Assessment of Operative Risk in Patients Undergoing Lung Resection* Importance of Predicted Pulmonary Function

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1 Assessment of Operative Risk in Patients Undergoing Lung Resection* Importance of Predicted Pulmonary Function David]. Kearney, M.D.; Thomas H. Lee, M.D.; John]. Reilly, M.D., F.C.C.A. ; Malcolm M. DeCamp, M.D.; and David]. Sugarbaker, M.D., F.C.P.P. Objective: To evaluate the ability of preoperative variables to identify patients at increased risk for complications after lung resection and the usefulness of predicted postoperative as a marker of risk for adverse outcomes. Design: Prospective analysis of a cohort of patients undergoing pulmonary resection. Complication rates were analyzed according to preoperative pulmonary variables, demographic variables, procedure performed, and predicted postoperative FEV 1 Predicted postoperative was calculated using a formula estimating the decline in preoperative based on the number of bronchopulmonary segments removed during surgery. Setting: A major teaching hospital and tertiary referral center. Patients: A consecutive series of patients undergoing pulmonary resection. Measurements and main results: Medical complications were recorded as part of an ongoing clinical database. The overall complication rate was low (17 percent rate of any complication, 1 percent death rate). Univariate predictors of complications included age ~ 6, male sex, history of smoking, a pneumonectomy procedure, and a low predicted postoperative FEV 1 Hypercarbia ( 45 ~ mm Hg) on preoperative arterial glood gas analysis, desaturation on exercise o x i m e 9 t rpercent), y ( ~ and a preoperative less than 1 L were not predictive of complications. When the effect of these variables was controlled for in a multivariate analysis, a low predicted postoperative remained the only significant independent predictor of complications. For each.2 L decrease in predicted, the odds ratio for complications was 1.46 (95 percent confidence interval [CI] 1.2 to 1.8). Conclusions: A low predicted postoperative appears to be the best indicator of patients at high risk for complications, and it was the only significant correlate of complications when the effect of other potential risk factors was controlled for in a multivariate analysis. Pulmonary resection should not be denied on the basis of traditionally cited preoperative pulmonary variables, and a prediction of postoperative pulmonary function by a technique of simple calculation may be useful to identify patients at increased risk for medical complications. (Chest 1994; 15: ) ABG = arterial blood gas; MVV = maximum voluntary ventilation; PPO =predicted postoperative ~ ncancer g is the most common cause of cancer death in the United States. 1 An estimated 168, new cases will occur this year, 2 and the majority will die within the first year after diagnosis. 3 For patients with non-small-cell carcinoma presenting as localized For editorial comment see page 654 disease, surgical resection remains the only potentially curative option 4 The high rate of coexistent medical conditions in lung cancer patients complicates referral of such patients to surgery. Smoking is highly associated with the development of lung carcinoma; 5 the incidence increases further in smokers with COPD.B- 9 Additionally, smoking and chronic lung disease are *From the Respiratory Division( Dr. Reilly), Division of Thoracic Surgery (Drs. DeCamp and Sugarbaker), Department of Medicine (Dr. Lee), Brigham & Women's Hospital, and Departme nt of Medicine (Dr. Kearney), Beth Israel Hospital, Boston. Manuscript received March 24, 1993; revision accepted July 23. Reprint requests: Dr. Srfgarbaker, Division of Thoracic Surgenj, Briglwmand Women's Hospital, Boston associated with atherosclerotic vascular disease, making these conditions prevalent in patients with lung carcinoma. Thus, the clinician is often faced with the problem of considering lung resection as the only curative treatment in a patient with significant comorbid disease and ventilatory impairment. A wide range of tests has been evaluated to aid the identification of patients at high risk for developing complications after lung resection. These tests have included spirometry, arterial blood gas measurement (ABC), exercise testing, and radionuclide lung scanning. Previously reported studies have sought to define values for each of these modalities that would identify patients at prohibitive risk Demographic variables such as male sex, advanced age, and smoking status have been shown to identify groups at increased risk i Reported complication rates after lung resection have ranged from a 4 percent rate of death or severe disability in the 195s and 196s to mortality rates of9 to 27 percent in the 197s} 2 18 ' 2 Advances in operative technique and postoperative care have led CHEST I 15 I 3 I MARCH,

