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Ann Thorac Surg 1999;68:995-1001
© 1999 The Society of Thoracic Surgeons
a Department of Thoracic Surgery "La Sapienza" University of Rome, Rome, Italy
Address reprint requests to Dr Rendina, Department of Thoracic Surgery, University "La Sapienza," 00161 Rome, Italy
Presented at the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio TX, Jan 25–27, 1999.
Abstract
Background. Lobectomy associated with reconstruction of the pulmonary artery (PA) is a technically feasible alternative to pneumonectomy in patients with lung cancer. However, concern about postoperative complications and long-term survival limited its acceptance so far.
Methods. Between 1989 and 1996, we performed a PA reconstruction in 52 patients (41 men, 11 women; age range 35 to 75 years, mean 60 years) with lung cancer. Eleven patients had induction chemotherapy. We performed 15 PA sleeve resections, 34 PA reconstructions by a pericardial patch, and three PA reconstructions by a pericardial conduit, associated with a bronchial sleeve lobectomy or bilobectomy (33), or with standard lobectomy (19). Immediate and long-term postoperative evaluation included spirometry, echocardiography, perfusion lung scans, computed tomography, and PA angiography. The follow-up ranged between 27 and 96 months and is complete for all patients.
Results. We had one specific postoperative complication (PA thrombosis) and no mortality. Perfusion scans and PA angiography were normal in all but the 1 patient having thrombosis. Mean forced expiratory volume (FEV) in 1 s and forced vital capacity (FVC) were, respectively, 72% and 80% preoperatively, 65% and 76% 1 month after surgery, and then they plateaued at 70% and 78% after 6 months. Echocardiography showed patterns in the normal range and normal estimates of PA pressures in all but 2 patients. Five-year survival was 38.3% for the entire group, 18.6% for stages IIIA and B, and 64.4% for stages I and II.
Conclusions. Morbidity, mortality, and functional data do not differ from what is currently reported for standard lobectomy. Long-term survival is in line with that reported for standard resection. These data support PA reconstruction as a viable option in the treatment of lung cancer.
Unlike bronchial sleeve lobectomy [1–3], sleeve resection and prosthetic reconstruction of the pulmonary artery (PA) has not yet gained acceptance as an alternative to pneumonectomy in lung cancer surgery. This is due in part to the concern of intraoperative and postoperative complications, but especially to a supposed decrease in the long-term survival [4]. In addition, there are no data in the literature regarding the long-term patency of the reconstructed PA and its impact on cardiopulmonary function. However, bronchial sleeve lobectomy is an oncologically adequate operation [1, 2] and its advantages in terms of respiratory capacity have been clearly demonstrated [3], just as much as the detrimental effects of pneumonectomy on right heart function [5–7]. These findings have consolidated the opinion that pneumonectomy is a "disease in itself" and should be avoided whenever possible [8]. The aim of our study was to evaluate the long-term viability of the reconstructed PA in terms of cardiopulmonary function and the efficacy of lobectomy associated with PA reconstruction to warrant complete resection of lung cancer and long-term survival.
Material and methods
Between May 1989 and July 1996, we performed a PA reconstruction in 52 patients with non–small-cell lung cancer. Preoperative workup included pulmonary function tests, blood gas analysis, electrocardiograph and Doppler echocardiography, fiberoptic bronchoscopy and total-body computed tomography (CT). The indication for PA reconstruction was anatomical feasibility; the procedure was therefore performed also in patients who had no functional contraindications to pneumonectomy.
