J. Physiol. (1973), 234, pp. 481-497 481With 4 text-figuresPrinted in Great Britain

CARDIORESPIRATORY ANDMETABOLIC COSTS OF CONTINUOUS AND

INTERMITTENT EXERCISE IN MAN

BY R. H. T. EDWARDS,* L.-G. EKELUND,R. C. HARRIS, C. M. HESSER, E. HULTMAN,

A. MELCHER AND 0. WIGERTZFrom the Departments of Aviation and Naval Medicine,

Karolinska Institutet, Clinical Physiology, Karolinska Sjukhuset,and Clinical Chemistry, S: t Eriks Sjukhus, Stockholm, Sweden

(Received 17 May 1973)

SUMMARY

1. Cardiorespiratory and metabolic responses to paired patterns ofcontinuous and intermittent exercise with the same average power outputwere studied in eight men. Heart rate, ventilation and pulmonary gasexchange were measured during the different patterns of exercise per-formed on a cycle ergometer. The recovery oxygen volume was measuredover 30 min of loadless pedalling. Needle biopsy samples of the vastuslateralis muscle were taken before, during and after completion of theexercise for measurement of muscle metabolites.

2. Heart rate, ventilation, oxygen intake, respiratory exchange ratio,and blood lactate concentration were generally higher with intermittentcompared with continuous exercise as were the accumulated totals forheart beats, ventilation and oxygen intake. Muscle biopsy samples tendedto have higher lactate and lower phosphocreatine contents in intermittentexercise. The lactate concentration in muscle and blood water was thesame during loadless pedalling before exercise but was significantly higherin muscle than blood during exercise. This concentration gradient waslarger in intermittent than in continuous exercise.

3. Work efficiency, calculated from the total oxygen cost of work inexcess of a loadless pedalling control, was significantly lower in intermittentexercise. The explanation is thought to be connected with the observationthat when the work was performed at a high rate in short bursts a largepart of the oxidative recovery took place after the contraction during therest periods, whereas in the low intensity continuous exercise the oxygen

* Present address: Department of Medicine, Royal Postgraduate Medical School,Du Cane Road, London, W12 OHS.

R. H. T. EDWARDS AND OTHERS

was mainly utilized while the work was being performed. This indicatesthat for part of the time in the intermittent exercise the muscle was work-ing under anaerobic conditions. Although the possibility exists that theefficiency of resynthesis of phosphagen may be reduced in this form ofactivity, it is more likely that the result described is due to the greateramount of lactate formed in the intermittent exercise.

INTRODUCTION

It is common experience that exercise is performed intermittentlywhenever the intensity is excessively high or when working capacity isreduced, e.g. normal people climbing at high altitude (Pugh, 1958) andpatients with chronic obstructive bronchitis climbing stairs (Edwards,1971a). Previous physiological studies (Astrand, Astrand, Christensen &Hedman, 1960a; Margaria, Oliva, di Prampero & Cerretelli, 1969) haveconcentrated on making comparisons between different patterns of inter-mittent exercise. In addition to making these comparisons Astrand et al.(1960a) reported measurements made during continuous exercise at thesame average power output but did not draw any conclusions from thelower heart rate and blood lactate concentrations in this pattern of work.

In a previous study (Edwards, Melcher, Hesser, Wigertz & Ekelund,1972) it was found that the higher rating of perceived exertion in inter-mittent exercise was closely correlated with the greater heart rate, venti-lation, oxygen intake and blood lactate concentrations in this form ofexercise compared with continuous exercise with the same average poweroutput. The present study investigates further the relative costs, in termsof the cardiorespiratory adaptations to exercise and utilization of localenergy stores in muscle, of the two types of exercise. Hitherto otherstudies of intermittent exercise have used rest as the reference level towhich recovery is followed and from which the excess cost of the exerciseand hence the work efficiency is calculated. The advantage of the loadlesspedalling control is that the extra energy needed for accelerating thelimbs from rest during each burst of activity is thereby eliminated (Whipp& Wasserman, 1969).

