Bronchial Carcinoma and the Lymphatic Sump: The Importance of Bronchoscopic Findings

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1 Bronchial Carcinoma and the Lymphatic Sump: The Importance of Bronchoscopic Findings Gordon F. Murray, M.D., Ormond C. Mendes, M.D., and Benson R. Wilcox, M.D. ABSTRACT The lymphatic sump of Borrie is an important area of regional node metastasis in each lung. The sump area is of increased importance on the right side, since bilobectomy has been recommended to ensure complete removal of lymphatic disease in patients with lower or middle lobe carcinoma. The role of bmnchoscopy in assessing lymphatic metastasis of bronchial carcinoma was investigated in 42 patients at the North Carolina Memorial Hospital. Because of the high incidence of associated lymphatic metastases, bilobectomy is indicated for right lower or middle lobe lesions observed at bronchoscopy. Simple lobectomy may be utilized when bronchoscopic findings are negative and when there is no involvement of the lymph nodes of the sump of Borrie at the time of operation. If there is gross nodal involvement of the lymphatic sump, pneumonectomy will be required. From the surgical point of view, the lymphatic sump of Borrie [l] is an important area of regional node metastasis in each lung. On the left side, the lymph nodes situated above the superior segmental bronchus of the lower lobe and lying along the inferior border of the lingular bronchus constitute the lymphatic sump. On the right side, the sump area is situated, in relation to the intermediate bronchus, between the upper lobe bronchus and the middle and apical lower lobe bronchi. The collection of lymph nodes in the area of the sump is frequently infiltrated by both upper and lower lobe growths, and this infiltration has a bearing on treatment by lobectomy [23. The sump area From the Division of Cardiothoracic Surgery, The University of North Carolina School of Medicine, Chapel Hill, NC. Presented at the Eighteenth Annual Meeting of The Society of Thoracic Surgeons, Jan 11-13, 1982, New Orleans, LA. Address reprint requests to Dr. Murray, Division of Cardiothoracic Surgery, 108 Bumett-Womack Bldg 229H, Chapel Hill, NC is of increased importance on the right side, because removal of both the loweir and middle lobes has been recommended to ensure complete extirpation of lymphatic disease in patients with lower lobe carcinoma [3,41. Recommendation of bilobectomy for treatment of bronchial carcinoma is credited to Churchill [3, 51 in his 1950 address before The American Association for Thoracic Surgery [6]. The description of the lymphatic sump by Borrie [l] in the following year and subsequent anatomical studies by Nohl-Oser [5] emphasized the principle of bilobectomy. Performance of this operation remains,a standard of modern thoracic surgical practice, as noted by Adkins in Gibbon's Surgery of the Chest [4]: "[Clarcinomas of the right lower lobe drain to this sump; consequently, in order to resect all possibie involved nodes for a carcinoma of the right lower lobe, the middle lobe and its regional nodes should be removed along with the lower lobe." On the other hand, preservation of lung tissue is also a guiding principle of thoracic surgery, and the initial pulmonary resection should be as conservative as the extent of disease allows [7-91. In an attempt to define the pathological limitations of conservative pulmonary resection in the treatment of carcinoma of the right lower and right middle lobes, the relationship between bronchoscopic findings and metastatic lymph node involvement of the sump of Borrie was investigated in 42 patients seen consecutively at the North Carolina Memorial Hospital. Materials and Methods Anatomical Considerations Lymphatic metastases occur with marked frequency in patients with carcinoma of the lung. The incidence of nodal involvement may reach 75% in patients undergoing resection; post by The Society of Thoracic Surgeons

2 635 Murray, Mendes, and Wilcox: Bronchial Carcinoma and the Lymphatic Sump Mediastinal 2 pts. 16 /42 pts. (38%) Fig 1. Bronchogram showing lymph node groups at risk in patients with bronchial carcinoma. Anterior and posterior mediastinal groups are not shown. (Retouched for clarity.) mortem examination often reveals an even higher incidence in those who die of the disease [lo]. The lymph node stations at risk may be divided into two main groups: pulmonary nodes and mediastinal nodes. The pulmonary lymph nodes are classified as intrapulmonary nodes or bronchopulmonary nodes, with the latter including hilar and interlobar lymph nodes (Fig 1). It is the interlobar nodes that make up the lymphatic sump of Borrie. On the left side, the sump lies in the main fissure, and clearance of these nodes by lobectomy is not readily achieved. For right lower, or middle, lobe growths, a right lower and middle lobectomy with high division of the intermediate bronchus will completely extirpate the sump. A simple lobectomy would not obtain the same result in this situation. Patient Population The right lower or middle lobe was the primary site of tumor in 42 of 629 patients with bronchogenic carcinoma who had surgical staging, pulmonary resection, or both between January 1, 1969, and December 31, Thirty-four men and 8 women were evaluated. The mean age of these patients was 61 years. Two patients lpt. Fig 2. Sites of lymph node metastases identified in 16 of 42 patients with carcinoma of the right lower or middle lobe. had mediastinoscopy only, 15 had a lobectomy, 11 had a bilobectomy, and 14, a pneumonectomy. The predominant cell type was epidermoid carcinoma, found in 23 patients. Adenocarcinoma was identified in 10 patients, and undifferentiated tumors, in 9. Oat cell carcinoma was notably absent in this series of right lower and middle lobe bronchial tumors. Lymphatic metastases were identified in 16 of the 42 patients (Fig 2). One patient had a positive intrapulmonary node only. Nine patients had involvement of the interlobar bronchopulmonary nodes, which make up the lymphatic sump of Borrie. Four patients also had hilar metastases, and 2 had mediastinal metastases. Results Bronchoscopic findings were evaluated in 41 of the 42 patients with carcinoma of the right lower or middle lobe (Table). The results of bronchoscopy were considered positive when a visible endobronchial lesion was identified. Macroscopic tumor was seen in the segmental bronchi in 20 patients; in 4 of these patients,

