Eur J Appl Physiol (1992) 64:503-507
Applied Physiology European Journal of
and Occupational Physiology © Springer-Verla9 1992
Thermoregulatory stress during rest and exercise in heat in patients with a spinal cord injury Jerrold S. Petrofsky Petrofsky Center for Rehabilitation and Research, Irvine, California; Wright State Lfniversity,Dayton, Ohio; and Universityof California, Irvine, California, USA Accepted January 25, 1992
Summary. Twelve subjects with spinal cord injuries and four controls (all male) were exposed to heat while sitting at rest or working at each of three environmental temperatures, 30, 35 and 40 ° C, with a relative humidity of 50%. Exercise was accomplished at a load of 50 W on a friction-braked cycle ergometer which was armcranked or pedalled. Functional electrical stimulation of the legs was provided to the subjects with quadriplegia and paraplegia to allow them to pedal a cycle ergometer. The data showed that individuals with quadriplegia had the poorest tolerance for heat. As an example, in this group, accomplishing armcrank ergometry while working at an environmental temperature of 40°C resulted in an increase in aural temperature of 2 ° C in 30 min. The aural temperature of individuals with paraplegia working for the same length of time under the same conditions rose approximately I°C. There was virtually no change in the aural temperature in the control subjects. Key words: Exercise - Thermoregulation - Heat stress Paraplegia - Quadriplegia
Introduction A spinal cord injury (SCI) usually results in permanent paralysis below the level of the lesion. Although the loss of voluntary movement is the most obvious problem seen in individuals with SCI, the secondary problems associated with damage to the autonomic nervous system cause the greatest medical consequences (Guttman 1976). Such secondary medical problems can include pressure sores, kidney and bladder infections (Young et al. 1982), and thermoregulatory impairment (Hutchinson 1875; Paget 1885; Guttman 1976; Attia and Engel 1983; Sawka et al. 1989). Because damage can occur to both peripheral temperature sensors and the ability to Offprint requests to: J. S. Petrofsky, Petrofsky Centers for Rehabilitation and Research, 13765 Alton Parkway, Suite E, Irvine, CA 92716, USA
sweat, SCI individuals become partially poikilothermic (Guttman et al. 1968; Downey et al. 1967, 1969, 1973, 1976; Attia and Engel 1983). When muscle temperature is allowed to vary, endurance can be effected (Petrofsky et al. 1981). The damage to the autonomic nervous system in SCI individuals seems to affect both sweating and the ability to vasoconstrict and vasodilate the peripheral vasculature. Therefore, it is not simply heat exposure, per se, that results in thermoregulatory difficulties. Pollock et al. (1951) have clearly shown that even immersion of an SCI individual in a warm water bath can have serious thermoregulatory consequences due to the lack of control of the peripheral circulation exhibited by such individuals. There is also evidence that individuals with paraplegia or quadriplegia may have a different thermoregulatory set point than able-bodied individuals (Downey et al. 1969; Attia and Engel 1983). This set point was suggested in studies by Atria and Engel (1983) to be variable and a function of the ambient conditions. It was viewed by these workers as an adaptive thermoregulatory process following SCI. In recent years, increasing emphasis has been placed on exercise in SCI individuals. Typically, exercise has been conducted with voluntary armcrank ergometry (Glaser et al. 1983, 1986). More recently, however, functional electrical stimulation (FES) has been used to exercise paralyzed leg muscles. Aerobic cycle ergometry exercise has been extensively investigated in paraplegics and quadriplegics using electrical stimulation to exercise the quadriceps, hamstring and gluteus maximus muscles (Petrofsky et al. 1983a, b, 1984, 1991). In addition, isokinetic exercise of paralyzed muscles in the lower body has been extensively used for the conditioning of paralyzed muscle (Petrofsky et al. 1982, 1985a, b; Petrofsky and Smith 1988). FES exercise is now becoming widespread as an accepted modality in rehabilitation centers for SCI individuals (Ragnarsson et al. 1988; Petrofsky 1992). However, the effect of computer-controlled exercise in relation to heat exposure has not been investigated. Since FES cycle studies have shown that metabolic demand can cause cardiac output to be over 15 1min -1 (Petrofsky and Smith 1988), the implication
504 is t h a t it m a y i n d u c e a c o n s i d e r a b l e h e a t l o a d d u e t o t h e high metabolism associated with the work. I n t h e p r e s e n t i n v e s t i g a t i o n , e x p e r i m e n t s o n ablebodied (control), paraplegic and quadriplegic individuals w e r e c a r r i e d o u t t o s t u d y t h e r m o r e g u l a t o r y stress resulting f r o m rest a n d exercise d u r i n g h e a t e x p o s u r e .