2 to a further decline in postoperative complication rates, with mortality rates of 2 to 11 percent reported in recent studies " 26 This decline in risk for patients undergoing lung resection has led to a reappraisal of many of the criteria that previously would have rendered a patient inoperable. The present study examines the relevance of many of these traditionally cited risk factors in the modem hospital setting and evaluates the use of a simple calculation of predicted postoperative pulmonary function as a predictor of postoperative complications. Patients METHODS The patient population consists of 331 patients who underwent single or multiple pulmonary wedge resections, lobectomies, or pneumonectomies. Subjects who underwent exploratory or staging thoracotomy procedures without resection of lung parenchyma were excluded from the study. This study population represents 86 percent (331) of 385 patients undergoing the above procedures during 24 months from August 1989, to August 1991, at the Brigham and Women's Hospital, Boston. The 54 patients (14 percent) meeting the above criteria not included in the analysis were omitted because they were inadvertently not entered prospectively in the clinical database. This occurred on a random basis without apparent selection bias. After surgery, all patients were cared for in a specialized intermediate care unit by the thoracic surgery service. The purpose of this unit is to provide specialized nursing care, respiratory therapy, pain control, and medical care to patients immediately after thoracic surgery. Emphasis is placed on aggressive pulmonary care, early ambulation, and pain control to minimize postoperative pulmonary complications. Data Collection All clinical data were recorded prospectively as part of an ongoing clinical database. Preoperative assessment included the documentation of historic information (symptoms, coexistent medical conditions, and tobacco use) as well as functional status (Kamofsky score). Preoperative pulmonary evaluation included ABC analysis (recorded in 95 percent of patients) and spirometry (recorded in 98 percent of patients). Patients also underwent measurement of room air oxygen saturation by oximetry at rest and with ambulation (recorded in 79 percent of patients). The ambulatory measurements involved a 6 -min walk on a level surface followed by two flights of stairs. The lowest percent saturation during this course was examined for this study. All patients were followed up prospectively after surgery and complications occurring during the patient's hospitalization that were identified in physician progress notes were recorded. For this study, "complications" were defined to include respiratory complications (pneumonia, atelectasis, mechanical ventilation for longer than 2 days, and respiratory failure), cardiac complications (myocardial infarction, supraventricular arrhythmias, ventricular arrhythmias), renal failure, and postoperative death. Predicted Postoperative Calculation of the forced expiratory volume in Ls (FEY 1 ) was performed using preoperative pulmonary function testing data and information on the number of bronchopulmonary segments removed (which usually can be predicted on the basis of preoperative radiologic studies). All operative notes were reviewed, and the 754 Table 1 - Ba eline Characteri.tic of 331 Patient Undergoing Lung Re ection No. of Characteristic Patients % Sex Male Female Age Mean± SD 58± 13. Range Type of Operation 1-3 wedge resection(s) <!: 4 wedge resections 9 3 Lobectomy Bilobectomies 4 1 Pneumonectomy Smoking history Past or present Still smoking 67 2 Never smoked Grade of dyspnea preoperatively (n = 274) Dyspnea with severe exertion only Dyspnea on hills or stairs Can walk indefinitely on level ground Dyspnea at 1 yds 1 4 Dyspnea with minimal activity 3 1 Kamofsky score (n = 279) Mean±SD 9.1 ± 1.1 Range 4-1 Pathology final diagnosis Benign 65 2 Malignant number of bronchopulmonary segments removed was recorded for each patient. Assuming that each of the 19 bronchopulmonary segments in the normal lung contributes equally to ventilatory function, each segment accounts for 5.26 percent of total lung function. The predicted postoperative FEY 1 was then estimated by the following formula: 17 predicted postoperative FEY 1 = preoperative FEY 1 x [1- (S x 5.26)/1), (S =number of bronchopulmonary segments removed). A right pneumonectomy was considered to cause a 55 percent decrement in preoperative FEY 1 and a left pneumonectomy to cause a 45 percent decrement. In patients undergoing wedge resections, each wedge resection was assumed to account for one bronchopulmonary segment. The right and left lower lobes were considered to have five bronchopulmonary segments, the right middle lobe to have two bronchopulmonary segments, the right upper lobe to have three bronchopulmonary segments, and the left upper lobe to have four bronchopulmonary segments. Statistics The relationships between potential predictors and postoperative complications were assessed in univariate and multivariate analyses. All statistical tests were two-tailed, with a significance level of.5. Categoric variables (sex, smoking status, preoperative Pco 2 45 mm Hg, complications, and FEY 1 > 1 L) were evaluated using a chisquare test or Fisher's exact test when the expected cell counts were less than five. Continuous variables (age, FEY 1 value) were evaluated using the Student's t test and a Wilcoxon rank sum test. A multivariate logistic regression analysis was performed to identify the independent correlates of complications. Operative Risk In Patients Undergoing Lung Resection (Kearney eta/)