3 636 The Annals of Thoracic Surgery Vol 34 No 6 December 1982 Importance of Bronchoscopic Findings in the Evaluation of Extent of Disease in 41 Patients with Carcinoma of the Right Lower or Middle Lobe Negative Bronchoscopic Positive Bronchoscopic Evaluative Evidencea Results (N = 21) Results (N = 20) Mediastinal metastases 0 2 Lymphatic sump positive 0 9 Bronchial margin involved 0 3 Pneumonectomy required 3 10 aincludes clinical, intraoperative, and postoperative treatment classification of disease. encroachment of the intermediate bronchus was observed. Malignancy was confirmed by bronchoscopic biopsy in 18 patients and by cytological examination in 2 patients; all 20 had a positive bronchoscopic examination. On the other hand, only 2 of the 21 bronchoscopically negative patients-those with no visible lesion-had positive cytological findings. Intraoperative evaluation and pathological examination of the sump nodes failed to demonstrate tumor in 18 of the 21 patients who had negative bronchoscopic results. Thirteen of these patients had a lobectomy, and 5 had an elective bilobectomy. Only 3 of these bronchoscopically negative patients required a pneumonectomy. The hilar nodes were positive in 2 patients, but no patient had mediastinal disease. Bronchoscopic results were positive in 20 patients. Nine of 16 patients undergoing bilobectomy or pneumonectomy had lymphatic extension to the sump nodes. Two patients had a lobectomy; in 1, the bronchial margin was involved with tumor. Mediastinal metastases were noted at mediastinoscopy in 2 other patients. There were no operative deaths in the patients who had either positive or negative bronchoscopic findings. However, long-term survival was markedly improved in the absence of bronchoscopic abnormality (Fig 3). Comment In his description of the lymphatic sump, Borrie [l] emphasized an important difference between the incidence of lymph node invasion in the upper lobe of the right lung and that in the lower lobe. While no more than 13% of resected O BRONCHOSCOPY NEGATIVE BRONCHOSCOPY POSITIVE I 1 I I I 0 I YEARS FOLLOWED Fig 3. Life-table analysis of 41 patients with bronchial carcinoma of the right lower or middle lobe. nodes were involved in upper lobe tumors, as many as 26% of the nodes in lower lobe lesions-particularly in the right lymphatic sump-were invaded at the time of operation. In the present study, lymphatic metastases were identified in 16 of 42 patients (38%), and 9 patients (21"/o) had involvement of the interlobar lymph nodes in the right lymphatic sump. Thus, an operative procedure designed to achieve complete clearance of all the nodes in the sump has a sound basis in pathology. With composite removal of the lower and middle lobe by high division of the intermediate bronchus, bilobectomy would accomplish this result. However, selective application of the sump principle would be desirable to salvage lung tissue in the severely compromised patient [7, 91, and also to enhance the patient's ability

