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* From the Section of Respiratory Medicine (Dr. J-S Wang), E-Da Hospital, Kaohsiung, Taiwan; Division of Respiratory Medicine (Dr. Abboud), University of British Columbia, Vancouver, BC, Canada; and the Division of Emergency Medicine (Dr. L-M Wang), Taipei Veterans General Hospital, Taipei, Taiwan.
Correspondence to: Jeng-Shing Wang, MD, MSc, 166 Min-Shiang St, Kaohsiung, Taiwan 800; e-mail: wangjs6{at}hotmail.com
Abstract
Objective: To evaluate the effect of lung resection on lung function and exercise capacity values, including diffusion capacity of the lung for carbon monoxide (DLCO), during exercise, and to determine whether postoperative lung function, including exercise capacity and DLCO during exercise, could be predicted from preoperative lung function and the number of functional segments resected.
Design: Prospective study.
Setting: Clinical pulmonary function laboratory in a university teaching hospital.
Patients: Twenty-eight patients undergoing lung resection at Vancouver General Hospital from October 1998 to May 1999, were studied preoperatively and 1-year postoperatively.
Interventions: We determined FEV1 and FVC, and maximal oxygen uptake (
O2max) and maximal workload (Wmax) achieved during incremental exercise testing. We used the three-equation modification of the single-breath DLCO technique to determine DLCO at rest (RDLCO) and during steady-state exercise at 70% of Wmax, and the increase in DLCO from rest to exercise (ie, the mean increase in DLCO percent predicted at 70% of Wmax from resting DLCO percent predicted [(70%-R)DLCO]). We calculated the predicted postoperative (PPO) values for all the above parameters using the preoperative test data and the extent of functioning bronchopulmonary segments resected, and compared the results with the actual 1-year postoperative results.
Results: Following lung resection, there was a significant reduction in FEV1, FVC, and DLCO with decreases of 12%, 13%, and 22% predicted, respectively. There were also significant decreases in O2max per kilogram of 2.1 mL/min/kg (8% of predicted O2max) and in Wmax of 12 W (7% of predicted Wmax). However, (70%-R)DLCO did not significantly decrease after lobectomy but decreased after pneumonectomy. The calculated PPO values significantly underestimated postoperative values after pneumonectomy but were acceptable for lobectomy.
Conclusions: Exercise tests may be better indicators of functional capacity after lung resection than measurements of FEV1 and FVC or RDLCO. PPO results calculated by estimating the functional contribution of the resected segments, are comparable with those obtained using ventilation-perfusion lung scanning and significantly underestimate postoperative lung function after pneumonectomy, but are acceptable for lobectomy.
Key Words: exercise capacity • exercise diffusing capacity of the lung for carbon monoxide • lung function • lung resection • predicted postoperative value
Despite recent advances in chemotherapy and radiotherapy, surgery offers the best chance of a cure in patients with nonmetastatic lung cancer. It has been recognized that such surgery may result in the impairment of lung function,12 which can reduce exercise capacity34 and affect quality of life. Several studies56 have predicted the change in exercise capacity after lung resection using perfusion lung scanning. However, there are no published studies predicting postoperative exercise capacity after lung resection by estimating the contribution of the resected lung tissue to lung function without the use of perfusion lung scanning. Previous studies have shown that predicted postoperative (PPO) values for FEV1 and single-breath diffusing capacity of the lung for carbon monoxide (DLCO) can be predicted from the preoperative test values, and the number of resected segments and their estimated contribution to preoperative lung function, based on radiologic and bronchoscopic criteria using simple equations.78
In a previous study,9 we have shown that preoperative DLCO during exercise is a good predictor of postoperative complications. We also showed that PPO values, which were calculated from the estimated contribution of the resected lung to lung function, were a good predictor of postoperative complications.10 In this study, we sought to determine the effect of lung resection on postoperative exercise DLCO in a subgroup of these patients, who were studied about 1 year postoperatively, and to evaluate whether postoperative function, including exercise capacity and exercise DLCO, could be predicted from the preoperative values by taking into account the estimated contribution of the resected lung to these parameters. As in our previous study,9 we used the three-equation DLCO technique (3EQ-DLCO) of Graham et al1112 to determine DLCO at rest (RDLCO) and during exercise following recovery from lung resection. This is the first study to evaluate the effect of lung resection on lung function and exercise capacity values, including DLCO during exercise, and to determine whether postoperative lung function, including exercise capacity and DLCO during exercise, could be predicted from the preoperative lung function and the number of functional segments resected.
