| | Exercise Testing and Training in a Cancer Rehabilitation Program: The Advantage of the Steep Ramp TestAbstract De Backer IC, Schep G, Hoogeveen A, Vreugdenhil G, Kester AD, van Breda E. Exercise testing and training in a cancer rehabilitation program: the advantage of the steep ramp test. ObjectiveTo compare the short maximal exercise capacity test (steep ramp test) with the submaximal test to determine the most appropriate exercise test in cancer rehabilitation. DesignA prospective study in which a submaximal test, a maximal short exercise capacity test (steep ramp test), and a maximal oxygen consumption test (V̇o2max test) were performed before and after an 18-week training program. V̇o2max testing, the criterion standard for the measurement of physical capacity, was compared with the submaximal test and the steep ramp test. SettingCommunity hospital and physiotherapy. ParticipantsThirty-seven cancer survivors (10 men, 27 women) treated with chemotherapy. The subjects’ mean age ± standard deviation (SD) was 48±11 years. InterventionAn 18-week training program including strength training, interval aerobic training, and home-based activities (endurance). Main Outcome MeasuresEstimated V̇o2max (submaximal test) and maximal workload (steep ramp test) were assessed during the exercise tests and compared with the results of the V̇o2max test. ResultsA paired t test showed a significant improvement in V̇o2max (+13%, P<.001) and maximal workload (+19%, P<.001) after the training program. This improvement was confirmed in the steep ramp test (maximal workload, +13%, P<.001) but not in the submaximal test (estimated V̇o2max, +4%, P=.192). Pearson correlation quantified only a moderate correlation between the V̇o2max test and the submaximal test and a high correlation between the V̇o2max test and the steep ramp test. Intraclass correlation determined the test-retest reliability of the submaximal test (.873) and the steep ramp test (.996). A linear regression model (V̇o2max, 6.7; steep ramp Wmax, +356.7) was estimated to predict V̇o2max from the steep ramp test outcome, implying a prediction margin of ±2 SDs (616mL/min). ConclusionsThe submaximal test proved to be invalid, whereas the steep ramp test seems to be a practicable, reliable, and valid test for the assessment of the training dose. The steep ramp test can be regularly repeated during the training program, providing information needed to readjust the training dose according to the progress made. DURING THE PAST FEW DECADES, the medical treatment of cancer has made substantial progress, and at the present time 60% of female and 46% of male cancer patients survive for 5 years. From 2000 to 2015, the number of cancer survivors in the Netherlands is expected to increase from 366,000 to 692,000.1 Similar observations have been found in other countries as well.2, 3 Cancer treatment, however, may be associated with substantial psychosocial and physical side effects such as decreased strength, reduction of lean body tissue, difficulty with sleeping, nausea, vomiting, pain, and fatigue.4, 5 In addition, certain types of chemotherapy may be associated with impaired cardiovascular function (anthracyclines, dose dependently) and pulmonary function (bleomycin). Fatigue is among the most frequently occurring and debilitating complaints. It affects between 75% and 96% of patients treated with chemotherapy and between 75% and 100% of patients treated with a combination of radiotherapy and chemotherapy.6, 7, 8, 9, 10 An unsatisfactory 30% of the patients still report episodes of fatigue years after the end of treatment.6, 8 In recent years, recommendations for the management of cancer-related fatigue have changed considerably. For instance, the traditional suggestion that rest is the cornerstone of treatment during episodes of fatigue has been replaced by physical activity programs that have been shown to reduce cancer-related fatigue.8, 11, 12, 13, 14, 15, 16, 17 Presently, exercise training is regularly recommended as an alternative for bedrest or reduced physical activity.13, 18 A physical active rehabilitation program has been shown to improve aerobic capacity, muscular strength, body composition, and quality of life.4, 13, 19 Although the overall opinion about the beneficial effects of physical rehabilitation programs is generally accepted, information regarding the type, duration, intensity, frequency, and timing of physical exercise is lacking.12, 16, 20 Furthermore, physical activity programs should be based on accurate exercise testing methods. These tests are essential to identify the physical loading capacity of an individual patient in concert with possible physical limitations.12 In addition, it is of key importance to determine individual physical progress or deterioration regularly throughout the training program. For this reason, reliable, valid, and accurate exercise tests are of paramount importance in optimizing a rehabilitation program. In a detailed review, Irwin and Ainsworth12 concluded that maximal oxygen consumption (V̇o2max) is the criterion standard for measuring cardiorespiratory fitness. In addition, by using V̇o2max testing, it is feasible to assess cardiopulmonary limitations during