Intermittent exercise of the type studied here comprises brief periodsof intense muscular activity alternating with periods of recovery. Earlystudies of the total oxygen cost (work+recovery) of single periods ofexercise of different durations showed that the total oxygen cost wasdisproportionately high in exercise of less than 2 min duration (Simonson& Hebestreit, 1930; Simonson & Sirkna, 1934; Asmussen, 1946; Christen-sen & H6gberg, 1950). As a result of these studies it has generally beenthought that the overall efficiency of anaerobic work is about half that of

482

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 483

work aerobically performed. An early dissenting report was that of Crow-den (1934) who found work efficiency to be independent of the durationof exercise. Recently Whipp, Seard & Wasserman (1970) came to thesame conclusion, though the total oxygen cost of exercise for 1-3 min wasdisproportionately high in comparison with that for 6 min exercise insome of their subjects.

Intermittent exercise with its repeated recovery intervals might rea-sonably be expected to exaggerate any differences in the oxygen cost ofrecovery processes compared with those supplying energy during work.However, Christensen, Hedman & Holmdahl (1960) reported that theefficiency of intermittent exercise was the same as that of continuousexercise. Recently a slightly lower work efficiency in intermittent exercisewas reported (Ekblom, Greenleaf, Greenleaf & Hermansen, 1971).

There is thus no agreement concerning the energetic cost of brief exer-cise and the work efficiency in intermittent exercise. The present study,the first detailed analysis of cardiorespiratory and metabolic adaptationsto different patterns of continuous and intermittent exercise with thesame average power output, was undertaken with a view to gaining agreater understanding of aerobic recovery following muscular activity inman.

METHODS

Vital statistics on eight healthy male subjects who volunteered to participate inthe study are given in Table 1. In the morning after an overnight fast the subjectsexercised in the upright position on an electrically braked cycle ergometer (ElemaSchonander). A constant pedalling frequency (60 rev/min) was used throughout allcontrol, exercise and recovery periods. The ergometer was adapted to allow square-wave work profiles to be performed under the automatic control of a digital pro-grammer. A pneumatic valve, linked to the digital programmer, was situated on theexpiratory side of the respiratory valve (dead space 15 ml.). This pneumatic valveallowed the gas expired during work to be collected separately from that expiredduring the recovery periods in both forms of exercise. All the gas expired during theexperiment was collected in Douglas bags (200-6001. capacity) suspended as closeas possible to the respiratory valves to minimize the dead space in the conductingtubing (3.8 cm diameter, volume 110 ml.). No correction for the unflushed deadspace gas was made as the error in derived gas exchange values contributed by thiswas estimated to be less than 1 %. From well mixed expired gas, duplicate sampleswere taken in mercury receivers for analysis with the Haldane apparatus. Thecoefficient of variation for the duplicate analyses was 2% (n = 50). Expiratory resis-tive pressure offered by the mouthpiece, respiratory valve, conducting tubing andDouglas bag was less than 3 cm H20 at a flow rate of 200 1./min.

Inspired gas flow was measured with a Venturi-type flow meter calibrated withstandard flows from rotameters. Analogue and digital computer facilities allowedcalculation of tidal volume, respiratory frequency, and total (inspired) ventilationon a breath-by-breath basis, as described previously (Wigertz, 1970). Instantaneousheart rate was monitored continuously with an electronic heart-rate meter (Lind-borg, Odman & Wigertz, 1970). Heart rate, inspired gas flow, tidal volume, respira-

484 R. H. T. EDWARDS AND OTHERStory frequency, inspired ventilation and ergometer power output were recordedsimultaneously on separate channels of a Brush 8-channel pen recorder. Roomtemperature averaged 20 30 C (range 18-22° C). Body temperature was measuredwith a rectal thermocouple (Ellab, Copenhagen). Capillary blood samples were drawnin duplicate at standard times from the hyperaemic finger tips of the left hand(warmed by an electrical heating element in the handle-bar of the cycle ergometer)for measurement of lactate by a microenzymatic method (Lundholm, Mohme-Lundholm & Vamos, 1963). The error of analysis for lactate in duplicate sampleswas 0-088 m-mole/l. or 2% of the mean value (n = 86).