Methods Subjects. The subjects in these studies were all males. Six had paraplegia, 6 had quadriplegia, and 4 were able-bodied controls. The average of the control group was 22.7 years, whereas that of the group with SCI was 23.4 years. The paraplegic group had complete SCI between T3 and T12; the quadriplegic group had injuries which were complete and located between C6 and C8. Subjects were medically examined prior to the studies and signed a statement of informed consent. All experimental procedures and protocols were approved by the Committee on Human Experimentation. Sweat rates. Sweat was collected in capsules over 2-min periods. The capsules had a surface area of 200 mm 2. They were located on the forehead, chest, thigh (above the quadriceps muscle) and forearm, and held in place with an elastic band. A circular piece of paper was put into the capsule and removed at 2-min intervals. The paper was weighed before being put into the capsule and after removal. The change in mass was used to calculate the sweat over that area. Body mass was recorded on a specially designed scale with an accuracy of plus or minus 1 g both before and after heat exposure under each of the experimental conditions. The change in body mass over a given time was used to calculate mean sweat rates (mass loss in 1 rain/body surface area = mean sweat rate/rain). Heart rate. Heart rate was measured by continuous ECG recordings. Electrodes were placed in the limb lead 2 position, and the ECG was continuously recorded throughout the heat exposure. Heart rate was counted from 15-s ECG recordings. Exercise on cycle ergometry under computer control. Cycle ergometry was accomplished on a modified cycle (Monark; Fig. 1) similar to one described previously (Petrofsky et al. 1983a, b, 1984, 1985a, b). The cycle was modified with a high-back seat and seatbelts to allow paralyzed subjects to sit comfortably. To protect the hips and knees from severe inward and outward rotation during cycling, knee stabilizers bars were added so that the exercise could be accomplished without abduction or adduction at the
Fig. 1. Computer-controlled exercise bike
hips. The knee stabilizer bars were secured to the leg by Velcro straps, as shown in Fig. 1. Special shoes were added with Velcro on the bottoms so that the feet could be secured to the pedals. A sensor was placed on the pedals so that the position of the pedals could be used as an input for a digital computer. The computercontrolled timing of the electrical stimulation to the quadriceps, hamstring and gluteus maximus muscles was such that cycling could be elicited. Three electrodes were placed over each respective muscle, with the reference electrode being applied over the center of the muscle and the active electrodes being placed diagonally across the ends. The 350-gs, biphasic square-wave stimulation that was applied sequentially across the three electrodes (Rack and Westbury 1969; Petrofsky et al. 1976, 1979) was varied in current from 0 to 180 mA at a frequency of 35 Hz. A more detailed description of the cycle ergometer is provided elsewhere (Petrofsky et al. 1983a, b).
Armcrank ergometry. Armcrank ergometry was accomplished on a friction-braked armcrank ergometer (Monark). A timer kept pace so that cycling could be accomplished at 50 rev. min-1 at a load of 50 W. The ergometer was modified to reverse the normal (forward) direction of rotation. This was necessary because the lack of the triceps surae muscles in quadriplegics makes normal cranking difficult. Reversing direction allows the non-paralyzed biceps muscles to be used. This mode of cranking was used by all three groups of subjects. Measurement of aural temperature. Aural temperature was measured by using a thermistor temperature probe (Yellow Springs Instruments, Yellow Springs, Ohio) placed near the eardrum. A cotton wick was used to hold the probe in place and provide insulation. The output of the temperature probe was transduced through a Wheatstone Bridge which was then amplified with a DC amplifier and recorded on a flatbed recorder (Houston Instruments, Houston, Tex.). Stat&tical analysis. Statistical analysis involved the calculation of means, standard deviation, analysis of variance, and t-tests. The level of significance was chosen as P < 0 . 0 5 . Training. After SCI, paralyzed individuals have so little strength in their muscles that they cannot accomplish computer-controlled cycling for more than a few seconds a session (Petrofsky et al. 1983a, b, 1984, 1985a, b). Therefore, a comprehensive training program was needed to accomplish the present investigation. Each subject began by exercising his quadriceps, hamstring, and gluteus maximus muscles on specially designed weightlifting equipment. The muscles performed isokinetic exercise, lifting ankle weights for 3 s of flexion, 1 s of hold, and 2 s of extension; 6 s were allowed between contractions. This protocol was accomplished for 30 rain. day-a, 5 d a y s ' w e e k - l , until the strength in the muscles (through progressively increasing the load on the muscles) was increased so that the quadriceps and glutens maximus muscles could lift a mass of 5 kg and the hamstring a mass of 3.5 kg for the full 15-rain exercise period. Computer-controlled cycling was performed by having subjects sit on the modified cycle ergometer. Subjects started at 0 W of work. When cycling could be accomplished for 1 h with 30 min at 0 W, the exercise was increased in 5-W increments. Training progressed until the subjects could pedal the cycle ergometer for a period of 30 rain at 50 W. Six more training sessions were accomplished at this level. In practical terms this required approximately 2.5 months. As with the paralyzed subjects, the control subjects underwent a training program. This program involved 2 weeks of training for 5 days" week -a on the cycle ergometer and the armcrank ergometer. On any one day, cycling was performed at a speed o f 50 r e v . m i n - a to produce work at 50 W for a period of 30 min. Once subjects had completed the armcrank and cycle training programs they were exposed for 30 rain daily for 2 weeks to an environmental temperature of 40 ° C at rest.
505
Experimental procedure. Three series of experiments were carried
T h e average a u r a l t e m p e r a t u r e o f the c o n t r o l , p a r a p l e gics a n d q u a d r i p l e g i c s was 37 ° C, 37.5 ° C, a n d 37.6 ° C, respectively, after passive e x p o s u r e in the h e a t c h a m b e r for 30 min. These differences were n o t statistically sign i f i c a n t ( P > 0.05). In c o n t r a s t , after exposures to 3 5 ° C a n d 40 ° C, even t h o u g h the i n d i v i d u a l s were at rest, the p a r a l y z e d i n d i v i d u a l s s h o w e d significantly higher a u r a l t e m p e r a t u r e s ( P < 0 . 0 5 ) when c o m p a r e d to rest. O n exp o s u r e to heat, a u r a l t e m p e r a t u r e rose d r a m a t i c a l l y . T h e m o s t d r a m a t i c d i f f e r e n c e in t e m p e r a t u r e o c c u r r e d in the q u a d r i p l e g i c g r o u p a f t e r 30 m i n o f exercise o n either the a r m c r a n k or cycle e r g o m e t e r where a u r a l t e m p e r a t u r e s a v e r a g e d 40.3 ° C. T h e rise in t e m p e r a t u r e in the p a r a plegic a n d q u a d r i p l e g i c g r o u p s with changes in the envir o n m e n t a l t e m p e r a t u r e were significantly d i f f e r e n t f r o m each o t h e r ( A N O V A ) ( P < 0.05). F i g u r e 3 shows the m e a n h e a r t r a t e o f the g r o u p s at the end o f 30 m i n o f h e a t exposure. F o r the three g r o u p s o f subjects, the h e a r t rate was a l m o s t directly r e l a t e d to the t e m p e r a t u r e d u r i n g h e a t e x p o s u r e at rest or d u r i n g exercise. H o w e v e r , the h e a r t rate at rest was higher in the p a r a p l e g i c a n d the q u a d r i p l e g i c g r o u p f o r a n y given e n v i r o n m e n t a l t e m p e r a t u r e . F o r e x a m p l e , the a v e r a g e h e a r t rate f o r the c o n t r o l g r o u p after 30 m i n o f e x p o s u r e to h e a t at 40 ° C during passive resting was
out. In the first, subjects sat or the ergometer at rest and were exposed to temperatures of 30, 35 and 40°C for 30 min. During this period, aural temperatures, heart rate and sweat rates were measured. In the second, the subjects were exposed to the same conditions but performed armcrank ergometry (50 W) throughout the entire 30-min period. In the third, subjects were again exposed to the heat stress, but pedalled at 50 W for the 30-min period. On any experimental day, each individual arrived at the laboratory 1 h before the experiments started and rested passively at room temperature (22 ° C, SD 1). During this time the subject changed into cut-off shorts and a physician's scrub top with cutoff sleeves. After resting, the subjects were carried into the heat chamber where they exercised or sat passively. Armcrank ergometry was done with volitional control in all subjects. Only the control group pedalled the cycle under volitional control. All experimental procedures were replicated; the order of presentation was selected at random.
