Parkinson's disease (PD) is a progressive degenerative neurologic syndrome resulting in a myriad of movement disorders. Major movement problems associated with the disease include slowness of movement (bradykinesia), freezing or akinetic periods, tremor, decreased mobility related to muscular rigidity, as well as dyskinesias (involuntary movements) associated with antiparkinsonian medications. Although the movement disorders associated with PD can cause considerable impairment and disability, the leading causes of death for those having PD are respiratory complications such as pneumonia and cardiovascular diseases.(9).
Cardiovascular abnormalities that are commonly seen in those having PD include orthostatic hypotension, cardiac arrhythmia, and, less commonly, hypertension. In relation to cardiac arrhythmia, the age group most often effected by PD also has the greatest likelihood of cardiovascular disease. Therefore, distinctions between symptoms related to aging and those that might be associated with PD are not clearly made. Cardiac arrhythmia in individuals having idiopathic PD have also been associated with almost all antiparkinsonian medications. Although these medications may contribute to arrhythmia, studies to date have not resulted in definitive conclusions regarding cardiac toxicity as a result of antiparkinsonian medications (10,13,21,29,30).
Another cardiac problem associated with PD is compromised cardiovascular reflexes, which can cause abnormal cardiac responses. One of the abnormal responses in those having severe compromise of cardiovascular reflexes is a fixed pulse rate (11,15,23,30,31). In individual cases having a fixed pulse rate, the typical tachycardia that occurs in response to certain stimuli such as exercise, will not occur. Therefore, it may be very important to identify these individuals in order to more closely monitor ensuing cardiac problems.
In addition to the cardiovascular problems that may be experienced by those having PD, respiratory problems have been documented in the literature since the original works of Parkinson (22). Neu et al. (20) and Lilker and Woolf (14) determined that approximately 87% of the patients studied having PD also had obstructive pulmonary dysfunction.
Varied physiological changes or symptoms in individuals having PD influence the respiratory system directly or indirectly. The progressive muscular rigidity, which so frequently occurs, not only impacts the appendicular (peripheral) musculature, i.e., extremities but the axial skeletal musculature as well. Consequently, the rigidity and stiffness in the vertebral and surrounding thoracic musculature, including the rib cage and the muscles of respiration, may have a direct or indirect effect on normal respiration. In addition, involvement of the facial and cervical muscles, as well as throat and esophageal regions, may also affect normal respiration.
Maximum oxygen consumption (O2max) is the traditional laboratory assessment of an individual's aerobic capacity or cardiorespiratory endurance (2,4,24). O2max is "the amount of oxygen one utilizes during exhausting work" and is an objective measure of the circulatory system's maximal capacity to deliver oxygen (3,18,19). The more aerobically conditioned the individual, the greater the O2max and the greater the capacity for aerobic energy transfer. As a result, this higher aerobic capacity may translate into a greater ability to participate in various physical activities without excessive fatigue.
Time to maximal exercise can be considered an indirect measure of an individual's endurance capability (1). Cardiorespiratory endurance is a function of how long an individual can perform an activity by using large muscle groups. The longer one is able to exercise before reaching exhaustion or a maximal exercise level, the greater the expected O2max. Therefore, as O2max increases with exercise training, the timemax should increase and therefore can be used to estimate O2max(1).
Poor cardiorespiratory fitness has been linked with numerous disease processes and in particular to cardiovascular disease, which continues to be the number one cause of death for older North Americans (25). Of these cardiovascular-related deaths, coronary artery disease accounts for 80% of all deaths.
Although cardiorespiratory problems have been identified in those having PD, little research has been conducted assessing the aerobic capacity of, or the impact that aerobic exercise might have on those having the disease. Because cardiopulmonary complications are the leading causes of death in those with PD (9), it is important to assess the cardiorespiratory capabilities of those having the disease. In addition, it is also important to determine the aerobic capabilities in those having PD compared with healthy cohorts. This information could be important in helping health professionals more appropriately prescribe aerobic exercise for those having PD, in conjunction with the generally prescribed ROM and flexibility exercises, thus providing a more complete and thorough exercise regime.
The purpose of this study was to assess and compare the cardiorespiratory responses (O2max and timemax) of those having PD with a group of healthy normal individuals. Because the movement difficulties typically experienced by individuals having PD often lead to decreased activity levels and possible cardiorespiratory abnormalities, it was hypothesized that those individuals having Parkinson's disease would have lower O2max values and take less time to achieve this maximal level (timemax) as compared with healthy normals.
