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Ann Thorac Surg 2001;71:1088-1093
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Visceral pleura invasion by non-small cell lung cancer: an underrated bad prognostic factor

^a Département de Santé Publique, Hôpital Fernand Widal, Paris, France
^b Service de Chirurgie Thoracique Hôpital Laennec, Paris, France
^c Informatique Medicale et Biostatistique, Hôpital Necker-Enfants Malades, Paris, France
^d Centre Chirurgical du Cédre, Boisguillaume, France
^e Laboratoire d’Anatomie Pathologique, Hôpital Laennec, Paris, France

Accepted for publication October 18, 2000.

Address reprint requests to Dr Riquet, Service de Chirurgie Thoracique, Hôpital Européen Georges Pompidou, 20-40 rue Leblanc, 75908 Paris Cedex 15, France
e-mail: marc.riquet{at}hop.egp.ap-hop-paris.fr

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Visceral pleura invasion (VPI) by non-small cell lung cancer is a factor of poor prognosis. A tumor of any size that invades the visceral pleura is classified as T2. Few studies have been conducted concerning the prognostic significance of VPI relative to other staging factors.

Methods. Between April 1984 and December 1996, 1,281 patients with T1 (n = 430) and T2 (n = 851) non-small cell lung cancer underwent curative surgical resection. Adjuvant radiation therapy was performed in 455 patients. There were 176 women and 1,105 men aged 30 to 86 years (mean, 60.9 years). Five hundred nineteen pneumonectomies, 742 lobectomies, and 20 segmentectomies were performed. In all patients, a complete mediastinal lymph node dissection was performed. International staging was stage IA and B (n = 697); stage II A and B (n = 247), and stage III A (n = 337). The patients were divided into two groups according to the existence of VPI (group I without, group II with). Both groups were compared with regard to the size of the tumors, histology, associated lymph node involvement, survival rates, and cause of death. Univariate and multivariate analyses were conducted.

Results. VPI (group II) was identified in 19.1% of the resected specimens: group I, n = 1036; group II, n = 245. The VPI was present in only 10% of non-small cell lung cancer 3 cm or less in size, reaching 33% of patients with non-small cell lung cancer larger than 5 cm (p = 0.0001). Squamous non-small cell lung cancer were significantly less accompanied by VPI (13.5%) than the other histologic categories. The VPI was associated with a higher frequency of N2 involvement (group I = 24.6%, group II = 33.4%, p = 0.01) and N2 involvement was more extensive (two or more N2 involved stations: group I = 8.2%, group II = 15.6%, p = 0.003). Actuarial survival rates were 51.8% at 5 years and 33.8% at 10 years in group I (median, 66 months), and 34.6% at 5 years and 27.9% at 10 years in group II (median, 30 months) (p = 0.000002). Long-term survival rates significantly decreased for larger tumors. Even in patients with N2 stage tumors, the difference of survival curves between the two groups was statistically significant. Cancer-related deaths were more frequent in group II and were mainly caused by distant metastases. By multivariate analysis, visceral pleura invasion proved to be a significant independent factor of poor prognosis.

