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Ann Thorac Surg 2007;84:1085-1091
© 2007 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Incidence and Risk Factors for Lung Injury After Lung Cancer Resection

Naveed Alam, MDa, Bernard J. Park, MDa,*, Andrew Wilton, MDb, Venkatraman E. Seshan, PhDb, Manjit S. Bains, MDa, Robert J. Downey, MDa, Raja M. Flores, MDa, Nabil Rizk, MDa, Valerie W. Rusch, MDa, David Amar, MDc

a Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York
b Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York
c Department of Anesthesiology and Critical Care Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York

Accepted for publication May 21, 2007.

* Address correspondence to Dr Park, Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, Room C-867, New York, NY 10021 (Email: parkb{at}mskcc.org).

Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.


General thoracic surgery: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Background: Lung injury, defined as acute hypoxemia accompanied by radiographic pulmonary infiltrates without a clearly identifiable cause, is a major cause of morbidity and mortality after major anatomic pulmonary resection. Our objective was to identify the incidence and risk factors for the development of postoperative lung injury.

Methods: A retrospective case-control study of consecutive patients undergoing resection for lung cancer at a single institution was performed. The severity of lung injury was defined using the American European Consensus Conference on ARDS (acute respiratory distress syndrome) criteria and the National Cancer Institute Common Terminology Criteria for Adverse Events version 3.0 (http://ctep.cancer.gov/reporting/ctc.html). Patients with lung injury were compared with matched control patients, based on age, sex, and extent of resection, for examination of a priori defined risk factors.

Results: From January 2001 to June 2004, 1,428 patients underwent attempted curative lung cancer resection. Postoperative lung injury occurred in 76 (5.3%) cases, 44 (3.1%) of which met criteria for acute lung injury or acute respiratory distress syndrome. After matching, there were no differences between cases and control patients with respect to use of induction therapy, perioperative transfusions, or tumor laterality. After univariate and multivariate analysis, increasing perioperative fluid administration and decreasing postoperative predicted lung function were significant risk factors for the development of lung injury. The overall mortality for patients with lung injury was 25%, compared with 2.6% for the control group.

Conclusions: Lung injury after lung resection has a high mortality. Lower predicted postoperative lung function, especially diffusion capacity, in combination with greater perioperative fluid administration were significant predictors of postoperative lung injury.

Improvements in patient selection, surgical technique, anesthesia, and intensive care management have decreased the mortality associated with lung resections in most modern series [1–4]. Although these changes have impacted on other causes of mortality, lung injury (acute hypoxemia accompanied by radiographic pulmonary infiltrates without a clearly identifiable cause) after major thoracic surgery remains a potential debilitating and mortal complication, and it now represents the leading cause of death from pulmonary surgery [4, 5]. It has variously been described as postpneumonectomy pulmonary edema [6–15], low pressure or permeability pulmonary edema [16], postoperative lung injury [17, 18], and more recently, acute lung injury (ALI). The most severe form of lung injury is acute respiratory distress syndrome (ARDS) [19–21]. Regardless of the terminology used, the risk factors, causes, and optimal therapy remain elusive.

Previous reports of lung injury after pulmonary resection have reported a range of incidences, from 4% to 7% after pneumonectomy to 1% to 7% after lobectomy [7, 11–17]. More recently, a consensus has emerged in the descriptions and definitions of lung injury, with several large series [19–21] using the guidelines set forth by the American-European Consensus Conference on ARDS [22]. This has been accompanied by the belief that this poorly understood process is another form of ARDS preceded by surgical lung trauma. Using this paradigm, the reported incidence of ALI after major thoracic surgery is 2% to 8% and postoperative ARDS is 2% to 5% [19–21].

Few studies in the literature have attempted to define perioperative factors that can identify high-risk patients in whom preventative or additional therapeutic interventions can be used. The rationale for undertaking this study was to examine the incidence of and risk factors for lung injury in a large cohort of patients undergoing surgical resection for lung cancer to develop interventions to reduce this dreaded complication.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 References
 
Approval for the study was obtained and the need for individual patient consent was waived by the institutional review board. An institutional review board–approved, prospectively maintained database of all patients undergoing thoracic surgery for lung cancer at a single institution was used to identify patients undergoing complete resection of a primary bronchogenic carcinoma. Patients who underwent incomplete or no resection were excluded to eliminate the potential influence of residual or extensive, unresectable disease.

