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Ann Thorac Surg 1996;61:1494-1500
© 1996 The Society of Thoracic Surgeons
Division of Pulmonary and Critical Care Medicine, Department of Medicine, and Department of Surgery, University of Tennessee, Memphis, Tennessee
Accepted for publication January 23, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Methods. We performed an open, prospective preoperative trial and a postoperative outcome evaluation with a combined medical, surgical, and exercise physiology evaluation at three university hospitals. All eligible patients had spirometry, lung volume determination, and quantitative perfusion scanning and performed a cardiopulmonary stress test, stair climbing, and a 12-minute walk for distance. Functional status was determined with an Eastern Cooperative Oncology Group score, a dyspnea score, and a cardiopulmonary risk index.
Results. We identified 12 patients who met strict criteria for borderline pulmonary function during a 1-year study period. The mean forced expiratory volume in 1 second (FEV1) was 1.38 L (48% of predicted). The mean predicted postoperative FEV1 based on pneumonectomy was 700 mL. Eleven of the patients did the stair climb and 10 passed. All 12 patients achieved a maximum oxygen consumption greater than or equal to 10 mL • kg-1 • min-1 (mean value, 13.8 mL • kg-1 • min-1). Thirteen operations were performed on the 12 patients. Nine complications occurred in 7 patients.
Conclusions. Patients with borderline pulmonary function can undergo resection safely if they have an FEV1 equal to or greater than 1.6 L or 40% of its predicted value, a predicted postoperative FEV1 of 700 mL or more, a maximum oxygen consumption of 10 mL • kg-1 • min-1 or greater, or stair climbing of three flights or more. Cardiopulmonary stress testing and stair climbing add valuable clinical information for patients with an FEV1 of less than 1.6 L.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Stair climbing and cardiopulmonary stress testing are two of the most commonly used exercise tests. Stair climbing has been used for years by thoracic surgeons to discriminate between patients who would and patients who would not tolerate resection regardless of static pulmonary function. This has been validated as a useful predictor in several fairly recent studies [3, 4]. The maximum oxygen consumption (VO2max) as measured by the cardiopulmonary stress test (CPX) has also been proposed as a better predictor of patient outcome. We have prospectively examined the role of preoperative cardiopulmonary stress testing in patients considered at high risk for lung resection. In particular, we wanted to examine three issues. What is the role of the CPX in preoperative risk stratification? Can the threshold where physiologic function is irreparably impaired be better defined? Do sophisticated tests such as the CPX provide better information than simpler and less involved tests such as the stair climb?
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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All patients had spirometry with and without a bronchodilator, measurement of lung volumes, and a quantitative perfusion scan and performed the CPX, stair climb with pulse oximetry, and 12-minute walk for distance with pulse oximetry. Spirometry and lung volumes were obtained on a Sensor Medics 2100 spirometer and an IBM Personal System/2 model 30 2886 computer. The spirometry was done according to American Thoracic Society standards using the race-adjusted normal of Knudson and associates [6]. The lung volume measurements were obtained at functional residual capacity using a Gould 2800 body plethysmograph.
The CPX was done using an electrically braked cycle ergometer (Ergoline 900) connected to a Sensor Medics 2900 metabolic cart, Sensor Medics Max 1 continuous electrocardiographic monitor, and an IBM Personal System/2 model 501 computer. Patients fasted for at least 2 hours prior to the test and exercised to symptom limitation. After being connected to the apparatus, patients were observed at no work load for 2 to 3 minutes during which time they were coached to adopt a regular breathing pattern. After this stabilization period, they were instructed to begin pedaling at 35 to 40 kilo-pond meters. The cycle ergometer was set initially at 10 W and work was increased by 10 W every minute until symptom limitation. An electrocardiogram was obtained at rest, at 1-minute intervals during exercise, and until return to baseline. Rest and maximum exercise arterial blood gases were obtained.