TABLE 1. Vital statistics on subjects

Age Height Weight *M=(yr) (cm) (kg) (kpm/min)

Subjects A-DMean 28-8 176-8 67-3 1500S.D. 5-0 4-3 3-2 200s.E. of mean 2-5 2-1 1-6 100

Subjects E-HMean 30-5 179-0 78-5 1600S.D. 5-1 4-2 5-0 316s.E. of mean 2-5 2-1 2-5 158

Needle biopsy samples were taken with Bergstr~m-Stille needles, under localanaesthesia, from the vastus lateralis muscle (Bergstrom, 1962; Edwards, 1971 b).Muscle samples were removed from the biopsy needle in 2-4 see with metal forceps,previously cooled in liquid nitrogen, and rapidly frozen in liquid Freon (VirginiaChemicals, Virginia, U.S.A.) at about - 1500 C. After freeze-drying, dissecting toremove connective tissue, and weighing (average sample weight 7-8 mg), analysesof ATP, phosphocreatine, creatine and lactate were performed using the enzymicmethods referred to previously (Edwards, Harris, Hultman, Kaijser, Koh & Nor-desj6, 1972). The error of the analyses, determined from paired analyses of sixteenbiopsy samples of resting muscle, was about 5% of the mean value. All biopsy analy-ses have been corrected to a standard total creatine (phosphocreatine + free creatine)of 120 ,umoles/g dry muscle (Edwards, Harris, Hultman, Kaijser, Koh & Nordesj6,1972; Edwards, Harris, Hultman & Nordesj6, 1972) to compensate for variationsin fibrous tissue content and blood contamination of individual biopsy samples.

ProcedureThe ergometer load setting which would lead to exhaustion in 6 min (*Mma.) was

first determined using the Tornvall test (Tornvall, 1963). On another day subjectsexercised once intermittently with work periods of 10 see (subjects A-D) or 30 see(subjects E-H), both with 30 see recovery intervals, and once continuously for thesame total time at the same average power output corresponding to 25 or 50% ofWmax respectively. The total recovery time including the intervals in intermittentexercise was always 30 min. The average power output during intermittent exercisewas calculated with the inclusion of the final 30 see recovery interval, thus keepingthe work: recovery pattern symmetrical.

Muscle biopsies were taken, with as short an interruption of pedalling as possible:(i) in the last 15 see of the control period, (ii) after one third, and (iii) after the wholeof the work had been completed. Biopsies were taken from the same leg on the firstoccasion, and from corresponding sites in the contralateral muscle when the second

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 485study was performed after an interval of one week. Ventilation and respiratory gasexchange were measured from the expired gas collection made during the finalthird of the exercise. The instantaneous heart rate was measured as the peak valueduring work averaged over one breath cycle to minimize the effect of sinus arrhyth-mia. The times of sampling and gas collections are shown in Fig. 1.

Total ventilation, oxygen intake and number of heart beats were calculated withreference to the loadless pedalling control state. Work efficiency was calculatedfrom the total excess oxygen intake (work + recovery), assuming that 1-0 1. s.t.p.d.of oxygen is equivalent to 4 9 kcal. The oxygen 'lag' volume (Harris, 1969), definedas the difference between the aerobic energy requirement and the measured oxygenintake, was determined during the first two thirds of the work. In continuous exer-cise it was given by the difference (2 x oxygen intake in collection 3- oxygen intake

