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ORIGINAL ARTICLE

Acute Peripheral Blood Flow Response Induced by Passive LegCycle Exercise in People With Spinal Cord Injury Laurent Ballaz, PhD, Nicolas Fusco, PhD, Armel Crtual, PhD, Bernard Langella, MD, Rgine Brissot, PhD

ABSTRACT. Ballaz L, Fusco N, Crtual A, Langella B,Brissot R. Acute peripheral blood ow response induced bypassive leg cycle exercise in people with spinal cord injury.Arch Phys Med Rehabil 2007;88:471-6.

Objective: To determine the acute femoral artery hemody-namic response in paraplegic subjects during a passive legcycle exercise.

Design: Case series.Setting: Department of physical medicine and rehabilitation

in a university in France.Participants: A volunteer sample of 15 people with trau-

matic 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, maxi-

mal (Vmax), and minimal femoral artery blood ow velocity atrest and immediately after the passive leg cycle exercise, usingquantitative duplex Doppler ultrasound. We calculated meanblood ow velocity (Vmean) and velocity index, representingthe 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 cycleexercise. Heart rate did not change. The velocity index de-creased from 1.23 0.15 to 1.16 0.21 (P .038).

Conclusions: The results of this study suggest that acutepassive leg cycle exercise increases vascular blood ow veloc-ity in paralyzed legs of people with paraplegia. This exercisecould have clinical implications for immobilized persons.

Key Words: Blow ow velocity; Doppler ultrasound; Fem-oral artery; Rehabilitation; Spinal cord injuries.

2007 by the American Congress of Rehabilitation Medi-cine and the American Academy of Physical Medicine and Rehabilitation

T HE INCIDENCE OF DEATH among people with spinalcord in jury (SCI) is signicantly higher than in the generalpopulation. 1 SCI subjects are prone to severe card iovasculardisorders that present an increased risk of mortality. 2 The risk increases with the degree of dependency, in particular fo rpeople who are totally dependent on wheelchairs for mobility. 3Two factors related to this risk are loss of autonomic control

and lack of movement, which lead to vascular disorders. 4,5 Thisinduces an important structural and functional remodeling inthe peripheral vascular system of paralyzed limbs; this remod-eling includes reduced dia meter of the common femoral arte ry(CFA), 5,6 arterial stiffness, 7 and lesser blood ow to the legs. 5,6

Another factor is the high occurrence of metabolic syndromes(eg, obesity, hypercholesterolemia) caused by a lack of phys-ical exercise, 8,9 which is recognized as a cardiovascular ischemiafactor.

Studies of people with long-lasting SCI have shown that thefemoral artery blood ow at rest is red uced by about 50% whencompared with able-bodied subjects. 5,6 This adaptation hasbeen related to muscular atrophy, and even though there isrelatively little change in the ow with respect to the muscle

mass,10

improvement in lower-extremity circulation is highlydesirable because decient lower-e xtremity circulation and ve-nous stagnation lead to thrombosis. 5 Thrombosis prevalence ishigher in the SCI populati on than in the general population,even in the chronic phase. 2,3 This vascular remodeling mayreect the consequences of reduced activity.

Arm exercises, which subjects with SCI could easily do,neither target the vessels in the lowe r limbs nor promotelower-limb circulation in those subjects. 11,12 The set of poten-tial lower-limb exercises is limited in the case of wheelchairusers. Since the 1990s, functional electric stimulation ( FES)has shown great promise as a cardiovascular stimulus. 13-17Some studies show that a relatively short period of FES legcycle exercise training may lead to peripheral vascular im-provement and enhance peri pheral circulation as measured by

an echo Doppler ultrasound.14,15,17

This technique, however,has been reported to carry the risks of skin burns, autonomicdysreexia, and bone fractures. 18

Ditor et al 19 have shown that body-weight support treadmilltraining (BWSTT) may increase femoral artery compliance insubjects with complete motor SCI (C4-T12; American SpinalInjury Association 20 [ASIA] grade A and B; years postinjury,7.6 9.4y). Hence, use of this technique should be encouragedas a means of improving cardiovascular health in the SCIpopulation. 19 Its widespread use, however, is hindered becauseBWSTT requires both trainers and expensive equipment. Thisstudy, however, demonstrates that passive movement can leadto structural peripheral vascular adaptation.