Subjects. Twenty individuals with Parkinson's disease and 23 healthy individuals were recruited from the Houston metropolitan area. Subjects were recruited over a 3-yr period for participation in two different studies. All subjects were volunteers and were selected based on the following criteria: 1) man or woman between the ages of 50 and 80 yr; 2) no existing or coexisting cardiopulmonary, musculoskeletal, neurologic, or acute or chronic systemic diseases; 3) ability to perform the exercise task; 4) subjects with PD diagnosed for at least 1 yr; and 5) subjects with PD within stages 2 or 3 of the Hoehn and Yahr disability scale (8). This study was approved by the Institutional Review Boards at Texas Woman's University and Baylor College of Medicine, Houston, TX; written informed consent was obtained from all subjects.
Instrumentation.O2max and timemax were measured using the Gould 9000IV Computerized Pulmonary Exercise Laboratory System (Gould Inc. Medical Products Division, Dayton, OH). This system has been tested for validity with an established refereed system showing correlations ranging from 0.972 to 0.992 for ventilatory exchange and 0.941 to 0.989 for O2(5).
The maximal exercise test was performed on an electronically braked bicycle ergometer. Heart rate was monitored using a NARCO physiograph (Narco Biosystems Model DMP-48, Houston, TX) with a standard CM-5 electrode placement (28) or the Quinton 4000 Stress test Monitor (Quinton Inc., Seattle, WA), using a 10-lead electrode configuration consisting of four limb electrodes and six pericardial leads.
Procedures. All subjects were recruited over a 3-yr period for two different studies. On the day of actual testing, explanation of the study and signing of consent forms were performed before all testing. For the day of testing, subjects were instructed to refrain from eating, drinking caffeine, and/or smoking for at least 3 h. Those individuals having PD were instructed to take their antiparkinsonian medications so that peak therapeutic response time would occur during the testing period.
On the day of testing, a medical history was taken for each subject. After the history, each subject received an explanation of all procedures and was prepped for the exercise test. Seat height on the stationary bicycle was adjusted for each subject to allow approximately 35° of knee flexion when the pedal was in the downward position. The breathing apparatus was then placed on the face of the subject and a 2- to 3-min time period was allowed for familiarization to the equipment. Once the individual was ready, a 1-min warm-up was done consisting of 50 revolutions per minute (rpm) at 20 W of resistance on the bicycle.
The incremental exercise protocol after the 1-min warm-up consisted of 2-min stages starting at 40 W with an increase at the end of each stage by 20 additional W. Each subject was instructed to exercise for as long as possible and to indicate by raising one hand when they could no longer maintain the RPM at 50 or continue to pedal. Oxygen consumption, measured in mL·kg−1·min−1, and respiratory exchange ratio (R) values were recorded every 20 s. Heart rate was monitored continuously throughout the exercise and was recorded the last 10 s of each 2-min stage and used as definitive data.
Exercise was considered to be at a maximal level if two of three of the following criteria were met: 1) HR was ±10 beats per minute of age predicted HRmax, 2) R value ≥1.10, and 3) subjective maximal fatigue was indicated by the subject. Verbal encouragement was given to all subjects during the higher levels of exercise. If the subject was within a stage of the exercise protocol when the signal to stop was given, they were encouraged to finish that stage if possible.
Once the subject indicated he/she must stop, resistance was decreased to zero, and the subject was instructed to continue pedaling at a self-selected slower rate for a 5-min cool-down. During this time heart rate was continuously monitored.
Maximum oxygen consumption was considered to be the highest value attained during the last stage of exercise with a corresponding R value ≥ 1.10. Time to maximal exercise was measured by the computerized clock and was considered to be the total time exercised minus the 1-min warm-up.
Data analysis. Dependent variables were O2max and timemax. It has been established that men and women of the same age and fitness level attain different O2max values due to gender differences (27). Therefore, all comparisons were made between subjects of like gender. Because the assumption of homogeneity of variance was not met for the dependent variable O2max in women, the nonparametric Wilcoxon-Mann-Whitney-U analysis was used. All other group comparisons were analyzed using an independent t-test. A Bonferroni adjustment was applied for multiple univariate comparisons between groups (2) for men and women, resulting in an alpha of ≤0.025 (7).
Descriptive statistics for each group include age, disease duration, number of medications, Hoehn and Yahr score, exercise performance predicted by workload normalized to body size, and percentage of predicted O2max attained.
All subjects recruited over the 3-yr period were included in the data analyses: 20 men (PD = 13, HN = 7) and 23 women (PD = 7, HN = 16). Table 1 provides the demographics for all subjects. The average number of different antiparkinsonian medications taken each day for the PD group at large was 3 (±1). The median score for the Hoehn and Yahr scale was 2.5 for both men and women. A Hoehn and Yahr of 2.5 means the individual has "mild bilateral disease, with recovery on pull test" (6).
