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Ann Thorac Surg 2000;70:234-239
© 2000 The Society of Thoracic Surgeons

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Original articles: General thoracic

Lobectomy with tangential pulmonary artery resection without regard to pulmonary function

^a Section of General Thoracic Surgery, Division of Cardiothoracic Surgery, Department of Surgery, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
^b Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA

Address reprint requests to Dr Shrager, Division of Cardiothoracic Surgery, Hospital of the University of Pennsylvania, 6 Silverstein, 3400 Spruce St, Philadelphia, PA 19104
e-mail: jshrag{at}mail.med.upenn.edu

Presented at the poster session of the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Ft Lauderdale, FL, Jan 31–Feb 2, 2000.

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Non–small cell carcinoma of the lung invading the pulmonary artery (PA) has traditionally been treated by pneumonectomy. Although PA resection and reconstruction (PAR) has begun to gain acceptance, previous series of PAR by the simplest technique of tangential excision and primary repair have been unfavorable. We have maintained a policy of performing PAR preferentially whenever anatomically feasible, and usually this has been possible by tangential excision and primary repair. This study sought to determine if this approach is sound.

Methods. Retrospective clinical and pathologic review.

Results. Thirty-three PARs were performed from 1992 to 1999. The patients, followed 6 to 65 months (mean 25), were aged 36 to 80 years (mean 61), and their tumors were pathologic stage IB (n = 7), IIB (n = 13), IIIA (n = 9), and IIIB (n = 4). The mean preoperative forced expiratory volume in 1 second was 70% predicted. The procedures included 14 bronchial sleeve lobectomies with PAR and 19 simple lobectomies with PAR. The PARs were performed without heparinization and included 19 tangential excisions with primary closure, 11 larger tangential excisions with pericardial patch closure, and 3 sleeve resections. There were no operative deaths and 2 (6.1%) early major complications, all unrelated to the PAR. Thirteen patients (39%) had early minor complications. Four-year Kaplan-Meier survival was 48.3% for stages I/II and 45% for stage III. Ipsilateral, central, intrathoracic recurrence occurred in 3 patients (9.1%).

Conclusions. These data are not dramatically different from those reported for standard resections. Although the numbers are small, the results suggest that lobectomy with PAR by tangential excision is an acceptable alternative to pneumonectomy whenever anatomically possible.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Although there have been scattered reports since 1967 [1, 2] of pulmonary artery resection (PAR) performed in isolation or concomitantly with bronchial sleeve resection for non–small cell carcinoma of the lung (NSCLC), this procedure has been slower to gain acceptance than reconstruction of the bronchus alone. Most of the published cases have been performed by circumferential pulmonary artery (PA) sleeve resection and reanastomosis or pericardial or prosthetic tissue reconstruction. Concerns of thoracic surgeons who continue to perform pneumonectomy in the circumstance of PA invasion or encroachment that is anatomically amenable to PAR have included the possibilities of intraoperative or postoperative hemorrhage, pulmonary vascular thrombosis, and increased bronchial anastomotic complications. Furthermore, some have voiced concern that PAR may represent a compromise of oncologic principles and lead to more local recurrences, diminished long-term survival, or both.

Because there are only two published series in the last decade with substantial numbers of patients undergoing PAR [3, 4], it has been difficult to address these concerns. We report 33 patients undergoing PAR for NSCLC with concomitant lobectomy or bronchial sleeve lobectomy. Our technique, in contrast to that in recent series, is in most cases tangential excision with direct repair without the use of heparin. This approach makes the procedure simple and expeditious. We present data documenting that PAR can be performed in this manner with perioperative complications no more frequent or severe than in recent historical controls following pneumonectomy or bronchial sleeve resection without PAR. Furthermore, although even in this relatively large series the number of cases per stage was small, survival data suggest that there is no compromise of the chances of oncologic cure following PAR.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Data collection
We retrospectively reviewed the inpatient and outpatient charts of all patients undergoing PAR with or without bronchial sleeve resection for NSCLC at the University of Pennsylvania Health System between 1992 and 1999. Only PARs encompassing the origin of at least two branches off of the main PA or at least 3 cm in length were included in the analysis. Routine postoperative follow-up included an office visit with history, physical examination, and chest radiograph every 3 months for 2 years and every 6 months thereafter for a total of 5 years. Patients who were free of disease at their last outpatient visit were contacted to determine their current disease status. Follow-up to end points defined as death, disease recurrence, or current status as alive and free of disease was 100%. Diagnostic studies were reviewed as necessary to document sites of recurrence. All surgical specimens were reviewed by a pathologist with attention to determining PA invasion versus abutment, and whether PA involvement was by primary tumor or lymph node.