4 637 Murray, Mendes, and Wilcox: Bronchial Carcinoma and the Lymphatic Sump to deal with future disease, including malignancy [ll]. To date, the major role of bronchoscopy in primary lung cancer has been in performing biopsy and microscopic verification of the clinical diagnosis; bronchoscopy has also provided valuable information relating to whether pneumonectomy or a bronchoplastic procedure should be done. It is important to note that when bronchogenic carcinoma visibly involves the mainstem bronchi, curative resection is rarely possible [12, 131. Furthermore, microscopic invasion by malignant cells is known to extend several centimeters proximal to the visible endobronchial component in some tumors arising in the segmental bronchi [ Therefore, the present study addresses another important consideration in evaluating bronchoscopic findings for operative management-the presence or absence of metastatic lymph node involvement of the sump of Borrie. Nearly all (18 of 21) of our patients with negative bronchoscopic results were free of metastatic lymph node involvement (see Table). Intraoperative evaluation of the lymphatic sump in 13 lobectomy patients and pathological examination of the sump nodes in 5 elective bilobectomy patients failed to reveal tumor. The hilar nodes were positive in 2 patients who required pneumonectomy, but no patient had mediastinal lymph node involvement. Baker and his colleagues [17] recently concluded that mediastinal exploration is not routinely indicated in patients with small peripheral bronchial carcinoma. These data also suggest that the contribution of mediastinoscopy to the evaluation of bronchoscopically negative lesions of the right lower or middle lobe is minimal. The ominous implications of positive bronchoscopic findings, which were noted in 20 patients, are apparent in the study (see Table). Metastatic invasion of the nodes in the lymphatic sump was demonstrated in 9 of 16 patients undergoing bilobectomy or pneumonectomy. Mediastinal metastases were found at mediastinoscopy in 2 patients, and hilar lymphatic metastases were present in 2 other patients. The fact that patients with visible endobronchial tumors had less favorable indications for treatment is reflected in the se- lection of operative procedure; while only 3 of the bronchoscopically negative patients underwent pneumonectomy, 10 patients with positive bronchoscopic results had to have an entire lung removed. On the other hand, a more favorable prognosis for patients with bronchoscopically negative disease is indicated by a life-table analysis of the 41 patients who had bronchoscopy (see Fig 3). The improved rate of survival for patients with negative bronchoscopic findings is statistically significant at each yearly interval. It is important to recognize that these results were achieved using a smaller pulmonary resection. As noted previously, malignant infiltration of the peribronchial or the bronchial submucous lymphatics proximal to a macroscopic lesion is known to be of surgical importance [14,151. The practical implication of this observation is that the resection of the bronchus should ideally be at least 2 cm above the visible tumor [2], a recommendation reinforced by our study. Thirteen patients with negative bronchoscopic findings had a lobectomy, and the bronchial margin was clear in all. Among 4 patients with positive bronchoscopic results who initially underwent lobectomy, the bronchial margin was involved with tumor in 3; 2 of these patients then underwent bilobectomy, but all eventually died. The fourth lobectomy patient in the positive bronchoscopy group is living with recurrent disease. Bilobectomy has been reported to offer technical advantages over individual lower or middle lobectomy in reducing the incidence of middle lobe syndrome, fistula, and empyema [18]. However, no lobectomy patient in this study experienced complications. Since there were also no operative deaths in the entire series, it is clear that a decision regarding lobectomy may be focused on pathological considerations. It is concluded that because of the high incidence of lymphatic metastases, bilobectomy is indicated for right lower or middle lobe lesions seen at bronchoscopy. This procedure ensures the removal of the entire sump of Borrie and provides a safe bronchial margin. Lobectomy may be utilized when bronchoscopic findings

