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(Chest. 2005;127:1159-1165.)
© 2005 American College of Chest Physicians

Cardiopulmonary Exercise Tests and Lung Cancer Surgical Outcome*

Thida Win, MRCP; Arlene Jackson; Linda Sharples, PhD; Ashley M. Groves, MRCP; Francis C. Wells, FRCS; Andrew J. Ritchie, FRCS and Clare M. Laroche, FRCP

* From Thoracic Oncology Unit (Drs. Win and Laroche), Respiratory Physiology Department (Ms. Jackson), and Cardiothoracic Surgery Departments (Drs. Wells and Ritchie), Papworth Hospital, Papworth; MRC Biostatistics Unit (Dr. Sharples); and Department of Radiology and Nuclear Medicine (Dr. Groves), Addenbrooke’s Hospital, Cambridge, UK.

Correspondence to: Thida Win, MRCP, Consultant Chest Physician, Thoracic Oncology Unit, Papworth Hospital, Papworth Everard, Cambridge, CB3 8RE, UK; e-mail: thida.win{at}papworth.nhs.uk


   Abstract
TOP
 Abstract
Introduction
 Methods and Materials
 Results
 Discussion
 Conclusions
 References
 
Study objectives: Surgical resection remains the treatment of choice for anatomically resectable non-small cell lung cancer. However, the presence of associated comorbid conditions increases the risk of death and surgical complications. Several studies have evaluated the usefulness of preoperative exercise testing for predicting postoperative morbidity and mortality. The aim of this study was to establish whether exercise testing could predict poor surgical outcome in lung cancer surgery and whether the absolute value or percentage of predicted value is the better predictor of the surgical outcome.

Design: The study was designed as a prospective study.

Patients and setting: One hundred thirty patients with potentially operable lung cancer at Papworth Hospital over 2 years were recruited; of these, 101 underwent curative surgery.

Interventions: Spirometry and cardiopulmonary exercise tests were performed for every patient (n = 99), except for two patients with back problems. We also recorded the outcome of surgery, in particular, complications and mortality.

Measurements and results: Mean maximum oxygen transport at peak exercise (O2peak) was 18.3 mL/kg/min (SD, 4.7 mL/kg/min), and mean percentage of predicted O2peak value was 84.4% (SD, 30%). Poor surgical outcome was significantly related to O2peak percentage of predicted (p < 0.01) but not to the actual oxygen uptake value.

Conclusions: The use of the percentage of predicted O2peak value would be a better indicator of surgical outcome, since it predicts the surgical outcome better, and corrects for normal physiologic ranges. The threshold of O2peak for surgical intervention could be set between 50% and 60% of predicted without excess surgical mortality.

Key Words: exercise test • lung cancer • surgical outcome


   Introduction
TOP
 Abstract
 Introduction
Methods and Materials
 Results
 Discussion
 Conclusions
 References
 
Surgical resection remains the treatment of choice for anatomically resectable non-small cell lung cancer.12 However, the presence of associated comorbid conditions increases the risk of death and surgical complications for patients undergoing lung resection.3 Conventional preoperative evaluation of these patients is based on spirometry and estimation of postoperative pulmonary function from radioisotope, regional, ventilation-perfusion lung studies. Although the relationship between the patient’s performance status and pulmonary function is well documented, a stronger correlation has been found between dyspnoea and the results of exercise tests.4 This indicates that exercise capacity is not dependent on pulmonary function alone. There are several other factors: cardiac function, hemodynamic performance, and peripheral tissue oxygen utilization. Because both thoracotomy and the immediate postoperative period represent a severe stress to both the circulatory and respiratory reserve, preoperative exercise capacity should be the more sensitive predictor of postthoractomy morbidity and mortality.

The British Thoracic Society (BTS)5 and American College of Chest Physicians guidelines6 for selection of patients for lung cancer surgery suggest that patients of borderline operability should undergo exercise tests to measure maximum oxygen transport at peak exercise (O2max). If the O2max is < 15 mL/kg/min, patients are regarded as high risk for surgery. However, the use of this absolute value may discriminate against older people, short people, and/or female patients who have normal predicted absolute values < 15 mL/kg/min.

