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Ann Thorac Surg 2001;72:1705-1710
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Stair-climbing test to evaluate maximum aerobic capacity early after lung resection

^a Department of Thoracic Surgery, University of Ancona, Ancona, Italy

Accepted for publication July 12, 2001.

* Address reprint requests to Dr Brunelli, Department of Thoracic Surgery, University of Ancona, Via S. Margherita 23, Ancona 60129, Italy
e-mail: alexit_2000{at}yahoo.com

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. The aim of this study was to investigate the extent of reduction in maximum oxygen consumption in the early postoperative period after lung resection for lung carcinoma.

Methods. A total of 115 patients who underwent lung resection (95 lobectomies, 20 pneumonectomies) performed a maximal stair-climbing test the day before operation and the day of discharge from the hospital (8 ± 3.3 days after the operation).

Results. The postoperative test showed a 15% reduction in maximum oxygen consumption (O₂max) with respect to the preoperative test (Student’s t test, p < 0.0001). This reduction was greater after pneumonectomy (21.4%) than after lobectomy (14%) (Student’s t test, p < 0.05). A multiple regression analysis showed that the only significant independent predictors of both preoperative and postoperative O₂max were the age of the patient and the level of arterial oxygen content.

Conclusions. The early postoperative reduction in O₂max was greater after pneumonectomy than after lobectomy and the exercise performance was significantly influenced by the level of arterial oxygen content both before and early after the operation.

	Introduction

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Maximal cardiopulmonary exercise tests are increasingly used to assess the aerobic capacity of a candidate for lung resection. Patients with marginal aerobic reserve have greater difficulty dealing with the multiple pathophysiologic changes that accompany major surgical procedures [1]. In the normal postoperative period a rise in oxygen consumption of a variable extent is expected [2]. The onset of a complication may further increase the oxygen requirements beyond that which the patient can provide, inducing an oxygen debt. If this debt remains critically high over specified periods of time, then a multiorgan failure may ensue [3].

The aim of the present study was to investigate the influence of lung resection on the reduction of the maximum aerobic capacity in the early postoperative period, by using a technically simple, low-cost, maximal exercise test such as the stair-climbing test.

	Material and methods

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One hundred twenty candidates for lung resection for non–small cell lung carcinoma from December 1999 through November 2000 were enrolled prospectively in our study after giving informed consent. Five patients were excluded from the analysis (1 died postoperatively; 4 refused to perform the postoperative exercise test). The remaining 115 patients (88 men and 27 women) formed the database of the study. Ninety-five lobectomies and 20 pneumonectomies were performed through a muscle-sparing lateral thoracotomy. Preoperative functional evaluation included pulmonary function studies and a maximal stair-climbing test.

Spirometry was performed according to American Thoracic Society criteria. The following spirometric variables were considered for the purpose of the study: forced expiratory volume in 1 second (FEV₁); carbon monoxide diffusion lung capacity corrected for alveolar volume (DLCO/VA); predicted postoperative FEV₁ (ppoFEV₁), calculated by the formula (preoperative FEV₁/number of preoperative functioning segments) x number of postoperative functioning segments; predicted postoperative DLCO/VA (ppoDLCO/VA), calculated by the formula (preoperative DLCO/VA/number of preoperative functioning segments) x number of postoperative functioning segments. Carbon monoxide diffusion lung capacity was measured by the single-breath method. The number of functioning segments was estimated by using quantitative perfusion lung scan. All spirometric values were expressed as a percentage of predicted for age, sex, and height, according to the European Community for Steel and Coal prediction equations [4, 5].

Stair-climbing test
All the patients in the study completed a symptom-limited stair-climbing test the day before the operation and the day of discharge from the hospital (8 ± 3.3 postoperative days). The test was performed on room air for all patients. Patients who experienced postoperative complications performed the test when they were stable. No patient in this series was excluded from operation because of the result at the stair-climbing test.