The stair-climbing test was performed at a moderate pace of the patient's own choosing. The test was considered completed once the patient stopped for any reason. Patients were encouraged to exercise to a symptom-limited maximum and to complete the flight of stairs they were on if possible. They were not allowed to use the handrail to pull themselves up the stairs. The rest and exercise pulses and oxygen saturations, the time necessary to complete the test, the number of steps climbed, and the reason for stopping were recorded. The step height was 17.5 cm, and there were 21 steps per flight. The 12-minute walk for distance was done on a level surface using a 30-m shuttle. Patients were instructed to cover the maximum distance possible in the time allowed. They were allowed to rest as needed. The distance covered to the nearest 10 m and the rest and exercise oxygen saturations were recorded.
The quantitative perfusion scan was performed by injecting 4 mCi of technetium 99m-labeled macroaggregated albumin. Using a gamma camera, counts were obtained either in the posterior projection or as the average of the anterior and posterior views, whichever was greater. The predicted postoperative FEV1 (FEV1ppo) was obtained by multiplying the percent perfusion to the uninvolved lung times the measured FEV1. Functional status was scored using the ECOG scale with 0 being asymptomatic and 4, bedridden [5]. Dyspnea was scored using a modified Borg scale with 0 being asymptomatic and 3, dyspnea at rest. The cardiopulmonary risk index as described by Epstein and colleagues [7] was also obtained. This index uses separate scales for cardiac and pulmonary risk indices that are then combined to describe the cardiopulmonary risk index. The pulmonary risk index is scored on a scale of 0 to 6, with one point each for obesity, recent cigarette smoking, productive cough, diffuse wheezing or rhonchi, spirometric obstruction, and carbon dioxide retention. The maximum cardiopulmonary risk index is 10, and a score higher than 4 has been associated with a higher risk of perioperative complications [7].
Patients were considered eligible for operation if they met any of the following criteria: FEV1 of 1.6 L or more, FEV1ppo of 700 mL or more, FEV1 equal to or greater than 40% of the predicted value, VO2max of 10 mL • kg-1• min-1 or greater, or stair climb of 3 flights or more for lobectomy or 5 flights or more for pneumonectomy. The extent of resection was at the discretion of the surgeon.
After hospital discharge, one of us (J.G.) who was blinded to the preoperative evaluation and predictions reviewed the charts. He scored them for the following events occurring within the 30 days immediately after operation: operation performed, length of stay in the intensive care unit, prolonged mechanical ventilation (>48 hours), respiratory insufficiency (defined as ventilator dependence or incapacitating dyspnea as determined by survey), persistent air leak (>10 days), and pneumonia. He also recorded all arrhythmias, myocardial infarction, pulmonary embolism, hypotension, atelectasis, days of intubation from preoperative intubation to postoperative extubation, and death. The modified Borg score and ECOG classification were ascertained 1 month postoperatively.
Data were analyzed to determine overall 30-day morbidity and mortality with the most important end points being death and respiratory insufficiency. Univariate analysis of the cohort was done for each variable (ie, FEV1, FEV1 % predicted, FEV1ppo, VO2max, and stair climb) to determine the ability of each variable to discriminate between patients who could and patients who could not tolerate lung resection.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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. All patients had chronic obstructive pulmonary disease with moderate to severe obstruction. The mean FEV1 to forced vital capacity ratio was 45.7%. Thirteen operations were performed on these 12 patients. One patient required a completion lobectomy after the initial wedge resection showed microscopic invasion at the margin. The other operative procedures were as follows: one pneumonectomy, five lobectomies, two segmentectomies, two wedge resections, and one thoracotomy without resection.
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lists the characteristics of those patients who had complications and the complications that occurred. Patient 2 had an air leak and respiratory insufficiency, which was treated for 3 days with noninvasive positive-pressure face-mask ventilation. Two patients had transient atrial fibrillation, which responded promptly to therapy and did not recur. However, patient 1 died suddenly at home 8 days after operation. At operation, the tumor was contiguous to the left pulmonary artery and pericardium with limited blood flow to the left lung, so no resection was attempted. Postmortem examination was not performed. Four patients had an abnormal baseline electrocardiogram, and 2 had complications.
