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Ann Thorac Surg 1996;62:1489-1493
© 1996 The Society of Thoracic Surgeons

Original Article: General Thoracic

Blood Vessel Invasion Is a Major Prognostic Factor in Resected Non–Small Cell Lung Cancer

Romain Kessler, MD, Bernard Gasser, MD, Gilbert Massard, MD, Norbert Roeslin, MD, Pierre Meyer, MD, Jean-Marie Wihlm, MD, Georges Morand, MD

Services de Chirurgie Thoracique and d'Anatomie Pathologique, and Département d'Information Médicale, Hôpitaux Universitaires, Strasbourg, France

Accepted for publication June 9, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. We examined the prognostic value of histologic indices in non–small cell lung cancer with particular interest in major blood vessel invasion.

Methods. We studied 593 patients who had curative resection between November 1983 and December 1988. We determined the histology, T and N status, peritumoral lung tissue invasion, tumor stroma, necrosis, mitotic rate, and blood vessel invasion.

Results. The median patient survival of the whole series was 3.2 years, with a 5-year survival of 38.9%. In univariate analysis, a high T stage, a high percentage of necrosis, blood vessel invasion, and N stage significantly worsened the survival. In multivariate analysis, only blood vessel invasion and, less significantly, T stage and lymph node metastasis remained independent prognostic factors.

Conclusions. These results highlight the negative prognostic value of blood vessel invasion in non–small cell lung cancer and suggest that blood vessel invasion, T stage, and node metastasis are three unrelated and distinctive characteristics of resected non–small cell lung cancer.


   Introduction
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 Introduction
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The TNM stage-based on pathologic extent of the primary tumor (T), the regional lymph nodes (N), and presence or absence of distant metastases (M)-is the most important prognostic factor in non–small cell lung cancer (NSCLC). Prognostic factors in patients who have undergone resection may identify groups with poor survival who could benefit from combination therapy (adjuvant chemotherapy or radiotherapy). In clinical trials, the knowledge of factors related to prognosis is essential to avoid biases in selecting control and treatment groups. Finally, prognostic factors may provide insight into carcinogenesis, which could lead to the development of new strategies of treatment [1].

Among the numerous prognostic factors that have been identified in NSCLC, pathologic factors have been little studied except for T and N categories. However, the pathologic features of the primary tumor are the global result of multiple steps on the biologic and cellular level in tumoral growth. Major blood vessel invasion (BVI), for example, needs tumoral growth around the vessels, destruction of vascular walls, and propagation of the tumor into the vascular lumen. Many biologic factors may act during these sequences; for example, metalloproteinases may destroy vascular walls. Surprisingly, large BVI has been studied extensively in only a few cancers [2], but its high prognostic value has been clearly demonstrated. Blood vessel invasion had been studied only in small series of NSCLC and in selected subgroups of patients [3–5] until the recently published work of Ichinose and colleagues [6].

The aim of our work was to establish the validity of pathologic prognostic factors, including large BVI, necrosis, peritumoral lung tissue invasion, tumor stroma formation, and mitotic rate, in a large series of resected NSCLC. We studied the prognostic value of these factors in relation to the N stage.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
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 Acknowledgments
 References
 
Patients
Between November 1, 1983, and December 1, 1988, a series of 593 consecutive patients underwent macroscopically complete resection of NSCLC. Characteristics of the patients are listed in Table 1Go. Patients with metastatic pleural effusion, N3 disease, massive N2 disease on chest computed tomography, or distant metastasis were excluded from the study. Patients who did not survive the operative period (<1 month) were excluded from the survival analysis.


