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Ann Thorac Surg 2000;69:376-380
© 2000 The Society of Thoracic Surgeons
a Department of Thoracic Surgery, Royal Brompton Hospital, London, England, United Kingdom
b Intensive Care Unit, Royal Brompton Hospital, London, England, United Kingdom
Address reprint requests to Dr Kutlu, Nispetiye Cad, Saydam Sok, 20/1, Levent 80600, Istanbul, Turkey
e-mail: cakutlu{at}turk.net
| Abstract |
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Methods. Patients that underwent pulmonary resection at the Royal Brompton Hospital between 1991 and 1997 were included. The case notes of all patients developing postoperative complications were retrospectively reviewed.
Results. The overall combined frequency of ALI and ARDS was 3.9%. The frequency was higher in patients over 60 years of age, males and those undergoing resection for lung cancer. ALI/ARDS caused 72.5% of the total mortality after resection in this series.
Conclusions. In our experience ALI and ARDS are major causes of mortality after lung resection.
| Introduction |
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The vast majority of postoperative complications are cardiopulmonary in nature, and although cardiac dysrhythmias are the most common event, pulmonary complications remain the leading cause of death [6]. In many series this is reported as respiratory failure without further clarification. Due to the lack of any proper definition, acute respiratory distress syndrome (ARDS) has been rarely reported as a complication after lung resection, although it has become widely recognized as a cause of acute respiratory failure, in association with many other serious medical and surgical conditions. The frequency and mortality of acute lung injury is further obscured by the variety of names applied to this condition; including postperfusion lung, noncardiogenic pulmonary edema, and adult respiratory distress syndrome [7].
In 1984, Zeldin and associates reported 10 cases following pneumonectomy, and coined the term postpneumonectomy pulmonary edema [8]. He suggested that excessive intraoperative fluid administration resulted in postoperative lung injury. While the pathophysiology and risk factors are still unclear, ARDS and acute lung injury (ALI) are increasingly seen after lung resection, and are associated with high mortality [8]. More recently, a consensus committee has provided objective criteria for the diagnosis of ARDS, and has defined ALI as a less severe form of ARDS. ALI and ARDS are characterized by acute onset, arterial hypoxemia refractory to oxygen therapy, and associated with diffuse infiltrates on chest radiograph (Table 1) [9].
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| Patients and methods |
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Preoperative evaluation included a complete history and physical examination, full blood count, biochemical profile and chest radiography. In patients with malignant disease a computed tomographic (CT) scan of chest, brain, and abdomen was performed and bone scans were performed selectively. All patients had routine arterial blood gas measurement and spirometry. In any patient judged to have limited lung function, a ventilation and perfusion scan was performed to predict residual postoperative function. All patients over 50 years of age had an electrocardiogram. If there was a history of ischemic heart disease, a cardiological evaluation was performed, usually supplemented by a stress test or thallium scan.
Preoperative bronchoscopy was routinely performed. All patients had a radial arterial catheter and central venous catheter for hemodynamic management perioperatively. Resections were performed through a full posterolateral or lateral muscle-sparing thoracotomy. Patients were intubated with a double-lumen endotracheal tube. For most of the operative time the lung was deflated to facilitate dissection, however while fissures were developed, the lung was temporarily reinflated. At the end of the procedure, the lung was reinflated and examined for air leak prior to closure. Systematic lymph node dissection was performed in patients undergoing lung resection for lung cancer. Most patients were extubated in the operating room or immediately after transfer to the recovery area. When stable, the patients were transferred to the high dependency unit. Postoperative pain control was achieved with continuous intravenous or epidural analgesia.
The case notes were reviewed for all patients developing postoperative complications requiring admission to the intensive care unit (ICU). Fever, if present, was noted. Investigations included arterial blood gas analysis, serial white blood cell counts, and cultures of blood and tracheobronchial secretions. Pulmonary artery wedge pressure was measured in severe cases.
ALI and ARDS were defined by the criteria established at The American-European Consensus Conference on ARDS (Table 1). Any fatality occurring before hospital discharge, even if more than 30 days postoperatively, was considered to be a postoperative death.