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lists the resection threshold criteria with the mean values for the group, the mean values for patients who had complications, and the mean values for those who did not. What follows is an analysis of each individual threshold in relation to surgical outcome.
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FEV1 Equal to or Greater Than 40% of Predicted Value
The mean FEV1 % predicted for the entire group was 48%. For those experiencing complications, it was 50% versus 46% for patients who did well. Seven patients met entry criteria for operation on the basis of an FEV1 equal to or greater than 40% of predicted, and 4 experienced complications. Three of the 5 patients with an FEV1 of lower than 40% of predicted had complications.
FEV1ppo of 700 mL or More
The mean FEV1ppo for the 11 patients who had perfusion scanning was 700 mL. The mean for patients experiencing complications was 716 mL, yet the FEV1ppo was 673 mL for those who did well. Two complications occurred in the 3 patients with an FEV1ppo of 700 mL or higher. Five of the 8 patients with an FEV1ppo lower than 700 mL had complications. One patient without complications declined the perfusion scan and the stair climb.
Stair Climb (
3 Flights for Lobectomy or 5 Flights for Pneumonectomy)
One patient climbed only two flights of stairs. Ten patients climbed more than three flights of stairs (63 steps or 11.0-m change in elevation), 9 climbed five flights (105 steps, 18.4 m), and 6 climbed six flights (126 steps, 22.1 m) at which point the test was terminated. Patients achieved a mean maximum heart rate of 156 beats/min, which was 83% of the predicted maximum. Patient 2 failed the stair-climbing threshold and experienced postoperative respiratory insufficiency and had a persistent air leak. Ten patients passed the stair climb, and 6 of them had complications.
VO2max of 10 mL•kg-1•min-1 or More
All 12 patients achieved at least 10 mL•kg-1•min-1. The mean work capacity (VO2max/predicted VO2max) was 53.6% of predicted. Patients exercised to a mean heart rate of 121 beats/min, which was 77.3% of predicted maximum. The mean breathing reserve (minute ventilation at maximum exercise/maximal voluntary ventilation) was 19.8%. This combination of a low total work capacity with near maximum ventilatory capacity and cardiac capacity indicates that all 12 patients had a combined ventilatory and circulatory limitation to exercise. The mean VO2max for the entire group was 13.9 mL•kg-1•min-1. The mean for patients experiencing complications was 14.1 mL•kg-1•min-1 versus 13.7 mL•kg-1•min-1 for those who did well.
We tracked additional markers that have been used to predict complications from lung resection procedures. There were no significant differences for the following variables between patients who had complications and those who did not: ECOG score, cardiopulmonary risk index, carbon dioxide tension, hematocrit, the 12-minute walk for distance, carbon monoxide diffusing capacity of the lung (DLCO), and maximum voluntary ventilation (see Table 1
). When patients were interviewed 30 days after operation, there were no significant changes in either the ECOG scores (preoperative score, 1.2; postoperative score, 1.9) or the dyspnea scores (preoperative score, 2.4; postoperative score, 2.1). All patients in this study are currently alive except for the 1 who died perioperatively.
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Spirometry with lung volumes, arterial blood gases, DLCO, and maximum voluntary ventilation are tests of static lung function that have been evaluated as outcome predictors for pneumonectomy. The most commonly used index to determine operability is FEV1, or more accurately, FEV1ppo. A patient is considered able to tolerate lung resection as long as the FEV1ppo is greater than 800 mL. This 800-mL level was established in a 1975 landmark study by Olsen and associates [9], who reported on 56 patients deemed to be at high risk for lung resection. They chose this level on the basis of their observation that patients with an FEV1 lower than 800 mL tended to have carbon dioxide retention and a reduced level of day-to-day function. To our knowledge, this threshold has not been systematically challenged since then.