The simple passive leg cycle exercise is easily performed bypeople conned to wheelchairs. 21,22 Powered cycle trainers that

subjects can use at home while sitting in a wheelchair are alsocommercially available. Very few studies have investigated thecentral cardiopulm onary response to passive leg cycle exercisein healthy subjects 23,24 or in SCI patients. 25-28 With regard toSCI subjects (T8-L1; ASIA grade A; years postinjury,14.6 8.8), Muraki et al 27,28 suggest that passive leg cycleexercise enhances the cardiac output by increasing the strokevolume, provided the exercise is performed at 40 rounds perminute (rpm). This increased cardiac output probably resultsfrom the activation of the muscular pump that increases thevenous return from the passively moved muscles. In a recentstudy, Ter Woerds et al 29 could not nd any alteration in thearterial leg blood ow either after passive leg movement by a

From the Physiology and Biomechanics Laboratory, Sports Department, Rennes 2University, France (Ballaz, Fusco, Crtual); 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 nancial interest in the results of the research

supporting this article has or will confer a benet upon the author(s) or upon anyorganization with which the author(s) is/are associated.

Reprint requests to Laurent Ballaz, PhD, Laboratoire de Physiologie et de Biom-canique de lExercice Musculaire, UFR-APS, Universit Rennes 2, Ave CharlesTillon CS 24 414, 35 044 Rennes Cedex, France, e-mail: [email protected].

0003-9993/07/8804-11035$32.00/0doi:10.1016/j.apmr.2007.01.011

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therapist or by passive cycling. This suggests that there is nosignicant effect on the peripheral vascular ow with passivelimb mobilization in therapy. This assumption requires furtherstudy.

Our purpose in this study was to determine the acute periph-eral hemodynamic response through passive leg cycle exercisein people with paraplegia. We assumed that passive leg cycleexercise increases the blood ow circulation and decreases theperipheral vascular resistance of CFA in subjects with SCI.

METHODSFifteen people (12 men, 3 women; age, 47 8y) with chronic

SCI (T3-12; ASIA grades AC; nonambulatory; years postinjury, 19 8y) were included in the study. Only 2 subjects hadnerve degeneration of the lower limbs resulting in lower mo-toneuron lesions. This was assessed, based on a physical ex-amination, by the level and the location of the injury. Partici-pants who had been injured at least 6 months before wererecruited from the department of rehabilitation at Rennes Hos-pital. Subjects with any of the following conditions were ex-cluded: history of smoking (past or current), cardiovascularhistory, metabolic or pulmonary disease, and severely reducedrange of motion (ROM) of hip or knee joints. Subjects did not

modify their usual treatment for the trial. Four subjects wereunder medication: 2 used alfuzosine for sphincter hypertoniaand the other 2 took baclofen for limb spasticity. The localethics committee at Rennes approved this trial before the studywas started. All patients were informed of the testing proce-dures and possible undesirab le side effects and gave theirwritten consent to participate. Table 1 summarizes their char-acteristics.

Exercise ProtocolSubjects 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 rehabilita-tion physician (RB) to ensure that the inclusion criteria weremet. The level of each subjects quadriceps spasticity was

measured with the Ashworth Scale.30

After the isokinetic mo-torized cycle a was installed, subjects performed a 10-minutesession of passive leg cycle exercise with their backs againstthe wheelchair back support. The pedaling speed was increased

regularly during the rst minute to reach the target pedalingrate of 40rpm without evoking any spastic contraction. Thelength of the pedal (7.515cm) was adjusted to ensure thehighest ROM. The ROM in the sagittal plane was at least 40in the knee and 30 in the hip, depending on the exibility andthe length of the subjects legs (L. Ballaz, PhD, unpublisheddata, June 2006). The test was performed between 10:00 AMand 1:00 PM in an experiment room in which the temperaturewas maintained at between 21 and 24C. The subjects werenot disturbed during the testing session.

Doppler Ultrasound ImagingWe measured red blood cell velocities of the right CFA

immediately before and after the exercise session. Measure-ments were always taken in a darkened environment, in thesame position, directly from a standardized wheelchair with theback bent backward (150). The measurement was taken withthe subjects feet on the pedals and the right leg in the mostextended position (right pedal placed forward). The restingmeasurement was taken before the exercise session, after a restperiod of 5 minutes in the sitting position. Postexercise mea-surement was always done within 7 seconds of the end of theexercise. The wheelchair back was tilted and the examiner

placed the probe in front of the end of the passive cycleexercise so that the measurement was taken immediately afterthe end of the exercise.

