exercise training for claudicants: changes in blood flow, cardiorespiratory status, metabolic...

Eur J Vasc Endovasc Surg 20, 72–78 (2000)doi:10.1053/ejvs.2000.1137, available online at http://www.idealibrary.com on

Exercise Training for Claudicants: Changes in Blood Flow,Cardiorespiratory Status, Metabolic Functions, Blood Rheology and

Lipid Profile

K. H. Tan1, D. Cotterrell2, K. Sykes2, G. R. J. Sissons1, L. de Cossart1 and P. R. Edwards∗1

1Department of Vascular Surgery, Countess of Chester Hospital, U.K.; 2Centre for Exercise and Nutrition Science,Chester College, U.K.

Objective: exercise training improves the walking distance of claudicants. The aim of this study was to investigatefactors associated with the improvement in the maximum walking distance (MWD) in respect to cardiovascular, respiratoryand metabolic adaptations.Methods: forty claudicants were studied. Common femoral artery blood flow (BF), heart rate (HR), oxygen consumption(VO2), respiratory exchange ratio (RER), lactate levels, blood rheology and lipid profiles were measured. Tests wererepeated after 3 months of exercise training.Results: fifteen patients did not complete the exercise program. For patients who did complete the program, MWDimproved by 82%. A significant reduction in HR and VO2 during exercise was demonstrated. No significant changesoccurred in BF or RER. Although MWD increased significantly, there was no increase in recovery VO2 (oxygen debt).A significant reduction in post-exercise lactate levels occurred. Blood rheology was unchanged, but an improvement inHDL levels was noted.Conclusions: many claudicants could not complete an exercise program, mainly due to osteoarthritis. Exercise trainingimproved exercise tolerance significantly without any increase in BF. The HR and oxygen cost of similar exercise wasreduced. An improved MWD did not correlate with a higher oxygen debt or lactate load. Favourable changes in lipidprofiles occurred.

Key Words: Claudicants; Exercise Training; Cholesterol; Oxygen; Lactate.

ing distance.8–10 Therefore, other mechanisms are in-Introductionvolved.

A recent study on cardiac patients showed aIntermittent claudication affects 1.8% of the populationfavourable effect of exercise training on the lipid pro-under 60 years of age, rising to 5.2% in the over-70s.1

files.11 It is well recognised that claudicants have a highThere is increasing evidence that exercise training isincidence of hypercholesterolaemia.12 This predisposesthe treatment of choice for patients with intermittentto coronary events, which are the main cause of deathclaudication. Many studies have shown the benefits ofin claudicants.13 One study showed that a 10%exercise rehabilitation in improving both the walking(0.6 mmol/l−1) reduction in total cholesterol level led todistance2,3 and quality of life score,4 whilst reducinga 38% reduction in ischaemic heart disease.14 Anotherthe overall cost of treatment.5 As a treatment modalitystudy has shown that therapeutic lowering of cho-for claudicants, exercise rehabilitation has similar ef-lesterol (by statins) improved endothelial mediatedficacy compared to angioplasty.6,7 However, the mech-vasodilatation, which is impaired in patients withanisms involved are not clearly understood. Vascularhypercholesterolaemia and atherosclerosis.15

bypass grafts improve the exercise tolerance of clau-This study was designed to determine the effects ofdicants by increasing blood flow to the lower limbs.

exercise training on a group of mild to moderateThis phenomenon does not occur after exercise train-claudicants in respect of the common femoral arterying, even with a significant improvement in the walk-blood flow, cardiorespiratory function, metabolic ad-aptation and changes in blood rheology. The secondary

∗ Please address all correspondence to: P. R. Edwards, Departmentobjective of this study was to examine the changes inof Vascular Surgery, Countess of Chester Hospital, Liverpool Road,

Chester CH2 1UL, U.K. blood lipids of claudicants after exercise training.

1078–5884/00/070072+07 $35.00/0 2000 Harcourt Publishers Ltd.

Exercise Training for Claudicants 73

Materials and Methods A constant load treadmill protocol was used. Thetreadmill speed was 1.8 kph and the gradient was

Patients set from 0 to 12%, depending on the ability of theindividual. On the day of treadmill testing, all the

This study was approved by South Cheshire Local equipment was calibrated. Patients were instructednot to perform any exercise for 24 h and to fast for atResearch Ethics Committee.

Between December 1998 and May 1999, all new least 6 h. After resting for 30 min, the patients walkedon the treadmill to their maximum walking distance.patients with intermittent claudication referred to the

Vascular Surgical Department at the Countess of Ches- After completion of exercise, the patients rested on achair (recovery phase). Simultaneous measurementter Hospital were invited to participate in this study.