Static pulmonary function tests, even using confidence intervals, can be biased against patients of short stature. The FEV1 % predicted has been shown to be more accurate than the FEV1 [10]. Use of the ventilation/perfusion scan to determine FEV1ppo is thought to give a more accurate prediction of residual function, but the accuracy of this test has been questioned [11]. Although there have been trials examining improved methods to evaluate high-risk patients, investigators [3, 7, 11–18] have tended to base their decision to operate on standard spirometric criteria and to then analyze retrospectively whether the new test would be a better predictor of postoperative complications. Our results also confirm that static pulmonary function studies do not have good discriminating value. If we had used the often quoted FEV1 of 2 L or greater as an entry criteria, we would not have operated on any patient in this series. If we had based our decision to operate solely on an FEV1 that was greater than 40% of the predicted value, we would have performed resection on only 7 of 12 patients. Although the FEV1 % predicted reduces some of the bias inherit in the raw FEV1, it still would have eliminated 5 of 12 patients from operative consideration.
We have reported our data for FEV1ppo using the worst-case scenario (ie, pneumonectomy). Using this method, if we had based our decision to operate on the FEV1ppo of higher than 800 mL alone, only 3 of 11 patients would have been qualified for operation. If we calculate the mean FEV1ppo from our data, with lobectomy projected as the minimum resection, it is 1.17 L (39.7% of predicted) for those who did well and 0.98 L (37.1% of predicted) for those who had complications. Using the 800-mL threshold, 10 of 12 patients would have qualified for operation with seven complications. When analyzed against morbidity, the FEV1, FEV1ppo, and the FEV1 % predicted did not clearly identify patients who would experience complications. Even when using more liberal thresholds for these tests (see Table 3), we found the same results.
Exercise testing has been advocated in the preoperative evaluation of patients for lung resection to assess cardiopulmonary reserve and demand after operation. The two factors most extensively studied are dyspnea indices related to work performed and maximal oxygen uptake, VO2max. The stair climb is an easily performed, noninvasive test that has only recently been evaluated systematically [3, 4]. The authors noted that the ability to climb three flights of stairs was associated with reduced postoperative morbidity. Other tests in this category include the 12-minute walk test and the DLCO. Markos and co-workers [18] found that a reduced DLCO, a predicted postoperative DLCO that was less than 40% of predicted, a FEV1ppo equal to or less than 35%, and oxygen desaturation with exercise on the 12-minute walk for distance were predictive of postoperative complications. In their study, VO2max did not correlate with postoperative complications.
The stair climb has been compared with the cycle ergometer and found to generate a similar or higher VO2max in patients with moderate to severe chronic obstructive pulmonary disease [19]. In addition to stating the number of flights of stairs achieved, we have reported our data as altitude changed (in meters). There has been confusion as to the work performed in previous stair-climbing studies because of variable definitions of a flight of stairs (eg, height of each step, stairs per flight, number of landings). We hope that this altitude methodology provides a format to consistently report stair-climb performance. Compared with the cycle ergometer protocol that we used, the stair climb is a shorter and more strenuous exercise to perform. Its strength lies in its simplicity and brevity. The usual test takes less than 3 minutes to perform, is inexpensive, and requires no special equipment or expertise. Patients tended to give a more maximal effort on stair climbing than cycle ergometry, especially when they could see the next landing. The average heart rate on this test was greater than 80% of its predicted value and 35 beats per minute higher than for the CPX, findings indicating a better effort.
In a recent report by Pollock and colleagues [19], patients with chronic obstructive pulmonary disease were able to generate a VO2max by stair climbing that was equivalent to that measured by cycle ergometry. In that study, a climb of one flight of stairs generated a VO2max of 7.9 mL•kg-1•min-1, whereas climbing 4.6 flights (83 steps) generated a VO2max of 20 mL• kg-1•min-1 or higher. Extrapolating from their data, we found that all of our patients produced a much higher VO2max by stair climbing than that measured by cycle ergometry using our low-wattage protocol. Because all but 1 patient in our cohort passed this test for an eventual operation, it is difficult to examine its ability to discriminate between those who had complications and those who did not. The data do show that the ability to climb three flights of steps is a reasonable performance threshold for lung resection.
