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Acute Peripheral Blood Flow Response Induced by Passive Leg Cycle Exercise in People With Spinal Cord Injury
Laurent Ballaz, PhD, Nicolas Fusco, PhD, Armel Crétual, PhD, Bernard Langella, MD, Régine Brissot, PhD
ABSTRACT. Ballaz L, Fusco N, Crétual A, Langella B, Brissot R. Acute peripheral blood flow response induced by passive leg cycle exercise in people with spinal cord injury. Arch Phys Med Rehabil 2007;88:471-6. Objective: To determine the acute femoral artery hemodynamic response in paraplegic subjects during a passive leg cycle exercise. Design: Case series. Setting: Department of physical medicine and rehabilitation in a university in France. Participants: A volunteer sample of 15 people with traumatic spinal cord injury. Intervention: Subjects performed a 10-minute session of passive leg cycle exercise in the sitting position. Main Outcome Measures: We measured heart rate, maximal (Vmax), and minimal femoral artery blood flow velocity at rest and immediately after the passive leg cycle exercise, using quantitative duplex Doppler ultrasound. We calculated mean blood flow velocity (Vmean) and velocity index, representing the peripheral resistance, for each condition. Results: Vmax and Vmean increased (from .80Ϯ.18m/s to .96Ϯ.24m/s, PϽ.01; and from .058Ϯ.02m/s to .076Ϯ.03m/s, PϽ.01; respectively) after 10 minutes of passive leg cycle exercise. Heart rate did not change. The velocity index decreased from 1.23Ϯ0.15 to 1.16Ϯ0.21 (Pϭ.038). Conclusions: The results of this study suggest that acute passive leg cycle exercise increases vascular blood flow velocity in paralyzed legs of people with paraplegia. This exercise could have clinical implications for immobilized persons. Key Words: Blow flow velocity; Doppler ultrasound; Femoral artery; Rehabilitation; Spinal cord injuries. © 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HE INCIDENCE OF DEATH among people with spinal cord injury (SCI) is significantly higher than in the general T population. SCI subjects are prone to severe cardiovascular

disorders that present an increased risk of mortality.2 The risk increases with the degree of dependency, in particular for people who are totally dependent on wheelchairs for mobility.3 Two factors related to this risk are loss of autonomic control

From the Physiology and Biomechanics Laboratory, Sports Department, Rennes 2 University, France (Ballaz, Fusco, Crétual); and Departments of Radiology (Langella) and Physical Medicine and Rehabilitation (Brissot), University Hospital Center, Rennes, France. Supported by the Brittany Regional Council through the CRITT health project. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Laurent Ballaz, PhD, Laboratoire de Physiologie et de Biomécanique de l’Exercice Musculaire, UFR-APS, Université Rennes 2, Ave Charles Tillon – CS 24 414, 35 044 Rennes Cedex, France, e-mail: 0003-9993/07/8804-11035$32.00/0 doi:10.1016/j.apmr.2007.01.011

and lack of movement, which lead to vascular disorders.4,5 This induces an important structural and functional remodeling in the peripheral vascular system of paralyzed limbs; this remodeling includes reduced diameter of the common femoral artery (CFA),5,6 arterial stiffness,7 and lesser blood flow to the legs.5,6 Another factor is the high occurrence of metabolic syndromes (eg, obesity, hypercholesterolemia) caused by a lack of physical exercise,8,9 which is recognized as a cardiovascular ischemia factor. Studies of people with long-lasting SCI have shown that the femoral artery blood flow at rest is reduced by about 50% when compared with able-bodied subjects.5,6 This adaptation has been related to muscular atrophy, and even though there is relatively little change in the flow with respect to the muscle mass,10 improvement in lower-extremity circulation is highly desirable because deficient lower-extremity circulation and venous stagnation lead to thrombosis.5 Thrombosis prevalence is higher in the SCI population than in the general population, even in the chronic phase.2,3 This vascular remodeling may reflect the consequences of reduced activity. Arm exercises, which subjects with SCI could easily do, neither target the vessels in the lower limbs nor promote lower-limb circulation in those subjects.11,12 The set of potential lower-limb exercises is limited in the case of wheelchair users. Since the 1990s, functional electric stimulation (FES) has shown great promise as a cardiovascular stimulus.13-17 Some studies show that a relatively short period of FES leg cycle exercise training may lead to peripheral vascular improvement and enhance peripheral