Intermittent claudication was diagnosed clinically and of heart rate (Polar Electro, Finland) and respiratoryparameters were undertaken during exercise and theconfirmed by the presence of an ankle brachial pres-

sure index (Multi-Dopplex, HNE Health Care) of less recovery phase. The subjects wore a respiratory maskthat was connected to a respiratory analyser (Cortexthan 0.9 after exercise on a Stresst’er calf ergometer

(Stu-ert Medical Device)16 for 2 min. The site of the Metamax, Germany). Ventilation parameters meas-ured were minute ventilation (VE), oxygen con-arterial disease was determined by colour duplex scan-

ning (Toshiba, SSA-270A). For the purposes of this sumption (VO2), carbon dioxide production (VCO2)and respiratory exchange ratio. Respiratory exchangestudy, mild to moderate claudication was defined as

a reported maximum walking distance of between 50 ratio (RER) was defined as VCO2/VO2. Patients withminimum claudication (defined in this study as thoseand 450 m. Patients were excluded if they had any

features of critical ischaemia, poor mobility leading to who walked for more than 15 min at 12% gradient,without stopping), during baseline testing, were ex-difficulty in walking and unstable cardiorespiratory

conditions. Patients on long-term medication con- cluded from trial. Treadmill testing was repeated afterthe exercise training was completed utilising the sametinued on their treatment. No new prescriptions were

introduced and any patients requiring a change in original treadmill settings for each patient.medication were excluded. Patients reporting a sig-nificant change in their walking distance between The exercise programreferral and entry into the study (approximately 2

The patients were instructed on an exercise programmonths) were considered to have unstable claudicationof walking 1 h each day to the claudicating limit, forand were excluded.5 days in a week. A patient information sheet and anexercise logbook were given. No further supervision

Methods was undertaken, apart from a weekly telephone con-sultation to monitor progress and encourage the

Common femoral artery blood flow patients in continuing their exercise training. PatientsThe common femoral artery blood flow of the affected were re-tested after 3 months of training.limbs was measured using a pulsed Doppler (6 MHz)incorporated within a 7.5 MHz Duplex probe (Sonicaid Blood samplingVasoview, U.K.). Measurements were performed whilethe patient was at rest (supine), during exercise for Blood sampling was facilitated by insertion of a 22-2 min on the Stresst’er calf ergometer and 2 min after gauge intravenous catheter into the basilic vein at thecompletion of exercise. Blood flow was derived from elbow. Blood for plasma viscosity, packed cell volumethe diameter of the artery, angle of the probe, mean and lipid profiles was obtained at rest (before treadmillvelocity over the cardiac cycle and pulsatility index. testing). Venous lactate levels were measured at rest,Calculation was performed by a commercial signal and at 1 and 6 min during the recovery phase followinganalyser (Scimed Dopstation). To reduce variability, a the exercise. Blood lipids were measured by Technicalsingle investigator performed all the scans and the Axon, venous lactate by Accusport, Rush Diagnosticangle of insonation was always set close to 60° (range and plasma viscosity by Coulter Viscometer.55–62°). Tests were repeated on completion of theexercise program. Statistical analysis

Treadmill testing protocol Results are expressed as mean±standard deviation(SD). All analyses were performed using paired t-Treadmill testing was performed after the patients

had been familiarised with walking on a treadmill. test, unless stated otherwise, with p<0.05 considered

Eur J Vasc Endovasc Surg Vol 20, July 2000

K. H. Tan et al.74

Table 1. Changes after exercise training.

Entry Post training MD 95% CI p value

MWD (m) 133.0±60.7 242.5±137.1 109.5 65.9 to 153.1 <0.0001ABPI (rest) 0.76±0.21 0.72±0.19 −0.04 −0.11 to 0.03 0.27ABPI (post exercise) 0.52±0.25 0.47±0.21 −0.05 −0.14 to 0.04 0.29BMI (kg/m−2) 26.7±3.4 26.6±3.6 −0.07 −0.36 to 0.23 0.61

RestingHR (beats/min−1) 85.9±19.7 81.8±16.3 −4.0 −12.3 to 4.2 0.32VE (ml/kg−1/min−1) 147.8±38.8 149.3±44.3 1.4 −16.2 to 19.1 0.87VO2 (ml/kg−1/min−1) 4.19±0.84 4.06±0.57 −0.12 −0.51 to 0.26 0.51

MD – Mean of differences.

significant. ARCUS QUICKSTAT (1.0) software wasused for statistical analysis.