Because of the relatively small numbers, patients in stages I and II were combined for survival analysis and patients in stages IIIa and IIIb were similarly combined. Postoperative survival rates were determined using Kaplan-Meier analysis.

Surgical technique
The PARs (Table 1) included 19 tangential excisions of the arterial wall with primary closure, 11 more extensive tangential excisions with reconstruction using a patch of autologous pericardium, and 3 PA sleeve resections with primary end-to-end anastomosis. Pericardium was used when it was estimated that a tangential excision involved more than 25% of the circumference of the vessel. The visceral aspect of the pericardium was oriented to serve as the blood–surface interface in these cases. Flow within the PA was controlled during PAR by temporary proximal occlusion of the vessel using an umbilical tape with tourniquet or atraumatic vascular clamp. Distal occlusion of either the PA or the pulmonary vein from the lobe to be preserved was performed in similar fashion. In no case was heparin administered. Removal of air was performed before tying down the running, 5-0 Prolene (Ethicon, Somerville, NJ) repair sutures. In cases of combined PAR and bronchial sleeve resection, the PAR was completed first to allow rapid reestablishment of flow within the vessel. The bronchial anastomosis was created with interrupted, simple 4-0 polyglycolic acid sutures. Vascularized tissue was interposed between the two repairs consisting of either pedicled pericardial fat (preferred) or pleura in cases where the fat pad was inadequate. Defects created by harvesting pericardium were closed primarily with interrupted Prolene sutures or with a polytetraflourethylene patch for more extensive defects.

	Results

Top Abstract Introduction Material and methods Results Comment References

The patients included 23 men and 10 women. They were 36 to 80 years of age (mean 61). Patients who it was anticipated could tolerate a pneumonectomy by standard preoperative evaluative criteria were not excluded from consideration for PAR. In fact, the mean preoperative forced expiratory volume in 1 second (FEV₁) was 1.98 L (70% of predicted). Nine patients (27%) had a preoperative FEV₁ of less than 60% of predicted.

Surgical staging of mediastinal lymph nodes was performed preoperatively on 14 patients (13 mediastinoscopies, 1 left thoracoscopy for lymph node sampling). One of our surgeons performs surgical mediastinal staging selectively on the basis of lymph nodes greater than 1 cm in diameter on chest computed tomography; the other 2 perform it nearly routinely. Three patients received preoperative chemotherapy on the basis of documented N2 disease; 1 received preoperative chemotherapy and radiation therapy. Five patients underwent postoperative radiation therapy, 2 patients postoperative chemotherapy, and 2 patients postoperative chemoradiotherapy. The tumors included 17 squamous cell carcinomas, 8 adenocarcinomas, 6 poorly differentiated NSCLCs, and 2 large cell carcinomas. The average size of the tumors was 4.6 cm and ranged from microscopic disease (following neoadjuvant therapy) to 10 cm. Postoperative, pathologic stages were IB (n = 7), IIB (n = 13), IIIA (n = 9), and IIIB (n = 4). As the International System for Staging Lung Cancer does not directly address the issue of tumors that approach the pulmonary artery, we adopted the following schema: all tumors, whether they frankly invaded or simply abutted the pulmonary artery, were considered to be T2 even if smaller than 3 cm in size, because it was thought that they must breach the visceral pleura to approach the PA this closely. Those tumors that frankly invaded the PA were also classified as T2 rather than arbitrarily upstaging them to T3.

On pathologic review (Table 3), most cases (19 of 33; 58%) showed tumor closely abutting the PA but not frankly invading the vessel wall (Fig 1). Actual vascular invasion of the PA was present in 14 of 33 (42%). Although such invasion was usually limited to the adventitia (Fig 2), 1 patient showed intraluminal invasion (Fig 3). The primary tumor mass itself encroached on the PA in all but one case; in 6 cases, there was additional involvement of the PA by lymph node metastases (Fig 4). In 1 case, nonmalignant, granulomatous lymph nodes could not be separated from the artery, requiring PAR. In 2 cases, there was a positive PA margin on permanent sections that had not been identified on frozen section. Both were cases of tangential excision—1 with primary repair and 1 with pericardial patch repair. Both tumors showed adventitial invasion.

View larger version (134K): [in this window] [in a new window]   Fig 1. Squamous cell carcinoma abutting but not invading the pulmonary artery. Note the adjacent mainstem bronchial cartilage. (Hematoxylin and eosin; x25 before 46% reduction. B = bronchial cartilage; PA = pulmonary artery; T = tumor.)

