Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 4 , Pages 471-476, April 2007

Acute Peripheral Blood Flow Response Induced by Passive Leg Cycle Exercise in People With Spinal Cord Injury

  • Laurent Ballaz, PhD

      Affiliations

    • Physiology and Biomechanics Laboratory, Sports Department, Rennes 2 University, France
    • Corresponding Author InformationReprint 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
    • ,
  • Nicolas Fusco, PhD

      Affiliations

    • Physiology and Biomechanics Laboratory, Sports Department, Rennes 2 University, France
    • ,
  • Armel Crétual, PhD

      Affiliations

    • Physiology and Biomechanics Laboratory, Sports Department, Rennes 2 University, France
    • ,
  • Bernard Langella, MD

      Affiliations

    • Department of Radiology, University Hospital Center, Rennes, France
    • ,
  • Régine Brissot, PhD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, University Hospital Center, Rennes, France.

Article Outline

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.

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 .80±.18m/s to .96±.24m/s, P<.01; and from .058±.02m/s to .076±.03m/s, P<.01; respectively) after 10 minutes of passive leg cycle exercise. Heart rate did not change. The velocity index decreased from 1.23±0.15 to 1.16±0.21 (P=.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

 

THE INCIDENCE OF DEATH among people with spinal cord injury (SCI) is significantly higher than in the general population.1 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 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, 14, 15, 16, 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, 7.6±9.4y). 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, 26, 27, 28 With regard to SCI subjects (T8-L1; ASIA grade A; years postinjury, 14.6±8.8), 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 therapist or by passive cycling. This suggests that there is no significant effect on the peripheral vascular flow with passive limb mobilization in therapy. This assumption requires further study.

Our purpose in this study was to determine the acute peripheral hemodynamic response through passive leg cycle exercise in people with paraplegia. We assumed that passive leg cycle exercise increases the blood flow circulation and decreases the peripheral vascular resistance of CFA in subjects with SCI.

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Methods 

Fifteen people (12 men, 3 women; age, 47±8y) with chronic SCI (T3-12; ASIA grades A–C; nonambulatory; years postinjury, 19±8y) were included in the study. Only 2 subjects had nerve degeneration of the lower limbs resulting in lower motoneuron lesions. This was assessed, based on a physical examination, by the level and the location of the injury. Participants who had been injured at least 6 months before were recruited from the department of rehabilitation at Rennes Hospital. Subjects with any of the following conditions were excluded: history of smoking (past or current), cardiovascular history, metabolic or pulmonary disease, and severely reduced range of motion (ROM) of hip or knee joints. Subjects did not modify their usual treatment for the trial. Four subjects were under medication: 2 used alfuzosine for sphincter hypertonia and the other 2 took baclofen for limb spasticity. The local ethics committee at Rennes approved this trial before the study was started. All patients were informed of the testing procedures and possible undesirable side effects and gave their written consent to participate. Table 1 summarizes their characteristics.

Table 1. Descriptive Characteristics of the Study Subjects (N=15)
SubjectsSexAge (y)Years PostinjuryLesion LevelASIA GradeQuadriceps Spasticity Ashworth Scale30 Score (R/L)
1M6232T11A0/0
2M603T11A0/1
3M4515T8A3/3
4F458L1A0/0
5M3718T12A0/0
6M3820T5C4/1
7F5530T5A1/2
8M3513T4C1/3
9F4833T6A1/3
10M4221T6A0/0
11M4017T9A0/0
12M4924T4A0/0
13M4613T3A0/0
14M4722T12A0/0
15M5520T12A1/3
Mean 4719
SD 88

Abbreviations: F, female; L, left; M, male; R, right; SD, standard deviation.