Our hospital has 16 flights of stairs, each flight comprising 11 steps. Each step is 0.155 m high. The patients were asked to climb, at a pace of their own choice, a maximum number of steps and stop only for exhaustion, limiting dyspnea, leg fatigue, or chest pain. The patients were also made aware of the importance of the "time" factor in the evaluation of their performance. The following measurements were recorded before and immediately after the exercise (within 30 seconds): arterial blood pressure, heart rate (HR), respiratory rate (RR), arterial and venous blood gas analysis, and arterial blood lactate concentration. During the exercise the patient’s pulse rate and capillary oxygen saturation were monitored by means of a portable pulse oximeter. Hemoglobin concentration (Hb) was assessed before the preoperative and postoperative exercise test, respectively, and it was used to estimate the arterial oxygen content (CaO₂) by the following formula: (1.34 x Hb x SaO₂/100) + (0.0031 x PaO₂) [6]. For each patient the number of steps climbed and the time taken to complete the test were recorded to deduce the following ergometric variables: work (height of the step [m] x steps per minute x body weight [kg] x 0.1635) [7]; O₂max, mL/min ([5.8 x weight] [kg] + 151 + [10.1 x work]) [7]; predicted O₂max, mL · min^-1 · kg^-1 (60 to 0.55 x age, for male subjects; 48 to 0.37 x age, for female subjects) [8]; O₂max expressed as percentage of predicted for age and sex, according to the former equations (O₂max%pred); O₂/body surface area (BSA), mL · min^-1 · m^-2; physical working capacity (PWC) (work/body weight); maximum O₂ pulse (O₂max/heart rate); oxygen extraction ratio, ER, at the end of exercise (C[artero-venous]O₂/CaO₂). Maximum predicted heart rate was estimated by the after formula: 220 - age [6], and the heart rate reserve in percent (HRR%) was calculated by the equation: (predicted maximum heart rate - actual maximum HR/predicted maximum heart rate) x 100, according to Wasserman and coworkers [6].

Furthermore, the main symptoms, which limited the stair-climbing test, were recorded for each patient in both exercises.

Statistical analysis
Comparison between preoperative and postoperative variables was made by means of a paired Student’s t test, for continuous variables, and by means of a ² test, for categorical variables. Multiple regression analyses were then performed using as dependent variables preoperative O₂max and postoperative O₂max, respectively. The following independent variables were regressed on preoperative O₂max: age, BSA, FEV₁, DLCO/VA, CaO₂, and presence of a concomitant cardiac disease. The after independent variables were regressed on postoperative O₂max: age, BSA, ppoFEV₁, ppoDLCO/VA, postoperative CaO₂, presence of a concomitant cardiac disease, type of operation, length of postoperative hospital stay, presence of postoperative complications.

Moreover a multiple regression analysis was performed to assess which independent variables (age, FEV₁, DLCO/VA, ppoFEV₁, ppoDLCO/VA, CaO₂, presence of a concomitant cardiac disease, oxygen extraction ratio, BSA, maximum O₂ pulse, HRR%, difference between the value of systolic blood pressure at the end of exercise and the one at rest) were predictors of the difference in O₂max between the preoperative and the postoperative exercise test (dependent variable).

For the purpose of the present study, cardiac disease was defined as follows: previous cardiac operation; previous myocardial infarction; history of coronary artery disease; and current treatment for arrhythmia, hypertension, or cardiac failure.

All the tests were two tailed and a p value less than 0.05 was considered statistically significant. The analysis was performed by using the Statview 5.0 software (SAS Institute, Cary, NC).

	Results

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The characteristics of the patients enrolled in the study are shown in Table 1. 22 patients developed 25 complications: 11 prolonged air leaks (lasting more than 7 days), 4 pneumonia, 4 atrial fibrillation requiring medical treatment, 2 fever higher than 38°C for longer than 3 days, 1 atelectasis requiring bronchoscopy, 1 pleural empyema, 1 cardiac failure, and 1 pulmonary edema. Those patients experiencing postoperative complications climbed significantly fewer steps in the preoperative test compared with patients without complications (96 ± 31.1 steps versus 131 ± 32.2 steps; Student’s t test = 4, p = 0.0001), and had a significantly lower O₂max (22.5 ± 3.2 versus 25.9 ± 4.5; Student’s t test = 2.8, p = 0.007). Mean time to complete the test was 113.5 ±30 seconds preoperatively and 105.3 ±37.8 seconds postoperatively. Table 2 shows the results of the comparison between preoperative and postoperative ergometric variables. In particular, in the postoperative test there was a 21% reduction in the number of steps climbed with respect to the preoperative test (p < 0.0001); a 21% reduction in work (p < 0.0001); a 15% reduction in O₂max, either expressed in mL/min, in mL · min^-1 · kg^-1, or as percent of predicted (p < 0.0001); a 15.3% reduction in O₂max/BSA (p < 0.0001); a 12.3% reduction in O₂ pulse (p < 0.0001); a 12% increase in respiratory rate (p = 0.003); a 19% reduction in arterial oxygen content (p < 0.0001); and a 12.7% increase in oxygen extraction ratio (p < 0.0001). The mean increase in systolic blood pressure, which is observed at the end of exercise (compared with the value at rest), was significantly less postoperatively compared with preoperatively (p = 0.047).

