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Ann Thorac Surg 2004;77:1173-1178
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Histological determinants of survival in completely resected T1-2N1M0 nonsmall cell cancer of the lung

Omar A. Khan, MRCSa*, James J. Fitzgerald, MRCSa, Mark L. Field, MRCSa, Irshad Soomro, MRCPathb, F. David Beggs, FRCSa, W. Ellis Morgan, FRCSa, John P. Duffy, FRCSa

a Thoracic Unit, Nottingham City Hospital, Nottingham, United Kingdom
b Department of Histopathology, Nottingham City Hospital, Nottingham, United Kingdom

Accepted for publication August 21, 2003.

* Address reprint requests to Dr Khan, Thoracic Unit, Nottingham City Hospital, Hucknall Rd, Nottingham, UK NG5 1PB
e-mail: omarkhan{at}iname.com


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The histologic determinants of survival after surgical resection of stage II nonsmall cell lung cancer are poorly understood. We analyzed the prognostic significance of a number of histologic features after complete resection of T1-2N1M0 nonsmall cell cancer of the lung.

METHODS: The case notes and histology of all patients who underwent a potentially curative surgical resection for T1-2N1M0 nonsmall cell carcinoma of the lung between 1991 and 1997 were reviewed retrospectively. The following histologic factors were recorded: histologic type of tumor; number of nodes with metastatic deposits together with their nodal station; the presence of vascular invasion, visceral pleural involvement, and cellular necrosis; and grade of tumor. The results from 98 patients were analyzed. Univariate and multivariate analyses were performed to identify prognostic factors.

RESULTS: Univariate analysis showed that only three factors had a statistically significant correlation with a poor prognosis: vascular invasion (p = 0.002), nonsquamous histology (p = 0.005), and visceral pleural involvement (p = 0.002). Multivariate analysis revealed that all three factors were significant independent adverse prognostic indicators.

CONCLUSIONS: Visceral pleural involvement, nonsquamous histology, and vascular invasion are all significant adverse prognostic factors after surgical resection of T1-2N1M0 nonsmall cell cancer of the lung. These findings conflict with previously published reports, and we advocate a prospective, large-scale study in order to clarify the prognostic significance of histologic characteristics in stage II disease.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Despite advances in the management of lung cancer, survival after successful surgical resection of nonsmall cell lung cancer (NSCLC) remains poor with a 5-year survival of approximately 50% [1, 2]. Although a large number of studies [3–6] have attempted to identify prognostic determinants after surgery, the majority of these have concentrated on outcome in node-negative disease. By contrast, relatively few studies have focused on the long-term survival of patients with N1 (ie, isolated ipsilateral pulmonary lymph node involvement) disease. Moreover, even those studies [7–13] that have concentrated on this subset of patients have provided conflicting evidence as to the prognostic importance of a variety of clinicopathologic factors. In addition, although some of the previous studies have examined the importance of a few histologic variables in N1 disease, there has, to date, been no comprehensive evaluation of the influence of histologic characteristics on postoperative survival. The purpose of our study, therefore, was to examine the histologic determinants of long-term survival in T1-2N1M0 NSCLC after a potentially curative lung resection.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 Acknowledgments
 References
 
The case notes of all patients who underwent a surgical resection for nonsmall cell lung cancer between January 1991 and December 1997 at Nottingham City Hospital were reviewed retrospectively. All operations were performed by the same team of four thoracic surgeons who used similar preoperative and postoperative management. None of these patients underwent any preoperative or postoperative chemotherapy or radiotherapy. Before thoracotomy, all patients underwent an assessment for fitness for surgery. This was performed using a variety of techniques including clinical examination, spirometry, capillary blood gas analysis, electrocardiography, exercise tolerance testing, and where appropriate ventilation-perfusion isotope scanning. In general, patients with an estimated postoperative FEV1 of less than 40% of the predicted value for their height and weight, or those unable to complete stage I of the Bruce protocol owing to symptoms or signs of myocardial ischemia or respiratory compromise did not proceed to surgery.

Patients also underwent a variety of screening tests to assess the resectability of their tumors. These included physical examination, hematologic and biochemical investigations, bronchoscopy, computed tomography (CT) of the chest and upper abdomen, and bone scans where appropriate. In addition, patients whose CT scans showed the presence of mediastinal lymph nodes greater than 1 cm in diameter underwent sampling of these nodes through cervical mediastinoscopy or anterior parasternal mediastinotomy. Patients who showed evidence of distant metastatic disease, those with histologically confirmed N2 involvement and those with tumors invading major irresectable structures (typically the aorta) did not proceed to lung resection.

