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(Chest. 2004;125:1581-1586.)
© 2004 American College of Chest Physicians

The Use of Cardiopulmonary Bypass During Resection of Locally Advanced Thoracic Malignancies*

A 10-Year Two-Center Experience

John G. Byrne, MD, FCCP; Marzia Leacche, MD; Arvind K. Agnihotri, MD; Subroto Paul, MD; Raphael Bueno, MD, FCCP; Douglas J. Mathisen, MD, FCCP and David J. Sugarbaker, MD, FCCP

* From the The Divisions of Cardiac Surgery (Drs. Byrne, Leacche, and Paul) and Thoracic Surgery (Drs. Bueno and Sugarbaker), Brigham & Women’s Hospital, Boston, MA; and the Cardiac Surgery Unit (Dr. Agnihotri) and Thoracic Surgery Unit (Dr. Mathisen), Massachusetts General Hospital, Boston, MA.

Correspondence to: John G. Byrne, MD, FCCP, Brigham & Women’s Hospital, Division of Cardiac Surgery, 75 Francis St, Boston, MA 02115; e-mail: JBYRNE{at}PARTNERS.ORG


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
The use of cardiopulmonary bypass (CPB) for locally advanced thoracic malignancies is highly controversial. The purpose of this study was to document the techniques and results of CPB to facilitate the resection of complex thoracic malignancies and to identify common themes that provided for successful outcomes. This was a retrospective study that took place from January 1992 to September 2002. Fourteen consecutive patients (median age, 59 years; age range, 18 to 69 years; seven men and seven women) underwent CPB during the resection of locally advanced thoracic malignancies at two Boston hospitals. CPB was planned in 8 of 14 patients (57%) with centrally located tumors, while 6 of 14 patients (43%) required emergent institution of CPB due to injury of the superior vena cava (2 patients), inferior vena cava (2 patients), or pulmonary artery (2 patients). Complete microscopic resection was achieved in 12 of 14 patients (86%). The operative mortality rate was 1 of 14 patients (7%) due to pulmonary embolism (ie, the elective group). The median ICU and hospital lengths of stay were 5 and 9 days, respectively. The overall 1-year, 3-year, and 5-year survival rates were 57%, 36%, and 21%, respectively. The planned use of CPB to facilitate complete resection of thoracic malignancies should be considered only after careful patient selection. The availability of CPB also provides a safety net in the event of injury to vascular structures during tumor resection.

Key Words: cardiopulmonary bypass • thoracic surgery • tumor


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
The use of cardiopulmonary bypass (CPB) during pulmonary operations, with the exception of lung transplantation, is highly controversial.123 Most surgeons are reluctant to perform lung procedures combined with cardiac procedures using CPB due to the adverse effects of CPB on hemostasis2 and lung function.4 There is also a theoretical possibility of enhancement of metastasis due to the immunosuppression caused by the pump and blood transfusion. However, surgical resection of central, locally advanced malignancies may require CPB because they involve, or are prohibitively close to, the heart and/or the great vessels. Thus, in a small subset of patients, CPB may facilitate, or provide a safety net to achieve, complete surgical resection. Since the literature is limited, consisting mainly of anecdotal cases only,567 we sought to analyze patient selection, indications, techniques, and results in patients who required CPB to facilitate the resection of thoracic malignancies at two hospitals, each with large cardiac and thoracic units.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
Patient Population
We retrospectively reviewed patient records and identified those who had undergone CPB during major general thoracic procedures between January 1992 and September 2002 at the Brigham & Women’s Hospital and Massachusetts General Hospital. Patients requiring CPB to facilitate lung transplantation or tracheal reconstruction for benign disease were excluded. Fourteen consecutive patients (median age, 59 years; age range, 18 to 69 years; seven men and seven women) from among the approximately 20,000 who underwent pulmonary resections for malignancy during the same time period were identified. Demographic data, symptoms and signs at presentation, preoperative induction radiation or chemotherapy, operative reports, anesthesia records, pathology reports, laboratory data, and imaging data were retrospectively reviewed. The decision to proceed with planned resection using CPB was determined on an individual basis after multiple imaging assessment, and consideration of patient-related and tumor-related factors. Imaging techniques to identify distant metastases included CT scans of the brain, chest, and abdomen, and bone scintigraphy. Patients with evidence of distant metastases by imaging techniques or a positive pleural effusion finding were excluded from surgery, with the exception of one 36-year-old patient with known metastatic mesenchymal chondrosarcoma in whom surgery was deemed appropriate to relieve the obstructive symptoms on the heart. Surgical resection was considered to be complete if microscopic margins were free of tumor.

