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Abstract

Purpose. To determine which mode of exercise is preferred by breast cancer survivors and to evaluate this response between graded exercise testing on a treadmill and on a cycle ergometer. Methods. Twelve breast cancer survivors completed 2 maximal aerobic stress tests on separate days. The women completed a ramp protocol on an electronically braked cycle ergometer and an incremental step protocol on a treadmill to volitional fatigue. Test order was randomized. Expired gases were collected for the determination of peak aerobic capacity (Vo_2peak). Results. Exercise mode had a significant effect on the graded exercise response in breast cancer survivors, P = .003. Treadmill Vo_2peak was significantly greater than bike Vo_2peak (28.7 ± 4.7 vs 23.9 ± 4.7 mL/min/kg, respectively, P = .003) and VE_max was equivalent between exercise modes (P = .731). Maximal heart rate was significantly higher by 11 bpm during the treadmill protocol (P = .004), and Ve/VCo₂ exhibited possible mode dependency (P = .018). Conclusion. This patient population felt more comfortable and produced significantly greater Vo2_peak values using the treadmill protocol. These results discuss the potential implications concerning the design and interpretation of exercise interventions for breast cancer survivors.

Keywords

breast cancer aerobic capacity exercise prescription exercise mode training intensity

Introduction

Exercise capacity in breast cancer survivors is a growing concern, with recent studies highlighting the importance of physical activity and overall mortality in survivors.^1,2 Many treatments can plague survivors with a variety of long-term side effects,^3,4 which, in turn, can decrease their quality of life, predisposing them to future disease and early mortality.^5,6 To combat these negative effects, researchers have implemented a variety of exercise interventions during treatment, immediately posttreatment, and years after primary treatment.^7-10

Exercise therapy as a rehabilitative tool is growing in popularity because of its potential to alter various biomarkers (estrogen¹¹ and adinopectin¹²) associated with cancer development and because of the positive correlation found between improvements in aerobic capacity and improved quality of life in cancer survivors.^13-15 In addition, physical activity can decrease the risk for cardiovascular disease, obesity, diabetes, and potentially diminish the chance of recurrence and increase overall survival.^16,17 Accordingly, aerobic stress testing in breast cancer survivors is becoming more common with recent guidelines demonstrating its safety,¹⁸ yet there is a lack of information concerning which mode of exercise this patient population should use to elicit a maximal response.

Past research has noted that as a general exercise preference, the survivor population prefers to walk^19-21; meanwhile researchers use a variety of modes and methods to administer stress tests and prescribe exercise to survivors. We speculate that the effectiveness of a personalized exercise prescription may decrease if the testing mode does not correspond to the preferred training mode. Even if the individual is capable of walking, the use of a cycle ergometer seems to be a preferred choice because of ease for the researcher and the ability to use additional sensitive equipment such as an electrocardiogram or pulse oximeter. The preference of mode for maximal exercise testing, within the survivor population, is yet to be evaluated.

Personalized exercise prescriptions are developed using a variety of variables produced from a maximal exercise test, such as heart rate, ventilatory threshold, power, and oxygen consumption. Previous research concerning the influence of exercise mode (between the cycle ergometer and the treadmill) on the outcomes of maximal stress testing has demonstrated similarities and/or discrepancies in these variables. The aforementioned variables used in exercise prescriptions have been shown to be similar or significantly different between modes depending on the gender being tested,²² the fitness level,²³ age,²⁴ and the clinical population chosen.^25-27 Many complications, which may influence the variables that are derived from a maximal test, can arise with breast cancer treatments: lung function may be altered, muscle strength can decrease, peripheral limitations can develop, and accelerated aging may occur. Consequently, it remains unknown if female breast cancer survivors elicit similar cardiopulmonary responses between these different modes of exercise and if these modes are interchangeable.

Therefore, the purpose of this study was to determine which mode of exercise breast cancer survivors prefer for the assessment of peak aerobic capacity and to evaluate this response to graded exercise testing.