Results

Forty patients met the inclusion criteria. At the baselinetesting, two patients were excluded because they couldwalk for more than 15 min at 12% gradient on thetreadmill. Fifteen patients did not complete the train-ing program. Six of these patients were unable to walkon the treadmill comfortably due to clinically mild Fig. 1. Common femoral artery blood flow (mean±SEM). (Β) Pre-osteoarthritis, although they were usually able to walk training; (Ε) post-training.unassisted. One patient developed severe angina andtwo had respiratory tract infection during the periodof study and therefore did not complete the training 3.6 kg/m−2, p=0.61) and no significant changes

occurred in ankle–brachial pressure index (ABPI)program. Six did not complete due to non-medicalreasons. No patients were excluded because of changes (Table 1).

Seventeen out of 23 patients completed the logbook.in medication. Of the remaining 23 patients, six werefemale and 17 were male. The mean age was 68.5±6.1 Of the 17, seven managed to exercise 1 h/day for 5

days/week. Six managed to exercise at least 4 days/years. The ankle brachial pressure index at rest was0.74±0.20 and 0.51±0.25 after 2 min of exercise on week and the remaining four exercised less than that.

Statistical analysis of these subgroups is consideredthe Stresst’er calf ergometer. Duplex scans revealedthat one had aortoiliac occlusion, 19 had superficial unreliable.

Common femoral artery blood flow (1): at rest, (2):femoral artery disease and three had distal vesseldisease (below trifurcation of popliteal artery). Dia- immediately after exercise for 2 min on the Stresst’er

ergometer (peak flow) and (3): during recovery, re-betes mellitus was present in five, hypertension in 10and ischaemic heart disease (stable angina) in four. At mained similar pre- and post-training (Fig. 1).

At rest, there was no significant difference betweencompletion of the study, nine out of an initial numberof 16 patients reported that they had stopped smoking, the pre- and post-training heart rate (HR) (85.9±19.7

vs. 81.8±16.3 beat/min−1, p=0.32). Oxygen con-but this was not confirmed by measurement of carb-oxyl haemoglobin levels. sumption (4.19±0.84 vs. 4.06±0.57 ml/kg−1/min−1,

p=0.51) and minute ventilation (147.8±38.8 vs.Exercise training increased the maximum walkingdistance (MWD) by 82%, from 133.0±60.7 to 149.3±44.3 ml/kg−1/min−1, p=0.87) remained similar

at rest (Table 1).242.5±137.1 m (p<0.05). Eighteen out of the 23 patientsmanaged to improve MWD by more than 20%. The After 3 months of training, each patient walked on

the treadmill to a distance that was exactly the sameimprovement in MWD has no correlation with smok-ing. These who continued to smoke improved the as the maximum walking distance achieved at the

baseline test. The average heart rate and the highestMWD by 116% while those who reported that theyhad stopped improved by 84%, p>0.05. The body mass heart rate observed during the exercise were sig-

nificantly reduced compared to pre-training (Tableindex (BMI) remained similar (26.7±3.4 to 26.6±



Table 2. Changes in parameters measured while walking to a fixed distance.


Average HR 108.4±18.5 97.8±16.1 −10.6 −18.3 to −2.9 0.009Maximum HR 131.2±23.3 107.9±17.7 −23.3 −32.1 to −14.4 <0.0001VE (ml/kg−1/min−1) 266.4±72.6 258.8±54.9 −7.7 −29.4 to 14.1 0.47VO2 (ml/kg−1/m−1) 0.355±0.076 0.323±0.062 −0.032 −0.058 to −0.005 0.02RER 0.84±0.04 0.86±0.06 0.02 0 to 0.03 0.09

The oxygen cost of exercise was measured as ml of oxygen used per kg of body mass per metre of walking distance. MD – Mean ofdifferences.

Fig. 2. VO2 (mean) while walking on a fixed treadmill protocol,with identical speed, distance and gradient. (Β) Pre-training; (Ε)

Fig. 4. Venous lactate levels (mean ±SD). (Φ) Pre-training; (Ε)post-training.post-training.

level remained similar pre- and post-training(1.15±0.51 vs. 1.06±0.37 mmol/l−1, p=0.51), the1-minute (1.75±0.71 vs. 1.35±0.61 mmol/l−1, p<0.05)and 6-minute (1.49±0.58 vs. 1.15±0.62 mmol l−1,p<0.05) lactate levels were significantly reduced post-training, even with an increased walking distance (Fig.4).

