Eur J Appl Physiol(1992) 64:487-492

Applied Physiology and Occupational Physiology © Springer-Verlag1992

The effect of training on endurance and the cardiovascular responses of individuals with paraplegia during dynamic exercise induced by functional electrical stimulation Jerrold S. Petrofsky mand Ralph Stacy m 1 PetrofskyCenter for Rehabilitation and Research, Irvine, California, USA 2 National Center for Rehabilitation Engineering, Wright State University, Dayton, Ohio, USA Accepted November 26, 1991 Summary. Endurance for dynamic exercise, cardiac output, blood pressure, heart rate, ventilation, and oxygen consumption was measured in eight individuals with paraplegia at the end of 4-rain bouts of exercise on a friction braked cycle ergometer. Movement of the subjects' legs was induced by electrically stimulating the quadriceps, gluteus maximus and hamstring muscles with a computer-controlled biphasic square - wave current at a frequency of 30 Hz. The friction braked cycle ergometer was pedalled at work rates which varied between 0 and 40 W. Measurements were repeated after 3 and 6 months to assess the affect of training. After 3 months of training it was found that endurance increased from 8 min at a work rate of 0 W to 30 min at a work rate of 40 W. Compared to the cardiovascular responses in non-paralyzed subjects, computerized cycle ergometry was found to be associated with higher relative stresses for a given level of absolute work. Mean blood pressure, for example, increased by over 30% during maximal work in individuals with paralysis compared to the typical response obtained for ablebodied subjects. Analysis of the data showed that instead of the 20-30% metabolic efficiency commonly reported for cycle ergometry, the calculated metabolic efficiency during computer-controlled cycle ergometry was only 3.6%. Key words: Exertion - Exercise - Paralysis - Paraplegic - Spinal cord injury

Introduction A spinal cord injury (SCI) can result in the inability to move muscles voluntarily, damage to the autonomic nervous system, and an impairment of the ability to feel (Guttman 1976). Although the loss of movement may be the most obvious symptom of SCI, the secondary Offprint requests to: J. S. Petrofsky,3765 Alton Parkway, Suite E, Irvine, CA 92718, USA

medical complications of the injury have the greatest impact on the health and mortality of the patient (Sunderland 1968; Guttman 1976; Foege 1985). For example, a recent publication of the National Research Council has listed pressure sores following SCI as the biggest medical problem in America today (Rurke and Murray 1975; Young et al. 1982; Foege 1985; Kennedy et al. 1986; Petrofsky 1991). Computer-controlled electrical stimulation used to induce exercise in paralyzed muscle has been used to try and reduce some of the above problems (Levine et al. 1985). This technology involves the use of functional electrical stimulation (FES) of paralyzed muscles to exercise the paralyzed part of the body (Petrofsky et al. 1983a, b, 1984). In addition to the obvious increase in muscle mass which FES exercise can induce (Vrbova 1963; Van der Meulen et al. 1974; Brown et al. 1976), FES exercise stresses the cardiorespiratory system (Petrofsky et al. 1983a, b, 1984, 1985). Preliminary reports point to an average reduction of over 50% in medical costs when SCI patients exercise on these types of devices (Petrofsky and Smith 1988; Petrofsky 1991). Cycle ergometry has always been a good form of exercise for the conditioning of muscles, the cardiovascular and the respiratory systems (Simonson 1971; Sawka 1976; Astrand and Rodahl 1977). Research on the physiology of cycling and its metabolic demand on the body dates back to the turn of the century with classic studies such as the ones reported by Benedict and Cathcart (1912). From these and later studies (e.g., Petrofsky et al. 1976), it is generally accepted that cycling has a metabolic efficiency of 20-30%. During cycling, the mean blood pressure usually increases very little since the increase in systolic blood pressure is matched by a reduction in the diastolic blood pressure (Astrand and Rodahl 1977). The heart rate, which is directly related to the intensity of the work being accomplished, may exceed 180 beats.min -1 during maximum exercise. Cardiac output, which increases in direct proportion to the workload, has been observed to be as high as 25 1. min-1 in extremely well-trained cyclists (Astrand and Rodahl 1977).

