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Ann Thorac Surg 1997;64:1626-1629
© 1997 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Diagnosis of Visceral Pleural Invasion in Resected Lung Cancer Using a Jet Stream of Saline Solution

Departments of Chest Surgery and Pathology, National Kyushu Cancer Center, Fukuoka, Japan

Accepted for publication June 10, 1997.

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Background. Visceral pleural invasion by the tumor is an important prognostic factor in patients undergoing resection for lung cancer. We developed a method to detect more accurately the presence of visceral pleural invasion in resected lung cancer.

Methods. The surface of the visceral pleura over 90 resected peripheral tumors was irrigated twice with a jet stream of saline solution using a 20-mL syringe with a 21-gauge needle, and then the fluid, which contained desquamated cells, was collected for cytologic analysis. When cancer cells were found in the collected fluid, the tumor was judged to have invaded the visceral pleura.

Results. Thirty-eight (42%) resected tumors were identified as having visceral pleural invasion either by our new method or by pathologic examination. Twenty-four cases were detected by the jet stream of saline method alone, 5 by pathologic examination alone, and 9 by both techniques. The sensitivity and accuracy of the two approaches in the diagnosis of visceral pleural invasion were 87% and 94%, respectively, for our new method, and 37% and 73%, respectively, for pathologic examination (p < 0.0001). Furthermore, among 38 patients who had a tumor demonstrating visceral pleural invasion, 5 (13%) and 9 (24%) patients, respectively, had cancer cells in the pleural effusion and intrapleural lavage fluid.

Conclusions. Our findings suggest that our method is useful in detecting cancer invasion of the visceral pleura, which is considered one of the causes of malignant effusion.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Visceral pleural invasion by the tumor is known to be one of the most important prognostic factors in patients who undergo complete resection of lung cancer [1–3]. Therefore, a T1 tumor measuring less than 3 cm at its greatest diameter is considered a T2 tumor when visceral pleural invasion is found by pathologic examination [1]. The diagnosis of visceral pleural invasion by pathologic examination usually is based on one or two cut slices of the resected tumor. Although pathologic examination can confirm visceral pleural invasion easily when the tumor is clearly visible on the visceral pleura, such cases are relatively rare. Therefore, it remains questionable whether a tumor can be considered reliably to have no visceral pleural invasion on the basis of pathologic examination alone.

To resolve this problem, we developed a simple method involving cytologic examination of cells desquamated from the visceral pleura by a jet stream of saline solution (JSS). Our findings showed the JSS method to be significantly more sensitive and accurate than ordinary pathologic examination in detecting visceral pleural invasion by lung cancer.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
From January 1992 to September 1996, 207 patients with peripheral non–small cell lung cancer that either did not adhere to or did not invade the surrounding tissue underwent surgical resection at the Kyushu Cancer Center. From this group, 90 patients with peripheral tumors that appeared to reach the visceral pleura were selected as the subjects for this study. The disease was classified by a staging system [4] in which a T1 or T2 tumor with a satellite tumor in the same lobe and any tumor accompanied by an additional tumor in the ipsilateral other lobe were defined as a T2 or a T3 and T4 tumor, respectively. The pathologic stage of the tumors in these 90 patients was I in 55 patients, II in 7 patients, IIIA in 19 patients, and IIIB in 9 patients. Histologic examination revealed 78 adenocarcinomas, 5 squamous cell carcinomas, and 7 other types of carcinomas.

Our technique for detecting visceral pleural invasion by the tumor was performed as follows: The surface of the visceral pleura over the peripheral tumor was obtained by surgical resection and irrigated twice by a jet stream of heparinized saline solution using a 20-mL syringe with a 21-gauge needle (Fig 1). When the resected tumor had a visceral pleural retraction, the main target of the JSS was a groove created by the pleural retraction. In the present study, 51 (57%) of 90 resected tumors had a visceral pleural retraction. The distance between the tip of the needle and the pleural surface was kept at about 2 cm, and a total of 40 mL of saline solution containing cells desquamated from the visceral pleural surface was collected and then centrifuged at 1,000 rpm for 10 minutes. Thereafter, the obtained sediment was stained by Giemsa and Papanicolaou's method for cytologic examination. Whenever it was necessary to distinguish cancer cells from reactive mesothelial cells, anticarcinoembryonic antigen staining, alcian blue staining, and periodic acid-Schiff reaction were performed.

View larger version (15K): [in this window] [in a new window]   Fig 1. . The technique of using a jet stream of saline solution to detect visceral pleural invasion of a resected lung tumor. Most of the resected tumors in this study had a visceral pleural retraction.

Among the 90 patients, a small amount of pleural effusion was found after thoracotomy and collected for cytologic examination in 13 patients. In the other 77 patients, to determine whether cancer cells were present in the intrapleural cavity without obvious effusion, the pleural cavity was filled with 500 mL of heparinized saline solution immediately after thoracotomy. Although the intrapleural cavity was washed gently by hand for 30 seconds, touching the visceral pleura over the tumor was avoided to ensure that only cells present in the intrapleural cavity were obtained. Two hundred milliliters of intrapleural lavage fluid then was collected and centrifuged at 1,000 rpm for 10 minutes for cytologic examination. However, in this study, the results of intrapleural lavage cytology were not used in determining the pathologic stage of the tumor.

