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Ann Thorac Surg 1995;60:640-645
© 1995 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Are Bilobectomies Acceptable Procedures?

Gilbert Massard, MD, Ahmad Dabbagh, MD, Pascal Dumont, MD, Romain Kessler, MD, Norbert Roeslin, MD, Jean-Marie Wihlm, MD, Georges Morand, MD

Department of Thoracic Surgery, University Hospital of Strasbourg, Strasbourg, France

Accepted for publication April 5, 1995.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background. Controversy about operative morbidity and oncologic value of bilobectomy has led to a review of our experience over the past 12 years.

Methods. The charts of 112 patients (100 men and 12 women with a mean age of 63 years) were reviewed for operative mortality and morbidity and long-term survival. Survival of patients with stage I or stage II disease was compared with that of stage-matched and age-matched groups having right pneumonectomy.

Results. Four patients (3.5%) died postoperatively. Nonfatal complications occurred in 55 patients (49%); the most frequent problem was pleural space disease (34%). Survival studies focused on the 96 patients with non–small cell bronchogenic cancer (44 in stage I, 32 in stage II, and 20 in stage IIIA). The overall 5-year survival rate was 40%; the 5-year survival rate was similar for stage I and stage II (41% for stage I, 50% for stage II, and 17% for stage IIIA). The incidence of local recurrence was significantly increased after bilobectomy for stage I cancer ({chi}2 = 5.066; p lt; 0.05) compared with pneumonectomy but did not affect 5-year survival. Local recurrence and survival were similar after bilobectomy and pneumonectomy in stage II.

Conclusions. These data demonstrate an increased morbidity after bilobectomy. Survival studies demonstrate an increased risk of local recurrence in patients with stage I disease, which might be partly explained by understaging.


    Introduction
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
See also page 645.

For at least three decades, lobectomy has been accepted as the gold standard of resection for bronchogenic cancer [1]. When tumor extent or anatomic location precludes lobectomy, pneumonectomy is generally performed. In select patients, however, intermediate procedures, a compromise between radical resection and preservation of functional lung tissue, can be carried out. In this regard, sleeve lobectomies have been popular for several years.

Specific anatomic conditions in the right side of the chest allow another type of resection, bilobectomy. Although bilobectomy falls between lobectomy and pneumonectomy, it is generally considered a standard radical procedure. Right upper and middle bilobectomy (RUM-BL) is performed for involvement of the minor fissure, double synchronous primary cancers in the upper and middle lobes, involvement of the superior pulmonary vein, and sometimes for incomplete minor fissures. Right lower and middle bilobectomy (RLM-BL) is performed for endoscopic involvement of the bronchus intermedius, invasion of the anterior part of the major fissure, N1 disease reaching the sump nodes close to the middle lobe takeoff, distal arterial involvement, and double synchronous primary cancers.

Postoperative and long-term results after bilobectomy have not been thoroughly evaluated, and to our knowledge, there are only two major reports [2, 3] on this procedure in the recent literature. The present study was designed to answer two questions on the basis of a single institution's experience. First, we wanted to evaluate the operative risk of bilobectomy. To legitimize this type of resection in preference to pneumonectomy, the rate of postoperative complications should be lower. However, bilobectomy, in particular lower and middle bilobectomy, might actually be subject to a higher complication rate with respect to pleural space disease. Second, the oncologic value of bilobectomy can be questioned. As the procedure is less radical than pneumonectomy, there is theoretically an increased risk of local recurrence and hence a probability of a less-valuable long-term survival. A third question addressing the functional value of the remaining lobe remains open and is currently under evaluation.


    Patients and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Patients
In a retrospective review of our database, we identified 112 patients who underwent bilobectomy between January 1, 1980, and December 31, 1992. There were 100 men and 12 women with a mean age of 63 ± 9 years (range, 26 to 83 years). The tissue diagnosis was non–small cell bronchogenic cancer in 96 patients: 81 had squamous cell carcinoma, 12 had adenocarcinoma, and 3 had large cell carcinoma. Another 12 patients had miscellaneous tumors: 5, small cell or neuroendocrine cancers; 4, carcinoid tumors, and 3, metastases of an extrathoracic primary cancer. Four patients had benign disease: 3 had bronchiectasis and 1, fibrostenosis.

An RLM-BL was performed in 94 patients and an RUM-BL, in 18. The indication in the 108 patients operated on for tumors is shown in Table 1Go. In particular, there were eight double primary lesions in seven synchronous primary non–small cell lung cancers (four in stage I and three in stage IIIA) and one double site of metastases.