Operative technique
All patients in our cohort underwent lobectomy, bilobectomy, sleeve lobectomy, or pneumonectomy—none of our patients with N1 disease underwent a segmentectomy or wedge resection. The choice of lung resection in each case was determined by the site and extent of the primary disease. In all cases, the aim was to obtain complete clearance of the tumor while preserving as much uninvolved lung parenchyma as possible. Pneumonectomy was only performed in cases of where tumor was seen to involve all the pulmonary lobes and cases where the central nature of the tumor or the presence of extensive hilar lymphadenopathy prevented the performance of a lobectomy or sleeve lobectomy. During lung resection, the hilar lymph nodes were dissected en bloc. In addition, routine systematic mediastinal lymph node sampling of multiple nodal stations including the paratracheal, subaortic, inferior pulmonary ligament, and subcarinal nodes was performed. The mean number of lymph nodes harvested per specimen was 16 (range, 8 to 27).

Pathology analysis
The surgical specimens were placed in formalin and transported to the laboratory. Pathology analysis was then performed by the same team of three histopathologists. On receipt in the laboratory, the site and size of the tumor was recorded. The specimens were then serially sectioned and multiple sections embedded. These sections were then examined microscopically, and the histologic subtype of the tumor was recorded using the World Health Organization international histologic classification of tumors [14]. The tumors were also categorized according to their grade (namely, well, moderately, or poorly differentiated, or undifferentiated). The T stage of the tumors was recorded using the revised international system for staging lung cancer of the Union Internationale Contre le Cancer [15]. In addition, all the harvested lymph nodes were examined for the presence of tumor deposits. Nodal status was classified using the criteria outlined in the regional lymph node classification for lung cancer staging [16]. In brief, this system divides N1 lymph nodes into hilar lymph nodes (station 10), interlobar lymph nodes (station 11), and peripheral intralobar nodes (stations 12, 13, and 14). In each case, the total number of involved lymph nodes together with their nodal station was recorded. In addition, a further distinction was made between lymph nodes involved by direct infiltration (defined as an infiltrative extension of viable tumor cells into a lymph node contiguous with the primary tumor) and those involved through direct metastatic spread.

Vascular space involvement was assessed through hematoxylin and eosin staining of multiple sections: cases in which tumor appeared to infiltrate the venous or arterial system as well as cases in which the presence of tumor emboli was noted in the vascular system were defined as having positive vascular invasion. Similarly, visceral pleural involvement was defined as present when tumor was seen to extend to within 1 mm of the visceral pleura margin, as well as cases in which tumor was present at the margin itself. Cellular necrosis was defined as present when visual inspection of routine sections revealed that more than one third of the tissue present was necrotic.

Data analysis
Exclusion criteria included cases of surgical mortality (defined as death within 30 days of operation, or during the same hospital admission irrespective of the time elapsed from operation), incomplete excision (defined as cases with the presence of microscopic tumor within 1 mm of the proximal margin of excision), patients with N0 disease, T3 and T4 tumors, small cell carcinomas, carcinoid tumors, synchronous tumors, and tumors with distant metastases. In addition, we excluded all cases in which the presence of metastatic N2 lymph nodes was noted. After these exclusions, the results of 98 potentially curative lung resections for T1-2N1M0 NSCLC were analyzed in detail. The case notes and operation notes of these patients were reviewed, and their survival data were recorded. Patients were followed up for life after their operation, with outpatient clinic review every 3 months for the first year, every 6 months for the next 4 years, and yearly thereafter. There was a 100% follow-up rate with a minimum follow-up period among the survivors of 5 years.

Statistical analysis was performed using commercially available software packages. The patients' sex, operative procedure, and histologic type of tumor; number of N1 nodes with metastatic deposits; site of nodal involvement and mode of nodal spread (ie, through direct infiltration or metastases); presence of vascular invasion, visceral pleural involvement, and cellular necrosis; and grade of tumor were then categorized. Univariate analysis was performed using a {chi}2 test to establish any relationship between these factors and 5-year survival. Factors that had statistical significance (p < 0.05) on univariate analysis were then entered into a multivariate analysis using a Cox proportional hazards model to identify independent predictors of survival.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 Acknowledgments
 References
 
Patient and tumor characteristics
Of the 98 patients, 64 were male and 24 were female with a mean age of 61.8 years (range, 45 to 78). Fifty-eight patients underwent a pneumonectomy, and 40 underwent either a lobectomy, bilobectomy, or sleeve lobectomy. A summary of the histologic characteristics of the specimens is shown in Table 1. Details of the patients' nodal involvement are listed in Table 2.


