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Eur J Cardiothorac Surg 2003;23:859-864
© 2003 Elsevier Science NL

En-bloc chest wall and lung resection for non-small cell lung cancer. Predictors of 60-day non-cancer related mortality

A.E. Martin-Ucar, R. Nicum, I. Oey, J.G. Edwards, D.A. Waller*

Department of Thoracic Surgery, Glenfield Hospital, Groby Road, Leicester LE3 9QP, UK

Received 31 October 2002; received in revised form 18 February 2003; accepted 20 February 2003.

* Corresponding author. Tel.: +44-116-256-3959; fax: +44-116-236-7768
e-mail: debra.grew{at}uhl-tr.nhs.uk


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 
Objective: Predictors for early mortality after isolated pulmonary resection have been identified and clear guidelines regarding fitness for surgery have been produced. However, the additional risk of en-bloc chest wall resection has not been extensively studied. Aim: We analyzed our total experience of combined chest wall and lung resection for non-small-cell lung cancer (NSCLC) to identify additional risk factors for early non-tumour related mortality. Patients and methods: A retrospective review of 41 consecutive patients, with median age of 69 (range 37–84) years, operated by a single surgeon over a 4-year period. Univariate analysis was performed to assess the relationship of selected preoperative and operative variables on mortality within 2 months from surgery. Results: Low preoperative body mass index, age over 75 years, and preoperative FEV1 of less than 70% of predicted were associated with a significantly increased 60-day mortality. In those patients with any of these risk factors 60-day mortality was 47% (8 of 17). In those with none of the above there was no mortality (of 24 patients) (P=0.0004). Discussion: En-bloc pulmonary and chest wall resection for NSCLC should be avoided in the elderly, those with limited respiratory reserve or significant weight loss. These factors render the patient highly susceptible to chest complications leading to increased mortality.

Key Words: Prognostic factors • Locally advanced lung cancer • Malnutrition • Elderly


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 References
 
Surgical resection provides the best chances of long-term survival for non-small cell lung cancer (NSCLC) involving the chest wall. On the basis of improved survival T3N0M0 tumours involving the chest wall were downstaged into stage IIb in the latest revision of the staging system [1]. Results of alternative therapies using chemo and/or radiotherapy in patients with locally advanced disease (1-year survival of less than 10%) are not comparable to surgical outcomes [2]. Survival is related to the pathological stage and the completeness of resection [3–6]. Therefore techniques that involve en-block excision of a portion of the chest wall and the affected lung (with or without chest wall reconstruction) are preferred to extrapleural resection [6].

In isolated pulmonary resection the risk of mortality has been predicted from preoperative variables, and guidelines in term of fitness for surgery have been set [7]. However, in locally invasive disease involving the chest wall the additional risk of the chest wall resection has not been extensively studied. It has been stated that if a patient is considered fit for pulmonary resection then should be eligible for extended pulmonary resections [8], and also that postoperative mortality could not be predicted from particular risk factors from operations that require extended resections [8]. Therefore an aggressive surgical approach irrespective of particular risk factors has been advocated in extended resections [8,9].

In order to identify predictors of early mortality unrelated to cancer in patients undergoing en-bloc chest wall and pulmonary resection for NSCLC we analyzed our own experience.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 References
 
2.1. Study design
In a 4-year period between April 1997 and October 2001, a total of 469 patients were operated upon by a single surgeon for NSCLC. Forty-one (9%) of them (25 male and 16 female) underwent en-bloc lung and chest wall resection for locally advanced disease. We retrospectively analyzed the perioperative course of these patients. Preoperative pulmonary function tests were available in all patients. Preoperative FEV1 (as percentage of predicted) and an estimated postoperative predicted FEV1 (ppoFEV1) were calculated [10]. The nutritional status of the patients was assessed by determination of their body mass index (BMI). Patients were considered underweight when their BMI was less than 18.5 kg/m2. Routine staging computed tomography (CT) scan of chest and upper abdomen including views of the liver and adrenal glands was performed in every patient. In five cases an magnetic resonance imaging (MRI) was needed for further staging of superior sulcus tumours. Mediastinoscopy was reserved for patients in whom a CT scan revealed the presence of mediastinal nodes with a diameter greater than 1.5 cm.