Results
T h e d a t a f r o m the e x p e r i m e n t s a r e s h o w n in Figs. 2 - 4 . T h e d a t a are the m e a n for the g r o u p s a n d the d u p l i c a t e e x p e r i m e n t s . F i g u r e 2 shows the a u r a l t e m p e r a t u r e responses f r o m a resting a u r a l t e m p e r a t u r e o f 3 7 ° C d u r ing e x p o s u r e at a n e n v i r o n m e n t a l t e m p e r a t u r e o f 30 ° C.
AURAL TEMPERATURE (Oc) 42=
41 ~
REST
ARMCRANK
CYCLE
40 39 38 37 36 35
30
35
40
30
35
40
300
ENVIRONMENTAL TEMPERATURE (
35
c)
L 4O
Fig. 2. Aural temperature in control (i), paraplegic (El) and quadriplegic (O) subjects, measured at the end of a 30-min heat exposure at environmental temperatures of 30°, 35 ° and 40 ° C. Measurements were made on two occasions on each subject at rest and exercising on the armcrank or cycle ergometer
HEART RATE (beats min1) 200 REST
ARMCRANI
CYCLE
150
100
50
30
35
40
30
35
40
30
ENVIRONMENTAL TEMPERATURE (°C)
35
40
Fig. 3. Heart rate of controls (11), paraplegics (1~) and quadriplegics (D) at rest and during either armcrank or cycle ergometry accomplished during a 30-min exposure to environmental temperatures of 30°, 35 ° and 40 ° C. Each bar represents the mean (SD) for each experimental group on each of two occasions
506 2
-1
MEAN SWEAT RATE (g m rain ) 7' 6 5 4 3 2 1 0
30
35
40
30
ENVIRONMENTAL
35
40
TEMPERATURE
30
0
35
40
(C)
93 b e a t s . m i n - 1 , whereas the heart rate for the quadriplegic group averaged 140 beats, rain-1. The heart rate at the end of the exposure to an environmental temperature of 30 ° C, however, was not statistically different between the three groups of subjects (P>0.05). When engaged in either armcrank or cycle ergometry, the heart rates were greater in all three groups of subjects after exposure to any environmental temperature, but the heart rates were higher in the paraplegic and quadriplegic groups than the control group for all three environmental conditions. The largest increase in heart rate was seen in the quadriplegic group. For example, the average heart rate measured at the end of exposure to the 40 ° C environment was 182 b e a t s . m i n -1 in the quadriplegic group and only 144beats.min -1 in the control group during exercise on the cycle. There was no significant difference between the increase in heart rate associated with work between each of the three groups when individuals worked at the same environmental conditions. Sweat rate showed a similar response. As can be seen in Fig. 4, when individuals were at rest, mean body sweat rate was linarly related to the environmental temperature. The highest sweat rates were seen in the control group and the lowest in the quadriplegic group. These differences were exacerbated when individuals exercised in heat. When exercise was done in heat, although the sweat rate was linearly related to the environmental temperature, sweat rates were significantly higher in the control group than in the other two groups. Although aural temperature had risen dramatically in the paraplegic group during exercise at an environmental temperature of 40 ° C, whole body sweat rates were still lower than the sweat rate in the control group exposed to exercise in the 30 ° C room. Sweat capsule measurements confirmed that there was no increase in regional sweat rates below the level of the SCI. The entire reported sweat production for these individuals was f r o m sweat produced at a high rate in the unparalyzed portions of the body.
