A twenty-year analysis of the results of sleeve resection for primary bronchogenic carcinoma

A twenty-year analysis of the results of sleeve resection for primary bronchogenic carcinoma

A twenty-year analysis of the results of sleeve resection for primary bronchogenic carcinoma Ninety-six patients with primary bronchogenic carcinoma w...

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A twenty-year analysis of the results of sleeve resection for primary bronchogenic carcinoma Ninety-six patients with primary bronchogenic carcinoma were treated by lobectomy with sleeve resection of the bronchus, over a 20 year period (1958 through 1977). In 80 resections undertaken prior to 1973, a 5 year survival rate of 34 percent was realized, with an operative mortality rate of 7.5 percent. Survival at 10 and 15 years has been assessed. A review of factors influencing survival has been undertaken and the biologic behavior of these pulmonary neoplasms, modified by sleeve resection, has been outlined. Of interest is the high rate of local recurrence accounting for death within 5 years postoperatively and the late incidence in the survivors of second malignancies and other diseases of surgical interest. Sleeve resection represents a surgical alternative in selected cases of bronchogenic carcinoma in which wider resection may be hazardous, and the indications should be extended to include some lesions commonly managed by pneumonectomy.

W. Frederick Bennett, M.D., F.R.C.S.(C), Edmonton, Alberta, Canada, and Roger Abbey Smith, M.Ch., F.R.C.S., F.R.C.S.(Ed), Coventry, England

w3 leeve resection of the bronchus with upper lobectomy was performed in 96 patients with primary bronchogenic carcinoma, over a 20 year period (1958 through 1977). These procedures represented 8 percent of all pulmonary resections done during the same interval. Preservation of lung combined with adequate resection of malignant disease is an established principle in the surgical management of bronchogenic carcinoma. Lobectomy has become the procedure of choice for localized peripheral lesions and is associated with reduction in operative deaths, fewer postoperative complications, and better residual pulmonary function. Bronchoplastic procedures represent a further progression of the concept of limited resection of the bronchial tree in selected cases of lung cancer. In 1952 d'Abreu and MacHale1 described sleeve resection for benign lesions, and it was used later for the conservative treatment of lung cancer.2 Early recognition of lower operative mortality rate and better quality of life in survivors was followed by the realization of 5 From The Cardiothoracic Unit, Walsgrave Hospital, Coventry, England. Supported in part by The Department of Surgery, University of Alberta, Edmonton, Alberta, Canada. Received for publication May 23, 1978. Accepted for publication Aug. 14, 1978. Address for reprints: Dr. W. F. Bennett, 323 Royal Alex PI., 10106-111 Ave., Edmonton, Alberta, Canada T5G 0B4. 840

year survival rates comparable to those following pneumonectomy.3 Sleeve resection was feasible in that it accomplished nodal clearance similar to that with lobectomy and provided an adequate margin of bronchial resection.4 More recently, curative bronchoplastic procedures in selected, localized, central lesions have yielded 5 year survival rates that are higher than expected, following pneumonectomy, and approximate to those for lobectomy.5' 6 Of the 96 sleeve resections for bronchogenic carcinoma performed in the past 20 years, we reviewed 80 done before 1973 with follow-ups of 5 to 19 years. The age at resection varied from 39 to 71 years with an average age of 57.5. Seventy-four of the patients were men. Fifty-six procedures were sleeve resections of the right upper lobe; the remainder were sleeve resections of the left upper lobe, of which seven involved concurrent angioplastic procedures of the left pulmonary artery because of tumor invasion. This latter group of procedures included five sleeve resections of the artery and two in which a portion of the arterial wall was resected. Each resection was judged to be curative at the time of operation, based on the criteria of total removal of gross tumor and negative mediastinal exploration at thoracotomy. The bronchial resection margins were reported to be free of microscopic tumor. No patients were lost to follow-up. All survivors were reviewed during the last quarter of 1977. The method of follow-up has been described previously and it included interview, examination, and chest roentgen-