2.2. Preoperative characteristics
The median age was 69 (range 37–84) years. The mean FEV1 was 77% (range 37–100) of predicted, with a mean ppoFEV1 of 60.5% (19.4–84.2%). Other preoperative and operative details are shown in Table 1.


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  		Table 1. Non-tumour related variables: incidence of 60-day mortality

 
2.3. Operative data
The operations were carried out under a general anaesthesia through a posterolateral thoracotomy with the level of the intercostal space incision dictated by the anatomical location of the chest wall involvement. Analgesia was administered via a thoracic epidural catheter (levels T4–T6) with a continuous infusion of bupivacaine and fentanyl. The excision of the chest wall ensuring macroscopic clear resection margins was carried out and then en-bloc lung resection continued. Reconstruction of the chest wall was performed for defects of three or more ribs, unless covered by the scapula, using a combination of polypropylene mesh with acrylic cement (Fig. 1) . A single intercostal chest drain was inserted prior to closure. Patients were routinely extubated in the operating room at the end of the procedure. All patients returned to the Surgical High Dependency Unit where they were monitored postoperatively. A uniform protocol of care in our unit after pulmonary resection includes invasive methods of monitor such as arterial line for blood pressure and blood gases analysis and continuous central venous pressure measurements in all cases. In addition, urinary catheter and continuous cardiac monitoring are standards of care. Intensive physiotherapy and early mobilization was encouraged and helped by the administration of epidural analgesia postoperatively in all patients following a uniform protocol.



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  		Fig. 1. Postoperative CT scan following en-bloc chest wall and left upper lobe resection for a locally invasive Squamous Cell Carcinoma of the lung. The defect was covered with a combination of polypropylene mesh and acrylic cement.

 
2.4. Statistical analysis
The following factors were assessed as predictors of mortality within 60 days from surgery: FEV1 less than 70% of predicted, age greater than 75 years, non use of a prosthetic patch, excision of more than three ribs, history or evidence of cardiovascular disease, gender, body mass index less than 18.5 kg/m2, the use of neoadjuvant therapy, and operation length of over 2 h. Univariate analysis was assessed with the Chi-square and Fisher's exact test. Postoperative survival was plotted according to the Kaplan–Meier method and difference in survival between good and poor prognostic groups was evaluated with the Log Rank test. Statistical significance was defined by P values <0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 References
 
3.1. Operative
The mean anaesthetic time for all the procedures was 130 (range 75–270) min. The location of the chest wall involvement in relation to the angles of the ribs was posterior in 19 cases (46%), lateral in 12 cases (29%) and anteromedial in 10 (24%). The number of ribs excised ranged from 1 to 5 (mean of 2.6). Pulmonary resection included 33 lobectomy (80%), three pneumonectomy (7%) and five sublobar resections (12%). In two patients lobectomy and chest wall resection was only possible by bronchoangioplasty to ensure clearance of hilar lymph nodes. Reconstruction of the chest wall was required in 19 (46%) patients. The median length of stay was 8 (range 4–26) days and nine patients (22%) required admission to the Intensive Care Unit due to complications during the postoperative period with a median stay of 3 (1–20) days. The intercostal drain was removed at a median of 4 (range 1–20) days. Follow-up was routinely arranged 2 weeks after discharge from hospital and then at 3 monthly intervals and was complete in all patients. The criteria for discharge was uniform for all patients and requests from the patient to be ambulant and self-caring, the pain control to be adequate prior to discharge, and successful assessments by both physiotherapy and occupational therapy staff.