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  		Table 1. . Demographics and Treatment Modalities in Patients With Resected Non–Small Cell Lung Cancer
 
Preoperative assessment of the patients included chest roentgenography, computed tomography of the chest, bronchoscopy, and abdominal echography. Bone scans were performed in cases in which bone pain was present. Pulmonary function tests, arterial blood gases, and lung perfusion scans permitted evaluation of pulmonary reserve. Resection consisted of lobectomy, bilobectomy, or pneumonectomy. Routine sampling of lymph nodes from the lung hilum and subcarinal and paratracheal sites was performed without exception. The American Thoracic Society node mapping was used to classify nodal metastasis [7]. All operative specimens were analyzed and conventional pathologic features were recorded, including tumor stage, nodal stage, and histology according to the World Health Organization classification [8]. The staging of all patients was reported according to the New International Staging for Lung Cancer [9]. Mediastinoscopy was performed only in doubtful cases.

Postoperative adjuvant chemotherapy (six courses of cisplatinum-based regimens) was administered to 35 patients with N2 disease as part of a therapeutic trial. These patients were not excluded from the study because there was no difference in survival between patients receiving chemotherapy and control patients. Postoperative adjuvant radiotherapy was given to 180 patients with N2 disease or with direct tumor extension to the parietal pleura or to the chest wall. It has been shown that adjuvant radiotherapy is effective in preventing local relapses but has no impact on survival [10]. Therefore, these adjuvant treatment modalities should not have influenced our survival analysis.

Pathologic Studies
Macroscopic tumor features were recorded. Conventional light microscopic examination was used to assess the pattern of lung invasion (irregular infiltration or pushing borders), the presence or absence of a tumor stroma, the percentage of necrosis, and the presence or absence of peritumoral or intratumoral BVI [11]. It must be emphasized that we only considered invasion of either the main venous or arterial parabronchial vessels. Tumor sampling was performed perpendicular to the bronchial axis to investigate both the bronchial lumen and the adjacent vessels. At least two sections were needed to specify the relation between the tumor and the parabronchial vessels. Slides were stained with hematoxylin and eosin and, in about 30% of the cases, with elastic van Gieson to permit visualization of the blood vessel lamina in cases of diagnostic doubt about histology. Blood vessel invasion was defined as the presence of neoplastic structures inside the lumen of a vessel with either a totally or a partially recognizable wall. Vascular invasion was recorded as absent when tumor was seen in poorly preserved elastic-walled structures or in the case of medial invasion without intraluminal extension. Blood vessel invasion was nearly always characterized by neoplastic cells embedded in organized vascular thrombosis. In cases of intratumoral vascular thrombosis without evidence of neoplastic cells, serial sections were analyzed to assess a possible neoplastic vascular invasion. In contrast, the presence of a few neoplastic cells in the vascular lumen without thrombosis, which could have represented artifacts of sampling, was not considered BVI until serial sections had demonstrated either vascular wall infiltration or thrombosis. According to these criteria of BVI, the mean external diameter of the concerned vessels was 2 mm (range, 0.4 to 4 mm). The mitotic rate was assessed at 400x objective magnification and was defined as the number of mitoses per 10 high-power fields (area of the microscopic field, 0.196 mm2).

Statistical Analysis
The length of survival was calculated from the date of operation until the date of death or last follow-up. Deaths related to causes other than NSCLC were not excluded from the analysis. The final checkup was done between January 1, 1994 and June 30, 1994, at least 5 years after the inclusion of the last patient. Only 3 patients were lost to follow-up. Most patients were followed up in our outpatient clinic at 3- to 4-month intervals. When patients were surveyed in other centers, medical records were obtained and, if necessary, the primary care physician was contacted by telephone.

Statistical analysis was done with SPSS software (SPSS, Chicago, IL). Survival was estimated by the method of Kaplan and Meier [12]. Univariate analysis was performed using the log-rank test. The Cox proportional hazards stepwise model [13] was used for multivariate analysis. Numbers are expressed as the mean ± standard error of the mean.