3 Table 2 -Complications Occurring in 331 Patienn After Lung Resection No. of Complication Type Patients % Any complication Respiratory Pneumonia 8 2 Atelectasis ( ~ bronchoscopies 2 req) 13 4 Atelectasis (>2 bronchoscopies req) 1.3 Respiratory failure 6 2 Mechanical ventilation required for >2 days 4 1 postoperatively Cardiac Supraventricular tachycardia Ventricular arrhythmia 4 1 Arrhythmia req cardoiversion 1.3 My?Cardial infarction 2.6 Renal failure 4 1 Postoperative death 3.9 Study Population RESULTS The clinical characteristics of the 331 patients (mean age 58; 56 percent men) who underwent wedge resections, lobectomies, or pneumonectomies are summarized in Table 1. The most common operation, a lobectomy, was performed in 145 cases, while 46 patients underwent pneumonectomy. Two hundred forty-three patients had a history of tobacco use. Only 13 of the patients had dyspnea after walking 1 yards or less before surgery, and the mean Karnofsky score was 9.1. Two hundred sixty-six patients had malignant neoplasms as their final diagnosis. Complication Rate Complications occurring postoperatively are displayed in Table 2. Eight of 331 patients developed pneumonia, and 14 patients developed atelectasis, one of whom required more than two bronchoscopies postoperatively. Four patients required mechanical ventilation for more than 2 days after surgery, and respiratory failure developed in six patients. Cardiac complications included supraventricular arrhythmias that occurred in 37 patients and ventricular arrhythmias that occurred in 4 patients. One patient required cardioversion, and two patients developed postoperative myocardial infarctions. Renal failure occurred in four patients, and three patients died during hospitalization. Predictors of Postoperative Complications Variables often considered predictors of postoperative complications are displayed in Table 3. These include advanced age, male sex, smoking status, procedure performed, and preoperative pulmonary variables (FEV" Pco 2 data, and exercise pulse oximetry). Patients older than 6 years had a significantly higher rate of any complication. Thirty-seven (22 percent) of 167 patients aged 6 or older had complications vs 18 (11 percent) of 159 patients less than 6 years of age (p <.5). Male patients had a significantly higher overall complication rate. Complications occurred in 4 (22 percent) male patients vs 16 (11 percent) female patients (p <.5). Smoking status also was evaluated in patients undergoing surgery. Two hundred forty-three patients had a history of cigarette use, and 67 patients were still smoking at the time of surgery (Table 3). Eighty-eight patients denied any history of tobacco use. The number of adverse postoperative events was not significantly higher in patients still smoking at the time of surgery. Complications occurred in 12 ( 18 percent) of 67 patients still smoking vs 44 (17 percent) of 264 patients not using tobacco at the time of admission (p value not significant). When patients with any history of tobacco use (current or at any point in the past) were examined, a significantly higher rate of postoperative complications was found. Forty-eight (2 percent) of 243 patients with any history of tobacco use Table 3 -Clinical Correlates of Poltoperatiofl Complications No. No. (%)With Any Parameter Patients Complication p Value Age* <.5 ~ (22) < (11) Sex <.5 Male (22) Female (11) Smoker Current f Yes (18) No (17) Ever smoked Yes (2) <.5 No 88 8 (9) Preoperative :2:1 L (17) <ll 17 3 (18) Preoperative Pco 2 :2:45 mm Hg 3 4 (13) <45 mm Hg (17) Exercise %Sa 2 :2: (15) < (16) Procedure Pneumonectomy <.1 Yes (39) No (13) Lobectomy Yes (19) No (15) 1-3 Wedge resections <.1 Yes (6) No (24) *Data missing on 5 patients. t = not significant. CHEST I 15 I 3 I MARCH,