Exercise Protocol 

Subjects were requested not to drink caffeine and to empty their bladders before engaging in the passive leg cycle exercise. They also underwent a medical examination by the rehabilitation physician (RB) to ensure that the inclusion criteria were met. The level of each subject’s quadriceps spasticity was measured with the Ashworth Scale.30 After the isokinetic motorized cyclea was installed, subjects performed a 10-minute session of passive leg cycle exercise with their backs against the wheelchair back support. The pedaling speed was increased regularly during the first minute to reach the target pedaling rate of 40rpm without evoking any spastic contraction. The length of the pedal (7.5–15cm) was adjusted to ensure the highest ROM. The ROM in the sagittal plane was at least 40° in the knee and 30° in the hip, depending on the flexibility and the length of the subject’s legs (L. Ballaz, PhD, unpublished data, June 2006). 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. The subjects were not disturbed during the testing session.

Doppler Ultrasound Imaging 

We measured red blood cell velocities of the right CFA immediately before and after the exercise session. Measurements were always taken in a darkened environment, in the same position, directly from a standardized wheelchair with the back bent backward (150°). 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). The resting measurement was taken before the exercise session, after a rest period of 5 minutes in the sitting position. Postexercise measurement was always done within 7 seconds of the end of the exercise. 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.

Resting longitudinal images and simultaneous Doppler spectra were obtained from the CFA with a pulsed color-code Doppler device.b We also used a broadband linear array transducer of 5 to 10MHz. The sample volume was placed in the center of the vessel and the length of the volume adjusted to the diameter of the lumen. The equipment settings were kept constant during the protocol, fixed at an angle of 60° for pulsed Doppler. 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. Doppler spectra were registered thrice at the same location at rest and at end-stress. The same examiner (BL) took all the measurements. The reliability of this method of measuring blood cell velocity in the CFA has been demonstrated.31, 32

Another investigator (LB) analyzed an off-line recording of red blood cell velocities. Furthermore, from the corresponding Doppler spectrum waveform, the following parameters of blood velocity were determined among 6 successive cardiac cycles and subsequently averaged: (1) peak systolic blood velocity (Vmax), defined as the highest velocity measured in the Doppler spectrum of the cardiac cycle, and (2) minimal velocity (Vmin), defined as the lowest velocity. The other postexercise measurements were used to control the return to the basal level.

The mean blood velocity (Vmean) in the CFA was calculated using the equation:

where HR is heart rate.33 Because no dilatation of CFA during the exercise was previously reported,32, 34, 35, 36 we assumed that after passive leg cycle exercise there is a variation of blood flow. 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.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. The heart rate was calculated from the Doppler acquisition. The interval between 6 consecutive spectral waveforms was measured manually and converted to cardiac frequencies.

Statistical Analysis 

All values are described as mean ± standard deviation. 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, depending on the presence of a normal distribution. P values less than .05 indicate statistical significance.

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Results 

Exercise Compliance 

All but 1 subject completed the 10-minute exercise session at a rate of 40rpm; the 1 subject asked to stop the rise of the pedaling rate and completed the session at 30rpm. This subject’s results were averaged with the others. There was no significant spastic muscle contraction during the passive cycling exercise.

Effect of Acute Passive Leg Cycle Exercise 

Paired t tests were used for all comparisons because each parameter had a normal distribution. Maximal blood flow velocity (fig 1) and mean blood flow velocity (fig 2) in the femoral artery increased significantly after 10 minutes of exercise, from .80±.18 to .96±.24m/s (P=.001) and from .058±.02 to .076±.03m/s (P=.009), respectively. There were no differences in minimal blood flow velocity. Heart rate also remained unchanged after 10 minutes of exercise. The velocity index (fig 3) decreased significantly from the resting values after the exercise (ie, from 1.23±0.15 to 1.16±0.20m/s, P=.038).

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Discussion 

Hemodynamic Response to Passive Leg Cycle Exercise 

The main finding of this study is that in an SCI population, passive leg cycle exercise significantly increased blood flow velocity in the femoral artery by about 30%, without an increase in the heart rate. At rest, heart rate and hemodynamic values (Vmean, Vmax, Vmin) reported in this study were in agreement with previously reported values in the SCI population.14, 35, 38