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Table 1. . Indication for Operationa
 
Preoperative Assessment
Local-regional tumor extent was evaluated with chest radiographs, tomograms or computed tomographic scans, and fiberoptic bronchoscopy on a routine basis. Abdominal and retroperitoneal metastases were ruled out with sonogram, computed tomographic scan, or both. Brain computed tomographic scan and radionuclide bone scan were performed only in symptomatic patients. Associated neoplasms of the head and the neck were checked at physical examination, and screening for esophageal neoplasms was accomplished with barium swallow. Respiratory function studies included spirometry, diffusion of carbon monoxide, and blood gas analysis at rest and exercise. Postoperative breathing capacity was estimated with radionuclide lung perfusion scan. Mediastinoscopy was not performed on a routine basis but only to rule out contralateral N3 disease, as we consider ipsilateral N2 disease amenable to curative resection. Bilobectomies were planned as for a routine cancer operation and were carried out in patients who would have undergone pneumonectomy on functional grounds.

Perioperative Management
All procedures were performed through a standard posterolateral approach, the latissimus dorsi muscle being spared since 1990. Double-lumen intubation was used preferentially. Lymph node sampling was directed to the sump nodes of the resected lobes, the subcarinal nodes, the pulmonary ligament nodes, the azygos nodes, and the right paratracheal nodes.

Triple-suction drainage was left routinely after inferior and middle bilobectomies. Three straight silicone-rubber tubes (28F) were inserted through the eighth or ninth intercostal space between the anterior and posterior axillary lines and directed toward the apex, the axilla, and the posterior gutter, respectively. Strong suction, starting at 50 mm Hg in the operating room and increasing progressively to 150 mm Hg the following day, was used in all patients. Prolonged air leakage was defined as any air leak continuing after the tenth postoperative day and mandated routine fiberoptic bronchoscopy to rule out a bronchial stump dehiscence. Residual spaces after chest tube removal were drained with tube thoracostomy routinely to prevent empyema. Pneumoperitoneum (insufflation of 1.5 to 2 L of room air under local anesthesia) was created when the pleural space was not adequately filled despite a well-working drainage system. Postoperative radiation therapy was applied for pathologically staged N2 or T3 to T4 disease.

Collection of Data and Statistics
Patient demographics were detailed with respect to age, sex, tissue diagnosis, and indication for bilobectomy. The pTNM formulas were established and subsequently converted to stages according to the guidelines published by Mountain [4]. However, on the basis of a previous report [5], we considered hilar node involvement as N2 disease.

Operative mortality was defined as any death occurring during the first postoperative month or during the initial hospitalization. Nonfatal complications were divided into medical and surgical categories. Medical complications included any cardiovascular, respiratory, digestive, or neurologic complication requiring a specific treatment different from standard postoperative care or prolonging the postoperative hospital stay. Surgical complications included any event directly related to the operation, whether or not specific intervention was required. Follow-up data were updated to June 1, 1994.

Most patients had been followed at our outpatient clinic by the operating surgeon; missing data were collected through direct contact with the patient or his or her doctor. Metachronous cancer was defined as any peripheral tumor occurring more than 6 months after operation or centrally located neoplasms with a different tumor histology. Local-regional recurrence was considered to be for any relapse presumed to occur within hilar or mediastinal nodal areas.

Comparison of qualitative data was made with the {chi}2 test. Probability of survival was estimated with the Kaplan-Meier model; survival curves were compared with the log-rank test. To evaluate the oncologic value of bilobectomy, patients were compared with a sample population of age-matched and stage-matched patients having right pneumonectomy. Significance was considered a p value of less than 0.05.


    Results
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 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Operative Mortality and Complications
Four patients (3.5%) died postoperatively. A single death occurred intraoperatively and was due to a laceration of the pulmonary artery. The three other deaths were a result of myocardial infarction, cerebrovascular embolism and pneumonia at 1 day, 2 days, and 25 days, respectively. Two deaths (2.1%) occurred after RLM-BL and 2 (11.1%) after RUM-BL.

A total of 13 medical and 46 surgical complications were shared by 55 patients (49.1%); thus, only 53 patients (47.3%) had an uneventful postoperative outcome. Medical complications occurred in 13 patients and included deep venous thrombosis in 3 with episodes of pulmonary embolism in 2, supraventricular tachycardia in 4, congestive heart failure in 2, respiratory failure in 2, gastric ulcer hemorrhage in 1, and transient bowel obstruction in 1. All complications, including the gastric hemorrhage and the bowel obstruction, were amenable to conservative treatment.

