Ann Thorac Surg 1997;63:800-805
© 1997 The Society of Thoracic Surgeons
Original Article: General Thoracic
Pulmonary Arteriography for the Assessment of Technical Feasibility of Sleeve Resection in Lung Cancer
Rakesh M. Suri, MD,
Shafique H. Keshavjee, MD,
Steven Herman, MD,
Kenneth Sniderman, MD,
F. Griffith Pearson, MD
Divisions of Thoracic Surgery and Radiology, The Toronto Hospital, University of Toronto, Toronto, Ontario, Canada
Accepted for publication October 23, 1996.
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Abstract
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Background. Pulmonary arteriography has been reported to be useful in the preoperative assessment of patients with lung cancer to determine the technical resectability and feasibility of pneumonectomy by imaging the main right and left pulmonary arteries. In this report, we describe the use of selective pulmonary arteriography in the assessment of lobar resectability.
Methods. Selective pulmonary arteriography provides a detailed anatomic view of the lobar branches and has been used at our institution for the past 30 years to preoperatively investigate patients who are candidates for a sleeve lobectomy.
Results. Three cases are described that demonstrate the usefulness of selective pulmonary arteriography in the assessment of the technical feasibility of sleeve resection in patients with lung cancer.
Conclusions. Arteriographic findings may accurately show whether a sleeve lobectomy is technically possible, that only a pneumonectomy is possible, or that the only safe way to ensure clearance of the pulmonary artery is to perform arterioplasty. This information may obviate an unnecessary thoracotomy in patients who are judged on the basis of a physiologic assessment to be unable to tolerate a pneumonectomy.
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Introduction
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Pulmonary arteriography has been reported to be useful in the preoperative assessment of lung cancer patients to determine the technical resectability and the feasibility of pneumonectomy by imaging the main right and left pulmonary arteries. In this report we describe the use of selective pulmonary arteriography to delineate lobar vascular anatomy and thereby assess lobar resectability. Selective pulmonary arteriography provides a detailed anatomic view of the lobar branches and has been used at our institution for the past 30 years to preoperatively investigate patients who are candidates for a sleeve lobectomy. Arteriographic findings may accurately determine whether a sleeve lobectomy is technically possible, or that only a pneumonectomy is possible, or that the only safe way to ensure clearance of the pulmonary artery would be to perform an arterioplasty. This information may obviate an unnecessary thoracotomy in patients who are judged on the basis of physiologic findings, to be unable to tolerate a pneumonectomy. Knowledge of the nature of the pulmonary artery involvement in the affected lobe preoperatively may save a great deal of intraoperative time that would otherwise be spent on exploration, thereby allowing the surgeon to directly perform the planned resection in the most efficient manner possible. We report on 3 recent patients treated at the Toronto Hospital in whom the usefulness of pulmonary arteriography in the preoperative staging of lung cancer is illustrated. The preoperative definition of the lobar vascular anatomy in these patients assisted in the planning of the surgical approach and the performance of curative resection in patients who otherwise would potentially have been considered to have unresectable disease.