View larger version (141K): [in this window] [in a new window]   Fig 2. Adventitial infiltration of the pulmonary artery by poorly differentiated non–small cell carcinoma. (Hematoxylin and eosin; x100 before 46% reduction. L = lumen; PA = pulmonary artery; T = tumor.)

View larger version (141K): [in this window] [in a new window]   Fig 3. Pulmonary artery with intraluminal invasion by moderately differentiated squamous cell carcinoma. (Hematoxylin and eosin; x50 before 46% reduction. L = lumen; PA = pulmonary artery; T = tumor.)

View larger version (153K): [in this window] [in a new window]   Fig 4. Metastatic squamous cell carcinoma in a lymph node abutting the pulmonary artery. (Hematoxylin and eosin; x50 before 46% reduction. L = lumen; LN = lymphoid follicle in anthracotic lymph node; M = metastatic tumor in lymph node; PA = pulmonary artery.)

View larger version (20K): [in this window] [in a new window]   Fig 5. Kaplan-Meier survival curves for stage I and II patients combined and stage III patients. Numbers adjacent to the curves represent patients at risk.

	Comment

Top Abstract Introduction Material and methods Results Comment References

There are several differences between our series and previous series. In our hands, PAR was performed to avoid pneumonectomy in patients with anatomically suitable lesions without regard to pulmonary function; thus the average preoperative FEV₁ in our patients of 1.98 L. Furthermore, the technique performed in most of our cases was tangential excision and primary repair without heparinization—a technique that is significantly simpler and more expeditious than those predominately used in most earlier series [3–5, 9]. Finally, we performed careful pathologic review to determine invasion versus simple abutment of the PA, the degree of invasion, and whether primary tumor or lymph node caused the encroachment. There were no perioperative mortalities, and the complications, local recurrence rates, and survival curves were no worse than after pneumonectomy for similarly staged lesions.

It has been well accepted by the thoracic surgical community for several years that bronchial sleeve lobectomy is an acceptable alternative to pneumonectomy when complete resection can be performed by this operation [11]. Pulmonary artery resection, although conceptually similar, has not been embraced with the same alacrity. This hesitance may stem from the claim presented without supporting data by Vogt-Moykopf and colleagues [5] that "... it is always better to restore vascular continuity by means of a sleeve ... than to try a [tangential excision] which often ends with an occlusion of the vascular lumen." One might also point to the two small published series noting high intraoperative or postoperative morbidity and mortality rates when performing PAR by tangential excision and primary repair. Read and coworkers [6] reported that 5 of 11 patients who underwent attempted tangential excision and primary repair ultimately required pneumonectomy because of either "ischemia of the left lower lobe or disruption of the pulmonary artery with hemorrhage." Wada and coworkers [8] reported 7 cases of tangential excision in a series of 9 PARs, but they had 8 serious complications including cardiac failure, pulmonary embolism, and empyema. It is not surprising that, with these serving as the only reports of PAR by tangential excision and primary repair, surgeons would hesitate to perform this procedure.

Rendina and coworkers [3] have recently demonstrated that, on the contrary, PA resection with routine pericardial reconstruction using systemic heparinization can be performed with low morbidity and mortality rates. They reported a single PA thrombosis in 52 cases, no deaths, and a low 13.4% overall morbidity rate. It is our belief, however, that most thoracic surgeons, because of the complexity of repairs performed in this manner and the fear of heparinizing such patients, will continue to hesitate to perform PARs by this technique.

In the present series we demonstrated that PAR can be performed safely and successfully in most cases with the simpler technique. Noncircumferential, tangential excision and primary repair, without heparinization, was performed in this series without the previously reported high rates of morbidity and with zero mortality. The absence of evidence of infarction or embolism in the remaining lobe(s) suggests that heparinization is not necessary when an expeditious repair can be performed. To assure that heparinization is not necessary, we perform the arterial repair before the bronchial repair.

Concerns regarding intraoperative complications are not borne out by our experience. We were never forced to convert to pneumonectomy once the PA incision had been begun. Careful examination of the extent of PA involvement before deciding on the appropriate procedure is critical here. In cases in which more than 25% of the circumference of the vessel was believed to be involved, reconstruction was performed either with a pericardial patch (n = 11) or a PA sleeve resection with end-to-end anastomosis (n = 3). Pneumonectomy was performed when even these options were considered to be not feasible.