   Results
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Histology and TN Staging of Resected Non–Small Cell Lung Cancer
Table 2Go shows the pathologic characteristics of the resected NSCLC. The most prevalent histologic type was squamous cell carcinoma (66.5%). Staging showed that 88% of the patients belonged to the T1 or T2 subgroup, and 54% had no nodal involvement. Consequently, stages I and II included more than 70% of the patients. The median survival of the whole series of patients was 3.2 years, with a 5-year survival of 38.9% (Table 3Go). Comparisons of age (> or <60 years), sex, preoperative weight (body mass index < or >24), or smoking (nonsmokers versus smokers) showed no differences in survival. Similarly, the different histologic types or the degree of differentiation for squamous cell carcinoma had no significant influence on survival. In contrast, lymph node metastasis worsened survival dramatically, as shown in Table 3Go. We separated N1 patients into two subgroups [7]: lobar N1 (groups 12, 13, and 14 nodes) and hilar N1 (group 11 nodes). We observed that survival rates of the N1 hilar subgroup were similar to those of N2 patients. Indeed, the median survival times in these two subgroups were similar (671 ± 121 days in hilar N1 versus 468 ± 55 days in N2; p = 0.33).


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  		Table 2. . Histology and Staging of Resected Non–Small Cell Lung Cancer
 

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  		Table 3. . Survival After Resection in Non–Small Cell Lung Cancer by N Status
 
Prognostic Value of Histologic Features of Resected Non–Small Cell Lung Cancer
The pathologic features of the primary tumor are as follows. Lung tissue was usually infiltrated rather than pushed by the tumor (71% versus 29%). The presence of a tumor stroma and BVI were common features (73% and 48%, respectively). The median value for the mitotic rate was 16 per 10 high-power fields (mean ± standard error of the mean, 25.7 ± 1.26). Necrosis occupied a median of 5% of the tumor (mean ± standard error of the mean, 15.7% ± 0.9%). Univariate analysis (Table 4Go) demonstrated that an infiltrating margin (p = 0.0007), the presence of BVI, and T and N stages were significant prognostic factors (p = 0.0001). At a lesser significance (p = 0.0016), a higher percentage of necrosis predicted a poor survival. Finally, multivariate survival analysis (Table 5Go) identified three independent factors significantly related to survival: N status (p = 0.0001), BVI (p = 0.0001), and, of lesser significance (p = 0.002), the T stage.


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  		Table 4. . Univariate Survival Analysis of Resected Non–Small Cell Lung Cancer
 

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  		Table 5. . Multivariate Survival Analysis of Resected Non–Small Cell Lung Cancera
 
Prognostic Value of Blood Vessel Invasion
The median survival of patients without BVI was 1,816 ± 176 days, versus 713 ± 56 days in patients with BVI (Fig 1Go). The highest difference between survival curves of resected NSCLC with positive BVI versus negative BVI was observed in N2 patients (p = 0.0007), whereas the lowest difference was seen in N0 patients (p = 0.0206). An intermediate result was noted in N1 patients (p = 0.0066) (Fig 2Go).



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  		Fig 1. . Survival curves after resection of non–small cell lung cancer according to blood vessel invasion (BVI). The number of patients in each subgroup is indicated in parentheses. The statistical significance between curves was calculated by log-rank test.

 


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  		Fig 2. . Survival curves after resection of non–small cell lung cancer according to blood vessel invasion (BVI) in each N subgroup. The number of patients in each subgroup is indicated in parentheses. The statistical significance between curves was calculated by log-rank test.