The use of formal cardiopulmonary stress testing in the evaluation for lung resection has been more extensively studied than stair climbing and walking, but the heterogeneity of the patient populations has produced mixed results. In 1972, the series of Reichel [17] on the use of a standard exercise tolerance test in assessing patients for pneumonectomy was published. Reichel found that patients who could not complete the exercise tolerance test had a higher cardiopulmonary complication rate. Eugene and coauthors [13] reported a higher complication rate among patients undergoing pulmonary resection if the VO2max was less than 1 L/min. Three of the 4 patients who underwent thoracotomy with a VO2max of lower than 1 L/min died, whereas there were no deaths among the 15 patients with a VO2max of greater than 1 L/min. In 1984, Smith and associates [14] found that exercise evaluation more accurately identified patients with postoperative complications than the FEV1 or DLCO. All 6 of their patients with a VO2max less than 15 mL•kg-1• min-1 had postoperative complications. Four of 6 with a VO2max between 15 and 20 mL•kg-1•min-1 experienced problems, but only 1 patient of 10 with a VO2max greater than 20 mL•kg-1•min-1 had a postoperative complication.
In a larger study (50 consecutive patients undergoing lung resection), Bechard and Wetstein [15] found a better correlation with postoperative morbidity and mortality using VO2max than standard spirometric data. In particular, they found a prohibitive complication rate for patients with a VO2max of less than 10 mL•kg-1•min-1, an increase in complications but no deaths for those with a VO2max between 10 and 20 mL•kg-1•min-1, and no complications for patients with a VO2max greater than 20 mL•kg-1•min-1. Further studies by Olsen and colleagues [12] confirmed that submaximal exercise testing is a better predictor of postoperative complications than calculations based on quantitative lung scanning. In that study, patients who tolerated operation had a VO2max of 11.3 ± 2.1 mL•kg-1•min-1, whereas those who did not had a VO2max of 7.8 ± 1.5 mL•kg-1•min-1. The authors also found significant correlations for low cardiac index and inadequate oxygen delivery during exercise.
In none of these studies [12–17, 19] was the decision to operate based solely on the exercise performance. The decision was usually based on the standard spirometric criteria and quantitative lung scan. The authors also tended to accrue patients sequentially, and the studies often included complications that could not possibly be anticipated by any form of pulmonary testing [16]. It is difficult to ascertain from these studies the degree to which the individual's cardiac and pulmonary performance was limited. One study [10] did base decisions on physiologic tolerance for lung resection on the VO2max. Thirty-seven patients who had an FEV1 that was 40% of the predicted value or lower, an FEV1ppo of 33% or less after lobectomy, or an arterial carbon dioxide tension of 45 mm Hg or greater were evaluated with formal exercise testing. If they had a VO2max of 15 mL•kg-1•min-1 or higher, they were referred for thoracotomy. Eight patients met inclusion criteria. There were no deaths and only two complications.
Our patients had limited cardiopulmonary function. The mean VO2max was 13.9 mL•kg-1•min-1, and only 4 patients had a VO2max greater than 15 mL•kg-1• min-1. If we analyze our data using 15 mL•kg-1•min-1 as the threshold, 4 patients would have passed with three complications, and 8 patients would have failed with four complications. None of our patients achieved 20 mL • kg-1 • min-1, but all were able to achieve at least 10 mL • kg-1 • min-1. We are unable to comment on the ability of the VO2max to distinguish between those who experienced complications and those who did not, except that patients with a VO2max greater than 10 mL•kg-1• min-1 have a reasonable performance threshold to tolerate lung resection.
We tried to pair each test with a less sophisticated test (ie, CPX versus stair climb versus FEV1) to address whether one test could outperform the other in an efficient, cost-effective manner. When compared against one another, no test was superior at distinguishing between those patients who did experience complications and those who did not. However, the VO2max and the stair climb did not eliminate patients from operative consideration unnecessarily. The FEV1ppo did not qualify for operation 1 patient who did not meet at least one other threshold criterion. The FEV1 and the FEV1 % predicted also tended to disqualify too many patients who had a successful resection. For this reason, the VO2max and the stair climb were superior to the tests of static pulmonary function.