exercise as well.21 In daily clinical practice, however, direct measurements of V̇o2max during a graded exercise test are expensive in terms of equipment and staff and put a serious burden on the patient as far as exercise time is concerned. For this reason, submaximal exercise tests are often used.22 Maximum exercise capacity is then deduced from the heart rate at a submaximal workload.23 Although submaximal testing is widely used, the outcome in terms of determining the patient’s loading capacity is inaccurate.24, 25 The major physiologic reason for this inaccuracy is that the heart rate varies substantially at any level of submaximal work, independently of the oxygen uptake. This variation in heart rate can be caused, for example, by emotional state, degree of physical conditioning, elapsed time after the previous meal, total circulating hemoglobin, the degree of hydration, alterations in ambient temperature, and hydrostatically induced changes resulting from prolonged erect posture.26 Recently, a short maximal exercise capacity test (steep ramp test) has been described in the exercise rehabilitation of patients with chronic heart failure. This test proved to be safe, practical in its use, and reproducible.27, 28 Therefore, the aim of the present study is to compare the short maximal exercise capacity test (steep ramp test) with the submaximal test to discover the most valid, reliable, and feasible exercise test in cancer rehabilitation. To make a good comparison, we analyzed whether the tests had enough discriminative power to detect the progress that was made in a training program, assessed the test-retest reliability in a representative group of patients, and compared the test results of the steep ramp test and the submaximal test with V̇o2max testing as a criterion standard. Methods  Participants Thirty-seven patients treated curatively with chemotherapy were included in the study. Patient characteristics are depicted in table 1. Training started a minimum of 6 weeks after completing chemotherapy to counteract bias resulting from spontaneous recovery after chemotherapy. | | |  | Characteristics | Value | % | |
|---|
| Age (y) | | | | |  Mean ± SD | 48±11 | | | | Range | 24−71 | | | | Sex (n) | | | | | Male | 10 | 27.0 | | | Female | 27 | 73.0 | | | Cancer type (n) | | | | | Breast cancer | 20 | 54.1 | | | Ovarian cancer | 5 | 13.5 | | | Non-Hodgkin’s lymphoma | 5 | 13.5 | | | Colorectal | 4 | 10.8 | | | Testis | 2 | 5.4 | | | Hodgkin’s lymphoma | 1 | 2.7 | | | Treatment (n) | | | | | Chemotherapy | 37 | 100.0 | | | Plus radiotherapy | 1 | 2.7 | | | Plus surgery | 11 | 29.7 | | | Plus radiotherapy and surgery | 20 | 54.1 | | | Chemotherapy (n) | | | | | AC, breast cancer | 6 | 16.2 | | | CMF, breast cancer | 5 | 13.5 | | | FEC, breast cancer | 9 | 24.3 | | | Carboplatin-paclitaxel, ovarian cancer | 5 | 13.5 | | | CHOP/CVP, non-Hodgkin’s lymphoma | 5 | 13.5 | | | 5-FU leucovorin, colorectal cancer | 4 | 10.8 | | | BEP/EP, testis | 2 | 5.4 | | | ABVD, Hodgkin’s lymphoma | 1 | 2.7 | | | | |
The following patients were excluded: (1) patients who were not capable of performing basic skills like sitting or lying down, (2) patients who had cognitive disorders or severe emotional instability, and (3) patients who were known to have other serious diseases that might hamper physical performance capacity (eg, heart failure, chronic obstructive pulmonary disease). The project was approved by the medical ethics committee of the Máxima Medical Centre Hospital, and informed consent was obtained from all subjects. Exercise Testing All exercise testing was performed on a cycle ergometer.a Before and after the training program, a maximal exercise test (V̇o2max test) was performed. The submaximal and steep ramp tests were performed before, during, and after the training program. V̇o2max Test A V̇o2max test was performed on a cycle ergometer, and an oximeter was used to collect expired gas that was sampled and analyzed breath by breath for oxygen (V̇o2), carbon dioxide (V̇co2), and volume.29 The oximeter was coupled to a computer, which plotted workload against V̇o2, V̇co2, and heart rate.b The heart rate and V̇o2 used for sampling and statistical calculations were taken from the means of every 30 seconds. Electrocardiographic activity was continuously monitored by using a 12-lead Jaeger electrocardiograph.b Ventilatory threshold was determined by using the oxygen equivalent method.30 Before the test, an estimation of the maximal workload (Wmax, in watts) was made by an experienced sports physician based on the patient’s sex, height, age, and history of physical exercise capacity. Based on this estimation, a ramp protocol was applied in which the subject was expected to reach the maximum load within 10 minutes. After 4 minutes of unloaded cycling, the selected ramp protocol was applied. Patients were instructed to cycle with a pedal frequency between 70 and 80rpm. The pedal frequency was displayed for the patient on a pedal rate indicator so that the rate could be easily maintained. Patients were instructed and encouraged to continue exercise until exhaustion. Next, the patient had to cycle unloaded until the V̇o2 values were back at baseline. This test