The most relevant surgical complication was pleural space disease, which occurred in 38 patients (34%) and explained a prolonged median drainage time of 7 days for the whole series (mean time, 10 ± 10 days; range, 2 to 85 days) (Table 2Go). The incidence of pleural space complications was similar for both types of bilobectomy ({chi}2 = 1.058; p > 0.3). Treatment necessitated tube thoracostomy in 19 patients and pneumoperitoneum in 11. Three patients underwent reexploration; 1 had early empyemectomy and drainage; 1, thoracoscopy for talc poudrage; and 1, open window thoracostomy.


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Table 2. . Postoperative Pleural Space Complicationa
 
Eight patients experienced miscellaneous surgical complications. Three patients required reexploration for postoperative bleeding; all 3 had diffuse oozing from extrapleural dissection areas. A hemorrhagic infarction of the remaining upper lobe occurred in 2 patients, 1 of whom required completion pneumonectomy. A single patient sustained a partial dehiscence of the bronchial stump; this event occurred without any pleural space disease and sealed spontaneously. One patient had a superficial wound infection and another patient, a subphrenic abcess, which was drained through an intercostal approach.

Long-Term Results
Survival studies focused on the 96 patients with primary non–small cell bronchogenic cancer. Pathologic staging assigned 44 patients to stage I, 32 to stage II, and 20 to stage IIIA (Fig 1Go). Of the 92 operative survivors, 59 had died and 33 were alive as of June 1, 1994 (Table 3Go). Thirty-seven deaths were cancer related and 13, not related to bronchial cancer; the immediate cause of death has not been identified in 9 patients. Of the surviving patients, 31 were free from disease and 2 had metastases at the conclusion of the study. A metachronous bronchogenic cancer had developed in 3 of the survivors, and 2 had been treated for an extrathoracic malignancy; these 5 patients were in complete remission.



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Fig 1. . Pathologic staging of 96 patients with primary non–small cell bronchogenic cancer. The sets of double lines distinguish stages I, II, and IIIA.

 

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Table 3. . Summary of Follow-up Dataa,b
 
Probability of survival at 3 years and 5 years was 49% and 40%, respectively. By stage, the 5-year survival rate was 41% for stage I, 50% for stage II, and 17% for stage IIIA (Fig 2Go). Probability of survival was similar for stages I and II ({chi}2 = 0.649; p = not significant); there was a significant difference between stage I and stage IIIA ({chi}2 = 3.891; p < 0.05) and between stage II and stage IIIA ({chi}2 = 8.78; p < 0.01).



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Fig 2. . Survival by pathologic stage.

 
When comparing follow-up of stage I patients having bilobectomy (n = 44) with stage I patients having pneumonectomy (n = 33), it appeared that the incidence of local recurrence was significantly higher after bilobectomy (Table 4Go); considering RLM-BL only, this difference increased ({chi}2 = 6.304; p < 0.02). However, survival curves were quite similar ({chi}2 = 2.358, p = not significant) (Fig 3Go). Conversely, in the stage II comparison, the incidence of local recurrence was similar after bilobectomy (n = 32) and pneumonectomy (n = 31) (see Table 4Go). Again, survival curves were similar ({chi}2 = 0.065; p = not significant) (Fig 4Go). Finally, the incidence of local recurrence was similar after bilobectomy for stages I and II ({chi}2 = 0.220; p = not significant).


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Table 4. . Incidence of Local Recurrence by Stage and Type of Resection
 


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Fig 3. . Comparison of survival between bilobectomy and pneumonectomy for stage I non–small cell cancer (log-rank test: {chi}2 = 2.358; p = not significant).

 


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Fig 4. . Comparison of survival between bilobectomy and pneumonectomy for stage II non–small cell cancer (log-rank test: {chi}2 = 0.065; p = not significant).

 

    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Although the first bilobectomy has been ascribed to Churchill [6] in 1932, estimation of long-term survival after this procedure has been combined with evaluation of lobectomy in most studies. Therefore, our results can be compared with those in only two major, specific reviews [2, 3] published fairly recently, the conclusions of which are dissimilar in some ways.

Postoperative results in the present series demonstrate an acceptable mortality rate of 3.5%, which is similar to the 4.2% reported by the group from Memorial Sloan-Kettering Cancer Center [2]. In particular, the observed mortality rate was lower than the 6% rate we observed after pneumonectomy over the same period (unpublished data). On the other hand, Deneuville and colleagues [3] reported a 6% mortality, which compared less favorably with the 4% rate after pneumonectomy in their experience.