5 638 The Annals of Thoracic Surgery Vol 34 No 6 December 1982 are negative and there is no lymph node involvement of the sump of Borrie at the time of operation. Pneumonectomy is, of course, required if there is gross nodal involvement of the lymphatic sump. References 1. Borrie J: Primary carcinoma of the bronchus: prognosis following surgical resection. Ann R Coll Surg 10:165, Nohl-Oser HC: Lymphatics of the lmg. In Shields TW (ed): General Thoracic Surgery. Philadelphia, Lea and Febiger, 1972, p Glenn WWL, Liedbow AA, Lindskog GE: Thoracic and Cardiovascular Surgery with Related Pathology. Third edition. New York, Appleton-Century-Crofts, 1975, p Adkins PC: Neoplasms of the lung. In Sabiston DC Jr, Spencer FC (eds): Gibbon s Surgery of the Chest. Third edition. Philadelphia, Saunders, 1976, p Nohl-Oser HC: An investigation into the lymphatic and vascular spread of carcinoma of the bronchus. Thorax 11:172, Churchill ED, Sweet RH, Soutter L, Scannell JG: The surgical management of carcinoma of the lung. J Thorac Surg 20:349, Paulson DL, Shaw RR: Results of bronchoplastic procedures for bronchogenic carcinoma. Ann Surg 151:729, Naruke T, Yoneyama T, Ogata T, Suemasu K: Bronchoplastic procedures for lung cancer. J Thorac Cardiovasc Surg 73:927, Bennett WF, Smith RA: Segmental resection for bronchogenic carcinoma: a surgical alternative for the compromised patient. Ann Thorac Surg 27:169, Naruke T, Suemasu K, Ishikawa S: Lymph node mapping and curability at various levels of metastasis in resected lung cancer. J Thorac Cardiovasc Surg 76332, Salerno TA, Munro DD, Blundell PE, Chiu RCJ: Second primary bronchogenic carcinoma: lifetable analysis of surgical treatment. Ann Thorac Surg 27:3, Stoloff IL: The prognostic value of bronchoscopy in primary lung cancer: a new perspective for an old procedure. JAMA 227:299, Rabin CB, Selikoff IJ, Kramer R: Paracarinal biopsy in evaluation of operability of carcinoma of the lung. Arch Surg 65:822, Griess DF, McDonald JR, Clagett OT: The proximal extension of carcinoma of the lung in the bronchial wall. J Thorac Surg 14:362, Cotton RE: The bronchial spread of lung cancer. Brit J Dis Chest 53:142, Habein HC, McDonald JR, Clagett OT: Recurrent carcinoma in the bronchial stump. J Thorac Surg 31:703, Baker RR, Lillemac KD, Tockman MS: The indications for transcervical mediastinoscopy in patients with small peripheral bronchial carcinoma. Surg Gynecol Obstet , Lindskog GE, Liedbow AA, Hales MR: Bilobectomy: surgical and anatomic considerations in resection of right middle and lower lobes through the intermediate bronchus. J Thorac Surg 18:616, 1949 Discussion DR. JAMES w. MACKENZIE (Piscataway, NJ): Dr. Murray and his co-authors have made a straightforward proposition: in patients with carcinoma of the middle lobe or of the right lower lobe, positive bronchoscopic findings indicate a high likelihood of metastatic involvement of the lymphatic riump of Bome. Their study has led them to make the following recommendations for such patients. 1. Lobectomy should be performed when bronchoscopy is negative and there is no involvement of the lymphatic sump. 2. Bilobectomy should be performed if the lesion is seen at bronchoscopy. 3. Pneumonectomy should be done if there is gross nodal involvement. Certainly, the authors main thesis regarding the importance of positive bronchoscopic findings is reasonable. It is consonant with the report of Stoloff on carcinoma of the main bronchus that they have cited in their paper, as well as with several other publications. Nevertheless, before I can accept the specific recommendations of Dr. Murray and his colleagues, I would like to have answers to several questions. In general, more distal lesions are less likely to be associated with positive sump nodes. Our ability to see and to perform biopsy of more peripheral lesions has increased considerably. Can Dr. Murray provide more details on the location of these lesions, and was the tissue specimen obtained by rigid bronchoscopy or by flexible bronchoscopy? One assumes, of course, that the more central lesions yielded positive bronchoscopic results, but this may not be so. Similarly, since nodal involvement is related to the size of the primary tumor in many series, I believe it would be helpful to know the size of the lesions in each group. These questions point out the importance of the TMN classification in reporting clinical studies of patients with bronchogenic carcinoma. In illustrations appearing in the works of Borrie and Nohl-Oser, both of whom have been cited by Dr. Murray and co-workers, one notes a substantial number of nodes in the lymphatic sump. I would like

6 639 Murray, Mendes, and Wilcox: Bronchial Carcinoma and the Lymphatic Sump to ask the authors how they evaluated the sump nodes at thoracotomy, and how they suggest that others do so. Many surgeons have difficulty recognizing gross nodal involvement, particularly if it is intranodal. Should all of the nodes be sampled? Moreover, if the nodes are negative in bronchoscopically positive patients, why not perform a lobectomy rather than a bilobectomy if there is an adequate bronchial margin? I wish to congratulate Dr. Murray and his associates on the lack of operative mortality in their series, and to thank them for bringing to our attention the importance of bronchoscopic findings and lymphatic spread in carcinoma of the middle and right lower lobes. DR. PAUL A. KIRSCHNER (New York, NY): This paper does not make it quite clear whether a mediastinoscopy was done in all patients, and whether there was a difference in the cell type of the more central lesions. I assume that they were identified by rigid bronchoscopy, which would favor squamous carcinoma; the more peripheral lesions, on the other hand, would be more likely to be adenocarcinoma. I wonder if Dr. Murray could comment on this. DR. MURRAY: In response to the questions that Dr. MacKenzie has raised, I am unable to detail the location and exact size of the various malignant lesions in our series. It is commonly recognized that lymphatic metastasis from very peripheral lesions is unusual. It is also apparent that invasive mediastinal evaluation contributes very little in evaluating patients with peripheral lesions, and this applies to the bronchoscopically negative patients in our study. Intraoperative evaluation of the sump nodes was made frequently by gross inspection and only occasionally by microscopic evaluation. As Dr. MacKenzie has pointed out, evaluating the lymphatic sump is difficult. Because of this real difficulty, we are recommending elective bilobectomy in the presence of positive bronchoscopic results. Dr. Kirschner, staging mediastinoscopy was performed in all of our patients. I have not examined the data to determine which cell types appeared in the more central lesions, but I suspect that most of them were in the epidermoid group.

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