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Case Reports
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Patient 1
A 59-year-old man was referred to the Toronto Hospital Thoracic Service after he was seen by his family physician because of a 2-year history of chronic cough, productive of small amounts of mucoid sputum, but no hemoptysis. There had been no other chest symptoms and no weight loss or decreased appetite. The patient reported a smoking history of over 90 pack-years and admitted to occasional alcohol use. Physical examination revealed a grossly obese man, but findings were otherwise unremarkable. A chest radiogram at this time showed an ill-defined opacity in the region of the left main pulmonary artery, as well as an obscured left heart border with the suggestion of a lingular infiltrate (Fig 1A
). Bronchoscopy demonstrated a tumor in the left upper lobe orifice. Pathologic examination of a biopsy specimen of the tumor revealed squamous cell carcinoma. A computed tomograph (CT) scan of the thorax revealed a 5-cm spiculated mass at the origin of the left upper lobe bronchus, with complete occlusion and subsegmental atelectasis distal to the lesion. The tumor seemed to encase the pulmonary artery of the upper lobe and extended very close to the left main pulmonary artery (Fig 1B). There was no evidence of lymphadenopathy. Computed tomographic scans of the abdomen and head showed no metastatic lesions. Mediastinoscopic findings showed no malignancy, and a total body bone scan also was reported to show no metastases. Pulmonary function testing revealed a total lung capacity of 5.6 L, a functional residual capacity of 2.9 L, a vital capacity of 3.2 L, a residual volume of 2.4 L, a forced expiratory volume in 1 second (FEV1) of 1.4 L (45% of predicted), a forced vital capacity (FVC) of 3.1 L, a FEV1/FVC of 74.2%, and a diffusion capacity of 29.3 (109% of predicted). Exercise testing revealed a relatively good tolerance to moderate activity, although the patient reported becoming short of breath on climbing two flights of stairs. A quantitative ventilation-perfusion scan revealed 43% of perfusion going to the left lung. On the basis of the CT findings, it was evident that the patient would most likely require a pneumonectomy, but physiologically he was regarded as a marginal candidate for the operation, owing to his poor pulmonary function. The calculated postoperative FEV1 would be 0.8, or 26% of predicted. The left upper lobe alone had a preoperative perfusion of only 6%, however. On the basis of his bronchoscopic examination, a sleeve upper lobectomy was considered technically possible, but the degree of involvement of the pulmonary artery was not certain. If it were involved, it was not known whether the best technique for resection would be an arterial sleeve or an arterioplasty. A pulmonary arteriogram showed an essentially intact left main pulmonary artery, suggesting that the tumor was technically resectable. A slight irregularity limited to the superolateral margin of the proximal left pulmonary artery indicated that the tumor might involve the pulmonary artery in this area, which could necessitate a pulmonary arterioplasty or arterial sleeve resection (Fig 1C).
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Fig 1. . (A) Chest x-ray study shows proximal left upper lobe tumor. (B) Computed tomographic scan shows left upper lobe tumor with possible involvement of the proximal left main pulmonary artery. (C) Preoperative digital subtraction arteriogram shows tumor invasion by encasement of the anterior segmental branch of the pulmonary artery to the left upper lobe. There is also evidence of flattening and irregularity of the superior surface of the left main pulmonary artery with no frank invasion of this region.
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At operation the tumor was indeed found to locally invade the wall of the left pulmonary artery in the area of the irregularity shown by arteriography. A sleeve resection of the left upper lobe and the anterolateral aspect of the left main pulmonary artery was carried out. Bovine pericardium was utilized for the reconstructive pulmonary arterioplasty. Pathologic analysis of the resected specimen showed it to be poorly differentiated squamous cell carcinoma and the resection margins were found to be negative. The patient experienced a rapid and uncomplicated recovery postoperatively.
Patient 2
A 79-year-old woman with a 12-year history of chronic lymphocytic leukemia was admitted to the hospital for treatment of a fractured hip. At that time she was found to have a 4-cm, irregular mass in the right upper lobe (Fig 2A). On presentation, the patient was relatively asymptomatic from a respiratory perspective, with a good appetite, no weight loss, no bone pain, and no other complaints. There was no history of smoking or of industrial or fiber exposure. A CT scan of the chest showed an irregular mass in the right upper lobe, measuring 5.8 x 5.6 cm and extending from the chest wall to the mediastinum, suggestive of a bronchogenic carcinoma (Fig 2B). Bronchoscopy showed complete extrinsic compression of the right upper lobe bronchus. Nodal biopsy specimens obtained during mediastinoscopy showed no evidence of metastatic spread, but a large, fixed right upper lobe mass was easily palpable. A metastatic survey, which included a bone scan and CT scans of the pelvis and abdomen, was normal. Pulmonary function testing demonstrated an FEV1 of 1.2 L (33% of predicted), an FVC of 3.2 L (33% of predicted), and FEV1/FVC of 37.5 (47% of predicted). Over the next several months constant pain developed in the patient's right chest below the axilla. Selective pulmonary arteriography performed before operation delineated the anatomy of the pulmonary artery lobar branches and identified intact vessels to the right upper lobe (Fig 2C). This indicated that a sleeve resection of the right upper lobe was technically feasible. At preoperative bronchoscopy, the trachea, carina, and right and left main stem bronchi were examined and tumor was seen to be invading the right main bronchus at the origin of the right upper lobe bronchus. The patient underwent an uncomplicated thoracotomy and sleeve resection of a large tumor in the right upper lobe. The patient made a satisfactory recovery and subsequently returned home. Pathologic analysis revealed that the resected 9-cm mass was an invasive tumor with spindle cell growth and a high degree of pleomorphism suggestive of a sarcoma.