Fig. 4. Whole body sweat rates for 4 control subjects (I), 4 paraplegics ([]) and 4 quadriplegics (Q) during 30 min of heat exposure in an environmental chamber at 30°, 35° and 40°C at a relative humidity Of 50%. Each bar illustrates the mean of each experimental group recorded on each of two occasions for individuals at rest or exercising on the armcrank or cycle ergometer
Discussion It has been established that SCI limits the thermoregulatory ability of the body to dissipate heat. The present investigation shows clearly that even exercise in a r o o m with 50% relative humidity results in a striking reduction in the ability to thermoregulate, especially in the quadriplegics. The sweat rates observed in the quadriplegics when working in a hot environment reflect a much higher regional sweat rate than was seen in the controls. The mean body sweat rate of the quadriplegics working at 40 ° C, for example, was nearly double that of the controls at 30 ° C. Since almost two-thirds of the sweat glands in the body are paralyzed in these individuals, the actual regional sweat rate is about six times higher than that observed in the controls. By observation, the sweat rate was so high that most of the sweat simply ran off the body and was ineffective in heat loss. It is unknown how the m a x i m u m sweat rate in a given area differed for controls and the test groups since the individuals never achieved their m a x i m u m sweating capacity. Further, cycling, which inherently is one of the most efficient types of exercise, is always considered to be at least 25°70 efficient. As such, 75% of the energy derived f r o m the breakdown of glucose during cycling should go to heat and 25% to work. With computer-controlled cycling, with published efficiencies of only about 3 % (Petrofsky et al. 1991), almost all of the glucose that is broken down is turned into heat rather than work. This is reflected in the higher strain seen in FES cycle work compared with voluntary armcrank ergometry at the same absolute level as assessed in the present investigation by the greater rise in body temperature in the paralyzed compared with control subjects. This points, then, to the fact that with computer-controlled cycling becoming ever present in the clinical setting (Ragnarsson et al. 1988; Petrofsky et al. 1991), exercise should be watched very carefully in SCI individuals to assure that the environment is kept cool. Certainly, if the humidity were higher than 50%, as commonly occurs in most parts of the country in the summertime, with environmental tern-
507 p e r a t u r e s o f over 35 ° C, it is easy to see h o w a q u a d r i plegic c o u l d d e v e l o p h e a t s y n c o p e f r o m the i n c r e a s e d t h e r m a l stress o f even light lower or u p p e r b o d y exercise. T h e d i a g r a m s p r e s e n t e d in this p a p e r s h o u l d f o r m a useful t o o l for g a u g i n g the e n v i r o n m e n t a l stress t h a t s h o u l d be a l l o w e d d u r i n g c o n c u r r e n t c o m p u t e r - c o n t r o l l e d exercise or v o l u n t a r y a r m c r a n k e r g o m e t r y in p a raplegics a n d q u a d r i p l e g i c s .
Acknowledgements. We gratefully acknowledge the support of the Petrofsky Neuromedical Research Foundation in this work. This work was also partially supported by a grant from the Veteran's Administration, Dayton, Ohio.
References Attia M, Engel P (1983) Thermoregulatory set point in patients with spinal cord injuries (spinal man). Paraplegia 21:233-248 Downey JA, Chiodi HP, Darling RC (1967) Central temperature regulation in the spinal man. J Appl Physiol 22:91-94 Downey JA, Miller JM, Darling RC (1969) Thermoregulatory responses to deep and superficial cooling in spinal man. J Appl Physiol 27 : 209-212 Downey JA, Huckaba CE, Myers SJ, Darling RC (1973) Thermoregulation in the spinal man. J Appl Physiol 34:790-794 Downey JA, Huckaba CE, Kelley PS, Tam HS, Darling RC, Cheh HY (1976) Sweating responses to central and peripheral heating in spinal man. J Appl Physiol 40:701-706 Glaser RM (1986) Physiologic aspects of spinal cord injury and functional neuromuscular stimulation. Cent Nerv Syst Trauma 3 : 49-62 Glaser RM, Simsen-Harold C, Petrofsky JS, Kahn S, Suryaprasad A (1983) Metabolic and cardiopulmonary responses of older wheelchair-dependent and ambulatory patients during locomotion. Ergonomics 26: 687-697 Guttman L (1976) Spinal cord injuries: comprehensive management and research, 2nd edn. Blackwell, Melbourne Guttman L, Silver J, Wyndham (1958) Thermoregulation in spinal man. J Physiol (Lond) 142:406-419 Hutchinson J (1875) Clinical lecture on temperature and circulation after crushing of cervical spinal cord. Lancet 1:715 Paget GE (1885) Case of remarkable risings and fallings of body temperature. Lancet II : 4-6
Petrofsky JS (1992) Metabolic, cardiovascular and respiratory responses which occur during computer-controlled aerobic exercise in patients with paraplegia. Arch Phys Med Rehabil (in press) Petrofsky JS, Smith J (1988) Computer aided rehabilitation. Aviat Space Environ Med 59:670-679 Petrofsky JS, Rinehart JS, Lind AR (1976) Isometric strength and endurance in slow and fast muscles in the cat. Fed Proc 35:291 Petrofsky JS, Lind AR (1979) Isometric endurance in fast and slow muscle in the rat. Am J Physiol 236:85-91 Petrofsky JS, Burse R, Lind AR (1981) The effect of deep muscle temperature on the cardiovascular responses of man to static effort. Eur J Appl Physiol 47:7-16 Petrofsky JS, Heaton HH, Phillips CA (1983a) Outdoor bicycle for exercise in paraplegics and quadriplegics. J Biomed Eng 5 : 296-297 Petrofsky JS, Phillips CA, Glaser RM, Heaton H (1983b) Application of the Apple as a microprocessor-controlled stimulator. Collegiate Microcomputer 1 : 97-104 Petrofsky JS, Phillips CA, Heaton HH, Glaser RM (1984) Bicycle ergometer for paralyzed muscle. J Clin Eng 9:13-19 Petrofsky JS, Phillips CA, Briggs R, Almayda J, Couch W (1985a) Aerobic trainer with physiological monitoring for exercise in paraplegics and quadriplegics. J Clin Eng 10: 307-315 Petrofsky JS, Phillips CA, Hendershot D (1985b) Cardiorespiratory stresses which occur during dynamic exercise in paraplegic and quadriplegic men. J Neurol Orthop Surg 6:252-258 Petrofsky JS, Smith J (1991) Aerobic exercise trainer for paralyzed and non-paralyzed. J Clin Eng 65 : 505-514 Pollock L J, Boshes B, Chor H, Finkelman I, Arief AJ, Brown M (1951) Defects of regulatory mechanisms of autonomic function in injuries to spinal cord. J Neurophysiol 14:85-93 Rack PM, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204: 443-460 Ragnarsson K, Pollack S, Petrofsky JS, O'Daniel W, Edgar R, Nash M (1988) Clinical evaluation of functional electrical stimulation after spinal cord injury, a pilot multicenter study. Arch Phys Med Rehabil 69:672-677 Sawka M, Latzka W, Pandolf K (1989) Temperature regulation during upper body exercise: able bodied and spinal cord injured. Med Sci Sports Exerc 21 : 132-140 Young JS, Burns PE, Bowen AM, McClutcheon R (1982) Spinal cord injury statistics: experience of regional spinal cored injury systems. Good Samaritan Medical Center, Phoenix, Ariz.
