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Ann Thorac Surg 2005;80:1841-1846
© 2005 The Society of Thoracic Surgeons


Original article: General thoracic

Resection for Tumors With Carinal Involvement: Technical Aspects, Results, and Prognostic Factors

Jean-François Regnard, MD * , Cédric Perrotin, MD, Riccardo Giovannetti, MD, Olivier Schussler, MD, Antonio Petino, MD, Lorenzo Spaggiari, MD, Marco Alifano, MD, Pierre Magdeleinat, MD

Thoracic Surgery Unit, Hôtel-Dieu Hospital, Paris, France

Accepted for publication April 22, 2005.

* Address correspondence to Dr Regnard, Service de Chirurgie Thoracique, 1 Place du Parvis Notre Dame 75004 Paris, France (Email: jean-francois.regnard{at}htd.ap-hop-paris.fr).


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Resection of tumors with carinal involvement remains a challenge because of specific problems of operative technique and airway management. We reviewed our experience with carinal resection and studied factors influencing postoperative course and long-term survival.

METHODS: Between 1983 and 2002, 65 patients underwent a carinal resection for non–small-cell lung cancers involving the carina (54 squamous cell carcinomas and 11 adenocarcinomas).

RESULTS: Fifty-eight right sleeve pneumonectomies and 2 left sleeve pneumonectomies were performed. In addition, five tracheocarinal resections with double bronchial reimplantation (no lung resection) were also performed. The intraoperative airway management consisted of high-frequency jet ventilation in 83% of patients and intermittent conventional ventilation through the operative field in the remaining 17% of patients. Operative mortality was 7.7%. Resection was complete in 61 patients. The overall 5-year and 10-year survival rates were 26.5% and 10.6%, respectively. Patients with N0 or N1 disease had a 5-year survival of 38% compared with 5.3% for those with N2 disease (p < 0.01). At multivariate analysis only nodal status (N0, N1 versus N2; p = 0.0046) had a significant impact on long-term survival.

CONCLUSIONS: Carinal resection provides acceptable results in terms of operative mortality and long-term survival rates. Patients should be carefully selected and probably enrolled in a multimodality treatment program in case of anticipated mediastinal lymph node involvement.


    Introduction
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Lung and tracheal tumors with carinal involvement are rarely resectable. Despite recent technical refinements in tracheal surgery and bronchial sleeve lobectomy, tumors with involvement of the carina remain a challenge for both thoracic surgeons and anesthesiologists.

Experience with this topic is generally not extensive, as most cases are diagnosed in advanced stage, and few series have been published so far. However some authors have reported satisfactory results in terms of survival with acceptable morbidity and mortality [1–3]. In the present paper we present our 19-year experience with 65 patients who underwent carinal resection for malignancies. Technical aspects of both carinal reconstruction and intraoperative airway management, as well as results and prognostic factors, will be presented and discussed.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
We retrospectively reviewed the clinical records of 65 consecutive patients who underwent resection and reconstruction of the carina (with or without concomitant pulmonary resection) for malignancy between October 1983 and November 2002. Benign diseases were excluded from the study. All the patients have been operated on by the same surgical team at Marie Lannelongue Surgical Center (Le Plessis Robinson, France) up to June 2000 and at Hôtel-Dieu Hospital (Paris, France) thereafter. There were 57 male and 8 female patients with a mean age of 59 ± 9 years (range, 36 to 79 years; 16 patients were 65 years old or more). Fifty-four patients had a squamous cell carcinoma, whereas the remaining 11 had an adenocarcinoma. Information and follow-up were obtained from hospital charts and referring physicians.

Preoperative Evaluation
Clinical preoperative evaluation included patient history and careful physical examination. Pulmonary function was assessed by spirometry, arterial blood gas analysis, and ventilation-perfusion lung scan. In case of planned concomitant pulmonary resection, a predictive postoperative forced expiratory volume in 1 second greater than 35% of theoretical forced expiratory volume in 1 second was used as a cutoff to determine functional operability. Special attention was also given to assess the cardiac function by physical examination, electrocardiography, and transthoracic echocardiography in all the patients. If coronary artery diseases were known or suspected, an isotopic cardiac scan was performed and coronary angiography prescribed in cases of abnormalities.