488 I n t h e last few years, cycling h a s b e e n i n d u c e d in the p a r a l y z e d t h r o u g h c o m p u t e r - c o n t r o l l e d e l e c t r i c a l stimulation. E l e c t r i c a l s t i m u l a t i o n has b e e n a p p l i e d to the q u a d r i c e p s , t h e h a m s t r i n g , a n d the g l u t e u s m a x i m u s a n d g l u t e u s m e d i u s m u s c l e g r o u p s to elicit c y c l i n g in the p a r a l y z e d o n a s t a t i o n a r y cycle e r g o m e t e r (Pet r o f s k y et al. 1982, 1983a, b, 1984). A l t h o u g h a n u m b e r o f studies h a v e b e e n p u b l i s h e d o n t h e b l o o d p r e s s u r e a n d h e a r t rate r e s p o n s e s d u r i n g c o m p u t e r - c o n t r o l l e d f r i c t i o n b r a k e d c y c l i n g ( P e t r o f s k y a n d P h i l l i p s 1983, 1984; R a g n a r s s o n et al. 1988), the w o r k l o a d s i m p o s e d b y t h e cycle h a v e b e e n quite low (5 W) a n d little h a s b e e n d o n e to t r a i n i n d i v i d u a l s to a c h i e v e h i g h e r t o l e r ances for exercise. S C I c a n cause s i g n i f i c a n t d a m a g e to t h e a u t o n o m i c n e r v o u s s y s t e m ( G u t t m a n 1976), a n d assessing t h e c a r d i o v a s c u l a r stress d u r i n g h e a v y e x e r c i s e in S C I i n d i v i d u a l s is i m p o r t a n t to c o r r e c t l y e v a l u a t e t h e p o t e n t i a l risks o f this t y p e o f t h e r a p y . T h e p u r p o s e o f the p r e s e n t i n v e s t i g a t i o n was to e x a m i n e t h e c a r d i a c o u t p u t , b l o o d p r e s s u r e , h e a r t rate, o x y g e n c o n s u m p tion, a n d v e n t i l a t i o n in eight i n d i v i d u a l s w i t h p a r a p l e g i a o n a n F E S cycle e r g o m e t e r a n d to d e t e r m i n e w h a t effects e x t e n s i v e p h y s i c a l t r a i n i n g w o u l d h a v e o n t h e i r c a r d i o r e s p i r a t o r y systems.

Methods Subjects. The subjects in these studies were eight volunteers with paraplegia whose ages ranged between 19 and 26 years. Their average weight (SD) was 72 (0.6) kg. The level of SCI was limited in these studies to complete injuries between the 4th and the l l t h thoracic vertebrae (T4-T11). All procedures were approved by the Committee on Human Experimentation and all experimental procedures were explained to each subject, who then signed a statement of informed consent. Heart rate. Heart rate was measured from a continuous recording of the electrocardiogram (ECG). Two electrodes were placed in the limb lead II position. Continuous recordings of the ECG on a Hewlett Packard data recorder were then used to measure the heart rate during the exercise by counting QRS complexes over 15-s period. Blood pressure. Blood pressure was measured by auscultation of the right arm. The same observer measured the blood pressure on each subject approximately every 30 s throughout and following the exercise. Oxygen consumption and cardiac output. Oxygen consumption and cardiac output were measured on a pulmonary function analyzer (Gould 9000). The Gould 9000 also had the ability to measure cardiac output by the carbon dioxide rebreathing technique. Cardiac output was measured approximately, every 15 s. The analyzer was calibrated both before and after each experiment. All gas volumes were reduced to standard conditions. Cycle ergometry. Cycle ergometry was accomplished on a modified Monark friction braked cycle ergometer similar to one described previously (Petrofsky et al. 1982, 1983a, b, 1984). The cycle, as shown in Fig. 1, was modified with a highback seat and seat belts to allow subjects with paralysis to sit on the seat comfortably and safely. Knee stabilizer bars were added so that exercise could be accomplished without abduction or adduction of the hips. Special adaptive shoes were used to hold the feet on the pedals. Finally, a sensor was placed on the crankshaft of the cycle to

Fig. 1. The modified Monark cycle ergometer

Table 1. Effects of training on performance Pre-train Maximum endurance 8.3 rain 0 W Blood pressure (kPa) 23/13.3 Heart rate (beats.min -1) 145 Ventilation (1.rain-l) 63