Applied Physiology European Journal of
and Occupational Physiology © Springer-Verla9 1992
Thermoregulatory stress during rest and exercise in heat in patients with a spinal cord injury Jerrold S. Petrofsky Petrofsky Center for Rehabilitation and Research, Irvine, California; Wright State Lfniversity,Dayton, Ohio; and Universityof California, Irvine, California, USA Accepted January 25, 1992
Summary. Twelve subjects with spinal cord injuries and four controls (all male) were exposed to heat while sitting at rest or working at each of three environmental temperatures, 30, 35 and 40 ° C, with a relative humidity of 50%. Exercise was accomplished at a load of 50 W on a friction-braked cycle ergometer which was armcranked or pedalled. Functional electrical stimulation of the legs was provided to the subjects with quadriplegia and paraplegia to allow them to pedal a cycle ergometer. The data showed that individuals with quadriplegia had the poorest tolerance for heat. As an example, in this group, accomplishing armcrank ergometry while working at an environmental temperature of 40°C resulted in an increase in aural temperature of 2 ° C in 30 min. The aural temperature of individuals with paraplegia working for the same length of time under the same conditions rose approximately I°C. There was virtually no change in the aural temperature in the control subjects. Key words: Exercise - Thermoregulation - Heat stress Paraplegia - Quadriplegia
Introduction A spinal cord injury (SCI) usually results in permanent paralysis below the level of the lesion. Although the loss of voluntary movement is the most obvious problem seen in individuals with SCI, the secondary problems associated with damage to the autonomic nervous system cause the greatest medical consequences (Guttman 1976). Such secondary medical problems can include pressure sores, kidney and bladder infections (Young et al. 1982), and thermoregulatory impairment (Hutchinson 1875; Paget 1885; Guttman 1976; Attia and Engel 1983; Sawka et al. 1989). Because damage can occur to both peripheral temperature sensors and the ability to Offprint requests to: J. S. Petrofsky, Petrofsky Centers for Rehabilitation and Research, 13765 Alton Parkway, Suite E, Irvine, CA 92716, USA
sweat, SCI individuals become partially poikilothermic (Guttman et al. 1968; Downey et al. 1967, 1969, 1973, 1976; Attia and Engel 1983). When muscle temperature is allowed to vary, endurance can be effected (Petrofsky et al. 1981). The damage to the autonomic nervous system in SCI individuals seems to affect both sweating and the ability to vasoconstrict and vasodilate the peripheral vasculature. Therefore, it is not simply heat exposure, per se, that results in thermoregulatory difficulties. Pollock et al. (1951) have clearly shown that even immersion of an SCI individual in a warm water bath can have serious thermoregulatory consequences due to the lack of control of the peripheral circulation exhibited by such individuals. There is also evidence that individuals with paraplegia or quadriplegia may have a different thermoregulatory set point than able-bodied individuals (Downey et al. 1969; Attia and Engel 1983). This set point was suggested in studies by Atria and Engel (1983) to be variable and a function of the ambient conditions. It was viewed by these workers as an adaptive thermoregulatory process following SCI. In recent years, increasing emphasis has been placed on exercise in SCI individuals. Typically, exercise has been conducted with voluntary armcrank ergometry (Glaser et al. 1983, 1986). More recently, however, functional electrical stimulation (FES) has been used to exercise paralyzed leg muscles. Aerobic cycle ergometry exercise has been extensively investigated in paraplegics and quadriplegics using electrical stimulation to exercise the quadriceps, hamstring and gluteus maximus muscles (Petrofsky et al. 1983a, b, 1984, 1991). In addition, isokinetic exercise of paralyzed muscles in the lower body has been extensively used for the conditioning of paralyzed muscle (Petrofsky et al. 1982, 1985a, b; Petrofsky and Smith 1988). FES exercise is now becoming widespread as an accepted modality in rehabilitation centers for SCI individuals (Ragnarsson et al. 1988; Petrofsky 1992). However, the effect of computer-controlled exercise in relation to heat exposure has not been investigated. Since FES cycle studies have shown that metabolic demand can cause cardiac output to be over 15 1min -1 (Petrofsky and Smith 1988), the implication
504 is t h a t it m a y i n d u c e a c o n s i d e r a b l e h e a t l o a d d u e t o t h e high metabolism associated with the work. I n t h e p r e s e n t i n v e s t i g a t i o n , e x p e r i m e n t s o n ablebodied (control), paraplegic and quadriplegic individuals w e r e c a r r i e d o u t t o s t u d y t h e r m o r e g u l a t o r y stress resulting f r o m rest a n d exercise d u r i n g h e a t e x p o s u r e .
Methods Subjects. The subjects in these studies were all males. Six had paraplegia, 6 had quadriplegia, and 4 were able-bodied controls. The average of the control group was 22.7 years, whereas that of the group with SCI was 23.4 years. The paraplegic group had complete SCI between T3 and T12; the quadriplegic group had injuries which were complete and located between C6 and C8. Subjects were medically examined prior to the studies and signed a statement of informed consent. All experimental procedures and protocols were approved by the Committee on Human Experimentation. Sweat rates. Sweat was collected in capsules over 2-min periods. The capsules had a surface area of 200 mm 2. They were located on the forehead, chest, thigh (above the quadriceps muscle) and forearm, and held in place with an elastic band. A circular piece of paper was put into the capsule and removed at 2-min intervals. The paper was weighed before being put into the capsule and after removal. The change in mass was used to calculate the sweat over that area. Body mass was recorded on a specially designed scale with an accuracy of plus or minus 1 g both before and after heat exposure under each of the experimental conditions. The change in body mass over a given time was used to calculate mean sweat rates (mass loss in 1 rain/body surface area = mean sweat rate/rain). Heart rate. Heart rate was measured by continuous ECG recordings. Electrodes were placed in the limb lead 2 position, and the ECG was continuously recorded throughout the heat exposure. Heart rate was counted from 15-s ECG recordings. Exercise on cycle ergometry under computer control. Cycle ergometry was accomplished on a modified cycle (Monark; Fig. 1) similar to one described previously (Petrofsky et al. 1983a, b, 1984, 1985a, b). The cycle was modified with a high-back seat and seatbelts to allow paralyzed subjects to sit comfortably. To protect the hips and knees from severe inward and outward rotation during cycling, knee stabilizers bars were added so that the exercise could be accomplished without abduction or adduction at the
Fig. 1. Computer-controlled exercise bike
hips. The knee stabilizer bars were secured to the leg by Velcro straps, as shown in Fig. 1. Special shoes were added with Velcro on the bottoms so that the feet could be secured to the pedals. A sensor was placed on the pedals so that the position of the pedals could be used as an input for a digital computer. The computercontrolled timing of the electrical stimulation to the quadriceps, hamstring and gluteus maximus muscles was such that cycling could be elicited. Three electrodes were placed over each respective muscle, with the reference electrode being applied over the center of the muscle and the active electrodes being placed diagonally across the ends. The 350-gs, biphasic square-wave stimulation that was applied sequentially across the three electrodes (Rack and Westbury 1969; Petrofsky et al. 1976, 1979) was varied in current from 0 to 180 mA at a frequency of 35 Hz. A more detailed description of the cycle ergometer is provided elsewhere (Petrofsky et al. 1983a, b).