Several studies789 have evaluated the usefulness of preoperative exercise testing for predicting the incidence of postoperative morbidity and mortality. In published studies, a variety of exercise parameters and recommendations are given. Eugene et al10 reported the importance of the absolute value of O2max. Smith et al8 and Bechard and Wetstein9 found O2max per kilogram of body weight was the best parameter. Bolliger et al1112 stressed the importance of poor exercise performance and concluded that O2max per kilogram of body weight expressed as a percentage of the predicted value was the best predictor of postoperative complications. However, conflicting evidence was found by Colman et al,13 Holden et al,14 and Markos et al,15 who suggested that poor exercise performance was not a good predictor of postoperative morbidity and mortality.

The aim of this study was to establish whether exercise testing was correlated with postoperative morbidity and mortality in patients undergoing lung cancer surgery, and whether the absolute value or percentage of predicted value was the better predictor of poor surgical outcome. We also aimed to establish the lowest maximum oxygen transport at peak exercise (O2peak) threshold value for safe lung cancer surgery.


   Methods and Materials
TOP
 Abstract
 Introduction
 Methods and Materials
Results
 Discussion
 Conclusions
 References
 
This was a prospective study of 130 patients with potentially operable lung cancer attending the thoracic oncology clinic at Papworth Hospital, UK, between January 2001 and December 2003. Two patients were unable to perform the exercise test due to back pain. Twenty-nine other patients were considered unsuitable for surgery: 22 because of staging issues, 5 due to poor cardiopulmonary fitness, and 2 who refused surgery. The test results of these patients are recorded in Table 1 . Patients 1 to 3 in Table 1 were rejected because of both a low O2max and poor FEV1, and patients 4 and 5 were rejected due to poor FEV1 alone.


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  		Table 1.. Results of Patients Who Were Not Referred for Surgery Due to Poor Cardiopulmonary Fitness (n = 5)

 
The remaining 99 patients made up the study sample. Spirometry and cardiopulmonary exercise tests were performed by all 99 patients. Informed written consent was given by all patients, and the study had local ethics approval.

Outcome Measures
Duration of hospital stay and outcome of surgery including complications and mortality was documented. Two outcomes were studied. First, a broad definition of complicated outcome was used to estimate the proportion of patients who had a complicated postoperative course, and to assess the effects of O2max on complications. Complicated postoperative course was defined if any of the following occurred: postoperative death, myocardial infarction (MI), heart failure, renal failure, respiratory failure, pulmonary embolism, septicemia, or pneumonia. Diagnostic criteria are presented in Table 2 . Second, a more restricted definition of poor outcome was used to estimate the proportion of patients who would not have been operated on had the outcome been known ahead, and which might have been predicted by cardiopulmonary exercise testing. Poor outcome was defined as postoperative death, MI, or respiratory failure.


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  		Table 2.. Criteria in Diagnosing Postsurgical Complications

 
Statistical Methods
O2max measurements are summarized as the mean and SD for each group under study. Associations between measures of O2max and outcome groups as well as mortality were assessed using the Student t test. These associations were adjusted for operation type (pneumonectomy/lobectomy) using analysis of variance, with outcome as a fixed effect and operation type as a covariate. Receiver operating characteristic (ROC) curves were plotted to assess the predictive value of O2max for poor outcome. Positive and negative predictive values for poor outcome were calculated for selected thresholds of oxygen uptake (O2), and using study estimates of the prevalence of poor outcome and mortality.

Spirometry
All lung function parameters were measured by spirometer in the respiratory physiology laboratory at Papworth Hospital. The spirometer and recording system were calibrated daily. At least three recordings were made until the results were reproducible. The best of three reproducible attempts was used for analysis.