Standard anesthesia induction and maintenance regimens, as well as intraoperative fluid restriction, were used for all patients. Postoperative pain relief was provided by continuous administration of epidural or intravenous opioid (usually fentanyl with bupivacaine 0.05%) administration. In all patients pulmonary resection was performed either by means of video-assisted thoracoscopic surgery or standard posterolateral thoracotomy using single-lung ventilation. Video-assisted thoracoscopic surgery lobectomy was defined as anatomic pulmonary lobectomy using a video thoracoscope and three non–rib-spreading incisions, the largest of which was a 3- to 4-cm utility incision. It is our standard practice in patients who have anatomic lung resection to perform systemic mediastinal lymph node dissection as previously described [23].

Postoperative lung injury was defined as pneumonitis, ALI, or ARDS occurring in the immediate postoperative period during initial hospitalization. Acute lung injury and ARDS were defined as acute onset of hypoxemia with abnormal oxygenation ratios (arterial partial pressure of oxygen to fraction of inspired oxygen: ALI, <300; ARDS, <200) and radiographic infiltrates characteristic of pulmonary edema according to American-European Consensus Conference on ARDS guidelines [22]. Pneumonitis was defined using similar criteria except with a lesser degree of hypoxemia (grade 3 or less) as outlined by the National Cancer Institute Common Terminology Criteria for Adverse Events version 3.0 (http://ctep.cancer.gov/reporting/ctc.html). Patients with unilateral infiltrates on chest roentgenogram were included, as there is evidence that the radiographic patterns of ARDS are asymmetric after lobectomies [24]. In contrast, patients who had cardiogenic causes of pulmonary edema, such as congestive heart failure, were excluded.

Specific risk factors to be examined were defined a priori by searching the existing literature. Studies of lung injury after anatomic pulmonary resection that included more than 500 patients total or more than 100 patients undergoing pneumonectomy were reviewed (Table 1). Based on this review, the examined factors included volume of perioperative fluid administered, extent of surgical resection, use of induction therapy, laterality, use of perioperative blood transfusion, and postoperative predicted lung function (estimated postoperative forced expiratory volume in 1 second [FEV1] and diffusing capacity of lung for carbon monoxide [DLCO]).


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  		Table 1 Risk Factors for Lung Injury After Thoracotomy
 
Perioperative fluid administration was defined as the sum of intraoperative fluids and all intravenous fluids given in the 12-hour period after surgery. Extent of surgery performed was defined as wedge resection, segmentectomy, lobectomy, bilobectomy, or pneumonectomy. Induction therapy included chemotherapy or radiotherapy. Postoperative predicted lung function was calculated as follows: Preoperative measured lung function x (1 – number of segments resected/total number of existing segments). Wedge resection was defined as one segment. Data on patient characteristics, operative details, and postoperative recovery were collected in a prospective database approved by the institutional review board and analyzed retrospectively. All complications were graded according to the National Cancer Institute Common Terminology Criteria for Adverse Events.

Cases were defined as patients who exhibited postoperative lung injury, whereas controls were patients without lung injury after curative lung resection for bronchogenic carcinoma. Patients were categorized into age and procedure bins. For patients with lung injury in every age-procedure bin a matched set of control patients were obtained by randomly sampling an equal number of control patients from that bin. The Fisher’s exact test was used for comparison of cases and controls based on T, N, and M status, as well as sex. Univariate analyses compared the two groups, stratified by age and procedure, using the Cochran-Mantel-Haenszel test for discrete factors and the stratified Wilcoxon test for continuous factors. Multivariate analysis was performed with a conditional logistic model and the log-rank test. Because of correlation between predicted postoperative FEV1 and predicted postoperative DLCO, the best model fits were those that included only one of the two, along with perioperative fluids.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 References
 
Review of the prospective database of thoracic surgical cases performed from January 2001 through June 2004 revealed 1,428 consecutive patients who underwent surgical resection for primary bronchogenic carcinoma. There were a total of 76 patients (5.3%) who exhibited primary lung injury postoperatively. Forty-four patients (3.1%) had ALI or ARDS unrelated to a separate organ system injury requiring mechanical ventilation and critical care admission. Thirty-two patients (2.2%) had pneumonitis that was successfully treated without requiring mechanical ventilatory support. After matching for age, sex, and extent of resection, there were a total of 152 patients eligible for analysis, 76 in each group. The patients in each group were well matched with the median age of both groups being 71 years (range, 44 to 87 years). The majority of patients underwent lobectomy (55 of 76, 72%), followed by wedge (8 of 76, 11%), pneumonectomy (7 of 76, 9%), segmentectomy (4 of 76, 5%), and bilobectomy (2 of 76, 3%).