circulation as measured by an echo Doppler ultrasound.14,15,17 This technique, however, has been reported to carry the risks of skin burns, autonomic dysreflexia, and bone fractures.18 Ditor et al19 have shown that body-weight support treadmill training (BWSTT) may increase femoral artery compliance in subjects with complete motor SCI (C4-T12; American Spinal Injury Association20 [ASIA] grade A and B; years postinjury, 7.6Ϯ9.4y). Hence, use of this technique should be encouraged as a means of improving cardiovascular health in the SCI population.19 Its widespread use, however, is hindered because BWSTT requires both trainers and expensive equipment. This study, however, demonstrates that passive movement can lead to structural peripheral vascular adaptation. The simple passive leg cycle exercise is easily performed by people confined to wheelchairs.21,22 Powered cycle trainers that subjects can use at home while sitting in a wheelchair are also commercially available. Very few studies have investigated the central cardiopulmonary response to passive leg cycle exercise in healthy subjects23,24 or in SCI patients.25-28 With regard to SCI subjects (T8-L1; ASIA grade A; years postinjury, 14.6Ϯ8.8), Muraki et al27,28 suggest that passive leg cycle exercise enhances the cardiac output by increasing the stroke volume, provided the exercise is performed at 40 rounds per minute (rpm). This increased cardiac output probably results from the activation of the muscular pump that increases the venous return from the passively moved muscles. In a recent study, Ter Woerds et al29 could not find any alteration in the arterial leg blood flow either after passive leg movement by a
Arch Phys Med Rehabil Vol 88, April 2007

Subjects did not modify their usual treatment for the trial. age. L. directly from a standardized wheelchair with the back bent backward (150°). June 2006). METHODS Fifteen people (12 men.31. Participants who had been injured at least 6 months before were recruited from the department of rehabilitation at Rennes Hospital. The subjects were not disturbed during the testing session. in the same position.472 PASSIVE CYCLING IN PARAPLEGICS WITH SCI. M. We assumed that passive leg cycle exercise increases the blood flow circulation and decreases the peripheral vascular resistance of CFA in subjects with SCI. subjects performed a 10-minute session of passive leg cycle exercise with their backs against the wheelchair back support. They also underwent a medical examination by the rehabilitation physician (RB) to ensure that the inclusion criteria were met. standard deviation. The sample volume was placed in the center of the vessel and the length of the volume adjusted to the diameter of the lumen. years postinjury. The equipment settings were kept constant during the protocol. nonambulatory. The resting measurement was taken before the exercise session. The same examiner (BL) took all the measurements. Doppler Ultrasound Imaging We measured red blood cell velocities of the right CFA immediately before and after the exercise session. Our purpose in this study was to determine the acute peripheral hemodynamic response through passive leg cycle exercise in people with paraplegia. The measurement was taken with the subject’s feet on the pedals and the right leg in the most extended position (right pedal placed forward). depending on the flexibility and the length of the subject’s legs (L. Arch Phys Med Rehabil Vol 88. 19Ϯ8y) were included in the study. Table 1 summarizes their characteristics. The reliability of this method of measuring blood cell velocity in the CFA has been demonstrated. by the level and the location of the injury. The local ethics committee at Rennes approved this trial before the study was started. This assumption requires further study. This suggests that there is no significant effect on the peripheral vascular flow with passive limb mobilization in therapy. left. The ROM in the sagittal plane was at least 40° in the knee and 30° in the hip. The probe was placed about 2cm away from the fork of the CFA by using superficial and deep femoral arteries as landmarks to be located on axial scans. 47Ϯ8y) with chronic SCI (T3-12. PhD. Postexercise measurement was always done within 7 seconds of the end of the exercise. fixed at an angle of 60° for pulsed Doppler. The test was performed between 10:00 AM and 1:00 PM in an experiment room in which the temperature was maintained at between 21° and 24°C.32 Another investigator (LB) analyzed an off-line recording of red blood cell velocities. Doppler spectra were registered thrice at the same location at rest and at end-stress. The pedaling speed was increased regularly during the first minute to reach the target pedaling rate of 40rpm without evoking any spastic contraction. unpublished data. Four subjects were under medication: 2 used alfuzosine for sphincter hypertonia and the other 2 took baclofen for limb spasticity. April 2007 . and severely reduced range of motion (ROM) of hip or knee joints. metabolic or pulmonary disease. right. Measurements were always taken in a darkened environment. 