3 Months

6 Months

30 rain 40 W

30 min 55 W

21.4/12.4

19.6/8.6

139

121

89

81

The conditions for the cardiovascular data were: pretrain - 4th min exercise at 0 W; 3 months train - 4th min exercise at 40 W; 6 months train - 4 t h rain exercise at 40 W

provide information as to the position of the legs for a digital computer. The timing of the electrical stimulation to the various muscle groups was computer controlled, the muscles stimulated in these studies were the quadriceps, hamstrings, and gluteus maximus muscles. Three electrodes were placed over each respective muscle group, with the reference electrode being applied over the center of the muscle and the active electrodes being applied diagonally across the ends. The 350-~ts biphasic square wave stimulation that was applied to the electrodes was varied in current from 0 to 180 mA and the frequency was kept constant at 35 Hz. A more detailed description of the cycle and the computer programs is given elsewhere (Petrofsky et al. 1982, 1983a, b, 1984). Training. After SCI, paralyzed muscles generally have only a fraction of the strength necessary to pedal a cycle ergometer. Therefore, a comprehensive training program was needed to accomplish the present investigation. Initially all patients started the training period with computer-controlled weight lifting. After an initial physical examination including radiography, magnetic resonance imaging, pulmonary function test and blood chemistry, each patient began exercising his quadriceps, hamstring and gluteus maximus mucles on specially designed weight-lifting equipment. The weight-lifting equipment, which has been described previously (Petrofsky et al. 1982, 1983b; Petrofsky and Smith 1988), used computer-controlled electrical stimulation of the paralyzed muscles. The initial load lifted by the muscle was 1.5 kg. The muscle contracted to lift the weight over a 3-s period, hold the load for 1 s, and then slowly reduce tension over another 3-s period; 6 s were allowed between contractions. This exercise regime was continued for a period of up to 15 min each day for each muscle group. When 15 rain of exercise against a target weight could be accomplished, the weight was increased by 0.5 kg the next day. Once subjects could lift 7 kg for 15 rain, they began

489 the computer-controlled friction braked cycle program. For the subjects in these studies, weightlifting was accomplished for a period of between 4 and 6 weeks. Computer-controlled cycling was done by having subjects sit on a modified Monark cycle ergometer, as described above, while electrical stimulation was applied to the quadriceps, hamstring and gluteus maximus muscles. The sequence of activation of the muscle groups was set by a computer so that smooth, dynamic exercise could be accomplished at a speed of 50 rev. min-~. Subjects initially started at a work rate of 0 W. When cycling could be accomplished for 1 h at 0 W, the exercise was increased in 5-W increments. Training progressed until patients could pedal the cycle ergometer for a period of 15 min at a work rate of 40 W. In practical terms, this took a minimum of 2 months and a maximum of 3 months for these subjects. Training was continued for 3 months in all individuals.

Heart rate (beats per minute) 16o 140 .

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Statistical analysis. All data were subjected to simple descriptive analysis which supplied means, standard errors, standard deviations, and indications of skewness of kurtosis. Data obtained for different conditions were compared using an unpaired Student's t-test. The P value associated with the t tests was obtained from standard statistical tables. A one-tailed analysis was assumed, and a P value equal to or less than 0.05 was considered statistically significant.

Results Training resulted in changes in both endurance and cardiovascular responses. When individuals first began cycling, the endurance was quite low. The average endurance (SD) was 8.3 (2.6) min for the first cycle session at a work rate of 0 W despite the fact that the muscles had been pretrained by weightlifting. At the end o f 3 months o f training, all subjects were able to pedal the cycle ergometer at a work rate of 40 W for at least 30 min. By the end of the 6-month training period, all individuals could pedal the cycle ergometer at a work rate o f 55 (8) W for at least 30 rain. These increases in endurance were statistically significant ( P < 0.01). The relationship between heart rate and work rate in trained individuals is shown in Fig. 2. As can be seen, there is an approximately linear relationship between heart rate and work rate imposed by the cycle ergometer. From a resting heart rate o f approximately 70 beats, m i n - 1 , heart rate increased directly in relation to the work rate such that when pedalling the cycle ergometer at a work rate of 40 W, the heart rate at the end o f a 3-month training period was 139 beats, min-1. It is interesting that the rate at the end of the initial cycle session at the start of training was much higher. At the end of this first session at a work rate o f 0 W the aver-