The increase in blood flow velocity after passive leg cycle exercise is not the result of an increase in heart rate, as shown in the study. The data are in accordance with other studies27, 28 that found that the heart rate remained at the basal level. In able-bodied persons, the heart rate slightly increases at the onset of passive movement because of peripheral afferent reflexes from exercising muscles.23, 24 In the case of nondisabled people, the heart rate value returns to a baseline24, 27, 28 within a few minutes after passive leg cycle exercise. In the SCI population, however, afferent reflexes from the paralyzed lower limbs during such exercise malfunction because the afferent pathways are interrupted. The results suggest that central cardiac factors do not play a dominant role; hence a peripheral mechanism can be hypothesized. During muscular contractions, the muscle pump promotes the blood flow by squeezing blood out of the venous capacitance vessels,39 thereby reducing the venous pressure with a subsequent gain in the gradient pressure across the vascular bed.40 This mechanical factor may partially promote a sudden initial increase in the blood flow at the beginning of the exercise.41, 42 In addition, rapid vasodilatation, which occurs in the venous system, participates in the increase in the arterial blood flow at the start of exercise.42 The role of each factor is still under discussion, however. Radegran and Saltin43 found that during passive knee extension, femoral arterial blood velocity and inflow during the relaxation phase of the movement was 3.3 to 4.4 times greater than the baseline values. This elevation, under passive conditions, results from muscle mechanical factors43 that can promote arterial blood flow during passive movement.

In this study, Vmean, measured in the CFA immediately after passive leg cycle exercise (<7s), increased by 30%. This increase is lower than the increase measured by Radegran and Saltin43 during passive knee extension. The circulation response induced by passive movement is dependent on mechanical factors and seems to be very transient. Therefore, we hypothesized that the circulatory response is higher during the movement than at the exact time of the measurement, as this measurement is taken immediately after the movement is completed.

In the SCI population, venous pools in the lower extremities11, 44 diminish the venous return.12, 45 Under physiologic conditions the muscle acts as a pump that propels the blood out of the muscle41, 42 toward the heart. 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, but with a smaller amplitude. Consequently, according to the Franck Starling law, this leads to an increase in the cardiac output. Studies have shown that in both SCI and able-bodied populations, passive movement such as passive leg cycle exercise increases cardiac output,2, 4, 25, 27, 28 whereas Figoni et al46 found no significant increase in cardiac output and stroke volume in SCI subjects with other kinds of passive movements, such as passive knee extensions. A cycling movement is the most efficient means by which to enhance the venous return in passive mobilization. During passive leg cycle exercise, the plantar vascular bed is compressed at each revolution of the pedal. The pressure exerted by the weight of the leg on the pedal is increased during the upward movement of the pedal. This rhythmic movement provokes an alternate effect of pumping that can be compared with a “peripheral heart.” In contrast, this mechanism does not exist during free passive knee flexion and extension.

Recently, Ter Woerds et al29 found that passive cycling does not alter the arterial leg blood flow in SCI subjects. Their results are not in agreement with our data from this study. Several protocol differences may explain this discrepancy. First, the cycling movement was performed at 35rpm, whereas in this study it was performed at 40rpm (except by 1 subject). Moreover, we adjusted the length of the pedal to ensure the greatest ROM. Second, in Ter Woerds’ study,29 the blood flow in the leg was measured after 1 minute, then subsequently every 2.5 minutes during cycling. The ergometer was stopped for about 10 seconds for each measurement. The intermittent character of this exercise could limit the circulatory response. Third, our sample included 15 people while Ter Woerds’ sample included only 8 people. The repeated-measures analysis revealed no changes over time for blood flow, with a P value at .14. With more subjects, the P value might reach the significant threshold.

Vascular Resistance 

The values of velocity index reported here are in accord with the results previously reported in the SCI population.14 We found a slightly significant decrease (6%) of the velocity index in the CFA in response to passive leg cycle exercise. This index is an indirect indicator of vascular resistance. It is hypothesized that passive leg cycle exercise leads to a slight decrease in arterial resistance. This is the first time that such a vascular response has been shown after passive movement in SCI subjects.