Expired gas collections--- -A---- ----2 A-4 3

OX L ]1 111111flfl l1 j 1fl fl Intermittent

-I~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

0 3 5 otiuu

Time (min)O0 6 10 14 18 42 48Loadless pedalling I--W/3- +--W/3-+--W13-. Loadless pedaling

(control) (recovery)

tt= Duplicate blood samples for L.A. + = Muscle biopsy

Fig. 1. Diagram showing gas collections and times of sampling blood forlactate (L.A.) determination and muscle biopsies in paired patterns of exer-cise at 50D% WmshoTimes of gas collection and sampling bore the samerelationship to the total work performed in the paired patterns of exerciseat 25% Wmax

in collection 2). In intermittent exercise the aerobic energy cost of the brief burstsof activity was estimated by a standard technique (Astrand & Rodahl, 1970). Thisinvolved extrapolating to Wma. the rectilinear relationship between oxygen intakeand power output based on measurements made in the same individuals duringsubmaximal exercise. Studies ofintermittent and continuous exercise were conductedin random order on each subject. Additional studies were performed on subjectR.H.T.E. (age 32-33 yr, height 173*5 cm, weight 65 kg) in both Stockholm (withD. Linnarsson) and London (with E. E. Davies and S. Spiro). Oxygen intake wasmeasured breath-by-breath, by two different computer based techniques, in thesame intermittent exercise patterns as those previously studied in subjects A-Dand E-H. Where relevant, tests of statistical significance have been performed witha paired t test.

486 ~R.H. T. EDWARDS AND OTHERS

]RESULTS

In subjects A-D, intermittent exercise with 10 see work periods alter-nating with 30 sec loadless, pedaling recovery periods gave an averagepower output of 375 kpm/min (±25 s.Eo. of mean), corresponding to25 % W~4ax (Table 2). Subjects E-H, exercising intermittently with30 sec work periods alternating with 30 sec loadless pedalling recovery,had an average power output of 800 kpm/min (± 79 s.E. of mean), corre-sponding to 50% Wnax (Table 3). The total amount of work performedwas not significantly different in the two patterns of intermittent exerciseand was, by design, the same as the total performed in 6 min of con-tinuous exhaustive work at U~ax The rise in rectal temperature wassimilar in each of the different patterns of exercise, averaging 0.30 0.In the subjects exercising at 25 % Wmax, the increases in heart rate,

ventilation, oxygen intake, respiratory exchange ratio and blood lactateconcentration (Table 2) above the loadless pedalling control were modestcompared with those in the subjects exercising at 50% ~'knax (Table 3).Similarly, smaller changes from the controls in muscle biopsy analyseswere found at the lower work rate. Mean values for heart rate, ventilation,respiratory exchange ratio, oxygen intake and blood lactate concentra-tions during the final one third of work and the lactates in recovery weregenerally greater for intermittent exercise than for continuous exercisewith the same average power output (Tables 2 and 3). Blood lactate con-centration had returned to the control level by the end of the 30 minrecovery period in all except the intermittent exercise runs at 50% W1.The heart rate and ventilation. during the final third of exercise (and therespective totals in both continuous and intermittent exercise) weresimilarly related to oxygen intake (Fig. 2).

Total oxygen intake was greater (P < 0-001) in intermittent than incontinuous exercise and as a consequence whole body work efficiency waslower (P < 0.01) at both power outputs (Table 4). A far greater proportionof the total cost (in terms of oxygen intake, ventilation and heart beats)occurred during recovery in intermittent than in continuous exercise(Table 4).The time course of oxygen intake during intermittent exercise with

30 sec work and loadless pedalling recovery periods is illustrated in Fig. 3(London experiment). (Similar results were found in all Stockholm andLondon experiments including those with 10 sec work periods alternatingwith 30 sec loadless pedalling.) Oxygen intake remained high throughoutthe 20 sec recovery intervals and it did not fall appreciably until 30 secafter the end of the last work period. In all these runs oxygen intake hadreturned to the loadless pedalling control level well before the end of the

486

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 487

TABLE 2. Exercise at 25% W.,. in subjects A-D (mean + S.E. of mean)

ExerciseC A i

Continuous Intermittent

Ergometer load (kpm/min)Heart rate (beats/min)Ventilation (1. b.t.p.s./min)Oxygen intake (1. s.t.p.d./min)Respiratory exchange ratioBlood lactate (m-moles/l.)