No significant changes in the blood rheology wereidentified post-training (Table 3). There was a trendtowards a reduction in total cholesterol and tri-glycerides, but this was not statistically significant.There was no change in LDL level, but a significantFig. 3. VO2 (mean) during the recovery phase, after walking to the

MWD. (Β) Pre-training; (Ε) post-training. improvement in HDL was found after training. Thetotal cholesterol:HDL ratio decreased significantlyafter training (Table 3).2). Furthermore, the oxygen consumed per metre of

walking distance was reduced (Table 2, Fig. 2). Mean-while, RER and VE remained similar.

Each patient then continued to walk to a new max- Discussionimum walking distance. The oxygen consumption dur-ing the first 5 min of the recovery phase following Exercise training has been recommended as a treat-

ment modality for patients with peripheral vascularthe treadmill exercise was compared pre- and post-training. Even though the maximum walking distance disease since 1898.17 In recent years, its role has been

overshadowed by advances in procedures such ashad increased by 82%, the total oxygen used duringthe recovery phase was similar (36.2±6.8 vs. 35.1±8.9 percutaneous transluminal angioplasty (PTA).18 Re-

cently, the role of PTA has been questioned followingml/kg−1, p=0.63), (Fig. 3). While the resting lactate


K. H. Tan et al.76

Table 3. Changes in blood rheology and lipid profile.


PCV 0.44±0.04 0.45±0.05 0.01 0 to 0.02 0.14Plasma viscosity (cP) 1.74±0.13 1.74±0.09 0 −0.04 to 0.04 0.97Cholesterol (mmol/l) 5.82±0.58 5.50±0.58 −0.29 −0.59 to 0.02 0.06HDL (mmol/l) 1.35±0.34 1.47±0.30 0.12 0.01 to 0.23 0.03LDL (mmol/l) 3.36±0.63 3.28±0.57 −0.08 −0.37 to 0.22 0.59Triglycerides (mmol/l) 2.35±1.00 2.01±1.08 −0.33 −0.67 to 0.01 0.06Total cholesterol/HDL 4.59±1.30 3.89±0.82 −0.70 −1.13 to −0.27 0.003

cP – Centipoise, MD – Mean of differences.

the publication of a study highlighting the ef- flow must therefore be implicated in improved exercisetolerance after training.fectiveness of conservative management for patients

with claudication.19 Accumulating evidence provesthat exercise training for claudicants improves the

Effects on heart ratewalking distance profoundly. The improvement of82% in the MWD in this study is similar to published

Patients with intermittent claudication have a highstudies20 and a supervised exercise program can showincidence of coronary artery disease. One study haseven greater improvements.8 However, we still lack ashown that 90% of claudicants scheduled for peri-complete understanding of the physiological changespheral vascular bypass operations had coronary arterydue to exercise training that could lead to an im-disease.24 Improving the cardiac function might haveprovement in walking distance in such patients.a significant impact on exercise tolerance. In normalsubjects, training improves the cardiac status, man-ifested by a decrease in the resting and exercising

Recruitment heart rates. In our study, exercise training also led toa significant reduction in the heart rate during exercise.

We selected patients for this study with reported clau- Physical training on atherosclerotic patients with isch-dication distances of between 50–450 m. Walking ex- aemic heart disease has shown a similar response,ercise programs are not suitable for all patients, as is suggesting an improvement in myocardial functionreadily apparent in our study. The number of patients and enhancement of myocardial oxygen availability.25

unable to complete this program and assessment, how-ever, is similar to other reported studies.21 For those

Effects on oxygen cost of exerciseunable to undertake a walking exercise program al-ternatives include an upper body training pro-

The significant decrease in the oxygen consumptiongramme.22 The assumption is that this also leads to anper workload correlates well with a previous study.26improvement in the cardiovascular and respiratorySuch a reduction may be due to an improvement insystems.the biomechanics of walking.27 It is likely that patientswith intermittent claudication perform minimalexercise, and subsequently develop features of disuse

Effects on blood flow atrophy. Ischaemia of the lower limbs resulting in gaitdisturbance has been reported in animal models.28

Studies on dogs with ligated femoral arteries have Exercise training may help to overcome some of theshown an increase in the blood flow to the lower limbs inefficiencies of walking associated with such gaitafter training.23 However, many studies have proved disturbances.that exercise training in claudicants does not improvethe blood flow to the lower limbs,8–10 although thereis some evidence to suggest that blood flows may be Effects on fatty acids and glucose utilisation during

exerciseredistributed around specific muscles in the absenceof an increase in the absolute flow rate. In our study