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Our study showed that BVI is an important prognostic factor in resected NSCLC. Blood vessel invasion is one of the steps leading to metastasis: It is known that during the early stages of tumor growth, angiogenesis is required to permit further expansion of the tumor. New intratumoral capillaries are generated from preexisting vessels. Tumor cells may then penetrate these vessels and escape from the primary site to distant organs. This relation between intravascular tumor cells, tumor vessels, and metastasis was studied in animal models [14] many years ago. For many of these premetastatic steps, the need for soluble factors such as chemotactic factors, angiogenic factors, or proteases has been questioned. As early as 1958, Collier and co-workers [3] demonstrated the prognostic role of BVI in lung cancer. The 5-year survival in their BVI-positive patients (n = 65) was 6%, versus 72% in the BVI-negative patients (n = 28). Conversely, in the series presented by Lipford and colleagues [4], arterial invasion (which was not clearly defined) was not a significant prognostic factor. This was a retrospective analysis, and the method of pathologic studies was not provided. In a recent published series, Ichinose and associates [6] distinguished among arterial, venous, and lymphatic vessel invasion. In stages I and IIIA, they found that venous invasion was a predominant prognostic factor, and in stage IIIA, confirming our own results, only two independent factors were retained by multivariate analysis: N stage and venous invasion. Unfortunately, Ichinose and associates [6] did not describe how they identified the different vascular structures. Macchiarini and colleagues [5] demonstrated that BVI was a predictor of poor survival in limited subgroups of NSCLC patients (T1-2, N0). They showed that a minority of these tumors had probably already entered the metastatic phase. In 83% of the patients who died because of metastases, the tumor demonstrated BVI at the time of operation. The team of Macchiarini and colleagues also studied other vascular manifestations of lung cancer, such as neovascularization using a microvessel counting and grading technique. They reported that angiogenesis was an indicator of metastasis [15] and correlated well with a poor disease-free interval [16]. They observed that in tumors with a high degree of angiogenesis, BVI was also significantly more frequent. In patients in whom the tumor showed a high degree of angiogenesis, the relative risk of metastasis was 5.6 (95% confidence interval, 1.6 to 20.2). Ogawa and associates [17] examined a series of stage I NSCLC with respect to BVI and also to the immunohistochemical expression of Sialyl-Lewis*, a carbohydrate ligand that is recognized by an E-selectin receptor on endothelial cells, as well as to proliferating cell nuclear antigen. They demonstrated that both BVI and Sialyl-Lewis* expression were determining factors in cancer recurrence. As a general rule, the interactions between tumor cells and vessel walls are important factors in metastases [18].

Information about BVI should be added to pathologic reports. Nevertheless, we must emphasize the possibility of interobserver variation, especially in assessing vascular invasion of small blood vessels. Therefore, some authors have advocated either elastic fiber staining or staining techniques using factor VIII or blood group antigens [2]. In our study, we chose to consider only vascular invasion of major, easily identifiable peribronchial vascular channels. The disadvantage of our option was to ignore some cases with BVI (false negatives).

The mechanism of tumor necrosis may occur in poorly vascularized tumors. In the literature, this factor was not found to be prognostic [4].

As in other studies, the mitotic rate was not independently related to survival. This factor, like other factors assessing the proliferative activity of NSCLC (bromodeoxyuridine labeling index, proliferating antigen Ki67), seems better correlated with the time of recurrence [15, 16]. In addition, the presence of a tumor stroma was not a significant factor for survival. However, Nagy and colleagues [19] showed that stroma generation is favored by leaky blood vessels, which might also support BVI.