Data concerning nonfatal morbidity are more controversial. We observed a high morbidity of 49.1%, which is similar to the 55% reported by Deneuville and colleagues [3] but different from the 19% rate reported by Keller and associates [2]. However, these other two series are slightly different. In the series of Keller and co-workers, 108 (65%) of 166 patients underwent RUM-BL, whereas in the series of Deneuville and colleagues, 127 (86%) of 148 patients underwent RLM-BL. The distribution in the latter is similar to that in our series.

The majority of complications were related to pleural space problems because loss of volume after bilobectomy is obviously larger than after single lobectomy. As loss of volume is more important after RLM-BL, one might expect a higher complication rate with this procedure. However, comparison between RUM-BL and RLM-BL disclosed similar results in both series [2, 3]. Deneuville and colleagues [3] also reported an 11% incidence of bronchopleural fistulas. This complication may be explained either by devascularization of the bronchial stump or by spontaneous drainage of empyema through the bronchial suture line. In our experience, the only bronchial dehiscence occurred without pleural space problem. Perhaps we have avoided some fistulas because of our aggressive handling of any residual pleural pocket with routine tube thoracostomy. In combination with tube thoracostomy, pneumoperitoneum is a very valuable adjunct to fit the size of the chest cavity to the reduced lung volume.

We also draw attention to the threat of venous infarction of the right upper lobe after RLM-BL [7]. Two of our patients experienced this complication. In the patient who underwent reexploration, a ligation of the central interlobar vein was discovered to be the triggering factor. This vein carries a major part of the venous return of the right upper lobe. As demonstrated by Hovaguimian and associates [7] and a patient of ours, venous infarction does not necessarily lead to completion pneumonectomy, as partial infarctions can resolve with conservative management. However, lobar torsion should be ruled out by bronchoscopy because reoperation is mandatory in this case.

The overall probability of a 5-year survival rate of 40% is in agreement with the accepted standard for resected bronchial cancer. However, survival analysis by stage disclosed a very similar outcome for stage I and stage II, a finding suggesting that our stage I tumors actually were unrecognized stage II lesions. The survival curves published by Deneuville and colleagues [3] show comparable behavior. Most probably, the missed N1 nodes were located at the root of the remaining upper lobe. This hypothesis is supported by a high local recurrence rate for patients with stage I tumors. We were able to demonstrate that the incidence of local recurrence after bilobectomy for stage I disease was significantly higher than that after pneumonectomy for stage I disease. We admit that the precise determination of local recurrence on chest roentgenograms after pneumonectomy is impeded by the opacified fluid-filled hemithorax. Lymph node sampling may miss micrometastasis to nodes. However, we doubt that even radical node dissection always provides exact staging, especially at the hilum of an unresected lobe.

The fact that the incidence of local recurrence after bilobectomy for stage I equaled that of recurrence in stage II disease further supports the hypothesis of the understaging of our stage I patients. The increased propensity for local recurrence in stage II has been documented by Immerman and colleagues [8] who demonstrated a 10% to 13% recurrence rate in stage I that rose to 41% in stage II.

Besides understaging, there are other factors that might explain the poor 5-year survival in patients with stage I disease. The fact that 4 of the 44 patients in this group were seen with double synchronous primaries may have contributed to an adverse effect on survival. In a review of multiple primary lung cancers, Deschamps and co-workers [9] reported a 5-year survival rate of only 15.7% after resection of synchronous cancers. In this study, we did not consider other prognostic factors such as blood vessel invasion [10]. However, such factors might introduce a distribution bias because of the small sample size. Further, 61% of our stage I patients had T2 tumors. This may have influenced survival, although a recent report by Martini and colleagues [11] reported a 68% survival rate in this subgroup. We did not try to correlate outcome with type of bilobectomy, mainly because of the very small sample having RUM-BL.

Because there is a lack of pertinent data on bilobectomies, a discussion of long-term results and especially of the increased rate of local recurrence in stage I can reference data on sleeve lobectomies. As a matter of fact, we [12] previously reported an increased risk of local recurrence after sleeve lobectomy compared with pneumonectomy. The same observation has been reported by Bennett and Smith [13] and Weisel and colleagues [14]. In a study by Mehran and associates [15], local recurrence after sleeve lobectomy was 16.6% in N0 and 23.1% in N1 patients; however, this slight increase did not reach significance. We therefore consider these two procedures to be analogous; both involve more than a routine lobectomy but are not as radical as a pneumonectomy, although others [1618] describe a lower incidence of local recurrence of 4% to 16%.