The statistical analysis between groups was calculated using the ² test. The statistical difference was considered to be significant when the p value did not exceed 0.05.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Of the 90 tumors evaluated that were located peripherally and suspected of reaching the visceral pleura, 38 (42%) tumors were diagnosed as invading the visceral pleura by pathologic examination, the JSS method, or both. As shown in Table 1, the diagnosis of visceral pleural invasion was obtained by the JSS method in 33 tumors and pathologic examination in 14 tumors. Nine tumors were found to have invaded the visceral pleura by both the JSS method and pathologic examination. Because no means of detecting a false-positive diagnosis of visceral pleural invasion exists, the presence of visceral pleural invasion for the 38 resected tumors diagnosed by the JSS method, pathologic examination, or both was considered a true-positive in the present study. There were 5 false-negative diagnoses with the JSS method and 24 with pathologic examination. When calculated using these data, the sensitivity and accuracy of the JSS method for the diagnosis of visceral pleural invasion were 87% and 94%, respectively (Table 2). In contrast, the sensitivity and accuracy of pathologic examination were 37% and 73%, respectively. The JSS method was significantly more sensitive and accurate than pathologic examination for the diagnosis of visceral pleural invasion (Table 2). The specificity could not be calculated because no false-positive diagnoses could be identified.

Table 3 shows the incidence of visceral pleural invasion diagnosed by the JSS method and by pathologic examination according to pathologic stage. There was no significant relation between the incidence of visceral pleural invasion and stages I through IIIA, apart from stage IIIB, which included 6 patients with carcinomatous effusion found at thoracotomy. When the primary tumors were classified by a maximum diameter of 3 cm, the larger tumors had a significantly greater incidence of visceral pleural invasion than did the smaller tumors (Table 4). However, in both tumor groups, the JSS method for detecting visceral pleural invasion was more sensitive than was pathologic examination.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

When the area of the tumor exposed on the visceral pleura spreads to some extent and is identified macroscopically, visceral pleural invasion can be confirmed easily by pathologic examination. In practice, the identification of such an exposed part is difficult in most cases. One of the advantages of the JSS method is that it is not necessary to select a specific part of the visceral pleura to irrigate, in contrast to pathologic examination.

As shown in this study, most peripheral tumors suspected of reaching the visceral pleura can be expected to have a visceral pleural retraction. The visceral pleural invasion in these tumors frequently is found at the bottom of the grooves made by the pleural retraction. It is impossible to inspect all the grooves by pathologic examination, but this can be done using the JSS method.

Intrapleural lavage cytology after thoracotomy in patients without any evidence of carcinomatous pleuritis has received widespread attention recently because the prognosis of patients with positive cytologic findings is poor compared with that of patients with negative findings [5–7]. Kondo and colleagues [5] reported that 11 (26%) of 42 patients with positive cytologic findings on intrapleural lavage eventually had a recurrence of carcinomatous pleuritis. Therefore, positive cytologic findings on lavage are considered to indicate a prestage of carcinomatous pleuritis. In the present study, the incidence of carcinomatous effusion and positive cytologic findings on intrapleural lavage in patients with a tumor invading the visceral pleura was significantly higher than that in patients without visceral invasion. Therefore, the poor prognosis of patients with visceral pleural invasion might be explained in part by these observations.

At present, the number of patients studied is too small and the follow-up too short to analyze fully the prognosis of patients with visceral pleural invasion diagnosed by the JSS method. We initiated a prospective study in March 1993 to address these questions in greater depth.

	Acknowledgments

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
This study was supported in part by a grant-in-aid for cancer research from the Ministry of Health and Welfare, Japan. We thank Mr Paul Shimizu for his critical review, and Miss Yumiko Oshima for her help in the preparation of the manuscript.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Address reprint requests to Dr Ichinose, Department of Chest Surgery, National Kyushu Cancer Center, 3-1-1, Notame, Minami-ku, Fukuoka 815, Japan (e-mail: yichinos{at}nk-cc.go.jp).

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 

1. Mountain CF. A new international staging system for lung cancer. Chest 1986;89(Suppl):225S–33S.[Free Full Text]
2. Martini N, Flehinger BJ, Nagasaki F, Hart B. Prognostic significance of N1 disease in carcinoma of the lung. J Thorac Cardiovasc Surg 1983;86:646–53.[Abstract]
3. Ichinose Y, Yano T, Asoh H, Yokoyama H, Yoshino I, Katsuda Y. Prognostic factors obtained by a pathologic examination in completely resected non-small-cell lung cancer. J Thorac Cardiovasc Surg 1995;110:601–5.[Abstract/Free Full Text]
4. The Japan Lung Cancer Society. General rules for clinical and pathologic record of lung cancer, 3rd ed. Tokyo: Kanehara, 1995.
5. Kondo H, Asamura H, Suemasu K, et al. Prognostic significance of pleural lavage cytology immediately after thoracotomy in patients with lung cancer. J Thorac Cardiovasc Surg 1993;106:1092–7.[Abstract]
6. Eagan RT, Bernatz PE, Payne WS, et al. Pleural lavage after pulmonary resection for bronchogenic carcinoma. J Thorac Cardiovasc Surg 1984;88:1000–3.[Abstract]
7. Buhr J, Berghauser KH, Morr H, Dobroschke J, Ebner HJ. Tumor cells in intraoperative pleural lavage: an indicator for the poor prognosis of bronchogenic carcinoma. Cancer 1990;65:1801–4.[Medline]

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Yukito Ichinose Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ichinose, Y. Articles by Katsuda, Y. Search for Related Content PubMed PubMed Citation Articles by Ichinose, Y. Articles by Katsuda, Y.