Thoracic, upper abdominal, and cerebral computed tomographic scans, as well as, in some patients (beginning in 2000), a positron emission tomography, were used to stage the disease according to the International TNM Staging System for Lung Cancer [4]. In all cases a fiberoptic bronchoscopy was performed. If removal of airway obstruction before the operation was considered necessary, it was achieved by rigid bronchoscopy. Both fiberoptic and rigid bronchoscopy were used to better assess the topography of the tumor and to evaluate the overall length of the tracheobronchial resection.

Mediastinoscopy was performed in case of suspicion of N2 disease (mediastinal nodes whose small axis was greater than 10 mm at computed tomographic scan) or in case of tracheal compression or suspicion of massive paratracheal tumor spreading. Patients with pathologically proven N2 non–small-cell lung cancer received induction chemotherapy. Preoperative or postoperative chemotherapy or radiotherapy was performed under the care of referring physicians, and different protocols were used.

Anesthesia and Ventilation Procedure
In case of sleeve pneumonectomy, a double-lumen tube was used to perform single-lung ventilation. The tube was pulled back into the trachea during the carinal resection. A high-frequency jet-ventilation catheter was passed through the endotracheal tube and positioned under visual control in the contralateral main bronchus. The surgeon was responsible for this maneuver. A sterile endotracheal tube of small diameter was always promptly available should direct ventilation through the operative field be necessary because of inefficiency of jet ventilation.

In case of tracheocarinal resection without parenchymal exeresis, endotracheal intubation with an extra-long and thin tube was used. Ventilation during carinal resection and anastomosis was achieved by two catheters of high-frequency jet ventilation, passed through the endotracheal tube and inserted in each main bronchus by the surgeon. After reimplantation of the first lung (left one in all instances), the endotracheal tube was pulled down in its main bronchus beyond the anastomosis, and a conventional one-lung ventilation was performed while performing the anastomosis of the other bronchus.

Surgical Procedures
The surgical approach varied according to the type of carinal resection and the side involved. In case of right sleeve pneumonectomy, a serratus anterior-sparing posterolateral thoracotomy through the fourth or fifth intercostal space was performed. In case of left sleeve pneumonectomy, an anterior approach by median sternotomy was performed if carinal resection was anticipated. Left thoracotomy through the fifth intercostal space was carried out if carinal resection was not anticipated by preoperative evaluation. In case of tracheocarinal resection with reimplantation of the two main bronchi, an anterior approach by sternotomy was performed in the first period of the series, but right thoracotomy is now preferred. To obtain a tension-free anastomosis, two procedures were used: either a laryngeal release by the Dedo-Fishman procedure in case of anterior approach, or a complete hilar release with a U-shape pericardial incision around the atrium in case of thoracotomy. Release of the inferior pulmonary ligament was systematically performed in cases of thoracotomy approach.

The deep (by the surgeon's point of view) portion of the anastomosis between the trachea and bronchus was performed with a running suture with an absorbable monofilament (4-0 or 3-0 polydiaxone; Ethicon, Inc, Somerville, NJ). The running suture was first passed and secondarily tied. For the superficial part of the anastomosis, simple interrupted sutures of 3-0 or 4-0 polydiaxone were used to correct size discrepancy (Fig 1). The knots were placed in a concentric fashion 3 to 4 mm apart from the cut edge of the airway, such that they will lie outside the airways when tied. The anastomosis was tested by hydropneumatic maneuver for leakage. In cases of partial resection of the carina (wedge resection), technical aspects of anastomosis remain similar, but a bridge of membranous portion was preserved.