3.2. Postoperative course
There were three in hospital deaths (7.3%). There were five (one within 30 days) further deaths within 2 months from surgery following re-admission due to complications, resulting in a 60-day mortality of 19% (Table 2).


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  		Table 2. Mortality within 60 days from surgerya

 
Other non-fatal complications included bronchopneumonia in one case and congestive heart failure in another. Completely uneventful recovery was recorded in 27 patients (66%).

3.3. Pathology
The pathological stages were: 25 (61%) T3N0; 3 (7%) T3Nx; 8 (20%) T3N1; 4 (10%) T3N2; and 1 (2.4%) T4N0 (satellite nodule found at pathology in the resected lobe). There were five superior sulcus tumours included in this series. Histological cell type was squamous cell carcinoma in 21 cases (49%); adenocarcinoma in 11 (27%) and undifferentiated large cell carcinoma in 9 (22%). In all cases complete macroscopic clearance was achieved. Microscopic analysis confirmed complete excision (R0) in 36 cases (88%)

3.4. Neoadjuvant therapy
The five patients with superior sulcus tumours underwent preoperative radiotherapy (15%). None of the patients received postoperative chemo or radiotherapy within 60 days after surgery. There were no postoperative mortalities within these patients.

3.5. Non-tumour predictors of 60 days mortality
On univariate analysis three variables were associated with an increase rate of early postoperative death: age over 75 years (P=0.007), preoperative FEV1 of less than 70% of predicted (P=0.007), and a BMI of less than 18.5 kg/m2 (P=0.009).

Based on the variables that were associated with an increased risk of early mortality the patients were then considered in two distinct groups (low and high risk): Group A consisted of 24 low-risk patients (58.5%) who were younger than 75 years, with a preoperative FEV1 greater than 70% of predicted and who were not underweight; and Group B that included the remaining 17 patients (41.5%) who presented at least one of the risks factors (Table 3).


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  		Table 3. Characteristics of high- and low-risk groups according to the isolated risk factors for 60-day mortality

 
Whilst there were no 60-day deaths in Group A, the 30 and 60-day mortality in Group B were 23.5 and 47% (P=0.03 and 0.0004), respectively.

3.6. Survival
With a median follow-up of 35 (2–57) months, the overall 1-year survival was 46±8% (95% CI). The survival was significantly better in Group A (low-risk group) with a 1-year survival of 68±10% (95% CI) versus 17±9% (95% CI) in Group B (P=0.0001) (Fig. 2) . At time of analysis 15 patients (62%) of group A and 2 (12%) of group B are still alive.



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  		Fig. 2. Comparison between: 24 patients younger than 75 years, with preserved respiratory function (FEV1 >70% of predicted) and normal weight (Low-risk group) versus the remaining 17 patients (High-risk group).

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
References
 
Combined en-bloc excision of lung and chest wall for locally invasive non-small cell lung cancer carries a significant rate of early, non-cancer related mortality. There are some patients in which the addition of chest wall resection carries a higher risk of mortality. In contrary to other views, the factors that determine an increase in early mortality on extended pulmonary resections can be identified. Therefore fitness for extended resections cannot be assessed in the same way as isolated lung resections. In this series, in which operability was determined by guidelines for isolated lung resection, we have identified this group of patients: the elderly, the underweight, and the one with a limited pulmonary reserve.

Elderly population carries an increased risk for developing complications after pulmonary resection for NSCLC. However, the results of series of resections limited to lobectomy are reasonable both in terms of mortality and survival [11]. The complication rates increase when pneumonectomy is necessary [12]. Unfortunately there is very limited data of results of combined lung and chest wall resection in elderly groups. Hospital mortality rates of up to 66% have been reported in very small series in elderly patients undergoing combined resection for locally invasive NSCLC [12–14].

Underweight patients have been shown to suffer more complications (especially respiratory) following thoracotomy and lung surgery [15–17]. Little data has been reported in combined lung and chest wall resection in this group. One of the reasons for these results may be the fact that under-nutrition is associated with decreased respiratory muscle mass and function [18], one of the factors for respiratory insufficiency (the most common cause of death in our experience). The same process occurs with age.