procedure was performed at week 0 and week 18 of the training program. Steep Ramp Test After 30 seconds of cycling at 25W, the load was increased by 25W every 10 seconds until exhaustion. The subject was instructed to cycle with a pedal frequency between 70 and 80rpm. The test ended when the pedal frequency fell below 60rpm. The obtained maximal workload (the maximum short exercise capacity), the time cycled at that load, and the heart rate at the end of the test were reported. This test was performed at the start of the program, week 5, week 9, week 13, and week 18. Submaximal Test The submaximal test was based on the maximal workload and the ventilatory threshold obtained with the V̇o2max test. The test started at 50% of maximal workload and was increased by 10% every 3 minutes. Heart rate was reported in the last 15 seconds of each section. At a heart rate corresponding to the ventilatory threshold (as assessed by the previous V̇o2max test), time and workload were recorded. The submaximal test ended when the patient reached a heart rate that was 10bpm higher than the heart rate at the ventilatory threshold. This test was performed at the start of the program, week 13, and week 18. Training Program The training program used in this study consisted of a supervised strength and interval aerobic training program lasting 18 weeks. For the first 12 weeks, patients underwent an intensive strength training program and interval aerobic training on a bicycle under supervision of a physiotherapist twice a week. In addition to the supervised training, patients were asked to perform homework activities (endurance training). During the last 6 weeks, subjects trained once a week under supervision, and the instructions for homework activities were intensified. Strength Training The strength program consisted of 6 exercises targeting the large muscle groups as follows: (1) vertical row (focusing on the longissimus, biceps brachii, rhomboideus), (2) leg press (quadriceps, glutei, gastrocnemius), (3) bench press (pectoralis major, triceps), (4) pull over (pectoralis, triceps brachii, deltoideus, trapezius), (5) abdominal crunch (rectus abdominis), and and (6) lunge (quadriceps, glutei, hamstrings). At first, strength exercises were performed at 65% to 80% of the 1-repetition maximum (1-RM), consisting of 2 sets of 10 repetitions. After week 12, the emphasis shifted from muscle strength to muscle endurance involving training with less resistance (35%−40% of 1-RM) but more (20) repetitions. Every 4 weeks, the training progress was evaluated, and the training result was adjusted by means of a 1-RM test. Interval Aerobic Training The interval aerobic training consisted of cycling 2 times 8 minutes, before and after the strength program. The first 8 weeks, the 8-minute periods consisted of 30 seconds at 65% of the maximal workload of the steep ramp test and 60 seconds at 30%; from week 9, the 8-minute periods consisted of 30 seconds at 65% and 30 seconds at 30% of the maximal workload of the steep ramp test. Endurance Training: Home-Based Activities In addition to the supervised training, the participants had to do endurance training at home (eg, walking, cycling, or swimming). The first 4 weeks, patients were advised to train at least 3 times a week, for between 30 and 60 minutes. After week 12, they were recommended to walk, cycle, or swim for 60 minutes, at least 4 times a week. These home activities were registered in an exercise log in which the patients subjectively determined the training intensity by Borg rating of perceived exertion and the duration of the exercise. The Borg rating was used for the home program for practical reasons; it was easy for the patients to register, and there was no need for equipment. Data Processing and Statistical Analysis Means and standard deviations (SDs) for physical characteristics and test results were calculated. Student t tests for paired samples were applied to compare the outcomes of the V̇o2max test, submaximal test, and steep ramp test before and after training. Significance was set at P less than .05. In the submaximal test, heart rates at different submaximal workloads (50%, 60%, 70% of Wmax) were used to calculate predicted V̇o2max values with a computer solution for the Astrand nomogram of Shephard.23, 31 The mean of these values was taken as the predicted V̇o2max. Intraclass correlation coefficients (ICCs) were calculated to examine the test-retest reliability of the steep ramp test and the submaximal test in a separate population of patients (n=23). The 95% confidence intervals (CIs) were determined for each ICC. The Pearson correlation coefficient quantified the relation between measured V̇o2max and (1) measured Wmax of the steep ramp test and (2) estimated V̇o2max of the submaximal test, at different test moments (before and after the rehabilitation program). Correlations were categorized by Munro,32 in which .26 to .49 is a low correlation, .50 to .69 is moderate, .70 to .89 is high, and .90 to 1.00 is very high. CIs were calculated by using a Fisher z transformation.33 A linear regression model was used to predict the maximal power and V̇o2max in the V̇o2max test from the steep ramp test outcome in a mixed linear