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  		Table 1. Distribution of Tumors According to T Stage, Tumor Type, Degree of Differentiation, Vascular Invasion, Visceral Pleural Involvement, and Cellular Necrosis (n = 98)

 

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  		Table 2. Summary of Pattern of Nodal Involvement Observed

 
Univariate analysis
Of the 98 potentially curative lung resections, a total of 43 patients survived for a 5-year period after operation, representing an actual 5-year survival rate of 44%.

An overall survival curve for the entire dataset was plotted using the Kaplan-Meier method, as shown in Figure 1.



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  		Fig 1. Overall survival after potentially curative surgical resection of T1-2N1M0 nonsmall cell lung cancer. Censored cases are represented by crosses (+).

 
Univariate analysis was performed to examine the relationship between the factors described in the methods section of this paper and the probability of 5-year survival after lung resection. The results of this analysis are shown in Table 3. Only visceral pleural involvement, vascular invasion, and nonsquamous histology achieved statistical significance.


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  		Table 3. Univariate Analysis of Clinical Characteristics and Survivala

 
Multivariate analysis
Multivariate analysis was then performed to identify independent prognostic determinants. The factors that achieved statistical significance are summarized in Table 4. As shown, visceral pleural involvement, vascular invasion, and nonsquamous histology were all independent adverse predictors of survival.


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  		Table 4. Multivariate Analysis of Histologic Characteristics Using Cox Proportional Hazards Model

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
Acknowledgments
 References
 
Under the TNM-based staging system for nonsmall cell lung cancer T1N1ML0, T2N1ML0, and T3N0ML0 tumors are jointly classified as stage II disease, with a further subdivision into stage IIA (for T1 tumors) and stage IIB (for T2 and T3 tumors) [15]. Although this staging system provides an anatomical classification of lung tumors, its secondary purpose is to allow the prognostic stratification of patients into homogenous groups after surgery [15, 16]. Our study, however, in common with previously reported series [7–13], suggests that patients with stage II disease have a heterogeneous outcome after surgery. Moreover, the only significant prognostic determinants we identified were vascular invasion, nonsquamous histology, and visceral pleural involvement—factors that are not fully incorporated into the current TNM-based staging system.

Within our cohort, vascular invasion was found to be the most important determinant of survival after surgical resection. Although the prognostic importance of vascular involvement has been documented in several studies of stage I disease [4, 6, 17], there has to date been only one study [12] investigating the significance of vascular invasion in stage II disease. In contrast to our findings, however, this study found that vascular invasion had no prognostic significance. Similarly, unlike most previous studies, we found nonsquamous cell histology to be an independent predictor of survival. Within the literature, there does appear to be considerable uncertainty regarding the prognostic importance of histologic cell type. Although the majority of studies do not appear to show any significant association between survival and cell type, it is noticeable that those studies that do show a difference tend to favor the squamous cell type [19, 20]. Finally, we also found visceral pleural involvement to be an adverse prognostic feature. The influence of visceral involvement, in common with most histologic characteristics in stage II disease, has been poorly investigated; however, the few studies that have examined this factor have also identified it as an important survival determinant [21, 22].

Although stage II disease is commonly regarded as representing an early stage of NSCLC, our 5-year survival rate was only 44%. This figure, while poor, is comparable with that of previous series, which have reported 5-year survival rates from 30% to 50% in this group of patients [11, 18]. It should also be noted that the majority of our patients (59%) underwent pneumonectomy. At first glance this figure appears quite high, but it should be noted that our pneumonectomy rate is similar to previous studies examining outcome in N1 disease [10, 23]. Although our unit's preference is to perform parenchyma-sparing procedures, in many of these cases the anatomical site of the tumor or the presence of extensive hilar lymph node involvement necessitated the performance of a pneumonectomy. Ironically, far from supporting our policy of performing parenchyma-sparing procedures, our results showed a trend toward improved outcome in patients who underwent pneumonectomy as opposed to lobectomy. This finding correlates with a recent study by Luzzi and colleagues [23] who found an association between improved survival and the performance of a pneumonectomy in cases with isolated hilar lymph node involvement.