Two-tailed
2 testing was performed to assess significance, with p less than 0.05 considered to be statistically significant.
| Results |
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The overall combined frequency of ALI and ARDS was 3.9% in this series. Although the frequency was related to the extent of lung resection, ALI and ARDS were seen after all types of resection (Table 2), the highest frequency being observed after extensive resection (12.9%), followed by pneumonectomy (6.0%), lobectomy (3.7%), and minor resection (1.0%). The frequency of ALI and ARDS was similar after right pneumonectomy (6 of 90, 6.6%) and left pneumonectomy (6 of 108, 5.5%) (p = 0.74). The frequency of these complications was 2.8% (15 of 533) in patients under 60 years of age and 4.9% (30 of 606) in patients over 60 years of age (p = 0.06), and was higher in male patients (5.8% versus 1.4%) (p < 0.01). ALI or ARDS was diagnosed in 37 of 625 patients undergoing resection for lung cancer (5.9%) and in 8 of 514 patients (1.5%) having lung resection for other diseases (p < 0.01).
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During the study period, 40 patients died after pulmonary resection with an overall mortality of 3.5% (Table 3). ALI or ARDS was the cause of death in 29 patients, 72.5% of the overall mortality.
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| Comment |
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Zeldin and colleagues reported 10 cases where lung injury complicated pneumonectomy, and coined the term postpneumonectomy pulmonary edema (PPE) [8]. PPE was diagnosed by a fall in arterial PO2 and an increase in lung water. The reported frequency of PPE after pneumonectomy ranges between 2.6% to 4% [13, 14]. Even if we consider noncardiogenic pulmonary edema and PPE to be synonymous with ALI and ARDS, the frequency of this complication after pneumonectomy in our series remains higher (6.0%) than in previous reports. The highest frequency of ALI and ARDS reported after pneumonectomy, was 15.1% and, not surprisingly, this was associated with a mortality rate which was much lower than that found in most series (9%) [15]. However, none of the previous reports is strictly comparable to our series, as the criteria used to diagnose this complication were different of those used in this series.
At variance with previously reports, we did not find right pneumonectomy to be a significant risk factor for the development of ALI or ARDS. However, the mortality of ALI and ARDS associated with right pneumonectomy is higher than that associated with left pneumonectomy. A greater reduction in lymph drainage and a larger volume of resected lung may be factors contributing to this.
ALI and ARDS have been reported after lobectomy [13]. We found the frequency of ALI and ARDS after lobectomy to be 3.7%. There is no comparable data in the literature. Waller reported the frequency to be 1% after resections more limited than pneumonectomy, and Matru reported that 3 of 5 of the cases of lung injury followed lobectomy, without giving the frequency [13]. We recorded cases of ALI and ARDS after minor resection, although the frequency was low (1.0%).
Preoperative spirometry and blood gas analysis have not been found to be predictors for the development of ALI and ARDS [16]. A univariate analysis by Parquin, confirmed that predicted postoperative the forced expiratory volume in one second (FEV1) is not a useful predictor of those patients who will develop lung injury after lung resection [15].
Although age appeared to have no influence on the severity of lung injury, we found the overall frequency of ALI or ARDS in patients over 60 years of age to be higher (p = 0.06). It was previously reported by our institution that patients aged over 60 years have a higher risk of developing ARDS after cardiopulmonary bypass (CPB) [17], although the frequency was lower (1.3%) than after lung resection (3.9%). We found that the frequency of ALI and ARDS is significantly higher in male patients (p < 0.01) and those undergoing resection for lung cancer (p < 0.01). The difference has not been observed in other studies [1315].
It has been suggested previously, that induction therapy may increase the resectability rate of locally advanced NSCLC in selected patients [18]. However, the morbidity and mortality following lung resection is significantly higher in patients who have had induction chemotherapy and/or radiotherapy (17.3% to 23%) [18, 19]. As in this study, ARDS occurred more frequently in patients undergoing pneumonectomy [20] but the frequency was higher than in previous reports (17.3% and 23%) [18, 21]. Parquin found that the incidence of ALI and ARDS was significantly higher in patients who had had preoperative chemotherapy (p < 0.01) and radiotherapy (p < 0.0001) [15].