Conclusions. The VPI is a factor of poor prognosis. Its frequent association with extensive N2 involvement supports the hypothesis that exfoliated tumor cells are drained through the pleural lymphatics by the mediastinal lymphatic pathways and then into the bloodstream. The VPI is an important prognostic factor and, as such should stimulate more studies to better select the patients who could benefit from adjuvant therapy.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Pleural invasion by lung tumor was recognized as early as 1958 by Brewer and colleagues [1] to be a factor of poor prognosis in lung cancer. Besides invasion of the chest wall or mediastinal pleura, visceral pleural invasion (VPI) appeared in the mid 1970s as a specific entity in the TNM classification that has remained unchanged until now: a tumor of any size that invades the visceral pleura is classified as T2 [2]. In 1995, Ichinose and associates [3] confirmed VPI to be a predominant prognostic factor in stages I and II. In 1997, Mountain [2] revised the TNM classification dividing stage I into stage I A (T1N0 M0) and stage IB (T2N0 M0) stage II into stage II A (T1N1 M0) and stage II B (T2N1 M0 or T3N0 M0), the other stages in particular stage IIIA (T1–T3N2) being unchanged. At present, further information is, however, lacking concerning the staging characteristics of resected lung cancers presenting with VPI. The purpose of this study was to evaluate the significance of VPI in non-small cell lung cancer (NSCLC) to better understand its role as a prognostic factor and to target adjuvant treatment.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
From April 1984 to December 1996, 1,585 patients underwent pulmonary surgical resection for bronchogenic carcinoma at Laennec Hospital and Boisguillaume Surgical Center. The surgical procedure was a potentially curative complete resection with extensive mediastinal lymph node dissection similar to that described by Martini and Flehinger [4]. All included patients had NSCLC (patients who had neoadjuvant chemotherapy or radiation therapy, as well as patients with prior history of malignancy were excluded). Among the included patients, 1,281 presented with T1 (n = 430) and T2 (n = 851) disease and formed the basis of this study. There were 176 women and 1,105 men aged 30 to 86 years (mean, 60.9 years; median, 52 years). Complete surgical resection consisted of pneumonectomy (n = 519), lobectomy (n = 742), or segmentectomy (n = 20). International staging [2] was stage IA and B (n = 697), stage IIA and B (n = 247), and stage IIIA (n = 337). Adjuvant radiation therapy was performed in 455 patients. Whatever their stage, the patients were divided in two groups according to the existence of visceral pleural invasion (VPI) by the NSCLC. Visceral pleural involvement was classified according to Hammar’s diagram [5]: px and p0 = tumor with no pleural involvement or that reaches the visceral pleural but does not extend beyond its elastic layer; p1 = tumor that extends beyond the elastic layer of the visceral pleural but is not exposed on the pleural surface; and p2 = tumor that is exposed on the pleural surface but does not involve the parietal pleura (Fig 1). p1 and p2 tumor, defined as having VPI, were included in group II in our study, whereas px and p0 tumors were classified in group I. These two groups were compared with regard to size of the tumors, histology, lymph node involvement, survival, and cause of death.

View larger version (88K): [in this window] [in a new window]   Fig 1. Example of direct pleural invasion by peripheral malignant tumor. After disruption of the elastic lamina, the tumor cells breach (arrow) the layer of mesothelial cells and seed the pleural surface (original magnification, x400).

Univariate analysis was conducted among the different groups. A ² test was used to evaluate the significance of the relationship between the positivity of VPI and each of the clinicopathologic factors. Actuarial survival curves were calculated by Kaplan-Meier method [7]; statistical comparisons were made using the log-rank test [8]. Multivariate analysis was proceeded using Cox’s proportional hazards model [9]. All analyses of data were conducted with two-sided test of hypotheses at the 0.05 significance level. NCSS and SAS version 6.12 software were used (NCSS Software, Dr Jerry Hintze, Kaysville, UT; SAS Software, Cary, NC). Variables with p less than 0.1 after the univariate analysis were entered into a multivariate analysis using Cox model to evaluate their independent prognostic roles in the overall survival. The level of significance was put at 5% (p < 0.05). After factors were entered in the model for the multivariate analysis: age at intervention, tumor size, tumor location, tumor histologic type, visceral pleural invasion, and adenopathy invasion (N staging).

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
The VPI (group II) was identified in 19.1% of the resected specimens: group I (n = 1,036), group II (n = 245). Survival rates were 51.8% at 5 years and 33.8% at 10 years (median, 66 months) in group I, and 34.6% at 5 years and 27.9% at 10 years (median, 30 months) in group II. The difference between groups was highly significant (p = 0.00002).