Looking at additional characteristics between the two groups (Table 2), there was a higher proportion of male patients in the lung injury group compared with the control group (57% versus 42%; p = 0.10), although this was not a statistically significant difference. Similarly, there was a trend toward a larger percentage of current smokers in cases versus controls (29% versus 16%; p = 0.08). There also was no difference in the pathologic T, N, or M status between groups. The median number of lymph node stations dissected for both groups was 4 (range, 0 to 9), with no statistically significant difference between groups in the distribution of node stations dissected when stratified by age and procedure (p = 0.55).


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  		Table 2 Patient Characteristics
 
The incidence of lung injury was analyzed by extent of surgery (Table 3). Pneumonectomy patients had the highest rate of lung injury with an overall incidence of 10.1% (7 of 69), followed by those undergoing lobectomy (5.5%, 55 of 1,007). Within the pneumonectomy subgroup there appeared to be similar rates regardless of laterality. Of note, even patients undergoing sublobar resections, including nonanatomic wedge resection, had a 4% rate of lung injury.


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  		Table 3 Lung Injury Incidence by Extent of Surgery
 
The results of univariate analysis to identify risk factors for the development of lung injury are shown in Table 4. Patients who exhibited lung injury received significantly higher median amounts of perioperative fluids than those in the control group (2,775 mL; range, 1,350 to 5,000 mL versus 2,500 mL; range, 1,400 to 4,500 mL; p = 0.05). An odds ratio of 1.2 (95% confidence interval, 1.0 to 1.4) per increase of 500 mL of perioperative fluid administration was noted. In addition, cases had lower median postoperative predicted lung function than controls, reflected both by FEV1 (59%; range, 25% to 91% versus 69%; range, 36% to 107%; p = 0.01) and by DLCO (48%; range, 16% to 104% versus 60%; range, 25% to 126%; p = 0.007). Odds ratios of 1.11 (95% confidence interval, 1.01 to 1.20) and 1.10 (95% confidence interval, 1.01 to 1.17) were observed for each 5% decrease in postoperative predicted FEV1 and DLCO, respectively. Receipt of induction therapy, perioperative transfusion, and the laterality of the procedure were not significant factors contributing to the development of postoperative lung injury.


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  		Table 4 Univariate Analysis for Risk Factors
 
Because of the correlation between FEV1 and DLCO on univariate analysis, for multivariate analysis the best model fit included either FEV1 or DLCO along with perioperative fluid administration (Table 5). The area under the receiver operating characteristics curve using FEV1 was 0.586, and 0.602 using DLCO. Using FEV1 in the multivariate analysis, both decreased postoperative predicted lung function and increased perioperative fluid administration remained independent predictors of postoperative lung injury. With DLCO only decreased postoperatively, predicted DLCO remained a significant, independent risk factor. Local regression estimate of the probability of ALI as a function of postoperative predicted lung function showed that there was a gradual increase in the incidence of lung injury with progressive decline in postoperative lung function with no clear inflection point (Fig 1).


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  		Table 5 Multivariate Analysis for Risk Factors
 

Figure 1
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  		Fig 1. Relationship between predicted postoperative lung function and acute lung injury (ALI). Each dot represents a patient where the x axis is the diffusing capacity of lung for carbon monoxide (DLCO) value (A) or forced expiratory volume in 1 second (FEV1) value (B) and the y axis is whether or not the patient had acute lung injury.

 
The cause of lung injury in most patients was not known. Twenty-eight patients had sputum cultures positive for bacteria, whereas the remainder were negative for pathologic organisms. The majority of patients were treated with intravenous steroids, antibiotic therapy, and diuresis as tolerated. Median hospital stay was 16 days (range, 5 to 107 days) in patients with lung injury and 5 days (range, 3 to 15 days) in the control group. Nineteen patients (25%) with lung injury died in the hospital compared with only 2 patients (2.6%) in the control group (Table 6). The majority of lung injury patients who died had either ALI or ARDS (17 of 19). Within the subset of ALI or ARDS patients, in-hospital mortality rate was 39% (17 of 44), whereas 94% (30 of 32) of the patients who had less severe pneumonitis survived. Three of 7 patients (43%) who exhibited lung injury after pneumonectomy died, whereas 14 of 25 (25%) with lung injury after lobectomy died (Table 6). One patient (8%, 1 of 12) who had a sublobar resection and exhibited lung injury died. The operative mortality for the entire cohort of patients treated during this time was 1.8% (23 of 1,428): 4.3% pneumonectomy, 5.7% bilobectomy, 1.4% lobectomy, 0% segmentectomy, and 1.5% wedge resection.