3 women. from the corresponding Table 1: Descriptive Characteristics of the Study Subjects (N‫؍‬15) Subjects Sex Age (y) Years Postinjury Lesion Level ASIA Grade Quadriceps Spasticity Ashworth Scale30 Score (R/L) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean SD M M M F M M F M F M M M M M M 62 60 45 45 37 38 55 35 48 42 40 49 46 47 55 47 8 32 3 15 8 18 20 30 13 33 21 17 24 13 22 20 19 8 T11 T11 T8 L1 T12 T5 T5 T4 T6 T6 T9 T4 T3 T12 T12 A A A A A C A C A A A A A A A 0/0 0/1 3/3 0/0 0/0 4/1 1/2 1/3 1/3 0/0 0/0 0/0 0/0 0/0 1/3 Abbreviations: F. Ballaz. SD. Furthermore. Ballaz therapist or by passive cycling.5–15cm) was adjusted to ensure the highest ROM. male. cardiovascular history. The length of the pedal (7. Only 2 subjects had nerve degeneration of the lower limbs resulting in lower motoneuron lesions. Subjects with any of the following conditions were excluded: history of smoking (past or current). R. female. The level of each subject’s quadriceps spasticity was measured with the Ashworth Scale. Resting longitudinal images and simultaneous Doppler spectra were obtained from the CFA with a pulsed color-code Doppler device. after a rest period of 5 minutes in the sitting position.b We also used a broadband linear array transducer of 5 to 10MHz. This was assessed. ASIA grades A–C. All patients were informed of the testing procedures and possible undesirable side effects and gave their written consent to participate. based on a physical examination. The wheelchair back was tilted and the examiner placed the probe in front of the end of the passive cycle exercise so that the measurement was taken immediately after the end of the exercise.30 After the isokinetic motorized cyclea was installed. Exercise Protocol Subjects were requested not to drink caffeine and to empty their bladders before engaging in the passive leg cycle exercise.

The other postexercise measurements were used to control the return to the basal level. *Differing significantly from rest (P<.001) and from . We used paired t tests for dependent groups or Mann-Whitney U tests to compare variables for vascular properties of the femoral artery before and after the exercise session. from 1.23. In the SCI pop- Fig 1. The heart rate was calculated from the Doppler acquisition.23Ϯ0.01).24m/s (Pϭ. Velocity index at rest and after passive leg cycle exercise.05 indicate statistical significance.PASSIVE CYCLING IN PARAPLEGICS WITH SCI.05).009). RESULTS Exercise Compliance All but 1 subject completed the 10-minute exercise session at a rate of 40rpm. There was no significant spastic muscle contraction during the passive cycling exercise. April 2007 .34-36 we assumed that after passive leg cycle exercise there is a variation of blood flow. the following parameters of blood velocity were determined among 6 successive cardiac cycles and subsequently averaged: (1) peak systolic blood velocity (Vmax). without an increase in the heart rate. Heart rate also remained unchanged after 10 minutes of exercise.14 This index was a slight modification of the pulsatility index37 and was independent of possible differences in the insonation angle of the Doppler probe during recording.33 Because no dilatation of CFA during the exercise was previously reported. *Differing significantly from rest (P<. the 1 subject asked to stop the rise of the pedaling rate and completed the session at 30rpm. defined as the lowest velocity. In able-bodied persons. P values less than .15 to 1. Effect of Acute Passive Leg Cycle Exercise Paired t tests were used for all comparisons because each parameter had a normal distribution.28 that found that the heart rate remained at the basal level. defined as the highest velocity measured in the Doppler spectrum of the cardiac cycle. respectively. This subject’s results were averaged with the others. The data are in accordance with other studies27. heart rate and hemodynamic values (Vmean.076Ϯ.14. The velocity index (fig 3) decreased significantly from the resting values after the exercise (ie. Vmin) reported in this study were in agreement with previously reported values in the SCI population.01).058Ϯ. *Differing significantly from rest (P<.18 to . Ballaz 