No significant differences were noted in terms of HRR between preoperative and postoperative tests.

The comparison between the main reasons to stop the exercise before and after the operation showed that the leading limiting symptom was dyspnea in both preoperative and postoperative tests (60% and 67% of patients, respectively). However, the number of cases of limiting dyspnea did not significantly increase after the operation. In the postoperative test more patients stopped climbing because of physical exhaustion (p = 0.053) and fewer patients for leg discomfort (p = 0.036) with respect to the preoperative test; only 6 patients stopped the postoperative climb because of chest pain from thoracotomy.

Patients who underwent pneumonectomy experienced a significantly greater reduction in number of steps climbed, work, O₂max, and O₂max %pred, compared with the patients who underwent lobectomy. Maximum O₂ pulse was also reduced, although not significantly (Table 3). Furthermore, the oxygen extraction ratio was not different in the two subsets of patients. In particular, the reduction of O₂max in the pneumonectomy group amounted to 21.4% with respect to the preoperative value (compared with 14.0% in lobectomy patients); maximum O₂ pulse was reduced by 14.7% in pneumonectomy (compared with 11.7% in lobectomy patients). There was no significant difference between pneumonectomy and lobectomy patients in terms of reasons to stop the exercise in the preoperative or postoperative periods. Within each type of operation, the only limiting symptom that varied significantly from preoperative to postoperative test was a reduction in leg discomfort in the lobectomy patients. For lobectomy, the number of cases of dyspnea and exhaustion in the postoperative test increased with respect to the preoperative test, although the difference did not reach statistical significance.

	Comment

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The appeal of stair climbing is its simplicity and the patients’ familiarity with the exercise, and we consistently use this test for risk stratification before operation. The test requires minimum equipment, time, and personnel, thus it is extremely economical and widely applicable. Symptom-limited stair climbing has been shown to be a greater stress than cycle ergometry or treadmill walking [12–14], yielding higher values of O₂max. This result may be partly explained by the fact that this test is extremely motivating for the patient who is pushed to reach a visible objective, represented by the next landing. Ninety-seven percent of our patients preoperatively, and 87% postoperatively, reached the landing before quitting the test.

We purposely chose to calculate O₂max rather than measure it, inasmuch as we wanted to adopt a technically simple, low-cost, widely applicable noninvasive method of exercise. Although the accuracy of the calculation of O₂max is not widely accepted, the same equation was used after the preoperative and postoperative test, respectively. Provided a discrepancy would exist between measured and calculated O₂max, this discrepancy would be similar for both tests. Thus, we consider the amount of O₂max reduction in percent to be a reliable value.

Many studies have investigated the postoperative exercise tolerance in lung resection patients [15–21], but only one focused on the early postoperative period [21]. None of them, however, used stair climbing as exercise test, which may account for some differences among the values of the data reported in those analyses and in ours.

The results generated in the present study showed a reduction in O₂max of 15% with respect to the preoperative value. Such decrease was less than that reported by Miyoshi and associates [21], which amounted to 28% in the early postoperative evaluation (mean 9 postoperative days). This discrepancy may lay in differences in methodology of exercise and sample size (they had only 16 patients in their study). Miyoshi and associates concluded that the exercise performance in the early postoperative period was reduced mainly by ventilation. In our study spirometric variables were not significant independent predictors of preoperative or postoperative exercise tolerance, confirming the findings of Pelletier and colleagues [15] and Nezu and colleagues [19]. However, definitive conclusions cannot be drawn from the present study, because direct measurement of the breathing reserve by expired gas analysis is needed to assess the role of ventilatory factors in the limitation of postoperative exercise test. Conversely, O₂max reduction was accompanied by a significant reduction in maximum O₂ pulse and in the rise of systolic blood pressure at the end of exercise. This finding may indicate that circulation may be a limiting factor in the early postoperative exercise, although a confirmation from more sophisticated exercise studies measuring hemodynamic variables in the early postoperative period is needed.

Heart rate reserve did not change between preoperative and postoperative exercises as also reported by Bolliger and associates [17], but contrary to assertions by Nezu and associates [19], who found a significant reduction at three months. The amount of preoperative HRR (around 20%) was consistent with the values reported in normal and chronic obstructive pulmonary disease patients by Killian and associates [22] and in candidates to lung resection by Bolliger and associates [17].