Interestingly, these results are in direct contrast to some previously published data concerning stage I disease where the performance of a pneumonectomy was associated with an adverse long-term outcome [4]. Quite why the performance of a pneumonectomy appears to have a different prognostic significance in stage I and stage II disease is unclear. One possibility may be that in N1 disease pneumonectomy provides improved local clearance of tumor tissue, and this provides a survival benefit that outweighs any long-term survival detriment due to cardiopulmonary compromise associated with pneumonectomy. It should be noted that both our study and that of Luzzi and associates [23] only showed a trend, as opposed to a statistically significant association, between operative procedure and outcome, and a larger scale study is required in order to clarify the relationship between the type of surgical resection performed and outcome in N1 disease.

It is notable that within our cohort of patients, a variety of factors appeared to have no prognostic importance. In particular, we found no difference in the survival pattern of patients with T1 and T2 disease. Although this may be a reflection of the small number of patients with T1 disease in our study, it should be noted that once again there appears to be contradictory evidence as to the prognostic significance of T1 versus T2 disease [7, 10, 11]. Similarly, we observed no correlation between outcome and the pattern of lymph node involvement.

The prognostic significance of lymph node involvement is a controversial subject and has been examined by a number of groups with conflicting results. Martini and associates [9] and Asumara and associates [12] found no association between the site of lymph node involvement and survival. By contrast, Tanaka and associates [7] and Yoshino and associates [11] reported significantly poorer outcomes in patients with hilar as opposed to intralobar lymph node involvement. This issue has recently been revisited in a large-scale study by Marra and associates [9]. This group found that there was a statistically significant difference in the survival of patients with intralobar and extralobar involvement. Moreover, they also demonstrated that patients with direct infiltration of the lymph nodes, as opposed to true metastatic spread, had a significantly improved survival. Our results appear to contradict these findings, however. Not only were we unable to find any association between the site of lymph node metastases and long-term survival, we also found no survival benefit in patients with nodal involvement due to direct infiltration. In addition, the number of involved lymph nodes appears to have no prognostic significance in our series. Indeed, our study would support the concept of considering N1 lymph nodes as a homogenous group, and we would question the validity of considering hilar lymph node involvement as representing early N2 disease, as has been proposed by other authors [10, 12].

We accept that this study does suffer from a number of potential limitations. For a start, although we have attempted to perform a comprehensive evaluation of the significance of conventional histologic factors, we accept that there may well be additional histologic prognostic markers we have not accounted for. In addition, it may be argued that as we performed mediastinal lymph node sampling as opposed to a formal clearance, it is possible that our cohort contains some patients with undiagnosed N2 involvement. Given our use of preoperative sampling of enlarged mediastinal lymph nodes together with our policy of extensive intraoperative mediastinal lymph node sampling, however, we believe that this risk of pathologic understaging is minimal.

Another possible criticism of this study is our use of all-cause mortality as an outcome measure. Although it may be argued that we should have excluded noncancer related deaths, it should be noted that in the United Kingdom, a patient who has been diagnosed with lung cancer will have this disease listed on the death certificate irrespective of the actual cause of death. This makes the identification and exclusion of noncancer-related deaths virtually impossible. Moreover, such an attempt may itself introduce bias by excluding the contribution of an undiagnosed recurrent malignancy in an apparently noncancer-related death [24]. Finally, we accept that the size of our cohort, while comparable to most previous studies on this subject, is relatively small. Nonetheless, despite these provisos, we believe that the meticulous design of our study, and in particular our use of standardized preoperative, operative, and pathologic protocols, adds considerable weight to the validity of our findings.

In conclusion, we have shown that T1-2N1M0 nonsmall cell cancers of the lung have a diverse prognostic outcome after surgery. In contrast to previous studies, we found that nonsquamous histology; vascular invasion, and visceral pleural involvement were the only significant adverse histologic predictors of survival. Given the contradictory nature of the literature on the whole topic of survival determinants in stage II NSCLC, we believe this issue requires addressing in the form of a large-scale prospective study.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
References
 
The authors would like to thank Lynda Beggs for her assistance with data collation and analysis. In addition, we gratefully acknowledge the contribution of Fayek Salama in the management of these patients.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

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