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Fig 2. . (A) Chest radiogram demonstrates an irregular mass in the right upper lobe. (B) Contrast-enhanced computed tomographic scan demonstrates an irregular mass in the right upper lobe measuring 5.8 x 5.6 cm. (C) Arteriogram identifies intact vascular tree to the right upper lobe. Narrowing of first (anterior) branch to right upper lobe beyond the origin of this branch is seen. These findings show that a right upper lobe sleeve lobectomy is technically feasible.
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Patient 3
A 55-year-old man presented with a 1-year history of weight loss and shortness of breath, but otherwise minimal symptomatology. He was unable to climb one flight of stairs or walk a block on the level without resting. There were no symptoms suggestive of metastatic disease or any other complaints. The patient had spent his life on a farm and had not been exposed to any industrial substances or fibers. He had a 40 pack-year smoking history and symptoms of mild chronic bronchitis. In addition, he had had rheumatic fever in childhood. The patient reported a history of considerable alcohol intake but had stopped drinking 3 years before presentation. Physical examination revealed a cachectic man who showed no clubbing or adenopathy and who was not in respiratory distress. There was equal chest excursion bilaterally and no stridor, and distant breath sounds were heard with some decrease over the right upper chest. A chest x-ray study showed a 13-cm lesion in the periphery of the right upper lobe, adjacent to the chest wall and crossing the minor fissure to involve the upper part of the right middle lobe (Fig 3A). A CT scan showed a 14-cm mass in the posterior segment of the right upper lobe. There was no significant mediastinal or hilar lymphadenopathy, and the remainder of the lungs were clear (Fig 3B). The tumor was adjacent to the superior vena cava. Digital subtraction angiography (DSA) demonstrated the intact outline of the main pulmonary artery, which was free of tumor invasion (Fig 3C). Visualization of the superior vena cava at angiography confirmed the absence of gross involvement of the vessel. Bronchoscopic examination showed that the bronchus was occluded by a mass that extended to the posterior segment of the right upper lobe and that the mass protruded into the right upper lobe bronchus. Brushings of the specimen showed abnormal cells and squamous metaplasia. The impression at this point was that the lesion was a large-cell primary carcinoma of the lung. Mediastinoscopic findings were normal. Pulmonary function testing demonstrated a severe obstructive defect with an FEV1 of 0.65 L (25% of predicted), which was elevated to 0.75 L after bronchodilation. The total lung capacity was 145% of predicted, and the diffusion capacity was 53% of predicted. Ventilation-perfusion studies revealed a right upper lobe ventilation of 11.5% (total to right lung, 44.6%) and a perfusion of 12% (total to right lung, 44%). Two-dimensional echocardiography showed that there might be some hypertrophy of the right ventricle but that the pulmonary artery pressures were normal. A bone scan and CT scan of the abdomen showed no metastases.