Pneumonectomy patients had a greater drop in postoperative O₂max compared with lobectomy patients. This finding confirmed previous investigations performed at 3 and 6 months after the operation [15, 17, 19, 20]. The extent of the loss in O₂max in our pneumonectomy cases was comparable to that reported by Bolliger and associates at 3 months [17] (21.4% versus 25%), but somewhat less than that reported by Nezu and colleagues [19] (21.4% versus 30.5%) and Nugent and colleagues [20] (21.4% versus 28%).

In the lobectomy patients the drop in O₂max was less than that reported by Nezu and colleagues [19] at 3 months postoperatively (14.0% versus 22%) and greater than that found by Bolliger and colleagues [17] at 3 months postoperatively (14.0% versus 9.2%). Bolliger and colleagues, however, included sublobar resections in their lobectomy group.

A qualitative subjective assessment was then performed to determine the leading symptoms limiting the stair climbing. Contrary to what has been reported [15, 17, 19], dyspnea was the most frequent limiting symptom, both in the preoperative and in the postoperative evaluation, without a significant difference between the two tests. The high percentage of patients experiencing dyspnea as a limiting symptom in both exercises may apparently contrast with the fact that spirometry did not significantly influence the maximum oxygen consumption. However, several mechanisms other than mechanical factors, contribute to respiratory effort including the strength, force, velocity and extent of respiratory muscle contraction, the cooperation between muscle groups, complex geometric factors, and the presence of fatigue, hypoxemia, and metabolic acidosis [6, 23]. Even though leg fatigue has been shown to contribute significantly to impair the exercise in patients with airflow limitation [22] and in the postoperative patients [15, 17, 19], this symptom was significantly less frequent in the postoperative test compared with the preoperative test in our study. The increase, although not significant, in the number of cases of dyspnea and physical exhaustion, and a vigorous program of postoperative rehabilitation and early mobilization may explain this reduction. The reduced frequency of leg discomfort as a limiting symptom in our series compared with other reports [15, 17, 19] may be a result of the different methodology of exercise and, perhaps, to a lower number of deconditioned patients undergoing operation [22]. Even though a formal preoperative rehabilitation program was not instituted, our patients were strongly encouraged to increase their physical activity in the weeks before the operation.

Chest pain from thoracotomy limited the exercise in only 5% of our patients and was not a significant factor despite the early postoperative evaluation.

Contrary to reports by Nezu and coworkers [19] and Pelettier and coworkers [15], we did not find a significant increase in dyspnea as a limiting symptom after pneumonectomy, presumably because most of the patients were already limited by dyspnea in the preoperative exercise.

We then performed a multiple regression analysis to find out which variables independently influenced the preoperative and postoperative maximum oxygen consumption, respectively. In both the preoperative and postoperative analyses, the arterial oxygen content and the age were the only significant predictor of O₂max. The decline of O₂max with age has been already reported in nonsurgical patients [6]. The CaO₂, which is dependent mainly by the hemoglobin concentration, was a better predictor of exercise performance than BSA, spirometry, presence of an associated cardiovascular disease, type of operation, presence of postoperative complications, or length of postoperative hospital stay. This result corroborated previous studies on submaximal exercise testing, which found that hemoglobin concentration significantly influenced the oxygen consumption at the anaerobic threshold, both before [24] and after lung resection [25].

Finally, a multiple regression analysis was performed to determine the predictors of postoperative loss in exercise capacity. Those patients with an old age, a small BSA, and a high oxygen extraction ratio, high maximum oxygen pulse, and high HRR in the preoperative test, were likely to experience a greater reduction in O₂max in the postoperative test. This finding may have clinical implication in the selection and preparation of candidates for lung resection, particularly for pneumonectomy.

Because the exercise performance was significantly influenced by the level of the arterial oxygen content, both before and early after the operation, this measurement may be optimized by increasing the hemoglobin concentration. This is our current practice, especially for those patients at higher risk of experiencing a relevant loss in postoperative exercise capacity and for those candidates for pneumonectomy. Increasing the aerobic reserve of patients undergoing lung resection for non–small cell lung carcinoma may improve the early postoperative quality of life and may reduce the risk of fatal complications.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Alessandro Brunelli Majed Al Refai Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Brunelli, A. Articles by Fianchini, A. Search for Related Content PubMed PubMed Citation Articles by Brunelli, A. Articles by Fianchini, A. Related Collections Lung - other