High vascular resistance has already been reported in the SCI population.15 De Groot et al47 showed that in an SCI population (N=11; ASIA grades A–B; level, T1-L1; time since injury, 11.6±7.9y), the flow-mediated dilatation was enhanced in the femoral artery of SCI subjects compared with the dilation in the control group. These authors indicated that people with SCI could have a preserved endothelial function in their inactive legs. Consequently, the increase of blood flow in CFA during passive leg cycle exercise may induce, by an endothelial mechanism, a slight dilatation of the artery, which leads to a decrease in peripheral resistance.

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. 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 = mean blood pressure/cardiac output). Their results support this hypothesis.

Clinical Implications 

The results of this study could have important clinical implications. According to the subjects, passive leg cycle exercise did not induce discomfort. Instead, they verbally reported a sensation of well-being. Therefore, this exercise seems to be an appropriate technique for increasing peripheral blood flow in SCI subjects. When prolonged treatment is required, 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, autonomic dysreflexia, or sensitive skin.16 Moreover, the electric stimulation leads to fatigue, particularly in people with SCI.29 Passive leg cycle exercise can be performed for a long period of time without fatigue or discomfort precisely because of its passive nature.

Study Limitations 

Doppler measurements were taken with subjects seated in the wheelchair with its back tilted back (150°). The measurement was not taken in the standard supine position because it was important that it be taken immediately after the exercise. Nevertheless, the position measurement was exactly the same for all data acquisition. The off-line analysis of Doppler spectrum waveform was performed by a single investigator who was not blinded. Hence, this methodologic problem might have affected the result. We did not use electromyography to confirm the passive condition during the exercise. Eight of the 15 subjects in this study, however, did not have quadriceps spasticity (Ashworth Scale score, 0). Moreover, there was no control group in this study. It is assumed that the cardiovascular system is solely evoked by passive leg cycle exercise. The cycle trainer used for the experiment is designed for self-powered home use. During this clinical trial, the subjects did not put their legs on the device so to maintain the cardiovascular parameters at their basal level.

Perspective 

It would be interesting to know what functional and structural vascular adaptation occurs after a training period of passive leg cycle exercise. The training should take place at home so that the performance of this home-based trainer can be properly evaluated.

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Conclusions 

The main finding of this study is that a 10-minute session of passive leg cycle exercise markedly increased the femoral mean and maximal blood flow velocity in an SCI population. Furthermore, passive leg cycle exercise leads to a slight decrease in the peripheral arterial resistance. It could also have clinical implications for immobilized people who are prone to lower-limb blood stasis. Hence, further research is required into the effect of passive leg cycle exercise training period on the cardiovascular system.