Resting longitudinal images and simultaneous Doppler spec-tra were obtained from the CFA with a pulsed color-codeDoppler device. b We also used a broadband linear array trans-ducer of 5 to 10MHz. The sample volume was placed in thecenter of the vessel and the length of the volume adjusted to thediameter of the lumen. The equipment settings were keptconstant during the protocol, xed at an angle of 60 for pulsedDoppler. The probe was placed about 2cm away from the fork of the CFA by using supercial and deep femoral arteries aslandmarks to be located on axial scans. Doppler spectra wereregistered 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 me asuring blood cell velocity inthe CFA has been demonstrated. 31,32Another investigator (LB) analyzed an off-line recording of

red blood cell velocities. Furthermore, from the corresponding

Table 1: Descriptive Characteristics of the Study Subjects (N 15)

Subjects Sex Age (y) Years Post in jury Lesion Level ASIA Grade Quadriceps Spastici ty Ashworth Scale 30 Score (R/L)

1 M 62 32 T11 A 0/02 M 60 3 T11 A 0/13 M 45 15 T8 A 3/34 F 45 8 L1 A 0/05 M 37 18 T12 A 0/06 M 38 20 T5 C 4/17 F 55 30 T5 A 1/28 M 35 13 T4 C 1/39 F 48 33 T6 A 1/3

10 M 42 21 T6 A 0/011 M 40 17 T9 A 0/012 M 49 24 T4 A 0/013 M 46 13 T3 A 0/014 M 47 22 T12 A 0/015 M 55 20 T12 A 1/3

Mean 47 19SD 8 8

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

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Doppler spectrum waveform, the following parameters of blood velocity were determined among 6 successive cardiaccycles and subsequently averaged: (1) peak systolic bloodvelocity (Vmax), dened as the highest velocity measured inthe Doppler spectrum of the cardiac cycle, and (2) minimalvelocity (Vmin), dened as the lowest velocity. The otherpostexercise measurements were used to control the return tothe basal level.

The mean blood velocity (Vmean) in the CFA was calcu-lated using the equation:

([Vmax 1 6 Vmin])(60 HR 1)

where HR is heart rate. 33 Because no dilatati on of CFA duringthe exercise was previously reported, 32,34-36 we assumed thatafter passive leg cycle exercise there is a variation of bloodow. We calculated a velocity index from the difference be-tween Vmax and Vmin divided by Vmax and used it as anindirect indicator of the peripheral resistance. 14 This index wasa slight modication of the pulsatility index 37 and was inde-pendent of possible differences in the insonation angle of theDoppler probe during recording. The heart rate was calculatedfrom the Doppler acquisition. The interval between 6 consec-utive spectral waveforms was measured manually and con-verted to cardiac frequencies.Statistical Analysis

All values are described as mean standard deviation. Weused paired t tests for dependent groups or Mann-Whitney U tests to compare variables for vascular properties of the femoralartery before and after the exercise session, depending on thepresence of a normal distribution. P values less than .05 indi-cate statistical signicance.

RESULTS

Exercise ComplianceAll but 1 subject completed the 10-minute exercise session at

a rate of 40rpm; the 1 subject asked to stop the rise of thepedaling rate and completed the session at 30rpm. This subjects results were averaged with the others. There was nosignicant spastic muscle contraction during the passive cy-cling exercise.

Effect of Acute Passive Leg Cycle ExercisePaired t tests were used for all comparisons because each

parameter had a normal distribution. Maximal blood ow ve-

locity (g 1) and mean blood ow velocity ( g 2) in thefemoral artery increased signicantly after 10 minutes of ex-ercise, from .80 .18 to .96 .24m/s (P .001) and from.058 .02 to .076 .03m/s (P .009), respectively. There wereno differences in minimal blood ow velocity. Heart rate also

remained unchanged after 10 minutes of exercise. The velocityindex (g 3) decreased signicantly from the resting valuesafter the exercise (ie, from 1.23 0.15 to 1.16 0.20m/s,P .038).