analysis of data of 2 test moments (before and after training), including a random intercept term for each patient. Detailed statistical analyses showed a similar pattern between male and female patients. Because all patients were provided with a training load independently of sex, analyses and data were performed without distinction between men and women. All statistical analyses were performed with SPSS.c Results All patients selected for the study were able to complete the training program. All exercise tests were tolerated well without complication. Prediction of o2max From the Steep Ramp Test Outcome A mixed linear regression model was fitted to allow a prediction of maximal workload and V̇o2max with the V̇o2max test from the measurements of the steep ramp test. Results are presented in Fig 1, Fig 2. The resulting regression equation to calculate maximal workload was as follows: The residual SD (including the random intercept variance) was 26.7, implying a prediction margin of ±2 SDs (53.4W). The resulting regression equation to calculate V̇ o2max was as follows: The residual SD (including random intercept variance) was 308, implying a prediction margin of ±2 SDs (616mL/min). Discussion The physical limitations after treatment for cancer vary widely among patients.34 Physical capacity may be affected by a variety of factors such as stage and type of cancer, previous history of physical activity, psychologic variables, type of treatment, and obesity.12 Consequently, there is a need to evaluate exercise tests used for assessing the initial physical fitness state, readjustment of the training load, and monitoring of the effects of a training intervention. V̇o2max testing is widely accepted as the criterion standard for the evaluation of physical capacity.35 In this category of patients, V̇o2max testing using gas exchange measurements and electrocardiographic registration, under supervision of a physician, is especially indicated because cancer survivors may have additional pulmonary or cardiac limitations caused by cardiotoxic (eg, anthracylins) or pulmotoxic (eg, bleomycin) medications or radiation therapy to the breast.8, 17, 36, 37, 38 V̇o2max testing serves, in this case, as a diagnostic tool. A shortcoming of both the steep ramp test and the submaximal test is that they do not have this diagnostic value. However, V̇o2max testing cannot be used frequently during rehabilitation because of its cost (personnel and equipment) and impact on the patient. There is a need, therefore, for exercise tests that can be easily applied during training. These tests have to be valid and reliable and provide sufficient information about the cancer patient’s physical capacity and training progress. In the present study, V̇o2max testing was performed before and after the training program to provide a criterion standard of the physical exercise capacity. As we expected, the group was very heterogeneous in terms of physical exercise capacity (resulting in large SDs and range), which emphasizes the importance of individual training assessment by means of appropriate tests. After the training program, there was a significant increase in V̇o2max (+13%), maximal workload (+19%), and V̇o2 at the ventilatory threshold (+24%). The respiratory quotient at the end of the test did not change after training and was above 1.15, indicating that maximal exhaustion was reached in both tests.29 These results all indicate that there is a substantial training progress in the cancer patients included in the training program. These results are in accordance with other training intervention studies in cancer patients that use V̇o2max as an outcome measure for physical capacity. Significant changes in V̇o2max fall within a range of 6% to 19%.4, 11, 14, 38 Remarkably, the training results appear to level off starting from week 13 in both the submaximal test and the steep ramp test. The lesser degree of supervision starting from week 13 can be considered as possible explanation; however, normal leveling off of the training effect is possible. The results of the submaximal tests were analyzed with the Astrand nomogram. Based on the assumptions of Astrand, there is a linear relationship between heart rate, exercise intensity, and oxygen consumption. Given this relation, the measurement of heart rate combined with workload and the age-related maximal heart rate provides a reasonable estimation of exercise capacity.23 The training progress has occurred when the heart rate decreases at a fixed submaximal workload, and, as a result, estimated V̇o2max will increase. Interestingly, the results of the present study show no significant decrease in heart rate at different submaximal workloads (50%, 60%, 70%). In contrast to the V̇o2max tests, based on the results of the submaximal test, we were not able to monitor training progress. Our results are in line with other investigations39 that found that submaximal tests designed to predict V̇o2max for the majority of disabled populations are not accurate because of the altered disability-specific physiologic responses. Furthermore, Chuang et al40 found in patients with chronic obstructive pulmonary disease that estimation of V̇o2max by submaximal