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Fig 3. . (A) Chest radiogram demonstrates a 13-cm lesion in the periphery of the right upper lobe, adjacent to the chest wall and crossing the minor fissure to involve the upper part of the right middle lobe. (B) Contrast-enhanced computed tomographic scan shows a 14-cm mass in the posterior segment of the right upper lobe extending from the pleural surface to the hilum. The lobar branches of the right pulmonary artery cannot be adequately visualized using computed tomography. (C) Arteriogram outlining the right main pulmonary artery shows is to be free of tumor involvement and clearly shows the lobar branches of the right upper lobe artery, which appear uninvolved at their origins. A standard right upper lobectomy proved possible.
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It was thought that this patient was a very questionable candidate for resection, owing to his limited reserve. The patient was therefore sent for 5 weeks of intensive rehabilitation and voluntarily stopped smoking at this time. Rehabilitation was successful in improving his exercise tolerance (FEV1 of 1.2), and it was thought that the patient could tolerate thoracotomy and right upper lobectomy. At thoracotomy a large tumor was visualized in the right upper lobe, which extended into the fourth and fifth ribs adjacent to the posterior segment. Both the major and minor fissures were intact, and the tumor did not appear to involve either the middle or lower lobes. The superior vena cava was not involved. Complete excision of the mass was achieved, and the chest wall was reconstructed with Marlex mesh (Meadox Medical, Inc, Oakland, NJ). No lymph node metastases were found, and bronchial resection margins were negative for malignancy. Thus a sleeve lobectomy was not required. The patient's condition markedly improved postoperatively, and he continued to show improvement up to the time of discharge 6 days later. Pathologic examination of the excised tumor revealed a 14-cm, moderately differentiated squamous cell carcinoma that extended through the visceral into the parietal pleura, with negative resection margins.
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Comment
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The use of pulmonary arteriography in the preoperative characterization of carcinoma of the lung was reported as early as 1938 by Steinburg and Robb [1]. The procedure gained popular acceptance in the 1960s to 1970s for the staging of lung cancer. In their series of 371 pulmonary arteriograms performed at this institution in 1970, Delarue and colleagues [2] reported that this method was extremely accurate in its ability to delineate the extent of invasion of the main pulmonary artery by tumor. Furthermore, several authors have thought that the specific and detailed imaging of tumors of the hilar region is essential to determine the feasibility of curative resection [2–4].
The possibility of performing a successful pneumonectomy was at least partially determined by whether the tumor was found to involve the proximal segment of one or the other main pulmonary artery. The arteriogram also permitted the adjacent cardiac chambers to be assessed; in the case of upper lobe lesions, the innominate veins and superior vena cava could be studied in the same procedure. Arterial abnormalities were found to reflect the extent of bronchopulmonary segment invasion. The presence or absence of right ventricular or pulmonary hypertension, as measured during arteriography, was a further factor used to determine the feasibility of resection [3].
With the advent of improved lung imaging techniques, including CT scanning, the use of pulmonary arteriography declined. The CT scan, however, is inaccurate in its delineation of pulmonary arterial anatomy at the lobar level. Selective pulmonary arteriography remains the best means of determining local involvement of the pulmonary vasculature. In particular, we have found that selective pulmonary DSA has been valuable in the preoperative evaluation of candidates for sleeve lobectomy. Recent advances in DSA technology, including the use of nonionic contrast media, have led to an increase in the safety of the technique (decreased renal toxicity and allergic reactions) and in the quality (resolution) of the information gained, as compared with conventional pulmonary arteriography.
In his report on the use of pulmonary arteriography in the evaluation of carcinoma of the lung, Greenough proposed a classification system for tumors invading or compressing the pulmonary artery. The terminology can be applied to selective arteriography as well. The term encasement is used to describe areas where tumor surrounds the arterial wall and causes a concentric narrowing of the opacified lumen. Displacement refers to a mass effect causing a shift of the pulmonary artery, and irregular narrowing refers to a jagged-edge appearance of the lumen. Finally, an abrupt truncation of the artery denotes complete arterial occlusion by tumor and is regarded as pathognomonic of a malignant tumor [3].