Comparisons of O2max measures for both men and women resulted in no significant differences. For the male PD and HN individuals, the independent t-test resulted in mean values for O2max of 23.52 (±6.49) vs 25.46 (±5.10) mL·kg−1·min−1, respectively, P = 0.50 (Table 2). For the female subjects, the Wilcoxon-Mann-Whitney-U resulted in median values of 20.10 vs 16.20 mL·kg−1·min−1 for the PD and HN group, respectively, P = 0.35 (Table 3).
Predicted maximum was calculated for each subject using the formula outlined by ACSM for leg ergometry (1). This value was then used to determine the percentage of predicted O2max attained by each subject. Results indicated that male subjects with PD attained 104% of their predicted value whereas those without PD attained 93%. For the women, those with PD attained 101% of predicted value whereas those without PD attained 88%.
Relative workload was calculated by normalizing workload to body size (W·kg−1). Values for men was 1.55 W·kg−1 for those with PD compared with 1.95 W·kg−1 for those without PD. For women, those with PD had 1.24 W·kg−1 compared with those without PD having 1.27 W·kg−1. Independent t-tests resulted in no significant differences between groups for men or women (P = 0.07 for men, P = 0.84 for women).
For timemax, the independent t-test analysis resulted in significant differences between the PD and HN men (Table 2). The mean values were 9.5 vs 13.1 min for PD vs HN, respectively (P = 0.02). Comparisons of timemax for the female subjects did not result in significant differences (mean values 5.2 vs 5.4 min, respectively, P = 0.84; Table 2).
In this study, which assessed and compared the O2max and timemax of individuals having PD and those considered to be healthy normals, the statistical results indicated that the O2max for men and women having PD was not significantly different than the O2max of individuals without the disease. Results did indicate that male individuals with PD took less time to reach O2max than those without the disease. For the women, the time it took to achieve O2max was no different than the time it took for the healthy individuals to achieve the same. Maximal relative workload was also the same between the male groups and between the female groups. For percentage of predicted O2max attained, the groups were also comparable.
Shephard (27) has suggested that the mechanical efficiency of movement decreases as we age and results in an increased energy expenditure. In relation to this, the movement disorders experienced by many having PD may also cause an additional mechanical inefficiency of movement, thereby increasing the required energy expenditure even further for any particular task. An example of this cumulative inefficiency could be when a person with PD has moderate to severe muscular rigidity in the lower extremities, particularly in the pelvic and hip regions. Under these circumstances, the demands for energy to pedal the bike could be greater for the person having PD who has to overcome the rigidity than for a healthy individual having no muscular rigidity to overcome. Therefore, the person having muscular rigidity as a primary symptom of PD might expend more energy during the task, which would be reflected in higher submaximal and maximal O2 values. Thus, the individual with PD might have a O2max value comparable to a healthy cohort although the level of O2 is reached sooner. This would also be reflected in submaximal O2 values, which would be higher at any comparable stage for the individual with PD as compared with the healthy individual.
A summary of submaximal oxygen consumption values by stage and group is presented in Figures 1 and 2. For the men (Fig. 1), in stages warm-up through VI, those having PD had higher oxygen consumption values for each stage. As indicated in the between-group comparisons of O2max, the PD subjects as a whole were unable to exercise as long in comparison with the HN subjects. In stage VI, 39% of the PD subjects completed the stage compared with 86% of the HN subjects. Even so, the PD subjects had a higher value in stage VI. Comparisons between the female subjects indicate that the subjects with PD had higher oxygen consumption values in stages I-III with 71% of those with PD completing the stage compared with 56% of the HN subjects. These results coincide with previous findings by Protas and colleagues (26).
Research assessing the resting energy expenditure in parkinsonian patients compared with healthy normals indicates that those with PD have significantly higher resting energy expenditure values both on and off antiparkinsonian medications (21.8% on, P < 0.01 and 50.8% off, P < 0.05) (12,16). In fact, the increase in resting energy expenditure is greater when off medications and appears to be related to the severity of muscular rigidity experienced by the individual. In addition, the increase in resting energy expenditure is even more significant when the individual experiences dose-related dyskinesias. In one such case, the resting energy expenditure was increased by as much as 140% (16). In addition, these researchers reported there was no increase in pulse rates associated with the increase in resting energy expenditure.