473 Doppler spectrum waveform. as shown in the study. Mean blood flow velocity at rest and after passive leg cycle exercise.24 In the case of nondisabled people.03m/s (Pϭ. Fig 3. the heart rate slightly increases at the onset of passive movement because of peripheral afferent reflexes from exercising muscles.96Ϯ.35. The interval between 6 consecutive spectral waveforms was measured manually and converted to cardiac frequencies.16Ϯ0. Arch Phys Med Rehabil Vol 88. There were no differences in minimal blood flow velocity.28 within a few minutes after passive leg cycle exercise. the heart rate value returns to a baseline24. The mean blood velocity (Vmean) in the CFA was calculated using the equation: (½[¼Vmax ϩ 1⁄6Vmin])(60 ϫ HRϪ1) where HR is heart rate. locity (fig 1) and mean blood flow velocity (fig 2) in the femoral artery increased significantly after 10 minutes of exercise. Maximal blood flow ve- Fig 2. and (2) minimal velocity (Vmin).32. Peak blood flow velocity at rest and after passive leg cycle exercise. Statistical Analysis All values are described as mean Ϯ standard deviation.02 to .20m/s. Pϭ. We calculated a velocity index from the difference between Vmax and Vmin divided by Vmax and used it as an indirect indicator of the peripheral resistance.27. At rest. from .038).80Ϯ.38 The increase in blood flow velocity after passive leg cycle exercise is not the result of an increase in heart rate. DISCUSSION Hemodynamic Response to Passive Leg Cycle Exercise The main finding of this study is that in an SCI population. depending on the presence of a normal distribution. Vmax. passive leg cycle exercise significantly increased blood flow velocity in the femoral artery by about 30%.

During muscular contractions.28 whereas Figoni et al46 found no significant increase in cardiac output and stroke volume in SCI subjects with other kinds of passive movements. this exercise seems to be an appropriate technique for increasing peripheral blood flow in SCI subjects. a slight dilatation of the artery. this methodologic problem might have affected the result. rapid vasodilatation. Therefore.12. they verbally reported a sensation of well-being. participates in the increase in the arterial blood flow at the start of exercise.29 the blood flow in the leg was measured after 1 minute. autonomic dysreflexia. The tissue lengthening and shortening induced by the movement of the paralyzed lower limb during passive leg cycle exercise may increase venous return and arterial circulation in a manner similar to the activity of the muscular pump during contraction. This index is an indirect indicator of vascular resistance. the cycling movement was performed at 35rpm. April 2007 Third.” In contrast.39 thereby reducing the venous pressure with a subsequent gain in the gradient pressure across the vascular bed.14. Moreover. We did not use electromyography to con- . In the SCI population. under passive conditions.2. This rhythmic movement provokes an alternate effect of pumping that can be compared with a “peripheral heart. This increase is lower than the increase measured by Radegran and Saltin43 during passive knee extension. however. A cycling movement is the most efficient means by which to enhance the venous return in passive mobilization. femoral arterial blood velocity and inflow during the relaxation phase of the movement was 3.29 Passive leg cycle exercise can be performed for a long period of time without fatigue or discomfort precisely because of its passive nature. passive leg cycle exercise did not induce discomfort. afferent reflexes from the paralyzed lower limbs during such exercise malfunction because the afferent pathways are interrupted. Vascular Resistance The values of velocity index reported here are in accord with the results previously reported in the SCI population. First.42 In addition. When prolonged treatment is required. Instead.42 The role of each factor is still under discussion. The repeated-measures analysis revealed no changes over time for blood flow.40 This mechanical factor may partially promote a sudden initial increase in the blood flow at the beginning of the exercise. which occurs in the venous system. Second.44 diminish the venous return. the P value might reach the significant threshold. High vascular resistance has already been reported in the SCI population. Several protocol differences may explain this discrepancy. Their results are not in agreement with our data from this study. in Ter Woerds’ study. Clinical Implications The results of this study could have important clinical implications. passive movement such as passive leg cycle exercise increases cardiac