4 z 4 t= 3 c ::; a. :::E 2 % 1- i 1 ~... (') "' C\1 < Predicted postoperative FEV1 : 1. l n= L n=56 > 1.4 L n=221 p <.1 p <.5 II) An y 2 Cardiac TYPE OF COMPLICATION 3 Respiratory FI<:l! HE I. Postoperati\ e complication rate according to predicted postope ratiq FE\' 1 ntlue. had a postoperative complication vs 8 (9 percent) of 88 patients without any history (p <.5). Patients with a preoperative of less than 1 L did not have an increased overall complication rate. Complications occurred in 3 (18 percent) of li i percent) patients with a less than 1 L vs.51 ( 1 of 3i patients with a preoperative greater than 1 L (p value not significant). Complication rates also were evaluated according to preoperative Pco., data on ABC analysis. No significant difference in the overall complication rate was noted for patients with a Pco 2 greater than or equal to 4.5 mm Hg preoperatively. Four ( 13 percent) of 3 patients with hypercarbia had complications vs 5 (li percent) of 285 patients without hypercarbia (p value not significant). Preoperative exercise pulse oximetry data also was assessed (as evaluated by recording the lowest percent saturation during a 6-min walk on a level surface followed by two flights of stairs). This was not associated with an increased occurrence of complications. Twelve ( 16 percent) of ii patients with desaturation on exercise pulse oximetry had complications vs 28 ( 1.5 percent) of 18.5 patients without desaturation (p value not significant). Patients were classified according to the extent of lung resection performed, and differences in complication rates were examined (Table 3). Patients undergoing a pneumonectomy had a significantly higher rate of complications. All deaths occurred in the group undergoing pneumonectomies. Eighteen (39 percent) of 46 patients undergoing a pneumonectomy had a complication vs 38 (13 percent) of 28.5 patients not having this procedure (p <.1). Patients undergoinig one to three wedge resections had a significantly lower rate of any complication. Eight (6 percent) of 12i patients having a wedge resection had a complication vs 48 (24 percent) of 24 patients having a more extensive procedure (p <.1). Patients who underwent lobectomies or four or more wedge resections did not have significantly different complication rates when compared with patients not having these procedures. Complication Rate by Predicted Postoperative Values Figure 1 shows the postoperative complication rate stratified according to predicted postoperative value. Complication rates were assessed for other complications, cardiac complications, and respiratory complications. Forty-seven patients had a predicted postoperative less than 1 L, and 16 of these (34 percent) had other complications, 9 ( 19 percent) had a cardiac complication, and i ( 15 percent) had a respiratory complication. Fifty-six patients had predicted postoperative of 1.1 to 1.4 L, and 14 (25 percent) of these had other complications, 12 (21 percent) had a cardiac complication, and.5 (9 percent) had a respiratory complication. Two hundred twenty-one patients had a predicted postoperative of greater than 1.4 L, and 24 ( 11 percent) of these had other complications, 2 (9 percent) had cardiac complications, and 6 (3 percent) had respiratory complications. As the predicted postoperative declined, a significant association \Vas found for an increased occurrence of other complications (p <.1), cardiac complications (p <..5), and respiratory complications (p <.1). 756 Operative Risk in Patients Undergoing Lung Resection (Kearney et a/)

5 Multivariate Analysis In a multivariate logistic-regression analysis adjusting for age, sex, preoperative Pco 2 greater than or equal to 45 mm Hg, exercise pulse oximetry saturation of less than 9 percent, history of tobacco use, history of coronary artery disease, and history of hypertension, postoperative was a significant independent predictor of complications. For each.2 L decrease in predicted, the odds ratio for complications was 1.46 (95 percent CI 1.2 to 1.8). Only the predicted postoperative subgroup remained associated significantly with an increased rate of other complications postoperatively when the effect of the other variables was controlled for in the model. DISCUSSIO:-; This study examined the postoperative course of a large cohort of patients undergoing lung resections and evaluated the significance of a number of preoperative variables as indicators of postoperative risk. The postoperative complication rate was quite low, and the best indicators of patients at high risk for the development of complications were a low predicted postoperative or a pneumonectomy as the procedure performed. The predicted postoperative remained the only significant predictor of complications when the effect of other traditionally cited markers of increased risk was controlled in a multivariate analysis. A low preoperative did not correlate with complications (although the small number of patients [ 17] with an less than 1 L limits the power to detect a significant difference). An elevated Pco 2 also did not correlate with a complicated postoperative course in this study. These results suggest that lung resection usually is tolerated well even in patients with significant ventilatory impairment and that estimation of the predicted postoperative by a simple calculation may be useful in identifying patients at high risk for a complicated course. The postoperative complication rate (less than 1 percent mortality rate and 17 percent rate of any medical complication) is somewhat lower than that reported in previous studies. Large studies in the 198s have reported mortality rates after lung resection as low as 2 to 5 percent with somewhat higher mortality rates in older patients and in series