Methods

Twelve females, who were currently disease-free after completing treatment (surgery and/or chemotherapy and/or radiation) for early-stage breast cancer, were recruited to undergo 2 different maximal aerobic stress tests on 2, nonconsecutive days, completed within 10 days of each other. Informed consent was obtained from each subject prior to testing. In a medical clinic, the women underwent a 15 W/min ramp protocol on an electronically braked cycle ergometer (Lode Excalibur; Groningen, the Netherlands) and an incremental step protocol on a treadmill that kept a constant, personalized speed (3.5 ± 0.5 mph) while the grade increased by 2% every 2 minutes till volitional fatigue. The test began only when the women felt comfortable walking without holding onto the handlebars. Test order was randomized. Using a mask, pulmonary ventilation and expired gas concentrations were collected with a TrueOne 2400 metabolic cart (Parvo Medics Inc, Sandy, UT) for the determination of peak aerobic capacity (Vo_2peak), ventilatory efficiency (Ve/VCo₂ slope), and ventilatory threshold (V_thresh, [V-slope method]). Peak oxygen consumption was determined by taking the highest value over a 15-second period. Relative and absolute Vo_2peak were compared. Heart rate (Polar T31 Heart Rate Monitor; Polar Electro Inc, Lake Success, NY) and rating of perceived exertion (RPE), using a modified Borg scale (from 0—no effort, till 10—maximal effort)²⁸ were recorded throughout each test and final power output was also noted at the end of the bike protocol. Treadmill power output was estimated by standard conversion of vertical work, body weight, and speed.^29,30 After completing both tests, women were asked which mode of exercise they preferred.

A 1-way multivariate analysis of variance (MANOVA, Hotelling’s Trace) was conducted using PSAW, version 18.0, to determine if there was an overall exercise mode effect on the key dependent variables used in exercise prescriptions (Vo₂, heart rate, ventilatory threshold). Univariate analyses of variance (ANOVAs) for each dependent variable were conducted as follow-up tests to the MANOVA, using Bonferroni method for controlling for type 1 error rates for multiple comparisons; each ANOVA was tested at .017 level. Other variables of interest were compared with paired t tests with Bonferroni adjustment. Data are reported as mean ± standard deviation.

Results

Twelve female, breast cancer survivors (age = 55 ± 6 years; height = 163.7 ± 6.6 cm; weight = 70 ± 12.8 kg, body mass index [BMI] = 26.3 ± 6.0) completed both maximal tests with no adverse advents. Descriptives concerning treatment are described in Table 1. Exercise mode had a significant effect on the response to graded exercise in this population, P= .003. As depicted in Figure 1, the Vo_2peak elicited using the treadmill was significantly greater than the Vo_2peak elicited when using the cycle ergometer (1.97 ± 0.2 L/min vs 1.64 ± 0.28 L/min, respectively, P = .003), while maximal ventilation was equivalent between modes (P = .731). During the treadmill protocol, ventilatory threshold occurred at 1.3 ± 0.2 L/min, while the cycling protocol elicited an earlier response at 1.0 ± 0.3 L/min (P = .008). As presented in Table 2, using the stationary bike resulted in a significantly shorter time to completion (P = .006), and Ve/VCo₂ slope indicated possible mode dependency, P = .018 (calculated with an n = 10 because of extreme outliers in the 2 women with a BMI > 35). Maximal heart rate was significantly higher by 11 bpm when obtained using the treadmill compared with using the cycle ergometer (P = .004), with a similar trend for the heart rate at ventilatory threshold (132 ± 19 vs 116 ± 16 bpm, respectively, P = .02). RPE scores at the end of the treadmill protocol exhibited a higher trend than with the bike protocol (P = .07). Ten of the 12 women preferred completing the maximal aerobic stress test on the treadmill than on the cycle ergometer. Two women, who were casual, seasonal, commuter cyclists, were indifferent to the mode.

Table 1.

Subject Treatment Characteristics^a

Characteristics	Subjects
Years from diagnosis
<5	6
>5	4
>10	2
Stage
I (T1N0)	5
IIa (T1N1, T2N0)	6
IIb (T2N1, T3, N0)	0
IIIa (T1N2 T2N2, T3N0)	1
Surgery	100%
Masectomy	8
Lumpectomy	2
Masectomy + tram	2
Chemotherapy	83%
ACTT	2
ACT	2
AC	3
FEC	2
Cisplatin + AT	1
Radiation	75%
Yes	9
Hormone therapy	58%
Yes	7

Data are presented as the number of subjects as well as the overall frequency (percentage) for categorical variables.

Figure 1.

Comparison of peak oxygen uptake values obtained in all subjects using the treadmill and the cycle ergometer

Table 2.