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  		Table 6 Lung Injury Mortality by Extent of Surgery
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 References
 
Owing to improvements in surgical technique, patient selection, and anesthetic and critical care management, postoperative morbidity and mortality from lung resection is low in the modern era [1–4]. Despite this fact postoperative lung injury remains a significant cause of morbidity and mortality. This potentially devastating complication has most commonly been described after pneumonectomy [6–8, 10–12], but can occur after any form of pulmonary removal, including sublobar resection [17, 20]. Variability in definition of lung injury has resulted in a range of reported incidences, ranging from 4% to 7% after pneumonectomy to 1% to 7% after lobectomy [7, 11–17]. With the acceptance of the American-European Consensus Conference on ARDS definitions of ALI and ARDS, the incidence of these most severe forms of lung injury has been shown to be from 2% to 8% after lung resection [17, 19–21]. In the current study of 1,428 patients undergoing lung cancer resection, we observed a 5.3% overall rate of lung injury and a 3.1% rate of severe injury in the form of ALI or ARDS. This represents the largest study evaluating the incidence and risk factors associated with postoperative lung injury.

This study suggests that increased perioperative fluid administration and decreased postoperative predicted lung function are independent risk factors associated with lung injury after surgery for lung cancer. By multivariate analysis in the model using postoperative predicted FEV1, the odds ratio for developing lung injury was 1.17 for each 500-mL increment in perioperative fluid administered and 1.10 for every 5% decrease in postoperative FEV1. Using postoperative predicted DLCO, the odds ratio for lung injury was 1.09 for each 5% decrement in postoperative DLCO, suggesting that there is a 9% greater chance of developing lung injury as DLCO drops 5%. There are a scant number of previous studies elucidating the mechanisms or risk factors associated with postoperative lung injury, particularly in nonpneumonectomy patients. A number of risk factors and possible mechanisms have been implicated, but none with sufficient consistency or based on adequate numbers of patients to be able to draw firm conclusions. Thus, to determine what factors we would evaluate, we reviewed studies that had either greater than 500 patients total or 100 pneumonectomy patients.

The notion that excessive perioperative fluid administration might promote postoperative lung injury (postpneumonectomy pulmonary edema) arose from the study by Zeldin and coauthors [6] that reported on 10 such patients. The majority (9 of 10) had right pneumonectomy and had increased fluid administration. Other studies have reported corroborative findings demonstrating an association between increased fluid administration and postoperative lung injury [11, 21]. Licker and colleagues [21] reviewed 879 patients who underwent pulmonary resection and showed in multivariate analysis that excessive fluid administration, high intraoperative ventilatory pressures, pneumonectomy, and preoperative alcohol abuse were independent risk factors for ALI [21].

There are many studies that show that decreased preoperative and postoperative predicted lung function are associated with increased postoperative morbidity after lung resection, but almost none demonstrating a correlation with lung injury. Parquin and colleagues [11] reviewed 146 patients who had pneumonectomy and demonstrated that postoperative perfusion of less than 55% and FEV1 of less than 45% were associated with postpneumonectomy pulmonary edema [11]. Our results further quantify this risk by showing an odds ratio of 1.1 for each decrease of 5% in either variable, and further suggest that postoperative predicted DLCO is perhaps the strongest risk factor associated with risk of lung injury. Moreover, the association between the two is continuous with no discernible level of DLCO at which risk rises precipitously.

The results failed to demonstrate any clear influence of mediastinal lymph node dissection in the development of postoperative lung injury. Little and colleagues [25] suggested in an animal model that lymphatic disruption contributes to postpneumonectomy pulmonary edema, but this has not been shown conclusively in human studies. The recent American College of Surgeons Oncology Group (ACOSOG) Z0030 randomized trial of mediastinal lymph node dissection versus sampling did not reveal any difference in morbidity or mortality associated with dissection [26].

Of interest is the number of patients who exhibited lung injury after lesser surgery, either wedge resections or segmentectomies. The incidence in this group was 4%, similar to that of patients who had lobectomies. A similar proportion was reported by Ruffini and colleagues [20] in an analysis of 1,221 patients who had thoracotomies for lung cancer. They found ALI in 3.2% (3 of 93) of patients who had sublobar resections, all of whom died. This is likely related to the fact that patients selected to undergo sublobar resections for lung cancer are generally in poor health to begin with and have reduced preoperative lung function compared with patients having lobectomies.