examining pneumonectomies a l o n e ' ~ The low occurrence of adverse outcomes in this series may be due to several factors. The method of recording complications by reviewing physician progress notes rather than by examining objective measures of disease (ie, reviewing chest x-ray films for evidence of pneumonia) is likely to have contributed to the low rate of postoperative complications. Treating patients after surgery in a specialized intermediate care unit, with emphasis on aggressive, preventive respiratory modalities (chest physiotherapy, incentive bronchospirometry, adequate anesthesia, and early ambulation) may also have led to a decreased occurrence of respiratory complications. Furthermore, this study was performed in a tertiary referral center with surgeons experienced in performing large numbers of lung resections. Also, the patient population operated on appears to have been relatively healthy. The small number of patients in this study with preoperative values less than 1 L (17 patients) suggests that selection of a patient population without severe ventilatory impairment is likely to have contributed to a low complication rate, and the relatively intact grades of preoperative dyspnea and Kamofsky scores support this hypothesis. Also, patients undergoing exploratory procedures without resection of lung parenchyma were excluded from the analysis. This may have contributed to the low complication rate as well, with the exclusion of patients with more advanced nonresectable disease who may be more likely to have a complicated course. Previous studies have yielded conflicting results regarding the use of preoperative pulmonary function tests as predictors of postoperative complications. The original work by Gaensler et al in 1955, 18 was based on the outcome of patients undergoing surgery for tuberculosis. He found that patients with a preoperative less than 7 percent predicted or with a maximum voluntary ventilation ( MW) less than 5 percent predicted had a 4 percent mortality rate. Subsequent investigators noted in the 196s and 197s that patients with an MW less than 5 percent or a depressed ( < 1.2 L or < 2 L and age > 6) had a high mortality rate when undergoing surgery for lung cancer Other investigators found no significant difference in between survivors or nonsurvivors in patients undergoing pneumonectomy or lobectomy Olsen et al 29 identified patients considered at high risk ( <2 Lor MW <5 percent predicted) and found that these patients could undergo resection with acceptable mortality rates if they did not have pulmonary hypertension or hypoxia on pulmonary occlusion studies, or had a predicted postoperative of greater than 8 ml by quantitative perfusion scanning.29 Interestingly, they note in this study that the predicted postoperative value of 8 ml as a cutoff point was not derived through studies of patients undergoing lung resection but through observation of the degree of ventilatory impairment usually tolerated by patients with severe obstructive lung disease. A postoperative value of less than 8 to 1, ml has been cited widely as a prohibitive level of pulmonary function since that time. One study since has shown that patients with marked impairment of pulmonary function (preoperative < 1 Lor MW <35-4 percent predicted) tolerated limited resec- CHEST I 15 I 3 I MARCH,

6 tions well. 3 The present study appears to confirm these findings. Limited resections (single or multiple wedge resections) were performed in 12 of the 17 patients with a preoperative ofless than 1 L, and the remaining 5 patients underwent lobectomies. These patients with markedly impaired preoperative pulmonary function did not have an increased incidence of complications. A predicted postoperative of less than 1 L was the best predictor of postoperative complications in this study (p <.1), whereas a preoperative of less than 1 L was not predictive of complications. While this appears to confirm the criteria of Olsen et al 29 that patients with a low predicted postoperative are at an increased risk of complications, the degree of risk does not appear to be prohibitive. Only two deaths occurred in this group ( 4.3 percent of the 47 patients), and two thirds of the patients had an uncomplicated postoperative course. These results also suggest that the magnitude of change in pulmonary function may be an important indicator of risk for postoperative complications. The group with a predicted postoperative ofless than 1 L necessarily includes all patients with a preoperative of less than 1 L, and this low preoperative value alone did not confer increased risk. When patients with a preoperative of greater than 1 L and a postoperative ofless than 1 L, however, are analyzed as a group including the patients with both preoperative and postoperative values less than 1 L, a predicted postoperative less than 1 L is the most significant predictor of complications. This suggests that patients with preoperative values greater than 1 L who have a predicted decline in to less than 