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Ann Thorac Surg 2002;74:348-354
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Prognostic implications of microscopic proximal bronchial extension in non-small cell lung cancer

Murat Kara, MD*a, Erkan Dikmen, MDa, Dalokay Kiliç, MDb, Serpil Dizbay Sak, MDc, Diclehan Orhan, MDc, Serdal Kenan Köse, PhDd, Sevket Kavukçu, MDb

a Department of Thoracic Surgery, Kirikkale University School of Medicine, Kirikkale, Turkey
b Department of Thoracic Surgery, Ankara University School of Medicine, Ibn-i Sina Hospital, Sihhiye, Ankara, Turkey
c Department of Pathology, Ankara University School of Medicine, Sihhiye, Ankara, Turkey
d Department of Biostatistics, Ankara University School of Medicine, Sihhiye, Ankara, Turkey

Accepted for publication April 21, 2002.

* Address reprint requests to Dr Kara, Güvenlik Caddesi, Esenlik Sokak 7/10, TR-06540, Asagiayranci, Ankara, Turkey
e-mail: muratkara66{at}hotmail.com


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The loss of approximately one third of early stage lung cancer patients undergoing complete resection by the end of 5 years implies the existence of unknown or undetected factors at the time of operation. We investigated the possible correlation between microscopic proximal bronchial extension (MPBE) and survival with clinicopathologic features in patients with non-small cell lung cancer.

Methods. The bronchial tree with the tumor was dissected and extracted from the lung parenchyma in a total of 62 surgical specimens with non-small cell lung cancer. The tumor-related bronchus was sectioned into serial blocks at a thickness of 5 mm in the transverse plane. Histologically, cut serial sections were examined for MPBE.

Results. A total of 15 (24.2%) specimens showed MPBE, whereas 47 (75.8%) specimens showed no evidence of MPBE. The median survival time of MPBE-positive patients was 10.0 months, whereas that of MPBE-negative patients was 42.0 months. The 5-year survival rates of MPBE-positive and MPBE-negative groups were 13.3% and 35.8%, respectively, which was a significant difference (p = 0.0203). Multivariate analysis revealed lymph node status (p = 0.0161), histology (p = 0.0268), and MPBE-positivity (p = 0.0447) as independent prognostic factors.

Conclusions. Microscopic proximal bronchial extension has an adverse effect on survival in non-small cell lung cancer.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Operation still remains the optimal treatment in patients with non-small cell lung cancer (NSCLC). Complete removal of the tumor with regional and mediastinal lymph nodes is mandatory for a complete resection. Nevertheless, the 5-year survival rate of patients with early stage lung cancer never reaches up to 90% to 100% even in case of a complete resection. Thus, investigators have conducted studies on the invisible factors at the time of operation that might have an adverse effect on survival. Numerous factors including the overexpression of different biologic markers [1, 2] and microscopic metastatic sites undetectable with conventional staging procedures have been claimed to contribute to the loss of these patients [3, 4]. It is very likely that if these factors were more apparent, the selection criteria for operation will be more accurate, and the value of resection in the treatment of lung cancer will increase.

Pioneering work on the bronchial safety margin concluded that 1.9 cm (0.75 inches) of apparently normal bronchus from the macroscopic tumor should be resected to achieve a tumor-negative bronchial resection margin (BRM) [5, 6]. However, clinicopathologic features of lung cancer, particularly the incidence of histologic subtypes, has been changing since these earlier studies. Thus, we recently conducted a study to reveal the current bronchial safety margin in which we investigated the microscopic proximal bronchial extension (MPBE) in a series of 70 patients with NSCLC [7]. Furthermore, we made a clarification of MPBE with special reference to tumor localization [8]. In this study, we further investigated the prognostic implications of MPBE to outline its role on survival, and analyzed the correlation between MPBE and clinicopathologic features.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 Acknowledgments
 References
 
We examined surgical specimens of 70 consecutive patients with NSCLC who underwent curative resection of the primary tumor with systematic lymph node dissection in bn-i Sina Hospital of Ankara University School of Medicine between September 1994 and July 1996. All patients apart from one were male, with a mean age of 55.7 ± 9.4 years (range, 35 to 76 years). Preoperatively, patients underwent a metastatic workup including bone scan, cranial-abdominal computed tomography, or abdominal ultrasonography.