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Fig. I. A, Preoperative chest x-ray film showing a tumor of the right upper lobe. This was a squamous cell carcinoma with no lymph node involvement which invaded the main bronchial wall. B, Current x-rayfilmof the same patient 13 years after sleeve resection of the right upper lobe. This man underwent vagotomy and pyloroplasty in 1975 and recovery was uneventful. ogram on each visit, with further investigations as indicated.7 Patient selection In all patients in this series, age, poor general health, or limited cardiopulmonary reserve dictated the choice of lobectomy with sleeve resection rather than pneumonectomy to manage tumors of the right or left upper lobar orifices. Radiographic appearance (Figs. 1, A, and 2), tomography, and bronchoscopic evaluation of the tumor and its extension in the main bronchial wall were utilized to assess the feasibility of sleeve lobectomy as a potentially curative procedure. Mediastinoscopy was not performed routinely. Operative technique All resections were done with the patient in the prone position. The tumor and the mediastinum were assessed through a posterior thoracotomy. If feasible, upper lobectomy with cylindrical sleeve resection of the main bronchus was performed. After division of the inferior pulmonary ligament, bronchial reconstruction was ac-

complished with closely placed, interrupted sutures of fine linen or Mersilene. When a marked discrepancy in lumen size existed, the proximal bronchus was outwardly crimped with one or two sutures at the superior extent of the cartilaginous portion. A horizontal mattress suture at this point of the anastomosis secured adequate apposition. With the exception of the membranous portion of the reconstruction, most sutures were tied within the bronchial lumen for convenience. If a portion of the pulmonary artery was involved in lesions of left upper lobe, this was resected after proximal and distal temporary occlusion with atraumatic clamps. Reconstitution was obtained with two running sutures of fine silk. Heparin was not employed. Postoperatively, posturing and vigorous physiotherapy were utilized to control secretions. Bronchoscopy was seldom undertaken. A tracheostomy was performed on only one patient. Radiotherapy was used only to treat diagnosed recurrence or suitable metastases; no patients in the series received chemotherapy.

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Table I. Complications in 80 patients following sleeve resection (1958 through 1972), excluding recurrent malignancies Complication

No.

Bronchovascular fistula* Pulmonary embolus* Congestive heart failure* Pulmonary artery thrombosis Persistent atelectasis Cerebrovascular accident Total

2 2 2 1 2 1 10

♦Operative deaths.

Table II. Site of malignancy in 42 patients who died of bronchogenic carcinoma within 5 years of sleeve resection (1958 through 1972)

Fig. 2. Chest x-ray film showing left upper lobe collapse distal to a squamous cell carcinoma at the lobar orifice. This patient was treated by sleeve resection of the lesion. Results Of the 80 patients subjected to sleeve resections prior to 1973, six (7.5 percent) died in the hospital within 30 days. Postoperative complications and the causes of death are shown in Table I. Autopsies were done in all these cases. Five patients died within 5 years of resection of progression of pre-existing diseases. All were found to be free of tumor at autopsy. Causes of death included two myocardial infarctions, one cerebrovascular accident, and two cases of respiratory failure secondary to pulmonary infection. All these deaths occurred more than 2 years after resection. Forty-two patients died within 5 years of histologically proved recurrent or metastatic carcinomaAutopsies were performed in 38 cases. Sites of malignancy are listed in Table II and were confirmed at autopsy or by bronchoscopic, mediastinal, or excisional biopsies during life. Local recurrence was diagnosed by obtaining diagnostic biopsies of endobronchial lesions contiguous with the bronchial anastomosis. All bronchial strictures in this series were confirmed as malignant.

Site

No.

Local recurrence Mediastinal metastases Distant metastases Recurrence in wound

20 16 5 1

Four patients underwent a second pulmonary resection within 5 years of the initial procedure. Three underwent completion pneumonectomies; one had a segmental resection of the contralateral lung. None of this group survived past 5 years following sleeve resection. Twenty-seven of 80 patients were 5 year survivors (34 percent). During his fourth year one patient had a local recurrence and survived 2 more years following radiotherapy. The other survivors were judged to be free of bronchogenic carcinoma 5 years postoperatively. Of 49 patients eligible, 10 lived for 10 years (20 percent) and a further nine patients are alive at 6 to 9 years after operation. Eight deaths occurred between the fifth and tenth postoperative years; three subjects died of recurrent tumor, two of a second primary carcinoma in the contralateral lung, and three of other diseases. Three of 16 patients eligible have survived past 15 years (19 percent). One is alive at }9 years and the other two have survived 16 years. In the latter patient an isolated metastasis in an jpsilateral axillary lymph node was excised during the fifteenth postoperative year. He is apparently free of malignant disease 18 months later. A further five patients are alive ) 1 to 14 years after resection. There were no deaths attributed to bronchogenic carcinoma after 10 years. Four of the seven patients (57 percent) who underwent simultaneous resection of lobe and pulmonary