The Cardiopulmonary Exercise Test (Treadmill O2 Test)
The cardiopulmonary exercise test was performed using the Oxycon-Pro Exercise System (Viasys Healthcare; Conshohocken, PA) and the standardized exponential exercise protocol (STEEP),16 adapted to include an additional 1-min warm-up period. The STEEP was devised to allow a single protocol to be selected for subjects with a wide range of exercise capacities, which could be applied to the treadmill. The treadmill test lasts for a maximum of 20 min, during which the patient exercises for 16 min (4 min are taken up with baseline measurements and recovery). Patients are required to exercise for as long as possible until they are symptom restricted. The ECG is monitored, and oxygen and carbon dioxide are measured from the expired air. The Borg breathlessness score17 and the reason for the termination of the test were recorded at the end of the test. The three O2 measurements over the final 30 s of the exercise phase were averaged and reported as maximum oxygen transport at peak exercise (O2peak). Predicted O2max was calculated using standard formulas based on patient age, sex, weight, and height.18

Lung Cancer Surgery
The decision of suitability for surgery was made at a multidisciplinary team meeting. Lung cancer surgery was performed by one of three dedicated cardiothoracic surgeons via standard posterolateral thoracotomy. The routine surgical and anesthetic procedure included single-lung ventilation using a double-lumen endobronchial tube during the operation. Postoperative physiotherapy included breathing exercises and early ambulation.


   Results
TOP
 Abstract
 Introduction
 Methods and Materials
 Results
Discussion
 Conclusions
 References
 
Of the 99 patients who had potentially curative surgery, 61 were men and 38 were women. Mean age was 68.4 years (SD, 8.0 years; range, 42 to 85 years). Thirty-four patients underwent pneumonectomy, 56 underwent single lobectomy, 6 underwent bilobectomy, and 3 underwent wedge resection. Twenty-six patients had borderline lung function (FEV1 < 1.5 L for lobectomy, < 2.0 L for pneumonectomy). Sixty patients had stage 1 tumors, 23 patients had stage 2, and 16 patients had stage 3.

Mean FEV1 was 2.06 L (SD, 0.67 L; range 1.0 to 4.7 L) and FEV1 percentage of predicted was 80.4% (SD, 20.3%; range, 37 to 119%). Mean O2peak was 18.8 mL/kg/min (SD, 4.6 mL/kg/min; range, 11 to 32 mL/kg/min), mean predicted O2peak was 23.1 mL/kg/min (range, 9.8 to 39.7 mL/kg/min), and mean percentage of predicted O2peak was 88.3% (SD, 31.1%; range, 41 to 189%). Predicted O2peak was < 15 mL/kg/min in 13% (13 of 99 patients).

Four patients (4%) died within 30 days, and 21 patients had a nonfatal, major complication, ie, 25 patients were considered to have a complicated postoperative course. Major complications are recorded in Table 3 . The most common major complications were pneumonia (19%) and respiratory failure (10%).


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  		Table 3.. Frequency of Major Complications Included in Complicated Postoperative Course and Poor Outcome*

 
Table 4 summarizes the differences in O2peak for patients with and without a complicated postoperative course, poor outcome, and mortality. Preoperative O2peak as percentage of predicted was significantly associated with a complicated postoperative course, poor outcome, and mortality, but the absolute value of O2peak was not. Results did not change substantially when adjusted for operation type (data not shown). There was no significant association between FEV1 (liters) and postoperative course (Table 4).


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  		Table 4.. O2max by Surgical Outcome*

 
Thirteen patients had poor surgical outcome defined by death, MI, or respiratory failure (Table 3). All four deaths had cardiopulmonary causes. The relationship between O2peak and poor surgical outcome is shown in Tables 4, 5 . O2peak expressed as a percentage of predicted is more closely associated with poor outcome than absolute values. There was no significant association between FEV1 (liters) and poor outcome (Table 4). Interestingly, the complication rate was higher in those patients with a predicted O2 ≥ 15 mL/kg/min (28%; 24 of 86 patients) than in those with a predicted O2 < 15 mL/kg/min (8%; 1 of 13 patients).