It has been suggested that perioperative fluid overload is an important contributory factor in the development of postoperative lung injury [8]. However, this has not been confirmed by clinical and experimental studies [13, 14]. An increase in pulmonary vascular resistance (PVR) occurs in 30% of patients following pneumonectomy [22]. An increase in PVR has been shown to result in an increase in fluid and protein flux in the remaining lung following pneumonectomy which is greater than that following lobectomy [23]. We found that the frequency of ALI and ARDS tends to be related to the extent of the lung resection. However, the occurrence of lung injury after minor resection in this series suggests that this is not the only factor which governs the development of ALI and ARDS.
Pulmonary lymph flow may safely increase up to 5 to 10 times the baseline rate [24]. This compensatory mechanism will be reduced by as much as 55% when one lung is removed. This finding has been confirmed following pneumonectomy and mediastinal interruption in dogs [20]. It is unlikely that the reduction in lymphatic drainage capacity alone is responsible for the development of lung injury, but may contribute to the occurrence of this complication. This may explain the higher frequency of ALI and ARDS in patients undergoing resection for lung cancer, in whom systematic nodal dissection was routinely performed. However, this concept has never been proven, and other factors such as underlying smoking-related lung damage have to be considered.
Lung injury may occur in response to any direct or indirect pulmonary insult. Recent clinical and experimental studies suggest that increased endothelial permeability, especially after pneumonectomy, plays a central role in the pathogenesis of pulmonary edema after lung resection [25]. The exact mechanism of endothelial damage is still unclear, but ischemia-reperfusion injury associated with one-lung anesthesia has been implicated, perhaps mediated by reactive oxygen species (ROS) [26]. It has been shown that more durable markers of ROS activity occur in ARDS with the loss of protein thiols and formation of protein carbonyls [27]. Williams and colleagues measured these markers in patients undergoing single lung ventilation during lung resection [28]. They observed that thiol levels fell perioperatively in all patients, recovering to some extent by 24 hours postoperatively, and recovering to a greater level following minor resection when compared to lobectomy and pneumonectomy. They also found an increase in plasma carbonyl levels during one lung ventilation, rising further in the first 24 hours after lung resection. This study suggests that a spectrum of lung injury exists, in which all patients undergoing lung resection may suffer to some degree [29]. The high frequency of lung injury in this series may be associated with the routine use of single lung ventilation during operation.
There is no specific treatment for ALI or ARDS and management consists essentially of supportive care [30]. Patients with ALI and ARDS require ventillatory assistance, usually escalating to intubation and mechanical ventilation. Despite intensive treatment the mortality is high, and patients generally die with multisystem organ failure. ARDS is now recognized to be a multisystem disease in which the lung is the most vulnerable organ, and the one which usually heralds the onset of this condition [30]. The reported mortality of ARDS varies from 53% to 74% depends upon the precipitating cause [31]. The overall mortality of ALI and ARDS in our series was 64.4%. ALI is a less severe form of lung injury and has a better prognosis than ARDS. The mortality rate of ALI and ARDS in this series is in agreement with that reported in the literature and similar to that reported from our institution for ARDS associated with a variety of injuries (66%) [32] including cardiopulmonary bypass (65%) [17].
The overall postoperative mortality rate in our series (3.5%) is in line with that reported in the literature. Pulmonary complications are the leading cause of death in most series, and we believe that ALI and ARDS are the main reasons for respiratory failure after pulmonary resection. All other postoperative complications together accounted for only 27.5% of postoperative deaths, a mortality rate of 0.9%.
In our experience, ALI and ARDS are the major cause of mortality after lung resection. This high incidence may be partially due to heightened awareness of the problem in our institution, where other complications have been successfully avoided or treated. However, other factors have to be considered such as systematic nodal dissection for malignant disease, and the routine use of one-lung ventilation. The frequency we report may still be an underestimate, since lesser degrees of lung injury, which were successfully treated in the ward, have not been considered. The frequency of this complication may well increase as a consequence of current trends in patient selection, when operating on an older population, undertaking more reoperative operation, or operation after induction chemoradiotherapy. We found the frequency of ALI and ARDS were significantly higher in patients over the age of 60 years, those who are male and in those undergoing operation for lung cancer. In our series, the mortality of ALI and ARDS after lung resection is unacceptably high, representing a major challenge to the thoracic surgeon and intensivist for the next decade.
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