Specimens of wedge bronchoplasties, postmortem materials, and those with tumor-positive BRM were excluded from the analyses, whereas 11 (17.7%) specimens of bronchial sleeve resections were included. Likewise, specimens showing extracapsular lymph node involvement at more proximal levels rather than BRM were excluded to avoid false-positive results. We also excluded patients who died within the first postoperative 30 days or of non-cancer-related causes. Two patients, who died in the early postoperative period, and another patient, who underwent a right upper sleeve lobectomy and showed a tumor-positive BRM, were excluded from the study. In addition, we excluded 5 patients who were lost to follow-up or died of non-cancer-related diseases. Conclusively, a total of 62 patients who met the research criteria were enrolled into this study. Seven (11.2%) lower lobectomies in the right hemithorax and 13 (20.9%) upper lobectomies in the left hemithorax accounted for the majority of the operative procedures on each side (Table 1). The histologic subtype was squamous cell carcinoma in 33 patients (53.2%), adenocarcinoma in 22 patients (35.5%), adenosquamous carcinoma in 4 patients (6.5%), and large cell carcinoma in 3 patients (4.8%).


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  		Table 1. Analysis of Operative Procedures (n = 62)

 
Of 19 patients (30.6%), in whom the BRM was examined with frozen sections, 10 (16.1%) showed tumor-positivity. Seven patients (11.2%) underwent reamputation of the bronchus, 2 patients (3.2%) had a sleeve lobectomy, and 1 patient (1.6%) had a tracheal sleeve pneumonectomy. Reamputated bronchi were always evaluated with the entire bronchial tree.

Technique
The tumor-related bronchus was sectioned into serial blocks at a thickness of 5 mm in the transverse plane after its dissection and removal from the pulmonary parenchyma with the tumor. Reference level for sectioning was regarded as the conjunction of the macroscopic tumor and apparently normal bronchus, and called "0 cm." We obtained ring-shaped cut serial sections; 5 mm apart from each other, beginning from the reference level toward the BRM, ranging from 1 to 9 (average, 5) in number for each specimen. Histologically, cut serial sections were examined by two pathologists for the most proximal microscopic tumor extension toward the BRM. Counterstaining was performed with hematoxylin and eosin. Histochemical and immunohistochemical staining was performed for tumor typing if necessary.

Data collection and follow-up
We retrospectively reviewed the data charts and survival of these patients. Follow-up data were obtained with the information of referring physicians and telephone calls, or direct clinical examination. Follow-up data were complete in all patients. The mean follow-up was 37.0 ± 26.9 months (range, 2 to 84 months).

Definitions and statistical analysis
The macroscopic extension pattern was related to the most proximal edge of the visible tumor, and this was regarded as reference level for sectioning as described previously [7, 8]. This feature was classified as peribronchial or endobronchial. Microscopic extension of the tumor at any cut serial section other than reference level was defined as MPBE, and MPBE patterns were grouped as endobronchial and peribronchial, the former including submucosal lymphatic invasion. The tumors were classified as central or peripheral according to the localization. Central tumors represented those developed in a main lobar or segmental bronchus, and peripheral tumors those which arose from subsegmental or more distal bronchi. Tumors were histologically classified according to the 1999 WHO/IASLC classification of lung and pleural tumors [9]. Staging was postoperative and performed according to the current International Staging System for Lung Cancer [10].

Statistical comparisons of baseline data between groups were performed by the {chi}2 and Fisher’s exact tests as appropriate. Age, operative procedure, resection type, tumor localization, tumor size, lymph node status, macroscopic and microscopic extension patterns, the length of MPBE, histology, and differentiation were included in the assessment of statistical comparisons with MPBE. Age and the length of MPBE were classified as a high- or low-group relative to the median value. Data were expressed as mean ± the standard deviation. The cumulative survival rates were calculated by the Kaplan-Meier method, and the significance was determined by the log-rank test. The Cox proportional hazard regression model was applied for univariate and multivariate analysis along with a forward procedure to confirm the prognostic impact of the factors on survival. A p value of less than 0.05 was considered statistically significant. All statistical analyses were performed with the Statistical Package for the Social Sciences (SPSS, version 8.0, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 Acknowledgments
 References
 