087+4

12-8 ± 0-80-534 + 0-0030-76 ± 0-0051P11 + 0411 (a)

(b)(c)

Muscle biopsy analyses (/zmoles/g dry muscle)ATP

Phosphocreatine

Lactate

22-1 + 1-0 (a)(b)

70-2 ± 2-8 (a)(b)

3-0+0-4 (a)(b)

Notes. Samples taken (a) after i, and (b) completion, of work (including the final30 see recovery interval in intermittent exercise) (c) after 30 min recovery.

TABLE 3. Exercise at 50% Wmnx in subjects E-H (mean + s.E. of mean)

Ergometer load (kpmfmin)Heart rate (beats/min)Ventilation (1. b.t.p.s./min)Oxygen intake (1. s.t.p.d./min)Respiratory exchange ratioBlood lactate (m-moles/l.)

Muscle biopsy analyses molesle/ATP

Phosphocreatine

Lactate

Loadlesspedallingcontrol

0

76+ 713-9±0-3

0-538 + 0-0050-79 ± 0-0161-78 + 0-18

Ig dry muscle)

Exercise

Continuous Intermittent

800 + 79145 + 648-0+ 3-61-98 + 0-140-90 + 0-019

(a) 3-23 ± 0-37

(b) 4-07 ± 0-85(c) 1-49 + 0-20

22-4 + 0-9 (a) 21-7 ± 1-0(b) 23-8 + 0-4

76-4 + 2-3 (a) 37-1 ± 4-8(b) 35-6 + 3-7

4-1 + 1-0 (a) 38-0 ± 2-6(b) 30-8± 10-1

1600 ± 158162 ± 962-8+3-12-16 ± 0-180-99+ 0-0203-82 + 0-655-77+0-973-04 + 0-61

20-6 + 2-619-4+ 1-622-3 ± 4-329-9 ± 6-670-7 + 15-070-0 + 23-1

Notes. Samples taken (a) after i, and (b) completion, of work (including the final30 see recovery interval in intermittent exercise), (c) after 30 min recovery.

Loadlesspedallingcontrol

375 + 25110+ 525-5 + 0-61-08 ± 0-0050-85 + 0-0171-26 + 0-271-35 + 0-370-85 + 0-29

24-4 + 1-622-8 + 2-060-7+4-955-2 + 1-35-8 + 1-67-5 + 1-6

1500± 100126+437-7 ± 1-71-46 + 0-0800-86 + 0-0201-55 ± 0-411-78 + 0-550-93 + 0-27

20-6 + 0-721-9+0-938-5 + 6-353-0 + 7 917-8 + 5-69-2+3-1

R. H. T. EDWARDS AND OTHERS

Loadless pedallingControls o AMean+ s.EtI. of mean shown

T160 I140

120 jY

100

80

60 -1140 0-

20 7

00 1.0 2-0

4.1

-oI-

0H

0

I-,

-a

0

H

(I. s.t.p.d./min)

Power output 25% W 50% WContinuous * AIntermittent 0 A

12500

1000-

750-

500II !

600 -

400

12 14 16 18 20 22Total excess (I. s.t.p.d.)

Oxygen IntakeFig. 2. Relationships between heart rate, ventilation and oxygen intakeduring exercise and for the cumulative totals of these measurements inexcess of those for loadless pedalling control state.