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  		Table 5.. Positive and Negative Predictive Probabilities of Poor Outcome (O2peak % Predicted)*

 
Figures 1, 2 show the ROC curve for O2peak measurements as predictors of poor outcome and mortality. These plots clearly show the superior predictive value of O2peak when corrected for age, sex, and size. The area under the ROC curve was 0.56 (95% confidence interval [CI], 0.41 to 0.76) for absolute O2peak, which is not significantly different from 0.5, the value indicating no predictive value for poor outcome. In contrast, the area under the ROC curve for percentage of predicted O2peak was 0.7 (95% CI, 0.65 to 0.90), which was significantly > 0.5 (p = 0.002). The areas under the ROC curves for O2peak measurements as predictors of mortality were 0.66 for absolute O2peak and 0.81 for O2peak percentage of predicted. Positive and negative predictive probabilities for poor outcome were calculated for a range of O2peak thresholds (Table 5). The proportion of cases predicted to be high risk increases as the threshold defining high risk increases. Therefore, the proportion of high-risk patients who have poor outcome decreases as the threshold increases. In contrast, there is little change in the proportion of cases above the threshold with satisfactory outcomes.



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  		Figure 1.. ROC curve to predict satisfactory surgical outcome from O2 actual value and percentage of predicted value area under the curve value. O2 = 0.56 mL/kg/min; O2 percentage of predicted = 0.7%.

 


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  		Figure 2.. ROC curve to predict survival from O2 actual value and percentage of predicted value area under the curve value. O2 = 0.66 mL/kg/min; O2 percentage of predicted = 0.81%.

 
Tables 6, 7 show the positive and negative predictive probability of 30-day mortality and poor outcome from O2peak in absolute values. Table 8 shows the positive and negative predictive probability of 30-day mortality from O2peak percentage of predicted value.


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  		Table 6.. Positive and Negative Predictive Probabilities of Poor Outcome (O2peak Absolute Value)*

 

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  		Table 7.. Positive and Negative Predictive Probabilities of 30-Day Mortality (O2peak Absolute Value)*

 

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  		Table 8.. Positive and Negative Predictive Probabilities of 30-Day Mortality (O2peak % Predicted)*

 

   Discussion
TOP
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
Conclusions
 References
 
By calculating O2max or O2peak, the cardiopulmonary exercise test uniquely provides an objective evaluation of functional capacity. Since exercise capacity in lung cancer patients is more likely to be symptom limited rather than physiologically limited, we considered that O2peak was the more appropriate measurement in our study. However, the terms O2peak and O2max are often used interchangeably in the literature. Moreover, O2peak is currently recommended as the most useful measurement from the cardiopulmonary stress test.18

We used the STEEP as it had important advantages for our patient cohort. It is validated against a wide range of patients with different exercise capacities.16 This was important since 26 of our patients had borderline lung function. The STEEP has also been validated in patients with coronary artery disease,19 and a number of our patients had evidence of myocardial ischemia. The STEEP has been compared to the modified shuttle walk test in cystic fibrosis patients.20 The STEEP can be used with either an exercise bike or treadmill, enabling its widespread use. However, even though there is a difference in duration compared to the other protocols, most of our patients exercised in excess of 6 min, bringing the STEEP into line with other exercise protocols.

We showed that poor exercise capacity as measured as a percentage of predicted O2peak was a good predictor of poor surgical outcome. Neither actual FEV1, actual O2peak, or predicted O2peak measurements were predictive of poor outcome. The poor predictive performance of absolute values reflects the nonphysiologic nature of such measurements since they fail to take into account normal values for female, elderly, or short patients. The current lung cancer surgical population is more heterogeneous, with a higher proportion of women and older patients than surgical populations in the past. Although absolute values are easier to use, they may discriminate against certain patients and lead to unnecessary restriction of curative surgery.

Our results are in agreement with other studies1221 with respect to the use of percentage of predicted O2peak, even though we used a different exercise protocol. For instance, Brutsche et al21 studied a similar group of patients, with comparable operation types, complication rates, and mortality. Although we found a slightly lower actual mean O2peak than their study, the mean percentage of predicted value was the same, suggesting that this is a reproducible measurement despite the use of a different exercise protocol.