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Fig 1. Anastomosis between the trachea and the left main bronchus after right sleeve pneumonectomy (surgeon's point of view). (A) Carinal involvement by the tumor. (B) Running suture of the deep portion of the anastomosis between the trachea and the left main bronchus. (C) Simple interrupted suture of the superficial part of the anastomosis.

 
Double bronchial reimplantation with no lung resection was carried out according to three different techniques (Fig 2A). The first approach consisted of termino-terminal reimplantation of the left main bronchus in the lower part of the trachea followed by reimplantation of the right main bronchus on the right lateral wall of the trachea (Fig 2B), after excision of a small part of the tracheal wall to obtain a sufficiently large anastomosis. The second approach consisted of a similar procedure, but the right main bronchus was reimplanted on the lateral part of the already reimplanted left main bronchus (Fig 2C). The third modality consisted of double reimplantation with creation of a neocarina (Fig 2D) as described by Mitchell and colleagues [5]. Complete mediastinal lymph node dissection was routinely performed in all cases.



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Fig 2. Double reimplantation without parenchymal exeresis for carinal tumor (A). Reimplantation of the left main bronchus to the distal portion of the trachea is followed by reimplantation of the right main bronchus to the lateral aspect of the trachea (B; procedure of choice). Reimplantation of the left main bronchus to the distal portion of the trachea is followed by reimplantation of the right main bronchus to the lateral aspect of the left main bronchus (C). Creation of a neocarina (D).

 
Adjuvant Therapy
Postoperative chemotherapy or radiotherapy was given under the care of the referring physicians. No standard protocol was defined.

Statistical Methods
Follow-up was obtained for all but 3 foreign patients until death or completion of the study. Survival curves, including postoperative deaths, were calculated by the Kaplan-Meier method. Postoperative mortality was calculated, including all the deaths observed within 30 days from the operation or during the same hospitalization. Statistical comparisons between survival curves were performed by the log rank test. A p value of 0.05 or less was considered statistically significant. Age, sex, induction treatment, different type of resection, T classification, nodal status, histologic type, and associated resection of adjacent organs or structures were evaluated by univariate and multivariate (Cox proportional hazard model) analyses.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Preoperative Procedures
All patients underwent preoperative fiberoptic bronchoscopy. Lesions were located on the lower part of the trachea and carina in 10 patients (15%), the proximal main bronchus in 28 patients (43%), the distal part of the main bronchus in 10 patients (15%), and the upper lobar bronchus in 15 patients (23%). In 2 patients no endobronchial tumor was seen, but an extrinsic compression of the proximal right main bronchus close carina was evident.

Rigid bronchoscopy was required in 3 patients to remove an obstructive tumor by laser coagulation. An initial mediastinoscopy was performed in 10 patients. Eleven patients (17%) with proven or suspected N2 disease received neoadjuvant chemotherapy. No preoperative radiotherapy was performed.

Surgical Procedures
Fifty-eight right sleeve pneumonectomies, two left sleeve pneumonectomies and five tracheocarinal resections with double bronchial reimplantations (no lung resection) were performed. Surgical approach was achieved by thoracotomy in 62 patients (58 right sleeve pneumonectomies, one left sleeve pneumonectomy, and three tracheobronchial resections with double reimplantation) and by median sternotomy in the remaining 3 patients (one left sleeve pneumonectomy and two tracheobronchial resections with double reimplantation). Intraoperative ventilation was carried out by high-frequency jet ventilation in 54 patients (83%) and by ventilation through the operative field in the other 11 cases.

In 34 patients a large wedge carinal resection was performed, whereas 26 patients underwent a complete carinal resection (25 right, one left). An associated resection of one or more adjacent organs was made in 7 patients, including the superior vena cava (n = 4), muscular layer of the esophagus (n = 1), and the left atrium (n = 4).

Postoperative Mortality and Morbidity
No intraoperative death occurred. The overall operative mortality was 7.7% (n = 5), and all deaths were related to pulmonary complications. Postoperative course was uneventful in 32 patients (49%), whereas significant complications occurred in the remaining 33 patients. Overall morbidity and causes of postoperative mortality are listed in Table 1. An age older than 65 years, induction treatments, positive margins at resection, or mediastinal lymph node involvement did not increase the postoperative complication rate. The median hospital stay was 22 days (range, 8 to 111 days).