Armcrank ergometry. Armcrank ergometry was accomplished on a friction-braked armcrank ergometer (Monark). A timer kept pace so that cycling could be accomplished at 50 rev. min-1 at a load of 50 W. The ergometer was modified to reverse the normal (forward) direction of rotation. This was necessary because the lack of the triceps surae muscles in quadriplegics makes normal cranking difficult. Reversing direction allows the non-paralyzed biceps muscles to be used. This mode of cranking was used by all three groups of subjects. Measurement of aural temperature. Aural temperature was measured by using a thermistor temperature probe (Yellow Springs Instruments, Yellow Springs, Ohio) placed near the eardrum. A cotton wick was used to hold the probe in place and provide insulation. The output of the temperature probe was transduced through a Wheatstone Bridge which was then amplified with a DC amplifier and recorded on a flatbed recorder (Houston Instruments, Houston, Tex.). Stat&tical analysis. Statistical analysis involved the calculation of means, standard deviation, analysis of variance, and t-tests. The level of significance was chosen as P < 0 . 0 5 . Training. After SCI, paralyzed individuals have so little strength in their muscles that they cannot accomplish computer-controlled cycling for more than a few seconds a session (Petrofsky et al. 1983a, b, 1984, 1985a, b). Therefore, a comprehensive training program was needed to accomplish the present investigation. Each subject began by exercising his quadriceps, hamstring, and gluteus maximus muscles on specially designed weightlifting equipment. The muscles performed isokinetic exercise, lifting ankle weights for 3 s of flexion, 1 s of hold, and 2 s of extension; 6 s were allowed between contractions. This protocol was accomplished for 30 rain. day-a, 5 d a y s ' w e e k - l , until the strength in the muscles (through progressively increasing the load on the muscles) was increased so that the quadriceps and glutens maximus muscles could lift a mass of 5 kg and the hamstring a mass of 3.5 kg for the full 15-rain exercise period. Computer-controlled cycling was performed by having subjects sit on the modified cycle ergometer. Subjects started at 0 W of work. When cycling could be accomplished for 1 h with 30 min at 0 W, the exercise was increased in 5-W increments. Training progressed until the subjects could pedal the cycle ergometer for a period of 30 rain at 50 W. Six more training sessions were accomplished at this level. In practical terms this required approximately 2.5 months. As with the paralyzed subjects, the control subjects underwent a training program. This program involved 2 weeks of training for 5 days" week -a on the cycle ergometer and the armcrank ergometer. On any one day, cycling was performed at a speed o f 50 r e v . m i n - a to produce work at 50 W for a period of 30 min. Once subjects had completed the armcrank and cycle training programs they were exposed for 30 rain daily for 2 weeks to an environmental temperature of 40 ° C at rest.
505
Experimental procedure. Three series of experiments were carried
T h e average a u r a l t e m p e r a t u r e o f the c o n t r o l , p a r a p l e gics a n d q u a d r i p l e g i c s was 37 ° C, 37.5 ° C, a n d 37.6 ° C, respectively, after passive e x p o s u r e in the h e a t c h a m b e r for 30 min. These differences were n o t statistically sign i f i c a n t ( P > 0.05). In c o n t r a s t , after exposures to 3 5 ° C a n d 40 ° C, even t h o u g h the i n d i v i d u a l s were at rest, the p a r a l y z e d i n d i v i d u a l s s h o w e d significantly higher a u r a l t e m p e r a t u r e s ( P < 0 . 0 5 ) when c o m p a r e d to rest. O n exp o s u r e to heat, a u r a l t e m p e r a t u r e rose d r a m a t i c a l l y . T h e m o s t d r a m a t i c d i f f e r e n c e in t e m p e r a t u r e o c c u r r e d in the q u a d r i p l e g i c g r o u p a f t e r 30 m i n o f exercise o n either the a r m c r a n k or cycle e r g o m e t e r where a u r a l t e m p e r a t u r e s a v e r a g e d 40.3 ° C. T h e rise in t e m p e r a t u r e in the p a r a plegic a n d q u a d r i p l e g i c g r o u p s with changes in the envir o n m e n t a l t e m p e r a t u r e were significantly d i f f e r e n t f r o m each o t h e r ( A N O V A ) ( P < 0.05). F i g u r e 3 shows the m e a n h e a r t r a t e o f the g r o u p s at the end o f 30 m i n o f h e a t exposure. F o r the three g r o u p s o f subjects, the h e a r t rate was a l m o s t directly r e l a t e d to the t e m p e r a t u r e d u r i n g h e a t e x p o s u r e at rest or d u r i n g exercise. H o w e v e r , the h e a r t rate at rest was higher in the p a r a p l e g i c a n d the q u a d r i p l e g i c g r o u p f o r a n y given e n v i r o n m e n t a l t e m p e r a t u r e . F o r e x a m p l e , the a v e r a g e h e a r t rate f o r the c o n t r o l g r o u p after 30 m i n o f e x p o s u r e to h e a t at 40 ° C during passive resting was
out. In the first, subjects sat or the ergometer at rest and were exposed to temperatures of 30, 35 and 40°C for 30 min. During this period, aural temperatures, heart rate and sweat rates were measured. In the second, the subjects were exposed to the same conditions but performed armcrank ergometry (50 W) throughout the entire 30-min period. In the third, subjects were again exposed to the heat stress, but pedalled at 50 W for the 30-min period. On any experimental day, each individual arrived at the laboratory 1 h before the experiments started and rested passively at room temperature (22 ° C, SD 1). During this time the subject changed into cut-off shorts and a physician's scrub top with cutoff sleeves. After resting, the subjects were carried into the heat chamber where they exercised or sat passively. Armcrank ergometry was done with volitional control in all subjects. Only the control group pedalled the cycle under volitional control. All experimental procedures were replicated; the order of presentation was selected at random.