Materials and Methods
In our previous study,9 a total of 57 patients with non-small cell lung cancer undergoing thoracotomy for lung resection at Vancouver General Hospital from October 1998 to May 1999 were evaluated preoperatively. The study was approved by the University of British Columbia Ethics Review Board, and all patients signed an informed consent form prior to participation.
Details of the lung function tests and exercise studies have been described previously.9 A computerized dry rolling seal spirometer was used for spirometry, according to the American Thoracic Society criteria.13 The 3EQ-DLCO system used in this study is identical to the one described in detail in our previous study9 and is similar to the original systems,1112 with slight modifications.
For determination of the resting 3EQ-DLCO, patients rested in a seated position for 15 min to minimize the effect of any prior activity on DLCO. To familiarize the patients with the breathing template, several practice runs of the breathing maneuver were performed with the patients breathing room air from the bag-in-box system; flow rates were adjusted according to the lung function of the patients. Then, the 3EQ-DLCO measurements were made at least 5 min apart; the mean of three measurements agreeing to within 10% of each other was taken as the resting 3EQ-DLCO (ie, RDLCO).
Exercise testing was performed using a cycle ergometer (model 800; SensorMedics; Yorba Linda, CA) and computerized breath-by-breath exercise testing equipment (max 229; SensorMedics), as described previously in more detail.9 Heart rate (HR), ECG, and oxygen saturation by pulse oximetry were continuously monitored. Minute ventilation, tidal volume, respiratory rate, oxygen uptake (O2), CO2 production, and respiratory exchange ratio (RER) were shown on the computer monitor during exercise. The exercise equipment was calibrated, and the calibration was verified daily. Maximal exercise capacity was determined using a step incremental protocol14 starting at a workload of 15 W, which was increased every minute by 15 W. Patients’ subjective assessment of perceived effort during exercise and at peak exercise was assessed by the Borg scale15; the subjects also indicated whether the reason for stopping the test was due to leg discomfort, dyspnea, or both. The maximal O2 (O2max) attained was taken to be the highest O2 at the maximal workload (Wmax) just before the end of exercise. We used the equations of Jones14 to determine the predicted O2max (in liters per minute) and expressed as milliliters per kilogram of body weight. The maximal predicted HR was calculated by subtracting two thirds of the patient’s age from 210.14 The percentage of breathing reserve (BR) was determined as follows: maximal voluntary ventilation (MVV) – volume of expired gas at maximal exercise (VEmax) x the percentage of MVV. The MVV was considered to be equal to FEV1 (in liters x 35). The percentage of HR reserve (HRR) is determined as follows: predicted maximal HR – HR at maximal exercise = the percent predicted maximal HR.
The 3EQ-DLCO determinations during steady-state exercise were made with patients seated on the cycle ergometer while ECG, BP, and oxygen saturation were monitored. After cycling with no workload for 1 min to warm up, the workload was increased to 35% of the previously determined Wmax and was maintained for 3 min, and then the 3EQ-DLCO was determined at that Wmax. The workload was then increased to 70% of the patient’s Wmax for another 3 min. The 3EQ-DLCO at steady-state exercise was then determined, and the measurement was repeated after another 1 min of exercise. It had been previously determined that this was an adequate length of time for the lung washout of carbon monoxide and CH4 from the preceding 3EQ-DLCO test, because of the increased ventilation during exercise.
The PPO values for FEV1, FVC, RDLCO, O2max per kilogram, Wmax, and exercise DLCO were calculated using the preoperative test data and the number of resected bronchopulmonary segments, according to the following equation,7 which takes into account lung segments that were nonfunctional due to endobronchial obstruction, atelectasis, or consolidation:
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One year after lung resection, patients were contacted and invited to return for follow-up lung function and exercise testing, as was done preoperatively; a total of 28 patients who had undergone lung resection participated in this follow-up study. The actual postoperative FEV1, FVC, RDLCO, exercise capacity, and exercise DLCO values determined 1 year after surgery were compared with the preoperative data and with the calculated PPO values.
Analysis of the data was done using a spreadsheet program (Excel 97; Microsoft; Redmond, WA) and a statistical software package (SPSS; SPSS; Chicago, IL) using a personal computer. Comparisons for continuous variables before and after surgery were made using a two-tailed paired Student t test, while the 
2 test was used for categoric variables. A p value of < 0.05 was considered to be statistically significant. The PPO values and the actual postoperative values were also compared by plotting them against the line of identity. To check the level of agreement,16 the differences between PPO and actual postoperative values were plotted against the actual postoperative values, and the mean and SD of the differences were determined.