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Table 1. Postoperative Morbidity and Mortality a
 
Late partial anastomotic stenosis occurred in 3 patients, and a treatment was necessary in 2 of them (silicone stenting and laser coagulation, one each).

Pathologic Diagnosis
The carina were involved in 45 cases (T4 tumors). In the other 20 cases, the tumor involved the origin of the main bronchus (T3), but standard pneumonectomy was not technically possible. Nodal staging was N0, N1, and N2 in 10 (15%), 32 (49%), and 23 (36%) cases, respectively. Complete resection was achieved in 61 cases, and incomplete in the remaining 4 at final histologic examination, despite negative systematic frozen sections. Histologic typing is shown in Table 2. Of note in all the patients treated by carinal resection with double reimplantation (no lung resection), an epidermoid cancer was found.


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Table 2. Outcome by Operative Procedure, Histologic Classification and Nodal Lymph Status
 
Postoperative Treatments
Postoperative treatment was performed in 33 patients: adjuvant radiotherapy, chemotherapy, and radiochemotherapy were administered to 25, 4, and 4 patients, respectively. No uniform protocol was adopted.

Survival
Complete follow-up was achieved in all but 3 foreign patients (95%). The mean follow-up of the overall population was 43 ± 47 months (range, 2 to 217 months). At completion of the study 11 patients were alive (9 disease free and 2 with tumor relapse) with a mean follow-up of 63 ± 66 months (range, 2 to 217 months). The 5-year and 10-year survival rates for the overall population were 26.5% and 10.6%, respectively (Fig 3). Incomplete resection occurred in 4 patients (6%) and all died within 4 years (Fig 4).



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Fig 3. Overall 5-year (26.5%) and 10-year (10.6%) survival, including postoperative mortality (n = 62).

 


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Fig 4. Ten-year survival rate after complete (line 1, n = 58) or incomplete resection (line 2, n = 4), including postoperative mortality.

 
At univariate analysis only the nodal status had an impact on survival. The 5-year survival rate was 38% in patients without mediastinal lymph node involvement (N0 or N1), as compared with 5.3% in N2 disease (p = 0.0064; Fig 5). Long-term survival was not affected by age, sex, induction treatment, type of resection (Table 2 and Fig 6), histologic type, T status (Fig 7), or resection of adjacent organs. At multivariate analysis only the N2 node status (p = 0.0046; relative risk 2.39; 95% confidence interval, 1.31 to 4.37) had an independent negative prognostic value.



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Fig 5. Ten-year survival rate by nodal status, including postoperative mortality; p = 0.0064. (line 1 = N0 or N1 [n = 40]; line 2 = N2 [n = 22].)

 


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Fig 6. Ten-year survival rate by type of resection, including postoperative mortality; not significant. (line 1 = sleeve pneumonectomy [SP; n = 57]; line 2 = double reimplantation without lung exeresis [DP; n = 5].)

 


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Fig 7. Ten-year survival rate by T category, including postoperative mortality; not significant. (line 1 = T3 [n = 18]; line 2 = T4 [n = 44].)

 

    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Surgical resection of lung or tracheal tumors with carinal involvement is an unusual condition and remains a challenge for thoracic surgeons because of difficult preoperative selection of surgical candidates and technical difficulties in carinal reconstruction and airway management. Moreover, tumors with involvement of the carina are classified T4 (stage IIIb), and the benefit of surgery in these patients remains questionable.

Anesthetic Procedure
In our opinion, high-frequency jet ventilation represents the optimal modality of ventilation for surgery of the distal portion of the trachea. In case of double reimplantations, both lungs can be ventilated in the majority of cases through the two small catheters, without technical difficulties or risks, either in case of thoracotomy or sternotomy. Should high-frequency jet ventilation be unsatisfactory, we recommend the use of intermittent conventional endotracheal tube through the operative field, as described by Mitchell and associates [5]. In any case, a sterile standard endotracheal tube must be promptly available to ventilate the patient through the operative field if high-frequency jet ventilation becomes insufficient, especially in patients with poor pulmonary function.