We are aware of one other study that has addressed the question of functional value of the remaining lobe. Deneuville and colleagues [3] used radionuclide perfusion scans to examine 21 patients who underwent bilobectomy. Mean perfusion of the remaining lobe was 24% ± 10%. We are currently collecting these data on our patients.

Should bilobectomies no longer be performed? Postoperative mortality was in an acceptable range; postoperative morbidity was amenable to conservative treatment in most cases. Therefore, operative risk per se does not preclude this type of operation. On the other hand, the high incidence of local recurrence in stage I observed in this series raises the question of its oncologic value and is difficult to accept in patients who functionally could sustain a pneumonectomy. Nevertheless, bilobectomy may give the chance of a curative resection to patients with disabled functional status. Finally, we lack extensive information regarding the functional value of the remaining lobe that might help to define a clearer role for bilobectomy.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Massard, Department of Thoracic Surgery, University Hospital of Strasbourg, 1 place de l'Hôpital, F-67091 Strasbourg, France.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Belcher JR. Thirty years of surgery for carcinoma of the bronchus. Thorax 1983;38:428–32.[Abstract/Free Full Text]
  2. Keller SM, Kaiser LR, Martini N. Bilobectomy for bronchogenic carcinoma. Ann Thorac Surg 1988;45:62–5.[Abstract]
  3. Deneuville M, Regnard JF, Coggia M, et al. The place for bilobectomy in bronchogenic carcinoma. Eur J Cardio-thorac Surg 1992;6:446–51.[Abstract]
  4. Mountain CF. A new international staging system for lung cancer. Chest 1986;89(Suppl):225S–33S.[Free Full Text]
  5. Roeslin N, Chalkiadakis G, Dumont P, Witz JP. A better prognostic value from a modification of lung cancer staging. J Thorac Cardiovasc Surg 1987;94:504–9.[Abstract]
  6. Churchill ED. The surgical treatment of carcinoma of the lung. J Thorac Surg 1933;2:254–66.
  7. Hovaguimian H, Morris JF, Gately HLM, Floten SH. Pulmonary vein thrombosis following bilobectomy. Chest 1991;99:1515–6.[Abstract/Free Full Text]
  8. Immerman SC, Vanecko RM, Fry WA, Head LR, Shields TW. Site of recurrence in patients with stages I and II carcinoma of the lung resected for cure. Ann Thorac Surg 1981;32:23–7.[Abstract]
  9. Deschamps C, Pairolero PC, Trastek VF, Payne WS. Multiple primary lung cancers. Results of surgical treatment. J Thorac Cardiovasc Surg 1990;99:769–78.[Abstract]
  10. Macchiarini P, Fontanini G, Hardin MJ, et al. Blood vessel invasion by tumor cells predicts recurrence in completely resected T1N0M0 non–small cell lung cancer. J Thorac Cardiovasc Surg 1993;106:80–9.[Abstract]
  11. Martini N, Bains MS, Burt ME, et al. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg 1995;109:120–9.[Abstract/Free Full Text]
  12. Dumont P, Roeslin N, Wihlm J-M, Massard G, Morand G. Sleeve resection in the treatment of bronchial carcinoma. Ann Chir 1992;46:732–7.[Medline]
  13. Bennett WF, Abbey Smith R. A twenty year analysis of the results of sleeve resection for primary bronchogenic carcinoma. J Thorac Cardiovasc Surg 1978;76:840–5.[Abstract]
  14. Weisel RD, Cooper JD, Delarue NC, Theman TE, Todd TRJ, Pearson FG. Sleeve lobectomy for carcinoma of the lung. J Thorac Cardiovasc Surg 1979;78:839–49.[Abstract]
  15. Mehran RJ, Deslauriers J, Piraux M, Beaulieu M, Guimont C, Brisson J. Survival related to nodal status after sleeve resection for lung cancer. J Thorac Cardiovasc Surg 1994;107:576–83.[Abstract/Free Full Text]
  16. Firmin RK, Azariades M, Lennox SC, Lincoln JCR, Paneth M. Sleeve lobectomy (lobectomy and bronchoplasty) for bronchial carcinoma. Ann Thorac Surg 1983;35:442–9.[Abstract]
  17. Faber LP, Jensik RJ, Kittle CF. Results of sleeve lobectomy for bronchogenic carcinoma in 101 patients. Ann Thorac Surg 1984;37:279–85.[Abstract]
  18. Deslauriers J, Gaulin P, Beaulieu M, Piraux M, Bernier R, Cormier Y. Long-term clinical and functional results of sleeve lobectomy for primary lung cancer. J Thorac Cardiovasc Surg 1986;92:871–9.[Abstract]

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