Surgical technique
The surgical technique that we employed for sleeve resection [9, 10], reconstruction by an autologus pericardial patch [9, 10], or conduit [11] has been described in detail elsewhere. The PA sleeve is usually performed after completion of the bronchial anastomosis to minimize manipulation of the vessel. In addition, the exposure of the bronchial stump is optimal when the artery is divided. After intravenous injection of 3,000 to 5,000 U of heparin sodium, the PA is clamped at its origin. On the left side, it is often necessary to transect the ligamentum arteriosum to clamp the artery far enough from the infiltrated zone. The artery is not occluded distally, and back flow is avoided by clamping the inferior pulmonary vein. After completion of the bronchial reconstruction, the end-to-end arterial anastomosis is performed with running sutures of 5/0 or 6/0 nonabsorbable monofilament material. If a pericardial patch reconstruction is indicated, this is usually performed before the bronchial anastomosis to reduce the arterial clamping time. In 31 patients, an autologous pericardial patch was used: the patch is created from the pericardium anterior to the phrenic nerve and trimmed to match the arterial defect. A leaflet larger than the arterial defect is harvested and the pericardial sac can be left open. Trimming the patch must be performed very carefully, because the pericardium shrinks markedly after harvesting and a proportional distension must be predicted after the reconstruction is completed. This is best obtained by immersing the pericardium in cold saline solution and cutting it to the appropriate shape by curved scissors with a continuous motion to avoid irregularity of the edges. In 3 patients, we employed a bovine pericardial patch (Bio-Vascular Inc, Minneapolis, MN). The bovine pericardium is stiffer, does not recoil, and is much easier to trim to the appropriate size and to suture to the artery. For extended circumferential defects in which end-to-end anastomosis is not feasible, we used a conduit of autologous pericardium. The pericardium is harvested as previously described, wrapped around a 28 F chest tube, and sutured longitudinally with 6/0 monofilament nonabsorbable material. A conduit of 1 to 2 cm is thus created. The conduit is then pulled out of the chest tube and anastomosed to the proximal stump of the PA by running 5/0 monofilament sutures. The distal anastomosis is performed last after the conduit has been trimmed to the appropriate length by overlapping the suture margins. All resection margins are checked by frozen section examination. Viable tissue (intercostal muscle, pleura, pericardial fat) is always interposed between the artery and the bronchus. At the end of the procedure, heparin is not reversed by protamine sulfate. Patients are routinely extubated in the operating room. Mild anticoagulation therapy (15,000 U/day subcutaneously) is administered for the first postoperative week.
Postoperative evaluation
Early postoperative PA angiograms were taken routinely within 1 week of the operation in the first 11 patients. In 3 additional patients, angiography was performed upon clinical indication to exclude early PA occlusion. After surgery, all patients underwent spirometry, electrocardiogram, Doppler echocardiography, and perfusion lung scans at 1, 6, and 12 months. These tests were repeated yearly thereafter. Doppler and two-dimensional echocardiography was particularly aimed at the evaluation of the right heart and PA pressure [12]. We recorded the transverse diameter of the right ventricle (RV) and the end diastolic RV area. Systolic PA pressure was calculated in patients with tricuspid incompetence, and pulmonary flow velocity and time to peak of pulmonary flow curve were assessed by pulsed Doppler. The long-term patency of the PA and the distal PA branching in the residual lobe were further evaluated by CT with injection of contrast material. CT was performed 6 and 12 months after the operation, and subsequently every year for the first 5 postoperative years also as part of the oncologic follow up. Angio-magnetic resonance (MR) was performed in 15 of the 17 patients currently alive as a noninvasive means to obtain better imaging of the reconstructed PA. The reason why only this group of patients underwent MR is that this technique became available only recently at our institution. Follow-up ranged between 2.3 and 8 years (mean 3.3 years) and is complete for all patients. Survival is calculated with the product limit method by Kaplan and Meier [13]. Differences among curves were analyzed by the log-rank test and the 
2 test.
Results
We operated on 52 patients with non–small-cell lung cancer (33 squamous cell, 15 adenocarcinoma, 4 large cell carcinoma). Forty-one patients were men and 11 women; age ranged between 35 and 75 years (mean 60 years). Following the 1986 staging system, 6 patients were at stage I, 16 at stage II, 18 at stage IIIA, and 12 at stage IIIB. Among the 12 stage IIIB patients, 10 had induction chemotherapy. Overall, 11 patients had induction chemotherapy and 3 had preoperative radiotherapy. Nineteen patients had N2, and 21 had N1 disease. We performed 15 PA sleeve resections, 34 PA reconstructions by a pericardial patch, and three PA reconstructions by a pericardial conduit. The reconstructive procedure was associated with a bronchial sleeve lobectomy in 31 patients, with a bronchial sleeve bilobectomy in 2, and with standard lobectomy in 19. The PA reconstruction was performed on the right side in 12 cases and on the left side in 40 cases. All patients underwent upper lobectomy, with the exception of 1 patient, who underwent left lower sleeve lobectomy and patch reconstruction of the lower aspect of the PA. Complete resection was achieved in 49 of 52 patients (94%). Postoperative complications occurred in 7 patients (13.4%). Complications occurring in 52 patients included:
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Cause of death in 9 patients dying of nonneoplastic causes included:
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One patient died of the hemoptysis 6 years after bronchial and vascular sleeve resection after induction chemotherapy. Necropsy failed to demonstrate a broncho-arterial fistula. One complication was specifically related to the PA reconstruction: PA thrombosis occurred in a 67-year-old woman with T3N1 adenocarcinoma who had undergone left upper sleeve lobectomy with pericardial patch reconstruction of the PA. This occurred after 35 uncomplicated procedures and after 5 years of experience in the field. On the second postoperative day, the patient developed occlusion of the left PA demonstrated by angiography (Fig 1). A technical error was probably the cause of the complication.