Subject Results^a,b

	Vo_2peak A (L/min)	Vo_2peak R (mL/min/kg)	HR_max (bpm)	TTC (s)	Ve (L/min)	V_thresh (L/min)	V_thresh (%HR_max)	Ve/VCo_2slope	Watts
Bike	1.64 ± 0.28^c	23.9 ± 4.7^c	161.8 ± 11^c	556 ± 122^c	59.2 ± 8.9	1.3 ± 0.2^c	72.3 ± 0.1	33.6 ± 2.4	145 ± 34^c
Treadmill	1.97 ± 0.20	28.7 ± 4.7	172.3 ± 11	727 ± 151	57.9 ± 9.4	1.0 ± 0.3	76.6 ± 0.1	30.9 ± 3.2	127 ± 23

Abbreviations: Vo_2peak A, absolute peak aerobic capacity; Vo_2peak R, relative peak aerobic capacity; HR_max, maximal heart rate; TTC, time to completion; Ve, ventilation; V_thresh, ventilatory threshold; V_thresh (%HR_max), ventilatory threshold as a percentage of the respective HR_max; Ve/VCo₂ slope, ventilatory efficiency; Watts, peak watts.

All the parameters are compared between the bicycle and treadmill maximal protocols.

Values are presented as mean ± standard deviation.

Significant difference, adjustment for multiple comparisons: Bonferroni, when compared to the maximal aerobic stress test on the treadmill.

Discussion

The major findings of this study were the following: (a) women achieved their highest Vo_2peak using a graded treadmill protocol, (b) women preferred the treadmill to the cycle ergometer when undergoing a maximal aerobic stress test, and (c) 24 maximal stress tests were completed in the survivor population with no adverse events.

Breast cancer survivors face many obstacles posttreatment. They suffer from cancer-related fatigue, changes in body composition, and decreased cardiovascular and respiratory function, which can lead to decreased physical functioning and an overall decline in quality of life. With growing evidence encouraging the use of physical activity to maintain a healthy body weight,^31,32 coupled with the strong association between healthy body weight and the ability to fend off recurrence or future disease,³³ health specialists are increasingly prescribing exercise interventions to combat these long-term side effects.

Common guidelines to improve overall health and fitness encourage the survivor population to engage in physical activity,^34,35 yet researchers are producing mixed results from their exercise interventions. Only small-to-moderate effects are being seen in aerobic fitness, overall quality of life, IGF-1, fatigue and other symptoms, and side effects.¹⁰ The varying outcomes may be because of an average adherence of only 70%³⁶ (up to 90%⁹), but even high adherence programs avoid commenting on compliance to the exercise prescription.⁹ It is unknown if researchers are tracking compliance rates or neglecting to publish these results.³⁷ If individuals are exercising below their prescribed intensity (low compliance rates), they may lack the ability to generate significant health changes. Intensity thresholds³⁸ have been discussed in other populations, implying that individuals must exercise above a specific threshold to cause enough stress on biological mechanisms to improve cardiorespiratory fitness. This study, which evolved from observations within our lab throughout the years of testing breast cancer patients, has confirmed previous thoughts that the survivor population prefers to walk during a maximal test, and when engaging in physical activity on a bicycle, the intensity decreases as well as motivation. Achieving the proper intensity and staying motivated are critical to adhering to a lifestyle change. The lower intensity and longer duration required to attain the desired results on a cycle ergometer may affect adherence and compliance rates.

As described in Table 2, the 17% difference in aerobic capacity as well as the differences in ventilatory threshold, heart rate, time to completion, and peak wattage reveals the inconsistency between 2 different maximal aerobic stress tests in the survivorship population. Cycling requires a different skill set than walking, and cycling is less relevant to the daily life of the general population.³⁹ This lack of skill could influence the results if using a Vo_2max test for a clinical diagnosis, for future clinical reference values, or for an exercise intervention. These variable results demonstrate how experience and local muscular fatigue may have been limiting factors during the cycling protocol and not central fatigue of the cardiorespiratory system, accordingly inaccurately portraying the patient’s level of aerobic fitness. Thus, an individualized exercise prescription that is based on a maximal aerobic stress test using a cycle ergometer may not prescribe a high enough intensity. This lower intensity level might be below the necessary threshold to induce the physiological changes required to produce the desired health benefits, such as weight loss or cardiovascular improvements.

Aerobic capacity is influenced by the recruitment of lean body mass, such that the treadmill can elicit greater oxygen consumption than on a cycle ergometer.^25,40 However, this 10% difference is not always seen in the athletic population,⁴¹ nor in certain clinical populations.²⁷ This study supports the notion that maximal aerobic stress testing in the breast cancer population is influenced by mode of exercise.