For patients requiring emergent implementation of CPB, the decision to institute CPB was undertaken intraoperatively by the thoracic and the cardiac surgeon. The general indication for emergent CPB was injury to a vital structure during tumor resection.

Patient characteristics are shown in Table 1 . Survival status was assessed through the social security death index. The survival curve was calculated using the method of Kaplan and Meier.


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  		Table 1. Patient Characteristics*

 

   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
Operative Techniques
Elective CPB:
The use of CPB was planned in 8 of 14 patients (57%) based on preoperative imaging and intraoperative confirmation of tumor involvement in the left atrium (3 patients), pulmonary artery (4 patients), or superior vena cava (1 patient). The operative approaches were based on tumor anatomy and reconstructive needs. In three of eight patients, the left atrium was known to be involved with tumor, and a median sternotomy (two patients) was deemed to be appropriate to enable central cannulation, aortic clamping, cardioplegia, and deairing. In the remaining patient with left atrium involvement, a right thoracotomy was used, with ascending aorta and bicaval cannulation, fibrillatory arrest, and transesophageal echocardiography-guided deairing. In two patients with known pulmonary artery tumor involvement and the need to reconstruct the pulmonary artery with a homograft, a median sternotomy was used. In two patients with known tumor involvement of the left main pulmonary artery, a left thoracotomy was used with cannulation of the descending thoracic aorta and femoral vein, and reconstruction of the pulmonary artery with autologous pericardium. In these patients, the left femoral vein was cannulated with a small-caliber catheter prior to turning the patient to the side. In the remaining elective CPB patient, who had a thymic carcinoma invading the superior vena cava, a median sternotomy was deemed to be appropriate.

Emergent CPB:
In the emergent group, CPB was required for the repair of injury to the superior vena cava (two patients), the inferior vena cava (two patients), or the pulmonary artery (two patients). In five of six patients, a right thoracotomy had been used, and emergent cannulation was achieved via the ascending aorta and right atrium or via bicaval cannulation. In the remaining emergent patient, a left thoracotomy had been used, and cannulation was achieved via the descending thoracic aorta and the main pulmonary artery. Injuries to the superior vena cava (two patients), the inferior vena cava (two patients), the right pulmonary artery (one patient), and the left pulmonary artery (one patient) were repaired primarily (one patient), with autologous pericardium (four patients), or with a synthetic fabric (Dacron; Dupont; Wilmington, DE) [one patient]. The mean (± SD) CPB duration was 111 ± 59 min, the mean CPB flows were 3.5 ± 0.8 L/min, the mean CPB pressure was 58 ± 11 mm Hg, and the mean CPB temperature was 30 ± 6°C.

Completeness of Resection:
A complete resection was achieved in 12 of 14 patients (86%). In the remaining two patients, one had known metastatic chondrosarcoma, was operated on for palliation of constrictive cardiac symptoms, and died on postoperative day 1 from a tumor embolus. The other remaining patient had residual microscopic disease.

Postoperative Course
Nonfatal complications that are common to general thoracic resections and are not necessarily attributable to the use of CPB included new atrial fibrillation (four patients), pulmonary failure requiring tracheotomy (three patients), pneumothorax (five patients), pulmonary embolism (one patient), pneumonia (four patients), pleural effusion (seven patients), and empyema (one patient). Complications that were more likely attributable to the use of CPB included low cardiac output syndrome (defined as the need for inotropic support to separate from CBP) [five patients], reoperation for bleeding (three patients), stroke (one patient), and pulmonary edema (one patient).

The median hospital length of stay was 9.5 days (range, 1 to 30 days), and the median ICU length of stay was 5 days (range, 1 to 24 days). The median duration of mechanical ventilator support was 2.5 days (range, 1 to 21 days). The median follow-up was 16 months (range, 2 to 107 months). The overall 1-year survival rate was 57% (8 of 14 patients), the 3-year survival rate was 36% (5 of 14 patients), and the 5-year survival rate was 21% (3 of 14 patients) [Fig 1 ]. The median durations of survival for the elective and emergent groups were 18 months and 13 months, respectively.