testing might be appropriate at the group level but is inaccurate in predicting the outcomes of each patient. Especially in cancer patients, the relationship between predicted V̇o2max and real V̇o2max may be distorted by several causes. For instance, Viniegra et al41 investigated cardiovascular autonomic function in 55 breast cancer patients. Thirty-one patients had been treated with cardiotoxic anthracyclin−containing chemotherapy regimens, and abnormal variations in heart rate were found in 81%. Finally, Greiwe et al25 reported that a submaximal test overestimates V̇o2max in healthy subjects and should not be used when an accurate assessment of V̇o2max is required. Given these results from the literature, one may wonder why in our research Pearson correlations of the submaximal test with the V̇o2max test are relatively high (.79, .79, .77, .71). A plausible explanation for this obvious contradiction is the fact that a large range in V̇o2max (17.4−51.6mL·kg−1·min−1) is observed in our research population, which would enhance the correlation. The correlation measures more or less how well subjects at the extreme ends of the scale can be distinguished. However, when an accurate estimation of a person’s V̇o2max is required, in this case for individual training assessment, a submaximal test seems to be unsuitable. According to the findings of the present study, submaximal tests seem to be of less value for training guidance in individual cancer survivors and may have limited value in assessing the exercise capacity in this category of patients. The results of the steep ramp test indicate a 15% increase in maximal workload after the training program. These results were in line with the results of V̇o2max testing. The steep ramp test used in the present study was developed to assess training in patients with severe chronic heart failure.27, 28 In the study with chronic heart failure patients, the steep ramp test was used weekly during the training program to enable readjustment of the exercise intensity according to the benefits achieved. The steep ramp test determines the maximum short exercise capacity, which partially reflects anaerobic capacity and muscle strength. Pearson correlation analysis indicates a strong relation between the results of the steep ramp test and the results of the V̇o2max test. The steep ramp test therefore proves a valid test for the assessment of the initial physical capacity and for monitoring the effects of a training intervention in cancer patients. By using regression analysis, we can deduce the maximal wattage obtained by V̇o2max from the steep ramp test results with a margin of ±2 SDs (53W), as presented in figure 1. V̇o2max can also be deduced from the steep ramp test results within a margin of ±2 SDs (614mL/min) (see fig 2). Because of its short duration (on average, 2min excluding recovery), the steep ramp test can be repeated regularly, and, consequently, it is easy to incorporate this test in a training program. The submaximal test lasts much longer (10min, excluding recovery) and thus is more difficult to integrate regularly into the program. In the present study, the steep ramp test was performed once every 4 weeks. Because there is a gradual improvement in the maximal workload (see table 5), the training can be readjusted according to the individual progress achieved. Maximal workload achieved in the steep ramp test can be easily translated into training intensity by calculating a percentage of the maximal workload. Because the steep ramp test has been used in patients with severe chronic heart failure and was tolerated by all of the patients in this study, it seems to be safe when it is correctly applied.27, 28 Conclusions The steep ramp test has proved to be a valid, safe, and practical means for prescribing the training load and for monitoring training progress in the rehabilitation of cancer patients. Submaximal testing proves to have only limited value in the assessment of exercise capacity and is less feasible and less reliable than the steep ramp test. Consequently, a steep ramp test should be recommended in cancer rehabilitation programs for the individual assessment of training. Supplier References 1. 1Werkgroep ‘Prevalentie van kanker’. Kanker in Nederland; trends, prognoses en implicaties voor zorgvraag. Den Haag: KWF Kankerbestrijding; 2005;. 2. 2Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A. 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a Department of Sports Medicine, Máxima Medisch Centrum, Veldhoven, The Netherlands b Department of Internal Medicine, Máxima Medisch Centrum, Veldhoven, The Netherlands c Department of Methodology and Statistics, Maastricht University, Maastricht, The Netherlands d Department of Movement Science, Nutrition and Toxicology Research Institute Maastricht (NUTRIM), Maastricht University, Maastricht, The Netherlands.  Reprint requests to Ingrid C. De Backer, MSc, Dept of Sports Medicine, Máxima Medisch Centrum, De Run 4600, 5500 MB Veldhoven, The Netherlands
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(07)00111-6 doi:10.1016/j.apmr.2007.02.013 © 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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