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Table III. Histologic results and 5 year survival in 80 cases of sleeve resection (1958 through 1972) Cell type Squamous cell Undifferentiated large cell Undifferentiated small cell Adenocarcinoma Totals

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Table IV. Second malignancies in 27 patients who survived 5 years following sleeve resection*

Five-year survivors

42 28 6 4

14 (33%) 9 (32%) 2* 2

80

27

♦Reconfirmed by independent pathologist.

artery survived for 5 years. Two have survived more than 10 years. Results of histologic examination of the 80 resected carcinomas are shown in Table III. Squamous cell carcinoma predominated in this series, but 35 percent were undifferentiated large cell carcinomas. There was no significant difference in survival of patients with these two cell types. The undifferentiated small cell carcinomas have been reconfirmed by subsequent independent pathological examination. Excluding immediate deaths and those patients who died within 5 years of causes other than tumor, we compared 5 year survival rates on the basis of nodal involvement. Eighteen of 40 patients (45 percent) with normal nodes survived for 5 years in contrast to nine of 29 patients (31 percent) with nodal metastases. No patients in this series were reported to have had diseased mediastinal nodes at the time of resection. The influence of operative site (left or right side) on survival was marginal. Nine of 26 (34 percent) patients with left-sided resections survived for 5 years, as opposed to 18 of 54 (33 percent) with right-sided resections. The average age of survivors at resection was identical to that of the whole series. Six of the 27 (22 percent) 5 year survivors developed second malignant tumors (Table IV). Three were second primary bronchogenic carcinomas; only one of these lung lesions was resected. Major operations were performed on seven of the 5 year survivors (total of 27) at intervals of 6 to 11 years following sleeve resection (Table V). Only one patient had respiratory complications. This 81-year-old man died of pneumonia following open reduction of an intertrochanteric fracture of the femur. Discussion Shields8 reviewed 13 series of pulmonary resections for bronchogenic carcinoma from 1955 to 1970 and found the average 5 year survival rates to be 24 percent following pneumonectomy and 34 percent following lobectomy. Rate of deaths immediately following

Malignancy

Year following sleeve resection

Treatment

Results

Second primary lesion Second primary lesion Second primary lesion Gastric carcinoma

Segmental resection Radiation

Breast carcinoma

Mastectomy

Uterine carcinoma

Radiation

Died within 1 yr. Died within 1 yr. Alive at lyr. Died within 4 yr. Alive at 5yr. Died within 2 yr.

Radiation Gastrectomy

*From a group of 80 sleeve resections.

Table V. Subsequent major operations occurring in 27 patients surviving sleeve resection at 6 to 11 years (>5 years) after initial procedure Segmental pulmonary resection Gastrectomy Mastectomy Aorto-femoral graft Retropubic prostatectomy Vagotomy and pyloroplasty Open reduction of fractured femur

1 1 1 1 1 1 1

pneumonectomy was twice that following lobectomy. Our series of 80 cases of sleeve resection shows results comparable to those associated with lobectomy in a selected group of patients, and substantiates previous reports.5, 6" 9 The high incidence of local recurrence accounted for 38 percent of deaths occurring within 5 years of resection, and this incidence continued over the next 5 years. This characteristic of tumor recurrence following sleeve resection can explain the encouraging results following preoperative radiotherapy in a group of 20 patients reported by Paulson and associates5 in 1970. Previous series in which 5 year survival was assessed have been composed largely of patients with squamous cell carcinoma. The superior prognosis for patients with this histologic type of bronchogenic carcinoma is widely recognized. The similarity in survival rates between patients with squamous cell and those with undifferentiated large cell carcinoma in our series is exceptional and may represent some instances of inappropriate classification of poorly differentiated squamous cell carcinomas. However, undifferentiated large cell carcinomas were resected in nine of 27 patients who survived for 5 years. In 1977 Mountain10 reported

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Fig. 3. Pulmonary angiogram done 6 months following sleeve resection of the left upper lobe and pulmonary artery. The satisfactory flow in the residual left lower lobe is shown. This patient is alive and well 13 years following operation.