Regarding morbidity and mortality, the absence of perioperative deaths in our series bears consideration. This mortality rate was better than even the most current operative mortality rates reported following pneumonectomy of 4.9% to 13.4% [11–13], although certainly most of these deaths occurred following right rather than left pneumonectomy. Our 6.1% incidence of major postoperative complications and 39% incidence of minor early complications are in the same range as those reported in recent series of bronchial sleeve lobectomy [11, 14, 15] and our own group’s experience with bronchial sleeve lobectomy (unpublished observations). These complication rates compare even more favorably with those reported for pneumonectomy in this decade [11–13].

Our incidence of benign, late anastomotic stricture (3 cases, 21% incidence) among the cases of PAR associated with bronchial sleeve resections was somewhat higher than the incidence in recent series of sleeve resections without PAR [11, 15], although in all of our cases these strictures have been successfully managed endoscopically. One might speculate that the relatively high rate of late stricture in our series was caused by the greater length of bronchus that had to be resected in these patients. Note that all of these tumors were carcinomas (as opposed to carcinoid tumors), and that cancers that encroach on the PA tend to be large (average tumor size 4.6 cm). It is notable in this regard that in our institution’s entire series of 63 bronchial sleeve resections, the only 3 strictures that occurred were in the 3 patients with concomitant PAR (unpublished observations).

Aside from the risk of surgical complications, the other reason surgeons have been slow to adopt PAR has been a feared lower rate of cure compared with pneumonectomy [16, 17]. Because of the relatively small numbers of patients that could be accumulated for this series of cases of an uncommon operation, we combined our stage I and II patients, and our stage IIIa and IIIb patients, to evaluate survival. The resulting 4-year estimated survivals of 48.3% for stages I and II, and 45% for stage III compared well with published survival data following standard pulmonary resections [18]. One must surmise that the improved survival in stage III versus accepted survival rates for this stage of disease following standard resections was a function of the small number of patients in this group.

Another major concern of those surgeons who have hesitated to perform PAR for oncologic reasons is a presumed increased risk of purely local recurrence. The 9.1% central, local recurrence rate demonstrated herein, however, was lower than that reported recently for patients in stage II following standard resections, approximately half of whom received adjuvant radiotherapy [19]. These results are especially notable in light of the fact that 39% of our patients were in stage III. If we count the 3 patients with peripheral recurrence in the ipsilateral, remaining lobe(s) as local recurrences, the local recurrence rate rises to 18.1%, still lower than the published data. Because this type of peripheral, ipsilateral, nodular "recurrence" either was present microscopically at the time of operation (in which case the stage was M1 from the start and the disease likely incurable) or was, in fact, late and distant metastatic disease, its occurrence would not seem to be a reason to perform pneumonectomy over lobectomy with PAR. If this late, peripheral, ipsilateral disease was believed to represent a new primary cancer, then the opportunity for surgical cure by completion pneumonectomy had not passed. Finally, because the vast majority of lung cancer recurrences occur within 2 years, it would be unlikely that our local recurrence rate would be dramatically increased with longer follow-up.

Our results allow us to comment regarding the appropriate staging of tumors invading the extrapericardial PA. Using conservative classification of these tumors that abut or invade the PA as T2, we have documented survival results not dramatically different from those reported for T2 tumors that do not involve the PA. Although, again, it is difficult to draw definitive conclusions from such a small group of patients, this finding at least suggests that such tumors need not be reclassified as T3 or higher. The findings that most of these lesions do not actually invade the PA but simply abut it, and that of the invading lesions only one was through the endothelium into the lumen, provide additional rationale for performing a PAR if possible rather than pneumonectomy. Without intraluminal invasion, there is no increased worry that the lesion might be prone to seed the remaining lobe.

In summary, this series consisted of 33 cases of PAR as an adjunct to pulmonary/bronchial resection for NSCLC. Our results with this procedure demonstrated that it can be performed with minimal mortality and with morbidity less than that of pneumonectomy, even when most cases are performed by a simple tangential excision and primary repair technique without heparin. Our pathologic review demonstrated that the vast majority of tumors requiring PAR do not extend transmurally into the PA lumen. This, and the fact that local recurrence and survival data are not significantly worse than following standard pulmonary resections without PAR, suggest that there is no need to reclassify tumors invading the extrapericardial PA as higher stage. There is a suggestion that the addition of PAR to bronchial sleeve resection may predispose to late stenosis of the bronchial anastomosis. On the basis of these results, we will continue our policy of performing PAR rather than pneumonectomy in all cases in which it is anatomically feasible, regardless of pulmonary function.

	References

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This Article Abstract Full Text (PDF) 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): Joseph B. Shrager Maher E. Deeb Larry R. Kaiser Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Shrager, J. B. Articles by Kaiser, L. R. Search for Related Content PubMed PubMed Citation Articles by Shrager, J. B. Articles by Kaiser, L. R.