In conclusion, we assessed the prognostic value of pathologic features related to the primary tumor in resected NSCLC in a large series of patients. The presence of major BVI in the primary tumor is associated with an unfavorable prognosis. In our resected NSCLC cases, BVI appeared to be the second factor independently related to prognosis, after the N stage and before the T stage. Our results suggest that BVI and nodal propagation are two distinctive characteristics of the aggressive behavior of NSCLC.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Mrs Ruth Hoekstra for her assistance in preparing the manuscript.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Kessler, Service de Chirurgie Thoracique, Hôpitaux Universitaires, 67000 Strasbourg, France.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Levine MN, Browman GP, Gent M, Roberts R, Goodyear M. When is a prognostic factor useful? A guide for the perplexed. J Clin Oncol 1991;9:348–56.[Abstract]
  2. Lee AK, DeLellis RA, Silvermann ML, Heatley GJ, Wolfe HJ. Prognostic significance of peritumoral lymphatic and blood vessel invasion in node-negative carcinoma of the breast. J Clin Oncol 1990;8:1457–65.[Abstract]
  3. Collier FC, Enterline HT, Kyle RH, Tristan TT, Greening R. The prognostic implications of vascular invasion in primary carcinomas of the lung: a clinico-pathologic correlation of two-hundred twenty-five cases with 100% follow-up. Arch Pathol 1958;66:594–9.
  4. Lipford EH, Eggleston JC, Lillemoe KD, Sears DL, Moore GW, Baker RB. Prognostic factors in surgically resected limited-stage, nonsmall cell carcinoma of the lung. Am J Surg Pathol 1984;8:357–65.[Medline]
  5. Macchiarini P, Fontanini G, Hardin JM, Pingitore R, Angeletti CA Most peripheral, node-negative, non–small-cell lung cancers have low proliferative rates and no intratumoral and peritumoral blood and lymphatic vessel invasion. J Thorac Cardiovasc Surg 1992;104:892–9.[Abstract]
  6. Ichinose Y, Yano T, Asoh H, Yokoyama H, Yoshino I, Katsudo Y. Prognostic factors obtained by a pathologic examination in completely resected non–small-cell lung cancer. An analysis in each pathologic stage. J Thorac Cardiovasc Surg 1995;110:601–5.[Abstract/Free Full Text]
  7. American Thoracic Society, Medical Section of the American Lung Association. Clinical staging of primary lung cancer. Am Rev Respir Dis 1983;127:659–64.[Medline]
  8. The World Health Organization histological typing of lung tumors (ed 2). Am J Clin Pathol 1982;77:123–36.[Medline]
  9. Mountain CF. A new international staging system for lung cancer. Chest 1986;89:225S–33S.[Free Full Text]
  10. Murren JR, Buzaid AC. Chemotherapy and radiation for the treatment of non–small-cell lung cancer. A critical review. In: Matthay RA, ed. Lung cancer. Clinics in chest medicine. Philadelphia: Saunders, 1993:161–71.
  11. Weigand RA, Isenberg WM, Russo J, Brennan MJ, Rich MA, and the Breast Cancer Prognostic Study Associates. Blood vessel invasion and axillary lymph nodes as prognostic indicators for human breast cancer. Cancer 1982;50:962–9.[Medline]
  12. Kaplan EL, Meier P. Non-parametric estimation from incomplete observations. J Am Stat Assoc 1958;53:457–81.
  13. Cox DR. Regression models and life tables. J R Stat Soc 1972;34:187–220.
  14. Liotta L, Kleinerman J, Saidel G. Quantitative relationships of intravascular tumor cells, tumor vessels and pulmonary metastasis following tumor implantation. Cancer Res 1974;34:997–1004.[Abstract/Free Full Text]
  15. Macchiarini P, Fontanini G, Hardin MJ, Squartini F, Angeletti CA. Relation of neovascularisation to metastasis of non-small-cell lung cancer. Lancet 1992;340:145–6.[Medline]
  16. Macchiarini P, Fontanini G, Dulmet E, et al. Angiogenesis: an indicator of metastasis in non–small cell lung cancer invading the thoracic inlet. Ann Thorac Surg 1994;57:1534–9.[Abstract]
  17. Ogawa J, Tsurumi T, Yamada S, Koide S, Shohtsu A. Blood vessel invasion and expression of sialyl Lewis* and proliferating cell nuclear antigen in stage I non-small cell lung cancer. Cancer 1994;73:1177–83.[Medline]
  18. Poggi A, Stella M, Donati MB. The importance of blood cell-vessel wall interactions in tumour metastasis. Bailliere Clin Haematol 1993;6:731–53.[Medline]
  19. Nagy JA, Brown LF, Senger DR, et al. Pathogenesis of tumor stroma generation: a critical role for leaky blood vessels and fibrin deposition. Biochim Biophys Acta 1989;948:305–26.[Medline]



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