Fifteen (24.2%; Table 2) specimens showed MPBE, whereas 47 (75.8%) specimens showed no evidence of MPBE. Microscopic proximal bronchial extension did not show any significant association with age, operative procedure, tumor localization, tumor size, macroscopic extension pattern, histology, and differentiation. However, patients who underwent a sleeve resection had a significantly greater rate of MPBE-positivity (55%), compared with that of patients who underwent a standard resection (18%; p = 0.010). Microscopic proximal bronchial extension positivity also significantly correlated with lymph node status (p = 0.015). The rate of MPBE-positivity in tumors with N0, N1, and N2 lymph node status were 11%, 36%, and 47%, respectively (Table 3). No significant difference was observed between the tumor stage and MPBE-positivity (p = 0.055), MPBE pattern (p = 0.164), and subgroups stratified by the length of MPBE (p = 0.223, data not shown).


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  		Table 2. Characteristics of Microscopic Proximal Bronchial Extension Positive Cases (n = 15)

 

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  		Table 3. Relationship of Clinicopathologic Features and Microscopic Proximal Bronchial Extension With Prognostic Values in Subgroups of Variables

 
The median survival time of MPBE-positive patients was 10.0 months, whereas that of MPBE-negative patients was 42.0 months. The 5-year survival rates of MPBE-positive and MPBE-negative groups were 13.3% and 35.8%, respectively, which was a significant difference (p = 0.0203; Fig 1). Comparison of 5-year survival rates in each subgroup stratified by MPBE revealed that MPBE had a statistically significant effect in subgroups defined by operative procedure (pneumonectomy), resection type (standard), tumor localization (peripheral), tumor size (T2), macroscopic extension pattern (peribronchial), histology (adenocarcinoma), and differentiation (well) (Table 3).



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  		Fig 1. Cumulative survival curves on the basis of microscopic proximal bronchial extension (MPBE) in 62 patients with non-small cell lung cancer.

 
Among the 15 patients showing MPBE, 9 (60%) had peribronchial extension, whereas 6 (40%) had endobronchial extension. The 5-year survival rates of patients with tumors showing peribronchial MPBE was 11.1%, and that of patients with tumors having endobronchial MPBE was 16.6%, which was not significantly different (p = 0.7642; Fig 2). The median length of MPBE was 10 mm. The length of MPBE was equal or more than 10 mm in 9 (60%) specimens, and it was less than 10 mm in 6 (40%) specimens. The 5-year survival rate of the latter group was 33.3%, whereas none of the patients in the former group survived by the end of 5 years (p = 0.0226; Fig 3) (Table 3).



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  		Fig 2. Cumulative survival curves according to microscopic proximal bronchial extension (MPBE) patterns.

 


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  		Fig 3. Cumulative survival curves with regard to the length of microscopic proximal bronchial extension (MPBE).

 
In univariate analysis, age (> 57 years; p = 0.0884), pneumonectomy as an operative procedure (p = 0.0701), and T2 tumor status (p = 0.0841) showed a strong but nonsignificant trend toward poor survival, whereas N1+N2 nodal involvement as lymph node status (p = 0.0171), adenocarcinoma as histologic subtype (p = 0.0189), and MPBE-positivity (p = 0.0197) were significantly associated with poor survival (Table 4).


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  		Table 4. Univariate Prognostic Factors Analysis of the 62 Patients by Cox Proportional-Hazards Regression Model

 
The multivariate analysis revealed lymph node status (p = 0.0161), histology (p = 0.0268), and MPBE-positivity (p = 0.0447) retained an independent prognostic impact on overall survival (Table 5), whereas T2 tumor status (p = 0.0529) appeared as a strong but nonsignificant prognostic factor.


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  		Table 5. Multivariate Analysis of Prognostic Factors by Cox Proportional-Hazards Regression Model

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
Acknowledgments
 References
 
Although pathologic tumor stage is the only well-established prognostic indicator in NSCLC, thoracic surgeons may encounter different outcomes in patients having the same tumor stage, same tumor histology, and undergoing the same operative procedure. Among the numerous factors participating in prognostic variability, one is shown to be the insufficient sensitivity of conventional histologic techniques for lymph node examination [11, 12]. Furthermore, tumor characteristics such as tumor necrosis, microscopic vascular or lymphatic vessel invasion, and pleural invasion have been investigated for a possible effect on survival. However, we are not aware of any study questioning the effect of MPBE on survival in NSCLC.