DISCUSSION

Hemodynamic Response to Passive Leg Cycle ExerciseThe main nding of this study is that in an SCI population,

passive leg cycle exercise signicantly increased blood owvelocity in the femoral artery by about 30%, without an in-crease in the heart rate. At rest, heart rate and hemodynamicvalues (Vmean, Vmax, Vmin) reported in this study were inagreement with previously reported values in the SCI popula-tion.14,35,38

The increase in blood ow velocity after passive leg cycleexercise is not the result of an increase in heart rate, as sh ownin the study. The data are in accordance with other studies 27,28

that found that the heart rate remained at the basal level. Inable-bodied persons, the heart rate slightly increases at theonset of passive movement be cause of peripheral afferent re-exes from exercising muscles. 23,24 In the case of nondisabledpeople, the heart rate value returns to a baseline 24,27,28 within afew minutes after passive leg cycle exercise. In the SCI pop-

Fig 1. Peak blood ow velocity at rest and after passive leg cycleexercise. *Differing signicantly from rest ( P < .01).

Fig 2. Mean blood ow velocity at rest and after passive leg cycleexercise. *Differing signicantly from rest ( P < .01).

Fig 3. Velocity index at rest and after passive leg cycle exercise.*Differing signicantly from rest ( P < .05).

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ulation, however, afferent reexes from the paralyzed lowerlimbs during such exercise malfunction because the afferentpathways are interrupted. The results suggest that central car-diac factors do not play a dominant role; hence a peripheralmechanism can be hypothesized. During muscular contrac-tions, the muscle pump promotes the blood ow by squeezingblood out of the venous capacitance vessels, 39 thereby reducingthe venous pressure with a su bsequent gain in the gradientpressure across the vascular bed. 40 This mechanical factor maypartially promote a sudden ini tial increase in the blood ow atthe beginning of the exercise. 41,42 In addition, rapid vasodila-tation, which occurs in the venous system, participates in theincrease in the arterial blood ow at the start of exercise. 42 Therole of each factor is still under discussion, however. Radegranand Saltin 43 found that during passive knee extension, femoralarterial blood velocity and inow during the relaxation phase of the movement was 3.3 to 4.4 times greater than the baselinevalues. This elevation, und er passive conditions, results frommuscle mechanical factors 43 that can promote arterial bloodow during passive movement.

In this study, Vmean, measured in the CFA immediatelyafter passive leg cycle exercise ( 7s), increased by 30%. Thisincrease is lower than the increase measured by Radegran and

Saltin43

during passive knee extension. The circulation re-sponse induced by passive movement is dependent on mechan-ical factors and seems to be very transient. Therefore, wehypothesized that the circulatory response is higher during themovement than at the exact time of the measurement, as thismeasurement is taken immediately after the movement is com-pleted.

In the SCI population, venous poo ls in the lower extremi-ties11,44 diminish the venous return. 12,45 Under physiologicconditions th e muscle acts as a pump that propels the blood outof the muscle 41,42 toward the heart. The tissue lengthening andshortening induced by the movement of the paralyzed lowerlimb during passive leg cycle exercise may increase venousreturn and arterial circulation in a manner similar to the activityof 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 haveshown that in both SCI and able-bodied populations, passivemovem ent such as passive leg cycle e xercise increases cardiacoutput, 2,4,25,27,28 whereas Figoni et al 46 found no signicantincrease in cardiac output and stroke volume in SCI subjectswith other kinds of passive movements, such as passive kneeextensions. A cycling movement is the most efcient means bywhich to enhance the venous return in passive mobilization.During passive leg cycle exercise, the plantar vascular bed iscompressed at each revolution of the pedal. The pressureexerted by the weight of the leg on the pedal is increased duringthe upward movement of the pedal. This rhythmic movementprovokes an alternate effect of pumping that can be comparedwith a peripheral heart. In contrast, this mechanism does not

exist during free passive kne e exion and extension.Recently, Ter Woerds et al 29 found that passive cycling doesnot alter the arterial leg blood ow in SCI subjects. Theirresults 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, whereasin this study it was performed at 40rpm (except by 1 subject).Moreover, we adjusted the length of the pe dal to ensure thegreatest ROM. Second, in Ter Woerds study, 29 the blood owin the leg was measured after 1 minute, then subsequentlyevery 2.5 minutes during cycling. The ergometer was stoppedfor about 10 seconds for each measurement. The intermittentcharacter of this exercise could limit the circulatory response.