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References 

  1. Soden RJ, Walsh J, Middleton JW, Craven ML, Rutkowski SB, Yeo JD. Causes of death after spinal cord injury. Spinal Cord. 2000;38:604–610
  2. DeVivo MJ, Kartus PL, Stover SL, Rutt RD, Fine PR. Cause of death for patients with spinal cord injuries. Arch Intern Med. 1989;149:1761–1766
  3. DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil. 1993;74:248–254
  4. Hopman MT, Nommensen E, van Asten WN, Oeseburg B, Binkhorst RA. Properties of the venous vascular system in the lower extremities of individuals with paraplegia. Paraplegia. 1994;32:810–816
  5. Nash MS, Montalvo BM, Applegate B. Lower extremity blood flow and responses to occlusion ischemia differ in exercise-trained and sedentary tetraplegic persons. Arch Phys Med Rehabil. 1996;77:1260–1265
  6. Hopman MT, van Asten WN, Oeseburg B. Changes in blood flow in the common femoral artery related to inactivity and muscle atrophy in individuals with long-standing paraplegia. Adv Exp Med Biol. 1996;388:379–383
  7. Schmidt-Trucksass A, Schmid A, Brunner C, et al. Arterial properties of the carotid and femoral artery in endurance-trained and paraplegic subjects. J Appl Physiol. 2000;89:1956–1963
  8. LaPorte RE, Brenes G, Dearwater S, et al. HDL cholesterol across a spectrum of physical activity from quadriplegia to marathon running. Lancet. 1983;1:1212–1213
  9. Garshick E, Kelley A, Cohen SA, et al. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord. 2005;43:408–416
  10. Olive JL, Dudley GA, McCully KK. Vascular remodeling after spinal cord injury. Med Sci Sports Exerc. 2003;35:901–907
  11. Kinzer SM, Convertino VA. Role of leg vasculature in the cardiovascular response to arm work in wheelchair-dependent populations. Clin Physiol. 1989;9:525–533
  12. Hopman MT, Verheijen PH, Binkhorst RA. Volume changes in the legs of paraplegic subjects during arm exercise. J Appl Physiol. 1993;75:2079–2083
  13. Thijssen DH, Heesterbeek P, van Kuppevelt DJ, Duysens J, Hopman MT. Local vascular adaptations after hybrid training in spinal cord-injured subjects. Med Sci Sports Exerc. 2005;37:1112–1118
  14. Gerrits HL, de Haan A, Sargeant AJ, van Langen H, Hopman MT. Peripheral vascular changes after electrically stimulated cycle training in people with spinal cord injury. Arch Phys Med Rehabil. 2001;82:832–839
  15. Hopman MT, Groothuis JT, Flendrie M, Gerrits KH, Houtman S. Increased vascular resistance in paralyzed legs after spinal cord injury is reversible by training. J Appl Physiol. 2002;93:1966–1972
  16. Nash MS, Jacobs PL, Montalvo BM, Klose KJ, Guest RS, Needham-Shropshire BM. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 5 (Lower extremity blood flow and hyperemic responses to occlusion are augmented by ambulation training). Arch Phys Med Rehabil. 1997;78:808–814
  17. Hooker SP, Figoni SF, Rodgers MM, et al. Physiologic effects of electrical stimulation leg cycle exercise training in spinal cord injured persons. Arch Phys Med Rehabil. 1992;73:470–476
  18. Jacobs PL, Nash MS. Modes, benefits, and risks of voluntary and electrically induced exercise in persons with spinal cord injury. J Spinal Cord Med. 2001;24:10–18
  19. Ditor DS, Macdonald MJ, Kamath MV, et al. The effects of body-weight supported treadmill training on cardiovascular regulation in individuals with motor-complete SCI. Spinal Cord. 2005;43:664–673
  20. Maynard FM, Bracken MB, Creasey G, et al. American Spinal Injury Association International Standards for Neurological and Functional Classification of Spinal Cord Injury. Spinal Cord. 1997;35:266–274
  21. Kakebeeke TH, Lechner HE, Knapp PA. The effect of passive cycling movements on spasticity after spinal cord injury: preliminary results. Spinal Cord. 2005;43:483–488
  22. Rosche J, Paulus C, Maisch U, Kaspar A, Mauch E, Kornhuber HH. The effects of therapy on spasticity utilizing a motorized exercise-cycle. Spinal Cord. 1997;35:176–178
  23. Nurhayati Y, Boutcher SH. Cardiovascular response to passive cycle exercise. Med Sci Sports Exerc. 1998;30:234–238
  24. Nobrega AC, Williamson JW, Friedman DB, Araujo CG, Mitchell JH. Cardiovascular responses to active and passive cycling movements. Med Sci Sports Exerc. 1994;26:709–714
  25. Figoni SF, Rodgers MM, Glaser RM, et al. Physiologic responses of paraplegics and quadriplegics to passive and active leg cycle ergometry. J Am Paraplegia Soc. 1990;13:33–39