The initial studies on the bronchial safety margin concluded that at least 0.75 inches (1.9 cm) of apparently normal bronchial tissue should be provided to eliminate the risk of residual microscopic tumor at the BRM [5, 6]. These results constituted a basis for the international TNM staging of lung tumors. However, clinicopathologic features of NSCLC have been changing in the meantime. Recently, we conducted a survey to outline the current safe BRMs in patients with NSCLC undergoing pulmonary resection. We found that a bronchial resection of 1.5 cm in length from the visible proximal edge of the tumor would be adequate for a tumor-negative BRM in 93% of NSCLC cases [7]. We also outlined that the length of MPBE in peripheral tumors, which was composed of mainly adenocarcinomas, was significantly greater than that of central tumors [8]. In this study, we compared the survival rate of patients showing MPBE with that of patients not showing MPBE to clarify the impact of this feature in NSCLC in the same series.

When we analyzed the correlation between MPBE and clinicopathologic features, we found a significantly greater rate of MPBE in patients who underwent a sleeve resection. Consistent with this finding, an increased risk of microscopic residual tumor at the BRM with an incidence of 6.9% to 13% has been shown in patients undergoing bronchial sleeve lobectomy [13, 14]. Likewise, tracheal sleeve pneumonectomy has been advocated to have a similar risk [15]. Although it was stated that a bronchial tissue section of at least 1 to 2 cm from the edge of the visible carcinoma is sufficient to maintain tumor-free BRM for bronchial sleeve resections [16], we believe that a careful examination of intraoperative frozen sections is necessary considering the high incidence of microscopic residual tumor. We also found that MPBE occurred frequently with nodal involvement, which might imply the aggressive behavior of the tumors showing MPBE.

The high incidence of MPBE in sleeve resections may at least, in part, be attributed to the advanced tumor stage in these cases, which may be associated with an increased rate of peribronchial tumor extension. As an MPBE pattern, peribronchial tumor extension occurs more than other patterns such as mucosal or submucosal extension [5–7, 17, 18]. Although residual carcinoma in situ does not affect survival per se, peribronchial extension has been shown to have an unfavorable prognostic impact on survival [19–21]. However, our results showed no significant different survival rates between the MPBE patterns.

Tumor positivity detected at the BRM either intraoperatively or postoperatively is a clinical problem in thoracic surgical procedures, and controversy exists about the fate of these patients. Although initial studies have underscored the significance of a tumor-positive BRM [22, 23], recent research showed that tumor positivity at the BRM had a negative impact both on local control of disease and on survival [17–19]. In this study, we found a significantly worse overall survival in patients showing MPBE. Microscopic proximal bronchial extension positivity had a negative impact on overall survival in the subgroups defined by standard resection as resection type, pneumonectomy as operative procedure, peripheral localization as tumor site, T2 tumor status, peribronchial extension as macroscopic extension pattern, and adenocarcinoma as histologic subtype. On analyzing the variables with multivariate analysis, we detected that adenocarcinoma as a histologic subtype, N1+N2 involvement as nodal status, and MPBE-positivity had a significantly adverse effect on survival. Unfortunately, the technical difficulty of dissecting the tumor with the related bronchus in each case makes the use of MPBE inappropriate as a prognostic factor in NSCLC in a routine surgical pathology practice.

The risk of tumor invasion [24] and tumor recurrence at the BRM [25] were found to be associated with the distance between proximal tumor and the BRM. Similarly, we observed a significant difference between the survival rates of subgroups defined by the length of MPBE in our series, which comprised patients with tumor-free BRM. Our results revealed an overall worse survival in patients showing a longer MPBE. A longer MPBE may simply be a consequence of a more invasive tumor that is destined for poor prognosis. However, it is tempting to speculate that there may remain a few undetected tumor cells by conventional histologic examinations at BRM in patients with MPBE that may be responsible for poor prognosis.

In conclusion, MPBE may contribute to the aggressive behavior of the tumor and a worse overall survival in patients with NSCLC.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
References
 
We thank Professor Yoh Watanabe from Kanazawa Medical University, Japan, for his valuable comments and critical review of the manuscript.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

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