Fig. 4. Occlusion of the left pulmonary artery shown 6 months after sleeve resection of the left upper lobe and pulmonary artery. The patient was asymptomatic. The occlusion occurred silently during this interval. He has no respiratory symptoms 11 years later.

identical survival rates of a large group of subjects with resected undifferentiated large cell carcinomas and with adenocarcinomas. In view of this report, we would suggest that patients with resectable carcinomas of these cell types can expect a survival rate following sleeve resection similar to that expected after lobectomy. On the basis of our results, lymph node involvement appears to have an adverse effect on 5 year survival, as would be expected, but 31 percent of patients with metastases involving intersegmental or interlobar nodes survived for 5 years. No patients in this series received preoperative radiotherapy and hence no metastases would be obscured microscopically. No patients with diseased mediastinal nodes were included in this series. A relatively good, late survival rate of patients undergoing concurrent angioplastic procedures is noted. These seven patients constitute a small group, but the results suggest that tumor invasion of the pulmonary artery does not represent a contraindication to bronchial sleeve resection (Figs. 3 and 4). The incidence of second primary lung carcinomas, other malignant lesions, and benign conditions necessitating later surgical intervention is notable. In the group of 27 patients who survived for 5 years, 26 percent underwent subsequent operations. Whether these patients would have been rejected as surgical candidates had they previously been subjected to pneumonectomy is uncertain. However, six patients survived

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general anesthesia and major operative procedures several years after sleeve resection. In addition to the successful result of sleeve resection in thse cases, the opportunity to reap the benefits of these subsequent surgical procedures constitutes a recommendation for the principle of pulmonary preservation. Conclusions Surgical resection is the treatment of choice for localized bronchogenic carcinomas. Sleeve resection in a selected group of patients extends the indications for lobectomy with comparable survival and operative mortality rates. The high rate of local recurrence in our series demonstrates the disadvantage of a limited bronchial margin of resection, but this factor is adequately balanced by lower rates of death and morbidity, better residual pulmonary function, and satisfactory longterm survival. The frequency of local recurrence suggests that preoperative irradiation may improve survival rates following sleeve resection. In suitable cases undifferentiated large cell carcinomas and adenocarcinomas should be managed by this procedure with reasonable expectation of survival; the procedure need not be confined to squamous cell carcinomas. Nodal involvement (excluding mediastinal nodes) and invasion of the pulmonary artery do not preclude a successful result.

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REFERENCES 1 d'Abreu AL, MacHale SJ: Bronchial "adenoma" treated by local resection and reconstruction of the left main bronchus. Br J Surg 39:355-358, 1952 2 Price Thomas C: Conservative resection of the bronchial tree. J R Coll Surg Edinb 1:169-171, 1956 3 MacHale SJ: Carcinoma of the bronchus. Survival following conservative resection. Thorax 21:343-346, 1966 4 Cotton RC: The bronchial spread of lung cancer. Br J Dis Chest 53:142-145, 1959 5 Paulson DL, Urschel HC, McNamara JJ, Shaw RR: Bronchoplastic procedures for bronchogenic carcinoma. J THORAC CARDIOVASC SURG 59:38-47, 1970

6 Rees GM, Paneth M: Lobectomy with sleeve resection in the treatment of bronchial tumours. Thorax 25:160-164, 1970 7 Abbey Smith R: Development and treatment of fresh lung carcinoma after successful lobectomy. Thorax 21:1-20, 1966 8 Shields TW: Carcinoma of the lung, General Thoracic Surgery, TW Shields, ed., Philadelphia, 1972, Lea & Febiger, Publishers, p 837 9 Jensik RJ, Faber LP, Milloy FJ, Amato JJ: Sleeve lobectomy for carcinoma. A ten year experience. J THORAC CARDIOVASC SURG 64:400-410, 1972

10 Mountain CF: Assessment of the role of surgery for control of lung cancer. Ann Thorac Surg 24:365-371, 1977