Results
The 28 patients who had undergone follow-up studies 1 year after undergoing lung resection had a mean (± SD) age of 64.6 ± 10 years; 17 patients (61%) were men, and 11 patients (39%) were women. The mean height was 168 ± 10 cm, and the mean weight was 71 ± 14 kg. The surgical interventions that had been performed were pneumonectomy (5 patients), lobectomy (19 patients), and segmental resection (4 patients). Preoperative data on these 28 patients are shown in Table 1
and are similar to those of the remaining 29 patients who did not undergo follow-up (data not shown). The mean FEV1 was 86 ± 18% predicted; some patients had mild or moderate obstructive ventilatory impairment. The Mean FVC was 92 ± 13% predicted, but some patients had mild restrictive ventilatory impairment. Maximal exercise capacity (in terms of O2max per kilogram) was reduced to < 75% predicted in about two thirds of patients, with a mean O2max of 18.5 ± 4.0 mL/min/kg, which is equivalent to 77.5 ± 13.4% predicted. The mean Wmax was 111 ± 31 W (or 87.5 ± 29.2% predicted). To adjust for differences in sex, age, and height in different patients, the 3EQ-DLCO results at rest and after exercise were expressed as the percent predicted resting single-breath DLCO. The mean RDLCO was 22.8 ± 8.4 mL/min/mm Hg (or 93 ± 33% predicted). The mean DLCO at 70% of Wmax (70%DLCO) was 28.9 ± 10.8 mL/min/mm Hg (119 ± 43% predicted RDLCO). The mean increase in 70%DLCO from RDLCO ([70%-R]DLCO) was 29.2 ± 18.0% predicted, with a significant interpatient variability.
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O2max of 2.2 mL/min/kg (equivalent to a decrease of 10% of the predicted O2max) and by a mean decrease in Wmax of 12 W (equivalent to a decrease of 10% of the predicted Wmax). The postoperative exercise 70%DLCO was significantly reduced (p < 0.001). However, because the RDLCO was also reduced by almost the same extent, the postoperative increase in DLCO during exercise was not significantly reduced compared with the preoperative results, with a mean decrease of only 2% of the predicted RDLCO (p = 0.27).
Figure 1
compares postoperative and preoperative results in FEV1, FVC, and DLCO (all expressed as percent predicted) for each type of lung resection. The postoperative FEV1 was significantly decreased after pneumonectomy (p < 0.001), lobectomy (p < 0.01), and segmentectomy (p < 0.01) by 23%, 9%, and 10% predicted, respectively, from the preoperative values. The postoperative FVC was significantly decreased (p < 0.001) after both pneumonectomy and lobectomy by 28% and 13% predicted, respectively, but there was no significant change after segmentectomy (mean decrease, 0.8% predicted). The postoperative RDLCO was significantly decreased after pneumonectomy (p < 0.001), lobectomy (p < 0.001), and segmentectomy (p < 0.01) by 33%, 22%, and 9% predicted, respectively, from the preoperative values. Figure 1 also compares postoperative with preoperative exercise parameters according to the type of resection. The postoperative O2max was decreased after both pneumonectomy (by 3.4 mL/min/kg or a 20% decrease from preoperative values; p < 0.025) and lobectomy (by 2.2 mL/min/kg or a 12% decrease from preoperative values; p < 0.005), but not after segmentectomy (mean decrease, 0.2 mL/min/kg). The postoperative maximal exercise capacity in watts (Wmax) was significantly decreased in patients who had undergone pneumonectomy and lobectomy (31 and 8 W, respectively, which were equivalent to mean decreases of 28% and 7% predicted from the preoperative values). The slight decrease (mean decrease, 10 W) in the four patients who underwent segmentectomy did not achieve statistical significance (p = 0.088), possibly due to the small number of cases. However, the increase in DLCO from rest to exercise was decreased postoperatively only in pneumonectomy patients by a mean 8% of predicted RDLCO (p = 0.05), which is equivalent to a mean decrease of 44% from preoperative values.