Results
T h e d a t a f r o m the e x p e r i m e n t s a r e s h o w n in Figs. 2 - 4 . T h e d a t a are the m e a n for the g r o u p s a n d the d u p l i c a t e e x p e r i m e n t s . F i g u r e 2 shows the a u r a l t e m p e r a t u r e responses f r o m a resting a u r a l t e m p e r a t u r e o f 3 7 ° C d u r ing e x p o s u r e at a n e n v i r o n m e n t a l t e m p e r a t u r e o f 30 ° C.
AURAL TEMPERATURE (Oc) 42=
41 ~
REST
ARMCRANK
CYCLE
40 39 38 37 36 35
30
35
40
30
35
40
300
ENVIRONMENTAL TEMPERATURE (
35
c)
L 4O
Fig. 2. Aural temperature in control (i), paraplegic (El) and quadriplegic (O) subjects, measured at the end of a 30-min heat exposure at environmental temperatures of 30°, 35 ° and 40 ° C. Measurements were made on two occasions on each subject at rest and exercising on the armcrank or cycle ergometer
HEART RATE (beats min1) 200 REST
ARMCRANI
CYCLE
150
100
50
30
35
40
30
35
40
30
ENVIRONMENTAL TEMPERATURE (°C)
35
40
Fig. 3. Heart rate of controls (11), paraplegics (1~) and quadriplegics (D) at rest and during either armcrank or cycle ergometry accomplished during a 30-min exposure to environmental temperatures of 30°, 35 ° and 40 ° C. Each bar represents the mean (SD) for each experimental group on each of two occasions
506 2
-1
MEAN SWEAT RATE (g m rain ) 7' 6 5 4 3 2 1 0
30
35
40
30
ENVIRONMENTAL
35
40
TEMPERATURE
30
0
35
40
(C)
93 b e a t s . m i n - 1 , whereas the heart rate for the quadriplegic group averaged 140 beats, rain-1. The heart rate at the end of the exposure to an environmental temperature of 30 ° C, however, was not statistically different between the three groups of subjects (P>0.05). When engaged in either armcrank or cycle ergometry, the heart rates were greater in all three groups of subjects after exposure to any environmental temperature, but the heart rates were higher in the paraplegic and quadriplegic groups than the control group for all three environmental conditions. The largest increase in heart rate was seen in the quadriplegic group. For example, the average heart rate measured at the end of exposure to the 40 ° C environment was 182 b e a t s . m i n -1 in the quadriplegic group and only 144beats.min -1 in the control group during exercise on the cycle. There was no significant difference between the increase in heart rate associated with work between each of the three groups when individuals worked at the same environmental conditions. Sweat rate showed a similar response. As can be seen in Fig. 4, when individuals were at rest, mean body sweat rate was linarly related to the environmental temperature. The highest sweat rates were seen in the control group and the lowest in the quadriplegic group. These differences were exacerbated when individuals exercised in heat. When exercise was done in heat, although the sweat rate was linearly related to the environmental temperature, sweat rates were significantly higher in the control group than in the other two groups. Although aural temperature had risen dramatically in the paraplegic group during exercise at an environmental temperature of 40 ° C, whole body sweat rates were still lower than the sweat rate in the control group exposed to exercise in the 30 ° C room. Sweat capsule measurements confirmed that there was no increase in regional sweat rates below the level of the SCI. The entire reported sweat production for these individuals was f r o m sweat produced at a high rate in the unparalyzed portions of the body.
Fig. 4. Whole body sweat rates for 4 control subjects (I), 4 paraplegics ([]) and 4 quadriplegics (Q) during 30 min of heat exposure in an environmental chamber at 30°, 35° and 40°C at a relative humidity Of 50%. Each bar illustrates the mean of each experimental group recorded on each of two occasions for individuals at rest or exercising on the armcrank or cycle ergometer
Discussion It has been established that SCI limits the thermoregulatory ability of the body to dissipate heat. The present investigation shows clearly that even exercise in a r o o m with 50% relative humidity results in a striking reduction in the ability to thermoregulate, especially in the quadriplegics. The sweat rates observed in the quadriplegics when working in a hot environment reflect a much higher regional sweat rate than was seen in the controls. The mean body sweat rate of the quadriplegics working at 40 ° C, for example, was nearly double that of the controls at 30 ° C. Since almost two-thirds of the sweat glands in the body are paralyzed in these individuals, the actual regional sweat rate is about six times higher than that observed in the controls. By observation, the sweat rate was so high that most of the sweat simply ran off the body and was ineffective in heat loss. It is unknown how the m a x i m u m sweat rate in a given area differed for controls and the test groups since the individuals never achieved their m a x i m u m sweating capacity. Further, cycling, which inherently is one of the most efficient types of exercise, is always considered to be at least 25°70 efficient. As such, 75% of the energy derived f r o m the breakdown of glucose during cycling should go to heat and 25% to work. With computer-controlled cycling, with published efficiencies of only about 3 % (Petrofsky et al. 1991), almost all of the glucose that is broken down is turned into heat rather than work. This is reflected in the higher strain seen in FES cycle work compared with voluntary armcrank ergometry at the same absolute level as assessed in the present investigation by the greater rise in body temperature in the paralyzed compared with control subjects. This points, then, to the fact that with computer-controlled cycling becoming ever present in the clinical setting (Ragnarsson et al. 1988; Petrofsky et al. 1991), exercise should be watched very carefully in SCI individuals to assure that the environment is kept cool. Certainly, if the humidity were higher than 50%, as commonly occurs in most parts of the country in the summertime, with environmental tern-
507 p e r a t u r e s o f over 35 ° C, it is easy to see h o w a q u a d r i plegic c o u l d d e v e l o p h e a t s y n c o p e f r o m the i n c r e a s e d t h e r m a l stress o f even light lower or u p p e r b o d y exercise. T h e d i a g r a m s p r e s e n t e d in this p a p e r s h o u l d f o r m a useful t o o l for g a u g i n g the e n v i r o n m e n t a l stress t h a t s h o u l d be a l l o w e d d u r i n g c o n c u r r e n t c o m p u t e r - c o n t r o l l e d exercise or v o l u n t a r y a r m c r a n k e r g o m e t r y in p a raplegics a n d q u a d r i p l e g i c s .