Surgical Procedure
Different surgical approaches were used. In cases of involvement of the right tracheobronchial tree a classic right posterolateral thoracotomy was carried out as reported by most authors. In cases of involvement of the left side of the tracheobronchial tree, two different approaches were performed. In cases of anticipated carinal resection, we think that sternotomy is the preferable choice, as reimplantation of the right lung is easier than by left thoracotomy and intraoperative ventilation is easier in the dorsal decubitus. In our experience only 1 patient underwent an unexpected carinal resection by left thoracotomy, a procedure considered very difficult by some authors. In our opinion, this difficulty can be partly overcome if the trachea is sufficiently mobilized, this maneuver being considered the key of dissection. This mobilization becomes easier when the double-lumen tube is pulled back into the trachea by the anesthesiologist.

In case of carinal resection without parenchymal sacrifice, the optimal approach is represented, in our opinion, by right thoracotomy. We think that the best reconstruction modality is reimplantation of the left bronchus in the trachea followed by reimplantation of the right bronchus in the trachea. At the beginning of our experience, the anterior approach was used, but we think that the dissection of the distal part of the left main bronchus is very difficult with this approach.

Postoperative Course
Initial large series dealing with carinal resection and reconstruction of the lower part of the trachea reported high postoperative mortality, with figures ranging from 29% to 40% [6–11]. However, improvement in anesthetic and postoperative management as well as progress in surgical techniques can explain the improvement of results observed in more recent series. The overall postoperative mortality rate reported in our study (7.7%) was slightly lower compared with figures reported in such recent studies, ranging from 8.2% to 15% [1–3]. We could not identify predictive factors of postoperative deaths, but all the fatalities were caused by pulmonary complications. No intraoperative death occurred in this series as in other recent series [1, 2]. Of note postoperative mortality rates for sleeve pneumonectomy were similar to those reported for conventional pneumonectomy, ranging from 5% to 15% in most surgical series [12, 13].

Long-Term Outcome
This study confirms the acceptable long-term results of carinal resection in selected patients (5-year survival rate was 26.5%). These results are especially encouraging in case of complete resection and absence of mediastinal nodal involvement (5-year survival rate of 38%). Incomplete resection occurred in only 4 patients (6%), and all died within 4 years. These results confirm the necessity of an aggressive workup before expected carinal resection.

Our overall 5-year survival rate is slightly lower than those reported in recent series [1, 2], probably because of a higher number of patients with homolateral mediastinal nodal involvement. In our experience 35% of patients had N2 disease, and this percentage was higher that than reported by Mitchell and colleagues (18.3%; [1]) or Dartevelle and coworkers (20%; [2]). We observed a 5-year survival rate of only 5.3% in patients with N2 disease, and mediastinal lymph node involvement was the only factor negatively affecting survival at multivariate analysis. Few data are available in the literature about the outcome of patients with carinal involvement and N2 disease because most authors think that this condition represents a contraindication to surgery and perform routine mediastinoscopy. The majority of reports found that mediastinal nodal involvement negatively affects the outcome [1–3, 14]. Dartevelle and colleagues [2] reported no long-term survivors among patients with N2 disease. Mitchell and associates [1] found that N2 disease had a negative impact on 5-year survival rate (N0: 51%; N1: 32%; N2, N3: 12%), whereas Pornahov and coworkers [14] reported a 5-year survival rate of 7.5% for N2 disease versus 32% for N0 or N1 disease.