Even fewer studies have been performed to determine whether any intervention can decrease the incidence of ALI or ARDS after pulmonary resection. Cerfolio and coauthors [14] reported on the administration of steroids before ligation of the pulmonary artery in patients undergoing pneumonectomy, suggesting that this strategy reduced the incidence of postpneumonectomy pulmonary edema. It should be noted that this study was designed primarily to assess the safety of administering steroids. In addition, the patients receiving steroids were compared retrospectively with unmatched patients from a different period.

The use of steroids in the treatment (rather than prevention) of ALI or ARDS has received much attention. Earlier studies that focused on short courses of high-dose glucocorticoids showed them to be ineffective and possibly harmful [27]. The ARDS Clinical Trials Network performed a randomized, placebo-controlled trial of methylprednisolone in patients who had persistent ARDS [28]. Steroids (or placebo) were started at least 7 days after the diagnosis of ARDS. They found no difference in overall mortality, and in the subgroup of patients who received steroids more than 2 weeks from diagnosis mortality was increased. The authors concluded that the routine use of steroids in persistent ARDS is not supported.

In a similar vein, there have been no prospective studies looking at the efficacy of fluid restriction in preventing postoperative ALI. The ARDS Clinical Trials Network did, however, perform a randomized trial of conservative versus liberal fluid management in patients with already established ALI of all causes [29]. This revealed improved lung function and shorter duration of mechanical ventilation in the conservatively managed group, although no difference in 60-day mortality was observed.

Although the rates and mechanisms of lung injury after thoracic surgery are somewhat varied, what is unequivocal is that lung injury in the postoperative setting carries results in significant mortality rates that range from 52% to 100% in most large series [11, 12, 15, 17, 19–21]. This was confirmed by the results of this study. The overall in-hospital mortality rate was 25% in the lung injury patients compared with only 2.6% in the control group. As expected, mortality from lung injury was highest after pneumonectomy (43%) and in the subset of patients who met criteria for ALI or ARDS (39%). These mortality data are also consistent with a previous report from our institution by Dulu and colleagues [30] examining the incidence and outcomes of exhibiting ALI or ARDS after thoracic surgical procedures for a wider variety of indications. They determined that the incidence of ALI or ARDS was 2.45% with an overall mortality of 40%.

There are several limitations of our study. This is a retrospective review and subject to the limitations of an observational study, despite efforts to obtain matched groups for analysis. Furthermore, establishing the diagnosis of ALI or ARDS based on American-European Consensus Conference on ARDS criteria was not always possible because of the lack of blood gas data on all patients. This may have resulted in underestimation of the true incidence of ALI or ARDS. The number of patients who had preoperative chemotherapy or radiotherapy was also too small to convincingly determine whether these regimens served as risk factors, although they have been implicated in other studies [11]. Although the results of this study identify clear risk factors for the development of lung injury, it does not elucidate the mechanism of injury, ie, whether increasing fluid administration causes injury or is an effect of the injury itself.

Acute lung injury and ARDS remain significant sources of morbidity and mortality after pulmonary resections for lung cancer. Risk factors associated with developing postoperative lung injury are increasing fluid administration and decreasing postoperative predicted lung function. Multivariate analysis revealed decreased postoperative predicted DLCO to be the strongest independent predictor of lung injury. This information should help develop both preventative and interventional strategies to minimize this uncommon, but potentially devastating, complication after major thoracic surgery.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
References
 
DR MICHAEL S. MULLIGAN (Seattle, WA): When you say that transfusion was not associated with an increased risk of lung edema, did you look at any particular breakdown of the component that was used? It’s always been alleged that platelet transfusion is associated with an increased risk of acute lung injury, particularly if it’s the second hit in the context of either reperfusion or postresection injury. Do you know whether or not any particular component, transfusional component, is associated with an increased risk?

DR ALAM: The majority of patients undergoing transfusion were given packed red blood cells. We did not specifically examine which other components were transfused, but we do have that data, so we could certainly look at that. It would be interesting.

DR MULLIGAN: One last question. I was fortunate enough to sit down with Hermes Grillo some years ago, and I fancied myself a scientist who was working on acute lung injury, and he asked me why we get postpneumonectomy edema. And I appreciate the elegant descriptive statistics that you produced, and certainly words of caution for us as we go forward, but why does this happen?

DR ALAM: I think that’s a question that we have been struggling to answer for many years. Certainly in the initial experiments by Dr Zeldin he thought that it was related to some form of increased permeability of the capillaries and increased hydrostatic effects. And some physiologic studies with animals have been done. But I do not think we really know. I think the consensus now is that this is really just another form of ARDS (acute respiratory distress syndrome) with the inciting factor being surgical lung trauma.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

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