1 L after surgery are at higher risk for complications. The higher rate of complications among patients undergoing pneumonectomies supports this possibility that a large decline in ventilatory function rather than a low preoperative value alone may be an important marker of increased risk. The use of the technique of estimating predicted postoperative pulmonary function by simple calculation is supported by previous studies comparing quantitative nuclear medicine scans, simple calculation, and actual measured postoperative spirometric values These studies have shown simple calculation to be as accurate as quantitative perfusion scans for this purpose. Estimation of predicted postoperative pulmonary function by simple calculation, however, is based on the assumption that each bronchopulmonary segment contributes equally to ventilatory function, and patients with severe atelectasis, hilar disease, or endobronchial involvement may have significantly unequal ventilation or perfusion. In cases where this is suspected, quantitative ventilation/perfusion scanning may be more useful in predicting postoperative pul- 758 monary function. Previous studies also have shown that low predicted postoperative values (using quantitative perfusion lung scanning) correlate with complications Markos et ap 5 examined the outcome of 55 patients undergoing lung resections, and they found a significantly increased mortality rate among patients with predicted less than 4 percent predicted. In a larger study, Wahi and colleagues21 analyzed 197 patients undergoing pneumonectomies, and they found a significantly elevated mortality rate among patients whose predicted postoperative was less than 1.65 L. Another study (involving only 22 patients) has shown no significant correlation between predicted postoperative pulmonary function values and complications rates.3 1 The present study is the first to our knowledge to examine the use of estimating the predicted postoperative by the technique of simple calculation alone. Our study indicates that with modem surgical techniques and improved postoperative care, the level of prohibitive pulmonary function as defined by calculation of predicted postoperative may be significantly lower than indicated by previous studies using this method. Although the rate of complications significantly was higher in our study among patients with a predicted postoperative less than 1 L, the magnitude of risk did not appear to be prohibitive. The level of prohibitive risk may lie lower than 1 L, possibly in the 6 to 8 ml range. Patients with hypercarbia on preoperative ABC measurement have been classified traditionally as being at very high risk for postoperative respiratory complications (as noted in a recent position paper by the American College of Physicians on pulmonary function testing). 32 The categorization of these patients as very high risk candidates for pulmonary resection is based on anecdotal reports in the literature and has never been studied formally in a large group of patients. The 3 patients in this study with a preoperative Pco 2 greater than or equal to 45 mm Hg did not have an increased occurrence of postoperative complications, and it appears that this should not be considered a contraindication to surgery. Previous investigators also have cited desaturation on pulse oximetry as indicating a high risk population for lung resection, 15 but in this study desaturation to less than 9 percent did not correlate with postoperative complications. Patients still smoking until the time of surgery did not have significantly more complications compared with those not still smoking. Prior studies of patients undergoing elective coronary artery bypass grafting have indicated that patients who choose to stop smoking at least 2 months before surgery have a lower incidence of complications compared with patients who stop smoking closer to their date of surgery.33 Unfortunately, it is not clear whether it is Operative Risk in Patients Undergoing Lung Resection (Kesmey et sl)

7 appropriate to extrapolate these data to patients undergoing lung resection, and the time interval from smoking cessation to surgery is not recorded in our database. Patients without any smoking history had significantly fewer overall complications. These data suggest that lung resection can be performed in patients with significant ventilatory impairment with a low rate of morbidity and mortality and that surgery should not be denied on the basis of preoperative variables such as a low FEV" hypercarbia on blood gas analysis, or exercise desaturation on pulse oximetry. Additionally, patients undergoing pneumonectomies or with a low predicted postoperative as estimated by simple calculation appear to be at increased risk for complications, but they may still undergo surgery with acceptable mortality rates. ACKNOWLEDGMENT: The authors thank Mary Sullivan Visciano for her editorial assistance. REFERENCES Centers for Disease Control. 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