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Preoperative spirometry disclosed mean values of forced expiratory volume in 1 s (FEV1) and forced vital capacity (FVC) of 72% ± 18% and 80% ± 15% of predicted. One month postoperatively, the values decreased to 65% ± 20% and 76% ± 18% and then plateaued at 70% ± 19% and 78% ± 17% after 6 months. Perfusion scans demonstrated normal perfusion (between 24% and 42% of total lung perfusion) of the residual lobe throughout the study period in all but 2 patients. The first patient is the one that had early thrombosis, and the second developed multiple bilateral pulmonary embolism 5 years postoperatively. This patient also developed signs of pulmonary hypertension and right heart failure. With the exception of these 2 cases, the remaining patients had electrocardiogram and Doppler echocardiography findings within normal limits throughout the follow-up period. No significant modification of the area of the RV nor of the RV free wall occurred. None of the patients developed signs of pulmonary hypertension (> 30 mm Hg). Moreover, the time to peak of pulmonary flow curve and pulmonary flow velocity remained within the normal range. In these patients, CT with injection of contrast material showed normal visualization of the reconstructed PA and normal PA branching in the residual lobe. Fifteen of the 17 patients currently alive underwent angio-MR for better imaging of the reconstructed PA 27 to 96 months after the operation. The patency of the PA was confirmed in all cases (Figs 2–4). Two patients who are currently asymptomatic and in good general health refused the procedure. These patients had normal CT, perfusion scans, and echocardiography at last check. Survival data are complete for all patients. Thirty-five patients died 1 to 76 months after surgery, and 17 are currently alive. Twenty died of metastasis, 4 had local recurrence, 2 died of neoplastic cachexia, and 9 died of nonneoplastic causes.
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During the last decade, a number of articles appeared in the literature that deal with the advantages of bronchial sleeve resection as an alternative to pneumonectomy in various settings of pulmonary surgery [1–3, 9]. Conversely, comparable procedures regarding the PA have not yet achieved full acceptance [4, 10, 14]. The reasons for this dim outlook are multiple; technical complexity might be the first, followed by the concern regarding postoperative complications and by the suspicion of decreased long-term survival [4]. We have examined the technical aspects of PA reconstruction previously [9–11], and have pointed out that the vascular procedure is often easier and faster than the bronchial anastomosis. With increasing experience, the various techniques for PA reconstruction are progressively acquiring specific indications according to the anatomical setting. Tangential resection and primary suture is not included in our review, and we believe it should be more appropriately considered as a variation of standard lobectomy. Pericardial patch reconstruction is a versatile technique but few points deserve attention. Extended circumferential defects (over 50% of the arterial wall) should probably not be reconstructed by a pericardial patch. Under these circumstances, it is very difficult to obtain a smooth and regular lumen. The residual strip of arterial wall connecting the two stumps is of no use, and a sleeve resection would be more appropriate and safe. The use of autologous pericardium has many advantages but this material shrinks after harvesting and stretches when the PA pressure is restored, thus making its trimming to the appropriate size difficult. In addition, the edges of the pericardial leaflet tend to recoil during suturing, and the reconstruction might not be straightforward. Bovine pericardium is stiffer and eliminates these problems; its patency remains satisfactory in the immediate and mid-term. We have not yet used bovine pericardium for tubular reconstruction; its adequacy in this setting remains therefore to be demonstrated. In most other cases, sleeve resection proved an adequate procedure. When a bronchial sleeve also is performed, the bronchial axis is shortened and the arterial stumps will easily reach with no tension. In the rare cases where this does not occur, the interposition of a pericardial conduit proved effective. With regard to postoperative complications, the only specific problem in our series was due to very easily detectable reasons such as technical error. In fact, the infiltration involved over 60% of the circumference of the PA, and the use of an autologous pericardial patch yielded an exceedingly long and irregular artery. This caused kinking of the vessel and impairment of blood flow. The kinking probably resulted from the rotation of the PA axis caused by the reexpansion and elevation of the lower lobe. The patient was then reoperated and completion left pneumonectomy was performed. In the seventh postoperative day after the second procedure, a full lumen bronchopleural fistula developed. The ensuing empyema was treated by tube thoracostomy and irrigation for 3 months, and the pleural space was subsequently filled by omentopexy. The patient is currently alive, with no evidence of disease, although with signs of pulmonary hypertension and RV dilatation, 51 months after the first operation.