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Experimentalprocedures. Once training had been completed, each of the subjects accomplished a modified Balke exercise protocol as described previously (Petrofsky et al. 1975). Each subject pedalled the cycle ergometer for periods of 4 min. During the 3rd and 4th min, oxygen consumption, blood pressure, heart rate, cardiac output, and ventilation were measured. Five minutes were then allowed for recovery of muscle function. The protocol was repeated at work rates of 0, 5, 10, 15, 20, 25, 30, 35 and 40 W. Each experiment was performed in replicate. The order of presentation of the tensions was selected at random so as not to bias the data. An additional 3 months of training was then carried out, and the experiments were repeated a second time.

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Fig. 2. Relationship between heart rate and work rate in eight subjects with paralysis. Each point is the mean of 16 experiments. Data were obtained following 3 and 6 months of training Blood pressure (mmHg) 200 i

50( 0

REST

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Fig. 3. Relationship between blood pressure and the work rate sustained during cycling. Each point shows the mean of 16 experiments. Data were obtained after 3 and 6 months of training

age heart rate and endurance was 145 (11) beats, m i n - 1 and 8 min respectively. In contrast, after an additional 3 months of training, the heart rate was 121 (9.2) b e a t s - m i n - 1 after 4 min of pedalling at a work rate of 40 W. The differences between heart rates after 3 and 6 months of training were statistically significant (P0.05) for the 3- and 6month training periods. However, at work rates of 20, 25, 30, 35 and 40 W, the values recorded after 3 and 6 months of training were statistically different ( e < 0.05). Diastolic blood pressure was also linearly related to work rate. However, as can be seen in Fig. 3, although the diastolic blood pressure was directly related to the work rate after 3 months of training, by the time 6 months of training had elapsed it was inversely related to the work rate. For example, although the resting diastolic blood pressure in the subjects averaged 9.8 (0.9) kPa, at the end of the 3-month training period, work accomplished at 40 W resulted in an average diastolic blood pressure of 12.8 (1.2) kPa. In contrast, after 6 months of training, a similar work rate resulted in a diastolic pressure of 8.8 (1.4) kPa at the end of the 4 min of work; these differences were statistically significant ( P < 0.01). Oxygen utilization during work is shown in Fig. 4. As can be seen, there was a linear relationship between oxygen consumption and work rate for the 4-min bouts of exercise. There were no statistically significant differences between the oxygen consumption for any work rate after 3 and 6 months of physical training when comparing the oxygen costs of exercise at similar level of work. However, oxygen consumption for all levels of work was high. For example, a work rate of only 40 W required a mean oxygen consumption of 2.5 (0.2) l.min -1. When the oxygen costs were converted to work (RQ was 4.6) and the efficiency calculated, efficiency was only 3.6%. Like oxygen consumption, cardiac output was linearly related to work rate (Fig. 5). The highest mean (SD) cardiac output recorded was 11.1 (2.6) 1.min -1 after 4 min of exercise at a work rate of 40 W after 6 months o f physical training. There was no significant difference between the cardiac outputs measured at the 3- and 6-month training periods at the same level of work. However, the maximum cardiac output in the 8min exercise session at the 1st day of training averaged only 8.1 (1.2) 1.min -1. Further, although data is only shown for a work rate of 40 W to compare the 3- and 6-month training data, the maximum cardiac output when exercising against a resistance of 55 W after 6 months of training averaged 14.3 (2.7) 1-min -~. Like blood pressure and heart rate, there was a linear relationship between the ventilation and work rate (Fig. 6). From a resting ventilation of about 10 (2) 1. min-1, the maximum ventilation recorded at the end of exercise at 40 W after 3 months of training averaged 89 (12) l-min -1, whereas after 6 months of training, ventilation was reduced to 81 (8) 1. min-~; these differences were statistically different (P

The effect of training on endurance and the cardiovascular responses of individuals with paraplegia during dynamic exercise induced by functional electrical stimulation.

Endurance for dynamic exercise, cardiac output, blood pressure, heart rate, ventilation, and oxygen consumption was measured in eight individuals with...
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