2N1M0 subset. In 1983, Martini et al43 reported the results of treatment in 75 patients with NSCLC and pN1 disease. In that study, the survival of 62 patients treated by resection alone was 49% at 5 years. In a more recent report from the Memorial Sloan-Kettering Cancer Center, 214 patients with resected T1N1 (n = 35) and T2N1 (n = 174) NSCLC lesions were analyzed with respect to survival and prognostic factors.44 In that series, the best survival rates were observed in patients with tumors <= 3 cm in diameter, and in patients who had a single node involved. Martini et al insisted that this group of patients should be treated surgically and that complete resection with mediastinal lymphadenectomy is necessary to ensure that no nodal metastasis in the mediastinum is overlooked. In similar analysis, the Ludwig Cancer Study Group has reported median survival figures of 4.8 and 2.3 years for patients with T1N1 and T2N1 disease, respectively.45 46

Similar to what is observed in T1N0M0 and T2N0M0 subsets, the histologic classification of the tumor is a significant prognostic factor. In LCSG data, the 5-year survival rate following surgery was 75% for squamous cell carcinoma and 52% for adenocarcinoma in the T1N1 subset (p = 0.04), and 53% for squamous cell carcinoma and 25% for adenocarcinoma in the T2N1 category (p = 0.01).21 22 Similarly, Ichinose et al17 have shown in a multivariate analysis that histologic classification (squamous vs nonsquamous; p = 0.0359) was a predominant prognostic factor in patients with pT1N1 and pT2N1 disease. Naruke et al47 also observed differences in survival based on histology. In 1992, however, Martini et al44 failed to demonstrate a difference in survival between patients with squamous carcinoma vs adenocarcinoma (p = 0.238), although the pattern of recurrence after resection of T1N1 or T2N1 tumors differed by histology. Local or regional recurrence was more frequent in patients with squamous carcinoma, whereas distant metastases were more commonly seen in adenocarcinomas, with the brain as the most frequent site of metastasis. In that series, there was no significant difference in survival between patients whose tumors had visceral pleural invasion compared with those who did not (p = 0.294).

The location and number of N1 nodes as prognostic factors has been looked at by Martini et al44 and Yano et al.48 In the study by Martini et al,44 there was a statistically significant (p = 0.016) difference in survival rates between patients with involvement of a single N1 node (45% at 5 years) vs multiple N1 nodes (31% at 5 years). In a study of 78 patients with pathologic N1 disease, Yano et al48 also reported that the survival associated with lobar N1 disease (stations 12 to 14) was significantly (p = 0.014) better than that of hilar N1 disease (station 10; American Joint Committee on Cancer nodal map; 64.5% vs 39.7% at 5 years).

The role of adjuvant therapy in these subsets of patients has been addressed by many cooperative groups. In a LCSG trial, 210 patients with complete resection of stage II (T1N1, T2N1) or stage III squamous carcinoma received either surgery plus radiotherapy (n = 102) or surgery alone (n = 108).49 There was no survival benefit from radiotherapy, but a significantly lower rate of local recurrences (p < 0.001). Based on these results, it may be advisable to irradiate these patients postoperatively in order to maintain their quality of life for the longest possible time. There have been no clinical trials of adjuvant radiation therapy for stage T1N1 or T2N1 nonsquamous cell carcinomas.

Although some studies have suggested that chemotherapy administered in the postoperative setting may prolong survival and disease-free interval in the patients with stage II disease,50 51 a recent meta-analysis showed that postoperative chemotherapy with or without radiotherapy only resulted in a slightly reduced (statistically nonsignificant) risk of death among patients with surgically resected stage II and III-a.52 53 Feld and colleagues50 from the LCSG recently reported the results of a prospective randomized trial utilizing an adjuvant cisplatin-based regimen (cyclophosphamide, doxorubicin, cisplatin) vs control in patients with completely resected T1N1 and T2N0 NSCLC. There was no difference between treatment and control groups with respect to time of recurrence or survival, and the site of first recurrence was distant in 74% of patients. Although a number of ongoing trials are currently evaluating new chemotherapy regimens to be given postoperatively in patients with complete resection of T1N1 and T2N1 tumors, one of the main problem remains patient compliance with the regimen, which, in the postoperative setting, is in the range of 50 to 60%.50

At present, there is some evidence that retinoid or high-dose vitamin A chemoprevention may reduce the recurrence rate and improve the disease-free interval in patients curatively resected for stage I lung cancer.54


   Conclusion
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 Abstract
 Introduction
 Surgical Management of T1n0M0...
 Surgical Management of T1n1M0...
 Conclusion
References
 
Although it is clear that early stage NSCLC is best treated by surgical resection, the survival of patients with disease stages other than T1N0 is still in the 40 to 50% range. These figures must be improved by the addition of induction or adjuvant regimens, and based on the available literature, it is reasonable to suppose that combination induction chemotherapy or chemoradiation would be useful in these subsets of patients. In the future, the use of better imaging techniques such as positron emission tomography or use of video-assisted thoracic surgery to document N1 disease may help the selection of patients for these therapies.


   Footnotes
 
Abbreviations: NSCLC = non-small cell lung cancer; LCSG = Lung Cancer Study Group


   References
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