The VPI was present in 10.4% of tumors 3 cm or less, in 19.6% of tumors between 3 and 5 cm and was significantly more frequent (p = 0.0001) in tumors larger than 5 cm in diameter (33%) (Table 1). In the two groups, survival rates decreased when the size of the tumor increased (p = 0.0001) (Figs 2 and 3). This difference in survival was even more striking when visceral pleura (group II) was involved (Fig 3).

View larger version (17K): [in this window] [in a new window]   Fig 2. Survival curves for tumors without visceral pleura invasion (group I) 3 cm (n = 441), tumors > 3 cm and 5 cm (n = 394), and tumors > 5 cm (n = 201). Survival rates are gradually decreasing: 56. 5% (median, 81 months) versus 50. 6 (median, 63 months) and 43.4% (median, 42 months) (p = 0.0001).

View larger version (16K): [in this window] [in a new window]   Fig 3. Survival curves for tumors with visceral pleura invasion (group II) 3 cm (n = 50), tumors > 3 cm and 5 cm (n = 96), and tumors > 5 cm (n = 99). There is a decrease in 5-year survival rate when the tumor measures > 3 cm: 58.9% (median, 93 months) versus 30.8% (median, 30 months) versus 25.2% (median, 20 months) (p = 0.0005).

The VPI was associated with a higher frequency of N2 involvement compared to N0 or N1 patients (p = 0.01) (Table 1). Furthermore, among the N1 patients, VPI was more frequent in case of extralobar involvement (p = 0.003) and among the N2 patients, VPI was more frequent in case of involvement of two or more N2 stations (p = 0.01) (Table 1). Furthermore, whatever the N status of the patients (N0, N1, or N2) there was an important difference in survival rates when visceral pleura was invaded (Table 2).

View larger version (17K): [in this window] [in a new window]   Fig 4. Survival curves when stage IB (N0) is divided into group I and group II. There is a decrease in 5-year survival between group I (without visceral pleura invasion [VPI]: 56.3%; median, 73 months) and group II (with visceral pleura invasion: 45.6%; median, 59 months) (p = 0.0005).

View larger version (16K): [in this window] [in a new window]   Fig 5. Survival curves when stage IIB (N1) is divided into group I and group II. The 5-year survival rates between stage IIA and stage IIB group I (without visceral pleura invasion [VPI]) are not different (51.2% versus 55.5%). On the contrary, note the decrease in survival in stage IIB group II (with visceral pleura invasion): 37.6%; median, 41 months. However, this difference is not significant (p = 0.24).

View larger version (16K): [in this window] [in a new window]   Fig 6. Survival curves when stage IIIA (N2) is divided into group I and group II. The 5-year survival rates between stage IIIA (T1N2 mol/L0) and stage IIIA (T2N2 group I (without visceral pleura invasion [VPI]) is not significant (30.1% versus 28.3%). On the contrary, there is a significant decrease in survival rates for the stage IIIA T2N2 group II (with visceral pleura invasion): 17.8%; median, 16 months: p = 0.03.

View larger version (19K): [in this window] [in a new window]   Fig 7. Survival curves for the stage IIIA N2 subsets. Survival rates in case of one N2 station involvement without visceral pleura invasion (VPI) is 33.8% (median, 31 months), whereas the survival rate decreases to 21.7% (median, 18 months) (p = 0.005) in case of one N2 station involvement with visceral pleura invasion, which is close to what is observed in case of 2 or more N2 station involvement, whatever the visceral pleura invasion.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

We also observed that frequency of VPI is variable according to histologic subsets. We suggest that the poor prognosis observed in some histologic subsets (ie, adenosquamous) may be partially explained by a high incidence of VPI.