  26. Nash MS, Bilsker MS, Kearney HM, Ramirez JN, Applegate B, Green BA. Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons. Paraplegia. 1995;33:80–89
  27. Muraki S, Yamasaki M, Ehara Y, Kikuchi K, Seki K. Cardiovascular and respiratory responses to passive leg cycle exercise in people with spinal cord injuries. Eur J Appl Physiol Occup Physiol. 1996;74:23–28
  28. Muraki S, Ehara Y, Yamasaki M. Cardiovascular responses at the onset of passive leg cycle exercise in paraplegics with spinal cord injury. Eur J Appl Physiol. 2000;81:271–274
  29. Ter Woerds W, De Groot PC, Kuppevelt DH, Hopman MT. Passive leg movements and passive cycling do not alter arterial leg blood flow in subjects with spinal cord injury. Phys Ther. 2006;86:636–645
  30. Ashworth B. Preliminary trial of carisoprodol in multiple sclerosis. Practitioner. 1964;192:540–542
  31. Demolis PD, Asmar RG, Levy BI, Safar ME. Non-invasive evaluation of the conduit function and the buffering function of large arteries in man. Clin Physiol. 1991;11:553–564
  32. Radegran G. Ultrasound Doppler estimates of femoral artery blood flow during dynamic knee extensor exercise in humans. J Appl Physiol. 1997;83:1383–1388
  33. van Asten WN, Beijneveld WJ, Pieters BR, van Lier HJ, Wijn PF, Skotnicki SH. Assessment of aortoiliac obstructive disease by Doppler spectrum analysis of blood flow velocities in the common femoral artery at rest and during reactive hyperemia. Surgery. 1991;109:633–639
  34. Olive JL, Slade JM, Dudley GA, McCully KK. Blood flow and muscle fatigue in SCI individuals during electrical stimulation. J Appl Physiol. 2003;94:701–708
  35. Olive JL, McCully KK, Dudley GA. Blood flow response in individuals with incomplete spinal cord injuries. Spinal Cord. 2002;40:639–645
  36. Shoemaker JK, Phillips SM, Green HJ, Hughson RL. Faster femoral artery blood velocity kinetics at the onset of exercise following short-term training. Cardiovasc Res. 1996;31:278–286
  37. Johnston KW, Kassam M, Koers J, Cobbold RS, MacHattie D. Comparative study of four methods for quantifying Doppler ultrasound waveforms from the femoral artery. Ultrasound Med Biol. 1984;10:1–12
  38. Boot CR, van Langen H, Hopman MT. Arterial vascular properties in individuals with spina bifida. Spinal Cord. 2003;41:242–246
  39. Pollack AA, Taylor BE, Myers TT, Wood EH. The effect of exercise and body position on the venous pressure at the ankle in patients having venous valvular defects. J Clin Invest. 1949;28:559–563
  40. Folkow B, Gaskell P, Waaler BA. Blood flow through limb muscles during heavy rhythmic exercise. Acta Physiol Scand. 1970;80:61–72
  41. Sheriff DD, Rowell LB, Scher AM. Is rapid rise in vascular conductance at onset of dynamic exercise due to muscle pump?. Am J Physiol. 1993;265(4 Pt 2):H1227–H1234
  42. Tschakovsky ME, Shoemaker JK, Hughson RL. Vasodilation and muscle pump contribution to immediate exercise hyperemia. Am J Physiol. 1996;271(4 Pt 2):H1697–H1701
  43. Radegran G, Saltin B. Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol. 1998;274(1 Pt 2):H314–H322
  44. Figoni SF. Exercise responses and quadriplegia. Med Sci Sports Exerc. 1993;25:433–441
  45. Hopman MT, Oeseburg B, Binkhorst RA. Cardiovascular responses in paraplegic subjects during arm exercise. Eur J Appl Physiol Occup Physiol. 1992;65:73–78
  46. Figoni SF, Glaser RM, Rodgers MM, et al. Acute hemodynamic responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise. J Rehabil Res Dev. 1991;28:9–18
  47. De Groot PC, Poelkens F, Kooijman M, Hopman MT. Preserved flow-mediated dilation in the inactive legs of spinal cord-injured individuals. Am J Physiol Heart Circ Physiol. 2004;287:H374–H380
  48. Janssen TW, Hopman MT. Blood flow response to electrically induced twitch and tetanic lower-limb muscle contractions. Arch Phys Med Rehabil. 2003;84:982–987
  • a Ergo-dom; DCO Engineering Pack Technologie du Zoopole Developpement, 22 440 Ploufragan, France.
  • b Titan; SonoSite Inc, 21919 30th Dr SE, Bothell, WA 98021-3904.

 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.

PII: S0003-9993(07)00003-2

doi:10.1016/j.apmr.2007.01.011

Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 4 , Pages 471-476, April 2007

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