output. which leads to a decrease in peripheral resistance.27. measured in the CFA immediately after passive leg cycle exercise (Ͻ7s). Studies have shown that in both SCI and able-bodied populations. Recently. The circulation response induced by passive movement is dependent on mechanical factors and seems to be very transient. With more subjects. Ballaz ulation. this is especially important to counteract blood stasis that occurs in immobilized people. The value of increased femoral blood flow velocity induced by passive leg cycle exercise is close to the increase induced by electric stimulation in isometric conditions in healthy subjects.48 Electric stimulation treatment could be contraindicated for people with cardiorespiratory disorders. T1-L1. as this measurement is taken immediately after the movement is completed. Consequently. according to the Franck Starling law. such as passive knee extensions. the flow-mediated dilatation was enhanced in the femoral artery of SCI subjects compared with the dilation in the control group. The ergometer was stopped for about 10 seconds for each measurement. or sensitive skin.41. Muraki also suggested that there was a decrease in peripheral vascular resistance during the exercise because peripheral resistance is determined by cardiac output and blood pressure (peripheral resistance ϭ mean blood pressure/cardiac output).42 toward the heart. particularly in people with SCI. increased by 30%.4 times greater than the baseline values. 11.4. the increase of blood flow in CFA during passive leg cycle exercise may induce. this mechanism does not exist during free passive knee flexion and extension. Nevertheless.6Ϯ7. whereas in this study it was performed at 40rpm (except by 1 subject). Hence. Vmean. level. The intermittent character of this exercise could limit the circulatory response.3 to 4. hence a peripheral mechanism can be hypothesized. The measurement was not taken in the standard supine position because it was important that it be taken immediately after the exercise.5 minutes during cycling. we adjusted the length of the pedal to ensure the greatest ROM. we hypothesized that the circulatory response is higher during the movement than at the exact time of the measurement. Ter Woerds et al29 found that passive cycling does not alter the arterial leg blood flow in SCI subjects. According to the subjects. the position measurement was exactly the same for all data acquisition. by an endothelial mechanism. the electric stimulation leads to fatigue. Their results support this hypothesis. During passive leg cycle exercise. In this study.16 Moreover. Consequently.474 PASSIVE CYCLING IN PARAPLEGICS WITH SCI. but with a smaller amplitude. This is the first time that such a vascular response has been shown after passive movement in SCI subjects. This elevation. then subsequently every 2. Radegran and Saltin43 found that during passive knee extension. our sample included 15 people while Ter Woerds’ sample included only 8 people.15 De Groot et al47 showed that in an SCI population (Nϭ11.9y). These authors indicated that people with SCI could have a preserved endothelial function in their inactive legs. Therefore. The pressure exerted by the weight of the leg on the pedal is increased during the upward movement of the pedal. venous pools in the lower extremities11. results from muscle mechanical factors43 that can promote arterial blood flow during passive movement. time since injury. The off-line analysis of Doppler spectrum waveform was performed by a single investigator who was not blinded. the muscle pump promotes the blood flow by squeezing blood out of the venous capacitance vessels.45 Under physiologic conditions the muscle acts as a pump that propels the blood out of the muscle41. Muraki et al27 found that during passive leg cycle exercise by SCI subjects the cardiac output increased as a result of the elevation of the stroke volume without any increase in heart rate and blood pressure. It is hypothesized that passive leg cycle exercise leads to a slight decrease in arterial resistance. with a P value at . ASIA grades A–B.14 We found a slightly significant decrease (6%) of the velocity index in the CFA in response to passive leg cycle exercise. Study Limitations Doppler measurements were taken with subjects seated in the wheelchair with its back tilted back (150°). the plantar vascular bed is compressed at each revolution of the pedal.25. however. Arch Phys Med Rehabil Vol 88. The results suggest that central cardiac factors do not play a dominant role. this leads to an increase in the cardiac output.

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