Acknowledgements. We gratefully acknowledge the support of the Petrofsky Neuromedical Research Foundation in this work. This work was also partially supported by a grant from the Veteran's Administration, Dayton, Ohio.
References Attia M, Engel P (1983) Thermoregulatory set point in patients with spinal cord injuries (spinal man). Paraplegia 21:233-248 Downey JA, Chiodi HP, Darling RC (1967) Central temperature regulation in the spinal man. J Appl Physiol 22:91-94 Downey JA, Miller JM, Darling RC (1969) Thermoregulatory responses to deep and superficial cooling in spinal man. J Appl Physiol 27 : 209-212 Downey JA, Huckaba CE, Myers SJ, Darling RC (1973) Thermoregulation in the spinal man. J Appl Physiol 34:790-794 Downey JA, Huckaba CE, Kelley PS, Tam HS, Darling RC, Cheh HY (1976) Sweating responses to central and peripheral heating in spinal man. J Appl Physiol 40:701-706 Glaser RM (1986) Physiologic aspects of spinal cord injury and functional neuromuscular stimulation. Cent Nerv Syst Trauma 3 : 49-62 Glaser RM, Simsen-Harold C, Petrofsky JS, Kahn S, Suryaprasad A (1983) Metabolic and cardiopulmonary responses of older wheelchair-dependent and ambulatory patients during locomotion. Ergonomics 26: 687-697 Guttman L (1976) Spinal cord injuries: comprehensive management and research, 2nd edn. Blackwell, Melbourne Guttman L, Silver J, Wyndham (1958) Thermoregulation in spinal man. J Physiol (Lond) 142:406-419 Hutchinson J (1875) Clinical lecture on temperature and circulation after crushing of cervical spinal cord. Lancet 1:715 Paget GE (1885) Case of remarkable risings and fallings of body temperature. Lancet II : 4-6
Petrofsky JS (1992) Metabolic, cardiovascular and respiratory responses which occur during computer-controlled aerobic exercise in patients with paraplegia. Arch Phys Med Rehabil (in press) Petrofsky JS, Smith J (1988) Computer aided rehabilitation. Aviat Space Environ Med 59:670-679 Petrofsky JS, Rinehart JS, Lind AR (1976) Isometric strength and endurance in slow and fast muscles in the cat. Fed Proc 35:291 Petrofsky JS, Lind AR (1979) Isometric endurance in fast and slow muscle in the rat. Am J Physiol 236:85-91 Petrofsky JS, Burse R, Lind AR (1981) The effect of deep muscle temperature on the cardiovascular responses of man to static effort. Eur J Appl Physiol 47:7-16 Petrofsky JS, Heaton HH, Phillips CA (1983a) Outdoor bicycle for exercise in paraplegics and quadriplegics. J Biomed Eng 5 : 296-297 Petrofsky JS, Phillips CA, Glaser RM, Heaton H (1983b) Application of the Apple as a microprocessor-controlled stimulator. Collegiate Microcomputer 1 : 97-104 Petrofsky JS, Phillips CA, Heaton HH, Glaser RM (1984) Bicycle ergometer for paralyzed muscle. J Clin Eng 9:13-19 Petrofsky JS, Phillips CA, Briggs R, Almayda J, Couch W (1985a) Aerobic trainer with physiological monitoring for exercise in paraplegics and quadriplegics. J Clin Eng 10: 307-315 Petrofsky JS, Phillips CA, Hendershot D (1985b) Cardiorespiratory stresses which occur during dynamic exercise in paraplegic and quadriplegic men. J Neurol Orthop Surg 6:252-258 Petrofsky JS, Smith J (1991) Aerobic exercise trainer for paralyzed and non-paralyzed. J Clin Eng 65 : 505-514 Pollock L J, Boshes B, Chor H, Finkelman I, Arief AJ, Brown M (1951) Defects of regulatory mechanisms of autonomic function in injuries to spinal cord. J Neurophysiol 14:85-93 Rack PM, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204: 443-460 Ragnarsson K, Pollack S, Petrofsky JS, O'Daniel W, Edgar R, Nash M (1988) Clinical evaluation of functional electrical stimulation after spinal cord injury, a pilot multicenter study. Arch Phys Med Rehabil 69:672-677 Sawka M, Latzka W, Pandolf K (1989) Temperature regulation during upper body exercise: able bodied and spinal cord injured. Med Sci Sports Exerc 21 : 132-140 Young JS, Burns PE, Bowen AM, McClutcheon R (1982) Spinal cord injury statistics: experience of regional spinal cored injury systems. Good Samaritan Medical Center, Phoenix, Ariz.