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  		Figure 1. Overall survival after tumor resection, including one operative death.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
The use of CPB to allow extended resection of thoracic malignancies that invade the tracheal bifurcation, the left atrium, or the great vessels is not new. In 1961, Woods et al8 and Nissen9 demonstrated the feasibility and surgical technique for these resections. Since then, many advancements have been made in the treatment of thoracic malignancies, particularly extending the indications for resection and combining the surgery with adjuvant treatments (ie, chemotherapy, radiation therapy, or both). However, the selection criteria and outcomes of patients in whom CPB is used to facilitate the resection of locally advanced thoracic malignancies are still not clearly defined. Because these operations are rare, we combined the 10-year experience at two hospitals, each of which has large cardiac and thoracic units. We sought to identify common themes that provided for successful outcomes.

Choice of Incision and Cannulation Sites
In the emergent group, the use of CPB was a life-saving technique. In this group, resection in five of six patients had been approached via right thoracotomy, and the decision regarding cannulation was therefore more straightforward than in the one patient who had been approached via left thoracotomy. In patients who underwent right thoracotomy, emergent cannulation was easily achieved via the ascending aorta and the right atrium. In the emergent patient who underwent left thoracotomy, cannulation was achieved via the descending thoracic aorta and main pulmonary artery. Unlike in the elective group, in which two patients underwent resection via left thoracotomy, with the femoral vein cannulated with a small catheter while the patients were supine in the lateral decubitus position, femoral vein cannulation for CPB is much more difficult without the prior elective placement of a catheter in the femoral vein.10 In this setting, the only reasonable option for venous cannulation for CPB is the main pulmonary artery directing the cannulae into the right ventricle or opening the pericardium and cannulating the right atrium. However, exposure of the right atrium is highly variable, and this may prove to be troublesome in an emergent situation. In the planned surgery group, five of eight patients underwent resection via median sternotomy with routine central cannulation.

In our view, the choice of incision should be based first on whether complete surgical resection is feasible, after which the choice of cannulation sites should follow. With the peripheral cannulation site prepared before turning the patient to the side, this approach is usually reasonable.

Is an Aggressive Approach Justified in Elective Patients?
In our cohort of patients, non-small cell lung carcinoma (NSCLC) was present in half of the patients. The 5-year survival rate for stage I NSCLC is 65%, for stage II it is 50%, while for stages IIIA and IIIB it is as low as 23% and 6%, respectively.11 Therefore, this aggressive surgical approach is only justified in patients with early-stage cancer or in selected patients with advanced disease. In our elective group, three of eight patients had NSCLC, all with N0 disease at resection, making an aggressive approach reasonable. Our longest survivor was a patient who originally presented with N2-positive stage IIIA lung cancer and was treated with neoadjuvant chemotherapy prior to resection. She is still alive almost 9 years after undergoing surgery. The median survival time for the seven patients with NSCLC (both elective and emergent) was 18 months. The median survival time for the elective group (ie, with NSCLC and other pathologies) was also 18 months. Tsuchiya et al13 demonstrated a 17% overall survival rate at the 3-year follow-up in patients who underwent extended resection of NSCLC invading the great vessels and left atrium. Similarly, another study14 reported a 5-year survival rate of 19% after complete resection of advanced NSCLC invading the left atrium and great vessels, while those patients who had incomplete resection had a 0% survival rate at the 5-year follow-up. We were able to achieve complete microscopic resection in 12 of 14 patients with overall 1-year, 3-year and 5-year survivals rates of 57%, 36%, and 21%, respectively. In the two patients who had residual disease, one had known metastatic disease and surgery was palliative to relieve compressive cardiac physiology, and in the remaining patient the microscopic margins were positive. We think that our relative success in complete resection and survival is due to our careful patient selection utilizing radiographic imaging and intraoperative inspection, which we think are mandatory prior to undertaking this aggressive approach. Neoadjuvant chemotherapy and radiation therapy also should be considered in an attempt to downstage the patient and make successful resection more likely.

Complications
Complications that are more likely attributable to the use of CPB include low cardiac output (five patients), requirement of inotropic support to separate from CBP, stroke (one patient), pulmonary edema (one patient), and reoperation for bleeding (three patients).