Survival rates are known to be different between T1N0 and T2N0 status patients [2], and prognosis has been demonstrated to worsen when the size of lung tumor itself increased [13, 14]. We have observed comparable results, but in addition we have demonstrated that VPI was more frequent in the tumors exceeding 3 cm and that survival rates were worse when both features were associated (Fig 3). According to our results, the new international TNM that divides stage I into A (T1N0) and B (T2N0), stage II into A (T1N1) and B (T2N1), and that considers stage III A (T1–T3N2) as one group, appears insufficient. This conceals the real prognostic value of VPI. Our study suggests that stage I should be divided in stage IA = T1N0 (without VPI), stage IB = T2N0 without VPI, and stage IC = tumor of any size N0 with VPI, the invasion beyond interlobar pleura being also considered as VPI [15]. Stage IIB (T2N1 group) and stage IIIA could be further divided in the same way. Differences in survival rates observed in stage II (N1 involvement) between groups I and II (55.2% versus 37.6%) even if not statistically significant seemed relevant. A statistically significant difference was observed by Van Velzen and colleagues [16] in N1 patients and by Martini and associates [17] in a population of resected N1 NSCLC (58% without VPI versus 32% with VPI; p = 0.01). Nevertheless the latter researchers did not find this difference in a further study [18]. Other investigators believe that in stage IIIA, whatever the TNM subset, it is the stage per se, which is the only prognostic factor [3, 14]. In fact, our results show that in stage IIIA there is a difference in prognosis when the visceral pleura is invaded (group II) (Fig 6). This difference may be explained by the greatest number of metastatic mediastinal lymph node stations observed in case of VPI, the number of involved lymph node stations having itself a prognostic value [19]. Therefore, VPI seems to behave also as a supplementary lymph pathway, as demonstrated by Figure 7.

Brewer [20] explained the bad prognosis of lung cancer in the subpleural location by the rapid invasion of the pleura with dissemination of cancer cells throughout the pleural cavity in the stream of the pleural fluid. Indeed, once exfoliated in the pleural cavity, preformed stomas that connect subpleural lymphatics with the pleural space could account for the lymphatic and then the systemic tumor cells dissemination [21, 22]. The more frequent incidence of N2 disease as well as more numerous N2 stations involvement observed in VPI could reflect the passage of these malignant cells through the mediastinal lymphatic vessels up to the cervical venous circulation. It could also explain the greater incidence of death by cancer and diffuse metastases observed in group II as compared to cases without VPI (group I).

The poor prognosis that we observed in case of VPI is comparable in some ways to what is observed when tumor cells are identified in post thoracotomy pleural lavage. Buhr [23], Okumura [24], and Kondo [11] and their colleagues demonstrated that prognosis was significantly aggravated when pleural lavage performed after thoracotomy and before lung resection revealed malignant cytology. Both Okumura [24] and Kondo [11] have noticed that pleural lavage cytology (PLC) was positively significant more often in case of VPI. Buhr [25] also showed that positive PLC was more frequent in advanced tumor stages (stage II to IV versus I) and found a significantly increased rate of distant metastases in patients with positive PLC. Okumura and associates [24] observed that in patients with stage I or II disease, the cancer recurrence rate was significantly higher for the positive PLC (54.5%) than for the negative PLC (20%). However, positive PLC was also observed in cases without VPI as reported by Buhr [23, 25] and Kjellberg [26] and their associates. Because of the poor prognosis of positive PLC, Buhr and coworkers [25] suggest that cytologic examination of intraoperative pleural lavage fluid should be performed when assessing the final tumor stage in patients with lung cancer and that a positive result should be added to the pTNM classification.

To conclude, we believe these studies as well as ours should stimulate more work to improve the management of NSCLC. The VPI, as well as positive PLC, is a potential indication for adjuvant chemotherapy. If induction chemotherapy appears indicated in the future, even in case of stage I, the indication could perhaps be restricted to those with positive PLC or VPI. In our study, VPI has been detected on surgical specimen. If pretherapeutic assessment of the cTNM of both these entities (PLC and VPI) become mandatory, PLC may be then performed by video-assisted thoracoscopy. Ichinose and colleagues [27] have demonstrated that VPI seems to be detected more accurately by a jet stream of saline solution over the lung surface with cytologic analysis of the lavage fluid.

	References

Top Abstract Introduction Patients and methods Results Comment References

 

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