The incidence of complications following lung surgery in patients with a limited respiratory reserve has been reported previously, and seems more evident in extended than in limited procedures [15–17]. It may be explained by the ventilatory changes that occur immediately after thoracotomy and lung resection [19] (with an estimated recovery time of 4 weeks to 6 months) that may become more evident in a previously impaired function.

Although the physiological effects of both thoracotomy and pulmonary resection have been extensively studied [20,21], we only encountered one report of the early postoperative physiological consequences of combined chest wall and lung resection in humans [22]. There is little doubt that the use of thoracic epidural analgesia following thoracotomy and lung resection has been a major contributing factor in reducing pulmonary complications hence mortality. However in extended pulmonary and chest wall resections it may be an increase in postoperative pain depending on the level of the chest wall excision. There is the possibility of paradoxical movements of the chest wall after extensive resections thus decreasing chest wall compliance, although not observed using cine-MRI in the only study performed using this technique [22]. And it is possible that a combination of all these factors result in a more detrimental effect in particular groups at a higher risk, such as elderly, underweight and with respiratory dysfunction.

It is difficult to achieve a balance between what is resectable and what is operable when extended procedures are needed for locally invasive lung cancer. With the exception of few units, the use of extended procedures in the UK such as combined pulmonary and chest wall resection is very low. An indication is that our experience with this procedure represents over 12% of the total performed in the UK (with the inclusion of 47 centers) [23]. En bloc chest wall and pulmonary resections constituted 9% of our total primary lung cancer surgical workload while the national figure during the same time period reaches just 2% [23]. While achieving low mortality rates in series of procedures is of crucial importance, if the resection rates are low and the incidence of exploratory thoracotomy is high, the potential long-term benefits of surgery are denied to patients with potentially resectable lung cancer.

We acknowledge the potential areas of error in our report. It is a retrospective study and albeit we were able to complete the data and the follow-up in every case, we cannot provide any information of patients not referred for surgery or those in which surgery was not performed. There is a lack of objective data for other unidentified risk factors, such as coronary artery disease, although the presence of a previous history of cardiovascular disease was not related with an increased operative risk in our series. We cannot exclude the possibility that maybe elderly patients following extensive resection for lung cancer receive a less aggressive treatment when they are readmitted for complications than the younger patients. It can also be argued that malnutrition maybe a consequence of cancer, and therefore should not be included as a non-tumour factor. While we agree with this point of view, there is little doubt that underweight is very common in the elderly population and in patients affected by COPD [24]. All the patients with a BMI <18.5 kg/m2 in our series fell into one of these two groups.

We believe that our experience can provide help for the patient selection in our future management. Based in our results, with a 30 and 60-day mortality of 22 and 55%, respectively, we have modified our selection criteria for extended resections in patients aged over 75 years or those with limited respiratory function as expressed by a preoperative FEV1 of less than 70% of predicted. In these groups of patients, an approach of more limited resections such as extrapleural dissection preserving the chest wall may achieve better results. Other modalities of treatment have to be considered. Recent reports on the use of radical radiotherapy in elderly patients with locally advanced NSCLC include survival of up to 20% at 2 years [25] with low incidence of side effects, although survival is reduced when weight loss is present. Important consideration has to be given to the nutritional status of the patients. A protocol of perioperative nutritional support for underweight patients with suspected chest wall involvement may be beneficial, in a similar way to successful experiences reported in undernourished patients undergoing surgery for gastrointestinal malignancy [26].

In summary, en-bloc pulmonary and chest wall resection is associated with an unacceptable high early mortality in patients at risk: elderly, respiratory dysfunction and underweight. Most of the mortality is caused by postoperative respiratory complications. Fitness for isolated pulmonary resection does not imply fitness for more extensive procedures as combined pulmonary and chest wall resection.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 References
 

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