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O2max, and Wmax (p < 0.001 for all), but were not significantly different for RDLCO (p = 0.39), DLCO with exercise 70%DLCO (p = 0.08), and the increase in (70%-R)DLCO (p = 0.07). Figure 2
compares individual calculated PPO results for FEV1, FVC, and RDLCO with the corresponding actual postoperative values plotted on the x axes. There is scatter around the line of identity; the PPO values were lower than postoperative values, especially for patients who had undergone pneumonectomy, with only a minimal difference for the four patients who had undergone segmentectomy. Figure 2 also shows the differences between PPO and actual postoperative results for the same tests plotted against the actual postoperative results. It also indicates the mean difference and the limits of agreement for all cases (± 2 SDs from the mean difference) between calculated PPO results and actual postoperative results. Similarly, Figure 3
compares PPO values with actual postoperative results for O2max, Wmax, and (70%-R)DLCO; it also shows the differences between PPO and postoperative values. The calculated PPO values for pneumonectomy patients significantly underestimated the postoperative results, but the lobectomy PPO values generally only slightly underestimated postoperative results. A comparison of postoperative and PPO results in pneumonectomy and lobectomy patients are shown separately in Table 2
. This shows that whereas PPO values grossly underestimate postoperative lung function in patients who had undergone pneumonectomy, the underestimation in lobectomy cases is on the order of 10 to 15% for FEV1, FVC, and O2max, and is negligible for RDLCO and DLCO during exercise, suggesting that the calculation of PPO values by the equation given in the "Materials and Methods" section would be acceptable for lobectomy patients, but not for pneumonectomy patients.
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The main findings in this study were as follows: (1) the increase in DLCO with exercise was preserved after lobectomy; and (2) the calculation of PPO values for lung function and exercise test results from preoperative test data and the extent of functioning of the resected bronchopulmonary segments yielded acceptable results after lobectomy. Although there was a slight decrease in maximal exercise capacity after lobectomy, there was preservation of the (70%-R)DLCO after lobectomy, indicating that the capacity of the pulmonary capillary bed to expand with exercise was preserved.
As expected, there was a greater and more significant decrease in lung function and exercise capacity after pneumonectomy, compared with after lobectomy. The decreases from preoperative values for FVC, FEV1, and RDLCO were 30%, 28%, and 39%, respectively, after pneumonectomy, and 13%, 8%, and 20%, respectively, after lobectomy. After pneumonectomy, the indexes of maximal exercise capacity, O2max and Wmax, were reduced by 28% and 20%, respectively, of the preoperative values, while after lobectomy they were reduced by 12% and 8%, respectively, of the preoperative values. Our findings are similar to those of Larsen et al4, who reported a 6-month postoperative decrease in FEV1 of 23% after pneumonectomy and 8% after lobectomy, while exercise capacity decreased by 16% after pneumonectomy and 13% after lobectomy. Our results are also similar to those of Bolliger et al3 who reported decreases in FVC of 36% after pneumonectomy and 6% after lobectomy, while the decreases in O2max were 20% and 1%, respectively. In this study, the mean increase in DLCO with exercise after pneumonectomy was only 51% of the preoperative value, but was 96% of the preoperative value after lobectomy. The findings for exercise DLCO are consistent with a reduced capacity of the pulmonary capillary bed to increase with exercise after pneumonectomy and with a preserved capacity after lobectomy. In our previous study,9 the increase in DLCO with exercise was the best predictor of postoperative complications after lung resection. However, an analysis of our present data in the 19 lobectomy patients showed no significant correlation between the preoperative increase in DLCO (expressed as a ratio with the increase in O2 with exercise) and indexes of postoperative exercise capacity or lung function.
Our study indicates that the evaluation of the contribution of the resected lung to function from the total number of functional lung segments resected using a simple equation, the modified formula of Nakahara et al,7 in conjunction with preoperative lung function and exercise testing, yields a good estimate of postoperative lung function and exercise capacity after lobectomy but significantly underestimates the results after pneumonectomy. Only a few of our patients underwent quantitative radionuclide lung scans. However, we have compared our calculated PPO values for lung function and exercise variables relative to the actual postoperative values obtained in our study with those from the studies of Bolliger et al,5 and Larsen et al,6 both of whom used radionuclide scanning to calculate PPO results. The correlation between PPO and postoperative results, the underestimation of postoperative results by PPO values, and the scatter of data around the line of identity are similar in these two studies and ours. These comparisons indicate that the modified formula of Nakahara et al7 can predict the postoperative lung function and exercise capacity values as well as the calculations using ventilation-perfusion lung scanning, although more definitive conclusions would require a comparison of both methods in a larger number of patients in a prospective study.
The postoperative values for FEV1, FVC, and DLCO were somewhat more decreased (by 12%, 13%, and 22%, respectively) than those for O2max (by 2.1 mL/min/kg or 8%) and Wmax (decreased by 12 W or 7%), as shown in Table 1. However, the DLCO increase during exercise was not significantly decreased postoperatively compared with preoperatively, although the mean values were slightly lower. These findings suggest that lung function tests performed at rest may overestimate the functional loss compared with those performed during exercise, as indicated previously by Bolliger et al3 and Larsen et al4 The increase in DLCO with exercise may also be a useful indicator of exercise functional capacity after lung resection.