Bolliger et al12 reported the percentage of predicted O2peak and its relationship to surgical outcome. They found that percentage of predicted O2peak was significantly more sensitive than the absolute value. A value > 75% was an excellent indication (> 90%) of an uneventful operation, whereas a value of < 43% was a contraindication to any lung resection surgery, and values of < 60% were a contraindication for resections involving more than one lobe. Two additional studies2223 also corroborated the use of percentage of predicted O2peak. Both studies showed that values of < 50% were associated with a high risk of death related to cardiopulmonary causes23 and complications.22

Our results differed slightly from the above studies. There were four immediate postoperative deaths. One of these patients had a O2 measurement of 23.6 mL/kg/min (82% of the predicted value) and had undergone preoperative chemotherapy as part of a trial. The death was due to ARDS on the sixth postoperative day and might have been related to chemotherapy. However, the other three patients who died in the immediate postoperative period had a O2peak < 62% predicted. We also found that two of the three patients with a O2peak < 50% predicted had a poor surgical outcome. In pneumonectomy patients, there was a poor surgical outcome in both patients, with a O2peak < 50% predicted. One patient, with a O2peak < 50% predicted, survived a lobectomy but had a complicated postoperative course. In our study, patients with a O2peak > 75% of predicted had a risk of poor surgical outcome in 15% (3 of 20 patients).

The finding that the absolute value of O2peak was not predictive of a poor surgical outcome has been reported previously131415; however, these previous studies did not report the percentage of predicted O2peak values. Although in our series the absolute O2peak was not predictive of poor surgical outcome, it was useful if the values were categorized into groups (Tables 6, 7). However, the predictability from absolute values was less than that from using the percentage of predicted values (Table 8).

Due to the size of our study, the overall good outcome, and low mortality in our patients, it is difficult to define definitive threshold recommendations. A larger study would be useful to investigate further. Despite the fact that we operated on patients with low O2peak values, our 30-day mortality rate (4%) was lower than those described as acceptable in the BTS guidelines for lobectomy (4%) or for pneumonectomy (8%). This reflects recent improvements in surgical techniques and perioperative care. Nevertheless, our experience might suggest that patients with a O2peak < 50% of the predicted value should be aware of the increased surgical risk; 33% of patients with a O2peak < 50% of predicted died, while above that threshold 97% of patients survived. With regards to absolute values, only 12.5% of patients with a O2peak < 15 mL/kg/min died, while above that threshold 98% of patients survived.

We would not routinely recommend such low cut-off values without patients undergoing an extensive fitness assessment, discussion at multidisciplinary meetings, and surgeons with the necessary expertise to deal with difficult cases. Most patients and clinicians do not regard postoperative complications per se as a reason not to undergo surgery.24 Therefore, a final decision as to whether to proceed to surgery or to seek alternative treatment should be made at multidisciplinary team meetings with due regard to patient choice.


   Conclusions
TOP
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 Conclusions
References
 
Cardiopulmonary exercise testing is of value for the assessment of operative risk in patients undergoing resection for lung cancer. O2max per kilogram of body weight expressed as a percentage of predicted normal value is a better predictor of poor surgical outcome than absolute values and should be integrated into preoperative decision making.

The present American College of Chest Physicians and BTS guidelines regarding the selection of patients for lung cancer surgery may need revision to incorporate percentage of predicted values, since predicted values correct for normal physiologic ranges that represent current surgical populations and also have better predictive value for surgical mortality and morbidity. Our study suggests that the threshold of O2peak for surgical intervention could be set between 50% and 60% of predicted, without excess surgical mortality. However, ideally this new threshold should be prospectively assessed by a larger multicenter study.


   Footnotes
 
Abbreviations: BTS = British Thoracic Society; CI = confidence interval; MI = myocardial infarction; ROC = receiver operating characteristic; STEEP = standardized exponential exercise protocol; O2 = oxygen uptake; O2max = maximum oxygen transport at peak exercise; O2peak = maximum oxygen transport at peak exercise

Received for publication July 8, 2004. Accepted for publication October 20, 2004.


   References
TOP
 Abstract
 Introduction
 Methods and Materials
 Results
 Discussion
 Conclusions
 References
 

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