In this study, all parkinsonian subjects were instructed to take their antiparkinsonian medications so that they would be at peak-dose levels during the bicycle test. Consequently, several of these subjects experienced some degree of peak-dose dyskinesias (both men and women) at the time of the maximal exercise test. Therefore, it is possible that the associated dyskinesias created a mechanical inefficiency in the task-specific movement, which further increased energy expenditure levels. Consequently, this resulted in higher submaximal values for those with PD when compared with HN men and comparable O2max values although achieved in less time by those with PD. For the women, even though there were no statistical differences for O2max and timemax values, the women with PD had a clinically higher O2max achieved in the same amount of time as HN. Submaximal values for the women with PD were also higher; therefore, one could speculate that women having PD might also have increased resting energy expenditures and/or mechanical inefficiency of movement during exercise testing resulting in higher submaximal and maximal oxygen consumption values.
Even though dyskinesias are uncontrollable involuntary movements, it is not unusual that those experiencing dyskinesias will try to control the abnormal movements in some way to accomplish normal patterns of movement. In cases of violent dyskinesias, the task being performed might be trying to sit still in a chair. It also seems likely that abnormal, involuntary movements could certainly create a mechanical inefficiency whenever a person tried to perform voluntary movements. Therefore, it is speculated that the energy expenditure used to try and overcome the involuntary movements is greatly increased for those patients having dose-related dyskinesias.
There are several points that should be discussed in relation to these data. First, it is possible that a Type-II error has occurred. The chances of there being a Type-II error are high because of low power for all comparisons due to the small sample sizes and the difference in the amount of variance that exists within each group. When sample sizes are small and exhibit considerable and unequal variance within and between the groups, power is decreased thus increasing the chance of a Type-II error. Therefore, it is possible there is a statistical difference between the groups for O2max, but there is not enough power to detect the difference.
Second, it is possible that the values attained during this study were not truly maximal and represent peak O2 (O2peak) values. Peak O2 is the highest value of oxygen consumption attained during an exercise test when the criteria for O2max are not met (17). The decision to define the values as O2peak is also made when the performance of the test appears to be limited by "local factors" instead of "central circulatory dynamics" such as quadriceps fatigue during a stationary bicycle test. In relation to the female subjects tested in this study, 100% of the PD subjects did not meet at least one of the criteria set for attaining a O2max; 29% of the sample did not meet two of the criteria. Therefore, the values attained by the female subjects having PD may represent O2peak not O2max. For the HN female subjects, 38% of the sample did not meet at least one of the criteria. None of the HN sample failed to reach two of the criteria. In relation to male subjects, 69% of the subjects having PD did not meet at least one of the criteria; 8% (one subject) did not meet two of the criteria. For the HN subjects, 29% of the sample did not meet one of the criteria with one of these individuals not meeting two of the criteria. The criteria that most PD subjects failed to meet was that of HRmax. For the HN subjects, the criteria not met was evenly distributed between HRmax and the R value.
In relation to the results for male individuals, although O2max did not appear to be significantly different between those with PD and HN, the comparison of timemax indicates that those with PD are unable to exercise as long before reaching O2max. Thus, the data must be analyzed in its entirety in order to identify that those with PD compared with HN are not similar in relation to cardiorespiratory fitness. For the women, although those with PD had a higher O2max, no statistical differences were found for either O2max or timemax between those with PD and those considered to be healthy. For both the men and women, the values for oxygen consumption probably represent O2peak instead of O2max.
Based on the results of this study, it is concluded that individuals with PD, similar to those in this study, would be able to accomplish a maximal or submaximal exercise test using a stationary bicycle. To increase the chances for the test to be maximal, it is recommended that there be more than one trial in order to familiarize the individual with the testing procedures. In addition, it is recommended that as many variables as possible in relation to cardiorespiratory fitness be taken into account when assessing individuals with PD, i.e., heart rate, R values, time to maximal exercise, etc. This appears to be important in order to characterize an individual's true response to submaximal and maximal aerobic exercise. It is also important if comparing those with PD with age-matched healthy normals.
In addition, it is important to indicate under what conditions individuals with PD are tested, i.e., on or off antiparkinsonian medications, as well as assessing the severity of rigidity and peak dose dyskinesias. It is possible these factors may affect the response to aerobic exercise in those having PD.
Although the statistical results of this study may be unclear and open to interpretation, the results do indicate that when assessing individuals with Parkinson's disease during aerobic exercise it is important for the health care provider to do a thorough cardiorespiratory evaluation. If one were to assess only O2max values as attained in this study, one could conclude that those individuals with PD have similar cardiorespiratory fitness levels as HN of the same age. Only upon thorough evaluation of all the data, including submaximal oxygen consumption values, is it possible to conclude that these two populations are not comparable clinically.
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Keywords:© 1999 Lippincott Williams & Wilkins, Inc.
PARKINSONISM; CARDIORESPIRATORY; PEAK EXERCISE; OXYGEN CONSUMPTION; SUBMAXIMAL EXERCISE