Third, our sample included 15 people while Ter Woerds sampleincluded only 8 people. The repeated-measures analysis revealedno changes over time for blood ow, with a P value at .14. Withmore subjects, the P value might reach the signicant threshold.

Vascular ResistanceThe values of velocity index reported here are in acco rd with

the results previously reported in the SCI population. 14 Wefound a slightly signicant decrease (6%) of the velocity indexin the CFA in response to passive leg cycle exercise. This indexis an indirect indicator of vascular resistance. It is hypothesizedthat passive leg cycle exercise leads to a slight decrease inarterial resistance. This is the rst time that such a vascularresponse has been shown after passive movement in SCI subjects.

High vascula r resistance has al ready been reported in theSCI population. 15 De Groot et al 47 showed that in an SCIpopulation (N 11; ASIA grades AB; level, T1-L1; time sinceinjury, 11.6 7.9y), the ow-mediated dilatation was enhancedin the femoral artery of SCI subjects compared with the dilationin the control group. These authors indicated that people withSCI could have a preserved endothelial function in their inac-

tive legs. Consequently, the increase of blood ow in CFAduring passive leg cycle exercise may induce, by an endo-thelial mechanism, a slight dilatation of the artery, whichleads to a decrease in peripheral resistance.

Muraki et al 27 found that during passive leg cycle exerciseby SCI subjects the cardiac output increased as a result of theelevation of the stroke volume without any increase in heartrate and blood pressure. Muraki also suggested that there wasa decrease in peripheral vascular resistance during the exercisebecause peripheral resistance is determined by cardiac outputand blood pressure (peripheral resistance mean blood pres-sure/cardiac output). Their results support this hypothesis.

Clinical ImplicationsThe results of this study could have important clinical im-

plications. According to the subjects, passive leg cycle exercisedid not induce discomfort. Instead, they verbally reported asensation of well-being. Therefore, this exercise seems to be anappropriate technique for increasing peripheral blood ow inSCI subjects. When prolonged treatment is required, this isespecially important to counteract blood stasis that occurs inimmobilized people. The value of increased femoral blood owvelocity induced by passive leg cycle exercise is close to theincrease induced by electric stimulation in isometric conditionsin healthy subjects. 48 Electric stimulation treatment could becontraindicated for people with cardi orespiratory disorders,autonomic dysreexia, or sensitive skin. 16 Moreover, the elec-tric stimulation leads to fatigue, particularly in people withSCI. 29 Passive leg cycle exercise can be performed for a longperiod of time without fatigue or discomfort precisely becauseof its passive nature.

Study LimitationsDoppler measurements were taken with subjects seated in

the wheelchair with its back tilted back (150). The measure-ment was not taken in the standard supine position because itwas important that it be taken immediately after the exercise.Nevertheless, the position measurement was exactly the samefor all data acquisition. The off-line analysis of Doppler spec-trum waveform was performed by a single investigator whowas not blinded. Hence, this methodologic problem might haveaffected the result. We did not use electromyography to con-




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rm the passive condition during the exercise. Eight of the 15subjects in this study, however, did not have quadriceps spas-ticity (Ashworth Scale score, 0). Moreover, there was no con-trol group in this study. It is assumed that the cardiovascularsystem is solely evoked by passive leg cycle exercise. Thecycle trainer used for the experiment is designed for self-powered home use. During this clinical trial, the subjects didnot put their legs on the device so to maintain the cardiovas-

cular parameters at their basal level.

PerspectiveIt would be interesting to know what functional and struc-

tural vascular adaptation occurs after a training period of pas-sive leg cycle exercise. The training should take place at homeso that the performance of this home-based trainer can beproperly evaluated.

CONCLUSIONSThe main nding of this study is that a 10-minute session of

passive leg cycle exercise markedly increased the femoralmean and maximal blood ow velocity in an SCI population.

Furthermore, passive leg cycle exercise leads to a slight de-crease in the peripheral arterial resistance. It could also haveclinical implications for immobilized people who are prone tolower-limb blood stasis. Hence, further research is requiredinto the effect of passive leg cycle exercise training period onthe cardiovascular system.

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