Ideally, maximal heart rate is equivalent between both modes of exercise tests but can vary depending on the age range and experience.²⁴ As illustrated in Figure 2, this study demonstrates that breast cancer survivors within a similar age range did not achieve equivalent heart rates when comparing different modes of maximal stress tests. The significant lower value in heart rate during the cycle ergometer test depicts that the women ended the test too early, possibly because of lower leg discomfort. This peripheral limitation was the main reason reported for ending the cycle ergometer test, while the treadmill test elicited the 2 responses associated with central limitations: total body fatigue and/or dyspnea. If heart rate is to be a main variable in an exercise prescription, the large difference in peak heart rates encourages the use of the treadmill for exercise testing.

Figure 2.

Average oxygen consumption versus heart rate obtained at each minute of exercise during 2 maximal aerobic stress tests using the treadmill (−) and the stationary bike (- - - )

Ventilatory efficiency is not a common tool used to assess the health of breast cancer patients, even though ventilation–perfusion mismatching can occur because of the toxicity of cancer treatments. This relationship has not been evaluated in the breast cancer population. Researchers in other clinical populations are being encouraged to look at ventilatory efficiency and not just aerobic capacity, because of its ability to provide independent and complimentary information in clinical settings as well as with interventions.^42,43 We had 2 morbidly obese (BMI > 35) women participate in our study, and because of their extreme results between tests, their data for ventilatory efficiency was excluded from our results. Depending on mode, their results produced reference values that categorized them into opposing health categories. Their abnormal results may have been a result from episodes of hyperventilation during the test. Future analysis of this relationship in the obese survivor population is encouraged. Age, sex,⁴⁴ and mode dependency have been previously demonstrated in healthy women.²² Further testing in breast cancer survivors with a larger sample size would be beneficial.

Eleven of the 12 subjects had little or no experience using a treadmill or a cycle ergometer—a common occurrence in this age range. The women in this group had varied fitness backgrounds (low to moderate) and a multitude of long-term side effects (cardiomyopathies, minor neuropathies, and arthralgias), yet all completed both maximal tests safely and preferred the treadmill test. It was noted that extra precaution, posttest, had to be taken when dismounting from the cycle ergometer (than with the treadmill). Women felt unsafe, even with assistance, when trying to dismount from the bike. An unexpected observation occurred during testing, which could affect future studies in the field of exercise oncology: subjects revealed that they would return to complete the treadmill test, but would be less likely to return to repeat the test on the cycle ergometer. This remark correlated with our 4 dropouts. All dropouts completed the test on the cycle ergometer first and did not return for the treadmill test.

The results from this study provide an argument that mode selection for aerobic stress testing is important for developing an appropriate exercise prescription required for this population. The survivorship population must feel comfortable with the stress test administered, so that accurate values can be attained and not underestimated. Basic safety awareness of the patient is always a priority when determining which testing modality to use.¹⁸ The use of a treadmill elicits higher levels of oxygen consumption in survivors, and this elevated value will allow for accurate clinical assessments and more efficient intensities to be prescribed during exercise intervention programs. This improvement in design could produce greater changes in cardiorespiratory fitness, weight loss, and overall health. These findings have implications for potential epidemiological studies, which may use aerobic capacity to develop reference values within the breast cancer population, for the design and interpretation of exercise interventions, and it highlights the importance to define exercise testing within special populations.

We recognize that this is a small sample size that limits us from generalizing this conclusion to all breast cancer survivors. We also recognize that this study was developed to gear toward individuals who were medically cleared to begin an exercise intervention. All women were capable of walking and did not suffer from metastatic disease or severe neuropathies.

Conclusion

This study demonstrates that a group of breast cancer survivors were able to undergo 2 maximal stress tests with no adverse outcomes. This article supports the notion that exercise mode can influence the outcome of maximal aerobic exercise tests in the breast cancer survivor population.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The research for this article was funded by a grant from the BC Sports Medicine Research Foundation. LBD is supported by a Doctoral Research Award from the Canadian Institutes of Health Research.

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Optimal Mode for Maximal Aerobic Exercise Testing in Breast Cancer Survivors

Abstract

Keywords

Introduction

Methods

Results

Discussion

Conclusion

Footnotes

Declaration of Conflicting Interests

Funding

References