Arteriography should not be utilized in isolation to determine inoperability; in particular, this modality should not serve as the basis for excluding a patient as a candidate for resection [4]. The results of pulmonary arteriography should be interpreted in concert with information gained from CT scanning, mediastinoscopy, and pulmonary function testing before deciding on the surgical resectability of a patient's tumor.
Selective DSA was a key modality in the preoperative assessment of the lung cancer patients described here who were candidates for sleeve lobectomy. Patient 1 was a poor candidate for pneumonectomy because of his limited pulmonary reserve. Computed tomographic studies showed tumor involvement adjacent to the left main pulmonary artery, but the extent of involvement was not discernible. Digital subtraction angiography demonstrated that the tumor encased the anterior segmental branch of the left upper lobe pulmonary artery and indicated possible involvement of the superior aspect of the left main pulmonary artery wall. It allowed the surgeon to preoperatively plan a rational approach to resect the tumor as well as to strategically resect a portion of the left main pulmonary arterial wall, allowing subsequent reconstruction with a pericardial patch arterioplasty. The case of patient 2 demonstrates that selective DSA is a helpful tool to confirm vascular integrity when bronchoscopy and CT scanning indicate possible tumor involvement of the vascular tree. In patient 3, preoperative CT scanning indicated possible tumor involvement of the superior vena cava, making the prognosis for curative resection poor. However, DSA, which is more sensitive in its ability to rule out vascular involvement, clearly showed that the superior vena cava and the pulmonary vascular tree surrounding the area of tumor were free of tumor invasion. Clearly DSA played an integral role in allowing surgeons to embark on curative resection.
In conclusion, selective pulmonary arteriography may be a valuable tool in the staging of lung cancer in patients who are candidates for sleeve lobectomy. The increased safety of the modality and the higher resolution offered by DSA allow its possible regular use in the preoperative assessment of the pulmonary artery lobar vasculature to delineate the extent of vascular invasion. The technique has been shown to be particularly helpful in determining whether it is technically possible to perform a sleeve resection and thereby ensure technical resectability by lobectomy when a pneumonectomy is contraindicated in a patient because of compromised pulmonary status. Furthermore, we have shown DSA to have three unique applications, when used in conjunction with the CT scan assessment, in facilitating preoperative decision-making and the planning of the surgical strategy. When arteriograms of the vascular tree show arterial wall invasion, the surgeon can then plan an effective sleeve lobectomy or excision of the involved vascular wall with reconstruction by arterioplasty, or both procedures. Digital subtraction angiography may also be used to more accurately visualize the vascular tree surrounding the tumor to determine whether a sleeve lobectomy is possible in the face of equivocal CT scan findings. Finally, arteriographic imaging may be used as a more sensitive way to either confirm or reject the vascular involvement by tumor presumed on the basis of CT findings. In fact, pulmonary arteriography is the only examination that can accurately identify the origins of the upper lobe branches of the pulmonary artery. Therefore the modality has been shown to be an essential tool for the surgeon working to cure lung cancer patients using the smallest and most efficient surgical intervention, thereby allowing a reduction in intraoperative complications and mortality with preservation of pulmonary reserve in the functionally limited patient.
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Footnotes
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Address reprint requests to Dr Keshavjee, Division of Thoracic Surgery, The Toronto Hospital, 200 Elizabeth St, EN 10-224, Toronto, ON M5G 2C4, Canada.
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References
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- Steinburg I, Robb GP. Mediastinal and hilar angiography in pulmonary disease. Am Rev Tubercluosis 1938;38:557–69.
- Delarue NC, Sanders DE, Silverberg SA. Complementary value of pulmonary arteriography and mediastinoscopy in individualizing treatment for patients with lung cancer. Cancer 1970;26:1370–8.[Medline]
- Greenough WG. Role of pulmonary arteriography in carcinoma of the lung. Chest 1972;62:206–10.
- Fryjordet A, Klevmark B. Investigation of operability in cases of bronchial carcinoma. Scand J Thorac Cardiovasc Surg 1971;5:97–102.[Medline]
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Abstract
Introduction