Postoperative lung function was significantly decreased after lobectomy by a mean of 9% for FEV1, 13% for FVC, and 22% for DLCO, and after pneumonectomy by 23% for FEV1, 28% for FVC, and 33% for DLCO, as indicated in Figure 1. The mean postoperative exercise capacity as determined by Wmax (Fig 1) was decreased after lobectomy by 7 W (or 6%), while O2max decreased by 2.2 mL/min/kg (or 7%). After pneumonectomy, Wmax decreased by 31 W (or 20%), while O2max decreased by 3.4 mL/min/kg (or 20%), as indicated in Figure 1. However, the DLCO increase during exercise was decreased only after pneumonectomy by 8% (Fig 1). The increase in DLCO during exercise was the most conservative testing parameter in estimating functional loss, but additional studies will be required to determine whether this will be a better parameter than the measurement of maximal exercise capacity in evaluating functional capacity after lung resection.
Objectively, the mean RER at peak exercise was > 1.10; an RER of > 1.05 is considered to be evidence of enough motivation for the exercise test.17 There were significant decreases in the breathing reserve after pneumonectomy and lobectomy (Table 3). There was also a significant decrease in oxygen pulse after pneumonectomy, but not after lobectomy (Table 3), suggesting a decrease in cardiac stroke volume during exercise after pneumonectomy. These findings suggest that ventilatory capacity18 after both lobectomy and pneumonectomy may be limiting exercise, while circulatory capacity1920 may be limiting exercise capacity after pneumonectomy. Circulatory limitation could be a more important limiting factor for exercise capacity,1920 and may be due to the impaired filling of the left ventricle caused by the limitation of the increase in pulmonary blood flow with exercise. Oxygen pulse and the DLCO increase with exercise 1 year after lobectomy were similar to the preoperative values but were lower after pneumonectomy. The recovery in exercise capacity after lobectomy is most likely due to the expansion of the remaining lung on the side of the lung that was operated on, compensating for the resected lung tissue lost during lobectomy.
Prior to lung resection, most patients felt that their exercise capacity was limited by leg fatigue (Table 4). After segmental or lobar resection, leg fatigue was still the main factor limiting exercise after the operation, but the pneumonectomy patients were mostly limited by dyspnea postoperatively (Table 4). Leg fatigue before the operation indicates deconditioning, as supported by a large breathing reserve and HRR. Dyspnea and exercise limitation after pneumonectomy could be due to the decreased postoperative ventilatory and circulatory capacities, as indicated by the decreased BR and oxygen pulse.
The degree of impairment in lung function after pulmonary resection may be dependent on the timing of postoperative testing. Larsen et al6 showed that there is improvement in lung function 6 months after undergoing lobectomy compared with 3 months after undergoing pneumonectomy. Veneskoski et al.21 showed that 6 months after surgery there was no significant change in the impairment in lung function, and we selected 1 year as the time for our evaluation. Our results were obtained in a relatively small group of patients and may need confirmation in a larger number of patients.
Acknowledgements
The authors thank Drs. Kenneth Evans and Richard Finley for their cooperation in recruiting their patients for the study; Drs. Brian Graham, Jim Potts, and Sundeep Rai for their advice and help in setting up the 3EQ-DLCO technique; Dr. Sverre Vedal for supervising some of the exercise tests and for helpful advice; Dr. Harry Joe for his help with the statistical analysis and graphic presentation of data; and the Lung Function Staff for their help in recruiting patients.
Footnotes
Abbreviations: BR = breathing reserve; DLCO = diffusing capacity of the lung for carbon monoxide; HR = heart rate; HRR = heart rate reserve; MVV = maximal voluntary ventilation; PPO = predicted postoperative; RDLCO = DLCO at rest; RER = respiratory exchange ratio; 70%DLCO = mean diffusing capacity of the lung for carbon monoxide at 70% of maximal workload; (70%-R)DLCO = mean increase in diffusing capacity of the lung for carbon monoxide at 70% of maximal workload from resting diffusing capacity of the lung for carbon monoxide; 3EQ-DLCO = three-equation DLCO technique; VEmax = volume of expired gas at maximal exercise; O2 = oxygen uptake; O2max = maximal oxygen uptake; Wmax = maximal workload
Dr. Wang was supported in part by a Fellowship from the British Columbia Lung Association and by funds from the Vancouver General Hospital Foundation. The analyzers and computer for the 3EQ-DLCO were obtained through a grant from the British Columbia Medical Services Foundation, while the SensorMedics exercise equipment was purchased with a major equipment grant from the Tuberculosis and Chest Disabled Veterans Association.
Received for publication June 3, 2004. Accepted for publication October 26, 2005.
References
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= pneumonectomy; 
= lobectomy; 
= segmentectomy.