This high rate of N2 disease in our series can be explained by the lack of routine mediastinoscopy in our patients. Furthermore, we performed systematically a complete mediastinal lymph node dissection. Yet we did not contraindicate carinal resection in N2 disease, especially after induction chemotherapy. However, on the basis of poor prognosis of patients with carinal involvement and N2 disease, we think that routine mediastinoscopy should be considered, induction chemotherapy administered in case of proven N2 disease, and probably only those who respond to chemotherapy should undergo surgery (if complete resection is anticipated). Moreover the good long-term results in N0 or N1 disease confirm the necessity of performing surgery in this selected subset of patients with stage IIIb disease.

Conclusions
Tumors with involvement of the carina remain a rare condition, but surgical resection can be proposed in selected patients with acceptable morbidity and mortality rates. Selection of surgical candidates remains difficult. Our series confirms that long-term results are closely linked to the nodal status and completeness of resection. Routine mediastinoscopy should be performed, and patients with N2 disease should probably be treated by induction chemotherapy. Secondary surgical resection might be proposed only in case of a good response to induction treatment.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Mitchell JD, Mathisen DJ, Wright CD, et al. Resection for bronchogenic carcinoma involving the carinalong-term results and effect of nodal status on outcome. J Thorac Cardiovasc Surg 2001;121:465-471.[Abstract/Free Full Text]
  2. Dartevelle PG, Macchiarini P, Chapelier AR. Tracheal sleeve pneumonectomy for bronchogenic carcinomareport of 55 cases. Ann Thorac Surg 1995;60:1854-1855.[Free Full Text]
  3. Roviaro G, Varoli F, Romanelli A, Vergani C, Maciocco M. Complications of tracheal sleeve pneumonectomypersonal experience and overview of the literature. J Thorac Cardiovasc Surg 2001;121:234-240.
  4. Mountain CF. Revisions in the International System for Staging Lung Cancer Chest 1997;111:1710-1717.[Abstract/Free Full Text]
  5. Mitchell JD, Mathisen DJ, Wright CD, et al. Clinical experience with carinal resection J Thorac Cardiovasc Surg 1999;117:39-52.[Abstract/Free Full Text]
  6. Jensik RJ, Faber LP, Kittle CF, Miley RW, Thatcher WC, El-Baz N. Survival in patients undergoing tracheal sleeve pneumonectomy for bronchogenic carcinoma J Thorac Cardiovasc Surg 1982;84:489-496.[Abstract]
  7. Tsuchiya R, Goya T, Naruke T, Suemasu K. Resection of tracheal carina for lung cancer. Procedure, complications, and mortality J Thorac Cardiovasc Surg 1990;99:779-787.[Abstract]
  8. Deslauriers J. Involvement of the main carinaIn: Delarue NC, Echepasse H, editors. International trends in general thoracic surgery. 1. Philadelphia: WB Saunders; 1985. pp. 139-145.
  9. Deslauriers J, Beaulieu M, McClish A. Tracheal sleeve pneumonectomyIn: Shields TW, editor. General thoracic surgery. Philadelphia: Lea & Febiger; 1989. pp. 382-387.
  10. Maeda M, Nakamoto K, Ohta M, et al. Statistical survey of tracheobronchoplasty in Japan J Thorac Cardiovasc Surg 1989;97:402-414.[Abstract]
  11. Pearson FG, Todd TR, Cooper JD. Experience with primary neoplasms of the trachea and carina J Thorac Cardiovasc Surg 1984;88:511-518.[Abstract]
  12. Deslauriers J, Gregoire J, Jacques LF, Piraux M, Guojin L, Lacasse Y. Sleeve lobectomy versus pneumonectomy for lung cancera comparative analysis of survival and sites or recurrences. Ann Thorac Surg 2004;77:1152-1156.[Abstract/Free Full Text]
  13. Ferguson MK, Karrison T. Does pneumonectomy for lung cancer adversely influence long-term survival? J Thorac Cardiovasc Surg 2000;119:440-448.[Abstract/Free Full Text]
  14. Porhanov VA, Poliakov IS, Selvaschuk AP, et al. Indications and results of sleeve carinal resection Eur J Cardiothorac Surg 2002;22:685-694.[Abstract/Free Full Text]



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