In this study, we have prospectively examined the role of formal cardiopulmonary stress testing in the preoperative evaluation of patients at high risk for lung resection. We have simultaneously challenged the currently accepted limits for safe resection by establishing multiple entry points. The threshold levels we chose were lower than those quoted in the literature for FEV1, FEV1ppo, and VO2max. We used similar thresholds for the stair climb and the FEV1 % predicted [3, 10]. Each of the entry points (ie, FEV1, FEV1ppo, FEV1 % predicted, stair climb, and VO2max) if used alone would not have been adequate to separate patients who had complications from those who did not.
Because our original intent was to prospectively enroll patients with ``borderline'' pulmonary function, we did not enter all patients who had operation during the study period. Between March 1994 and March 1995, we enrolled only 10 of the 42 patients who had lung resection at the Memphis Department of Veterans Affairs Medical Center. Those patients with ``acceptable'' static pulmonary function (ie, an FEV1 >2 L) and nonlimited cardiac conditions were referred directly to the thoracic surgeons. As is apparent from our data, we enrolled a homogeneous population with both ventilatory and cardiac limitations. This schema for preoperative testing is most useful for this subgroup of patients and is not necessary for most patients who will have lung resection.
Ever since a concentrated effort to predict perioperative complications began, each test used has had the same limitation. For any test to prevent the most feared complication (ie, operative death), many patients who could have had successful resections have to be excluded. These studies have also been limited because their complication rates have not been prohibitively high compared with standard surgical morbidity and mortality figures [1, 20]. The operative mortality from curative lung resection ranges from 7.4% to 11.6% [1]. A current study [20] of lung cancer resection reported a mortality of only 3.8% but a morbidity of 27%. This seems to indicate that the lower limit for safe resection has not been reached. Our study suffers from the same limitations even though we chose criteria for lung resection that are lower than previously proposed ``standards of care.'' Although we may have identified a lower performance threshold for which lung resection can be applied, we have not presented that level of cardiopulmonary function that prohibits lung resection operations.
We recommend routine exercise testing for the evaluation of patients at high risk for lung resection. The information obtained by these tests gives the clinician additional useful data on which to base a clinical decision. Both the stair climb and the CPX have advantages. They can be used to test motivation and functional reserve. The stair climb is quick, simple, and inexpensive. The CPX provides detailed information on both the respiratory and circulatory systems and is performed under much more controlled circumstances than the stair climb. If exercise testing is used, microaggregate lung scanning adds little to the evaluation. We would not have qualified any patient for operation on the basis of this test who would not have been qualified by some other method. We believe that the current thresholds for deciding if a patient is an operative candidate for lung resection are too conservative. Patients can be safely operated on if they have an FEV1 higher than 1.6 L or 40% of its predicted value, a VO2max greater than 10 mL•kg-1•min-1, or a stair climb of more than three flights of stairs (11 m). We recommend cardiopulmonary exercise testing, stair climbing, or both for patients with an FEV1 lower than 1.6 L.
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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A. Carretta, P. Zannini, A. Puglisi, G. Chiesa, A. Vanzulli, A. Bianchi, A. Fumagalli, and S. Bianco Improvement of pulmonary function after lobectomy for non-small cell lung cancer in emphysematous patients Eur. J. Cardiothorac. Surg., May 1, 1999; 15(5): 602 - 607. [Abstract] [Full Text] [PDF]
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D. J. Wilson Preoperative Pulmonary Rehabilitation Seminars in Cardiothoracic and Vascular Anesthesia, September 1, 1997; 1(3): 208 - 214. [Abstract] [PDF]
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L. Wetstein and J. R. Mault Physiologic Evaluation of the Lung Resection Candidate Ann. Thorac. Surg., September 1, 1996; 62(3): 923 - 923. [Full Text]
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