In our series, low cardiac output was temporary, and the majority of patients were weaned from inotropic support within a few hours. Most patients had preserved left ventricular function, and the need for inotropic support was likely related to the effects of CPB on the myocardium.15 Bleeding related to systemic heparinization, particularly after pneumonectomy, is another concern when performing the resection of thoracic malignancies using CPB. In our series, all three patients requiring reoperation for bleeding had undergone pneumonectomy. In an attempt to avoid this problem, previous reports12 have suggested performing limited pulmonary resections before heparinization and the institution of CPB. Sometimes, this is not possible, and surgeons should understand that the frequency of reexploration for bleeding may be relatively high.

Possible systemic tumor dissemination due to alteration of the immune system or direct vascular dissemination is another concern during resections performed with CPB.16 The immunologic effects of CPB with activation of polymorphonuclear leukocytes tend to be greater in the first 3 to 12 h17 and to disappear within 24 h.18 Four patients in our series died within 6 months of surgery, two in the elective group (both at 4 months) and two in the emergent group (at 2 and 4 months). The earliest death in our series occurred at the 2-month follow-up. The patient died from respiratory failure due to Aspergillum infection developing 1 month after the initial surgery. It is difficult, if not impossible, to discern whether the immunologic system was depressed due to the delayed effects of CPB or the cachetic state of the patient was induced by the tumor itself. Another patient who died at 3.6 months of metastatic disease had a high-grade sarcoma at the time of surgery and later died from metastasis to the brain that had not been present (as determined by CT scan) at the time of surgery. We concur with Gillinov et al5 that unrecognized metastatic disease in this case is more probable than CPB-related dissemination. Currently, there are no data in the literature to support a role for the spread of malignancy by CPB that is attributable to immunosuppression.1219


   Conclusions
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
In our experience, the resection of locally advanced thoracic malignancies using CPB is rarely a necessity, but it can be safely achieved with low morbidity and mortality. With careful patient selection, acceptable midterm survival can be achieved. Furthermore, the emergent institution of CPB for the repair of injury to a vascular structure during pulmonary resection is life-saving and effective. The small number of patients in our series precludes any specific recommendations for surgical techniques. We think that a combined and well-coordinated effort among the general thoracic surgeon, the cardiac surgeon, the perfusionist, and the anesthesiologist is required for a successful outcome.


   Acknowledgements
 
We acknowledge the contribution of Suhas C. Bendre, MD, in data acquisition.


   Footnotes
 
Abbreviations: CPB = cardiopulmonary bypass; NSCLC = non-small cell lung carcinoma

Received for publication October 29, 2003. Accepted for publication December 23, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

  1. Miller, DL, Orszulak, TA, Pairolero, PC, et al (1994) Combined operation for lung cancer and cardiac disease. Ann Thorac Surg 58,989-993[Abstract]
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  4. Massoudy, P, Zahler, S, Becker, BF, et al Evidence for inflammatory responses of the lungs during coronary artery bypass grafting with cardiopulmonary bypass. Chest 2001;119,31-36[Abstract/Free Full Text]
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  6. Korst, RJ, Rosengart, TK Operative strategies for resection of pulmonary sarcomas extending into the left atrium. Ann Thorac Surg 1999;67,1165-1167[Abstract/Free Full Text]
  7. Ferguson, ER, Jr, Reardon, MJ Atrial resection in advanced lung carcinoma under total cardiopulmonary bypass. Tex Heart Inst J 2000;27,110-112[ISI][Medline]
  8. Woods, FM, Neptune, WB, Paltchi, A Resection of the carina and main-stem bronchi with the use of extracorporeal circulation. N Engl J Med 1961;264,492-494[ISI][Medline]
  9. Nissen, R Extrakorporelle zirkulation für langdauernde (30 minuten) atemunterbrechung zur operation bifurkationsnaher tracheal-geschwülste. Schweiz Med Wochenschr 1961;33,957-960
  10. Byre, JG, Aklog, L, Adams, DH, et al Reoperative CABG using left thoracotomy: a tailored strategy. Ann Thorac Surg 2001;71,196-200[Abstract/Free Full Text]
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  12. Fukuse, T, Wada, H, Hitomi, S Extended operation for non-small cell lung cancer invading great vessels and left atrium. Eur J Cardiothorac Surg 1997;11,664-669[Abstract]
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