Mid- and long-term evaluation of patients undergoing PA reconstruction are based upon three issues: (1) patency of the PA and perfusion of the residual lobe; (2) right heart function; and (3) analysis of survival.
Immediately after the operation, patency problems occurred in less than 2% of cases. In the absence of clinical symptoms, routine invasive evaluation of the PA as well as perfusion lung scans are therefore redundant. In the long term, 1 patient had multiple pulmonary embolism demonstrated by perfusion scans, associated with an increase of the systolic PA pressure and dilatation of the RV. The emboli were, however, bilateral, suggesting that their origin was peripheral. CT is a versatile noninvasive diagnostic tool, useful in evaluating both PA patency and distal PA branching, as well as the overall oncological status of the patient. Newer noninvasive techniques such as angio-MR provide outstanding imaging of the PA, and may be very useful in demonstrating patency problems even in the immediate postoperative period. However, once the normal blood flow through the PA has been restored and the new orientation of the PA due to the reexpansion of the residual lobe has taken place without kinking in the early postoperative period, patency impairment is very unlikely to occur.
Our cardiological follow-up was specifically intended to confirm the advantages in terms of right heart function and morphology obtained by the preservation of a normally perfused lobe. There is nothing new in this concept with respect to standard lobectomy as compared with pneumonectomy [15–18], but there are no data on right heart function after PA reconstruction. Bronchial sleeve lobectomy equals standard lobectomy in terms of pulmonary function [3]; our data indicate also that PA reconstruction equally relates to standard lobectomy in terms of RV morphology and function. Doppler echocardiography is an accurate technique for the evaluation of the RV and for the estimation of PA pressures [12]. More precise techniques such as the thermodilution method adopted by Reed and associates [19] are necessarily invasive and therefore inadequate for a serial long-term survey.
Because the reports on PA reconstructions have been rare in the literature so far, the long-term survival of these patients is uncertain [4, 10]. Also, comparison with other series is difficult because the size, demographics, inclusion criteria, and duration of follow-up are highly variable. We believe it is noteworthy that the survival in our series is comparable stage by stage to that reported in the major reviews on lung cancer surgery and sleeve resection in the literature [2, 20–22]. The impact of the nodal status on survival is also comparable with that reported for bronchial sleeve [2, 20] and standard resection [21]. In the face of N1 or N2 involvement, once the decision to resect the disease with intent to cure is taken, some surgeons would prefer pneumonectomy to achieve better tumor clearance. Our data support PA reconstruction as an adequate procedure as well in this setting. Also, there is no statistically significant difference between PA reconstruction alone or PA reconstruction associated with bronchial sleeve. This suggests that even complex lung-sparing operations can be pursued with intent to cure as long as a complete anatomical resection is obtained.
In conclusion, morbidity, mortality, spirometry, perfusion scans, and cardiological data of PA reconstruction do not differ from what is currently reported for standard lobectomy. Long-term survival is in line with that reported for standard resection. These data support PA reconstruction as a viable option in the treatment of lung cancer.
Acknowledgments
We thank Dr Susanna Sciomer and Dr Dario C. Vizza for performing and analyzing the echocardiographic studies, and Maurizio Seminara and Mario Passacantilli for preparing the illustrations. The consultant statistician for this work was Dr Claudio Ceccarelli, Italian National Institute of Statistics, ISTAT, Rome, Italy.
Footnotes
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/
References
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