Part of the metabolic adaptation that occurs withwe measured the flow rates in 13 patients, dem-onstrating no increase in the CFA flow rate. Mech- training in normal subjects is an increase in the ox-

idative capacity.29 A trained athlete utilises more freeanisms other than an increase in the absolute blood



fatty acids (FFA) during exercise,29 as it provides more of the upper limit of normal (1.72). In normal subjects,exercise training leads to a reduction in plasma vis-adenosine triphosphate (ATP) per gram of substance

than glucose. The increase in the utilisation of FFA cosity37 and a decrease in PCV.38 The decrease in PCVcan lead to a reduction of blood viscosity39 and con-leds to a fall in the respiratory exchange ratio (RER),

as the RER for glucose is 1, and for FFA is about 0.71. sequently an improvement in blood flow. Ernst hasshown a significant improvement in blood rheologyHiatt has shown a reduction in the RER in claudicants

following exercise training,30 in contrast to our own in claudicants following a supervised training pro-gram40 in contrast to our study and that of Ciuffetti.41results, although it is important to note that in Hiatt’s

study, the exercise program was more intensive andsupervised.

Effects of blood lipid profiles

For primary prevention, The British Heart FoundationEffects on recovery phase following exercise: oxygen debtand lactate levels recommends a total cholesterol level of less than

5.2 mmol/l−1 for normal adults. For secondary pre-Even though the MWD improved significantly after vention, the Drug and Therapeutics Bulletin suggests

starting treatment with a statin (3-HMG CoA Re-exercise training, the expected increase in the oxygendebt during the recovery did not occur. We are not ductase inhibitor) in any patient with LDL >3.3 mmol/

l−1 or total cholesterol >4.8 mmol/l−1.42 In this studyaware of any studies that have demonstrated thisfeature. Oxygen debt is defined as the net oxygen of 23 patients, 22 had serum a cholesterol of more

than 4.8 mmol/l−1, and 12 had serum LDL exceedingconsumption during recovery in excess of resting oxy-gen consumption, and increasing the workload or the 3.3 mmol/l−1. Many studies have shown conclusively

the benefit of lowering cholesterol for patients withduration of exercise leads to higher oxygen debt.31 Theoxygen is used to resaturate the myoglobin, replenish ischaemic heart disease in reducing coronary events.

Our study showed a favourable change in the lipidthe energy store (ATP and phosphocreatinine) to pre-exercise level and to oxidise the excess lactate that has profiles, with significant improvements in the HDL

level and total cholesterol to HDL ratio. Stampfer etaccumulated during the exercise.32 In this study theabsence of change in the oxygen debt, even though al. has shown that the total cholesterol to HDL ratio

was a strong discriminator of risk of myocardial in-the MWD had increased, could be due to an im-provement in the biomechanics of walking or a re- farction. A change of 1 unit in the ratio coincided with

a 37% reduction in risk of myocardial infarction.43 Induction in anaerobic metabolism. The decrease in thevenous lactate level after exercise in this study sup- this study, the ratio dropped by 0.7 units, which should

lead to a significant reduction in the risk of myocardialports the concept of a reduction in anaerobic meta-bolism. The reduction in lactate level following a infarction. However, the LDL level remained the same

as before training. This study showed that a com-training program has previously been shown to occurboth in normal subjects33 and claudicants.34 In athletes, bination of health education and exercise, for clau-

dicants with high cholesterol, could lower the totaltraining reduces lactate levels due to an increase inoxidative capacity, a decrease in glycolysis and higher cholesterol, possibly reducing the need for additional

treatment.utilisation of FFA, resulting in decreased pyruvateproduction (precursor or lactate).31 Similar mech-anisms probably occur in trained claudicants, sup-ported by studies showing an increase in the calf

Conclusionmuscle oxidative enzyme concentration,35 leading tobetter utilisation of oxygen and thus a reduction in

Exercise training increases the exercise tolerance offemoral venous oxygen saturation.36

claudicants. A multiplicity of physiological ad-aptations, such as improvement in cardiac status, re-duction of oxygen cost of exercise and a reduction oflactate load contribute to its success. Unlike surgicalEffects on blood rheologybypass grafts, exercise training does not improve theblood flow to the lower limbs. Other benefits includePatients with peripheral vascular disease have a high

incidence of abnormal blood rheology.12 In this study favourable changes in lipid profiles, which might re-duce the risks of coronary events.10 out of 23 patients had a plasma viscosity in excess


K. H. Tan et al.78

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19 Tunis SR, Bass EB, Steinberg EP. The use of angioplasty, bypassAccepted 29 February 2000


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