TABLE 4. Physiological costs of continuously and intermittently performed work(measured in excess of loadless pedalling control) (mean ± s.E. of mean)

Average power output

25% W.=a,Continuous Intermittent

Total cost (work and recovery)Total heart beats (beats) 637 + 38Total ventilation 360-1 + 62-9

(1. b~t~ps.)Total oxygen intake 14-01±+ 1-11

(1. s.t.p.d.)Oxygen 'lag' volume 0-60±+ 0-11

(1. s.t.p~d.)Recovery oxygen volume 1-50 ±0-94

(1. s.t.p.d.)

50% *WmaContinuous Intermittent

1194+39 1184+100 1478±40480-0+±30-2 429-2+±23-4 619-1 ±38-1

18-88+1-36 17-00+1-96 20-26+1-61

9-96+±0-18 1-49±0-50 7-32+±0-96

13-58+±1-14 1-50+±0-61 11-70+±0-76

Work efficiency (%) 31-1 +2-1 23-0+ 1-3 27-2+±1-1 22-6±0-6Percentage of total cost in recoveryHeart beats 15-0 + 2-8Ventilation 14-3 ± 6-6Oxygen intake 7-6 + 4.7

488

-E0(U

I-

0*

'-D

CL

0.

C,a,

64-6± 11-673-1+±0-771-7+± 1-2

42-8+±3-717-7+±2-68-7±3-3

70-7+±1-960-5+± 1-2579+± 1-0

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 489

30 min recovery period. Ventilation and heart rate were also elevatedduring recovery intervals in intermittent exercise.The biopsy analyses (Tables 2 and 3) showed little difference between

intermittent and continuous exercise for ATP but phosphocreatine waslower (P < 0.01) in the samples taken after completion of one third ofthe work during intermittent exercise at both power outputs. In the finalsamples (sample b), taken 30 sec after the last burst of activity in inter-mittent exercise, the phosphocreatine concentration tended to be higher

Intermittent Subject R.H.T.E.exercise

30 !EEEUEEEEE I

Ergometer load=2000 kpm/min

E Total- work~2*0 A.=12000 kpm

Average power output

.' l Loadless =1000 kpm/min' 1-0 pedalling>% ~~~~control

I I0 6 10 14 18 42

Time (min)

Fig. 3. Breath-by-breath measurement of oxygen intake in anintermittent exercise study (London experiment).

than in the samples taken immediately on completing a burst of activity(sample a) but the difference did not reach statistical significance. Musclelactate tended to be higher in intermittent exercise compared with con-tinuous exercise. To estimate the average lactate concentration in muscleduring the stable state in the final two thirds of work, the average wastaken of the values found in biopsy samples a and b. The concentration inmuscle water was calculated assuming the water content of a biopsysample to be 76% (Karlsson, 1971). Blood lactate measurements werere-expressed in terms of blood water assuming this to be 84% of wholeblood. During the latter part of work, lactate concentration in musclewater was higher (P < 0.05) than that in blood water and this difference

490

was greater (Percise (Fig. 4).

40

30

E1-E

._

J

103UA(I 20E

U

-j

10

R. H. T. EDWARDS AND OTHERS< 0.05) in intermittent exercise than in continuous ex-

A

A

AA

-- +50%00 ,..0+2S%

.e .y0

4 6 8Lactate in blood water (mM)

10

Fig. 4. Concentrations of lactate in muscle and blood water calculatedfrom present results (mean values given in Tables 2 and 3) assumingmuscle to be 76% water and blood 84%. Symbols as in Fig. 2.

DISCUSSION

The principal finding in this study is that the total oxgen cost of a givenamount of work is greater when the work is performed intermittentlythan when it is continuously performed. This fact cannot be disputed onthe grounds of the precise definition of 'same average power output',i.e. whether or not the final 30 sec recovery interval is included in thecalculation. In all forms of exercise studied, the work total and the timefor recovery was the same (equivalent to 6 min work at Wmax + 30 minrecovery). Incomplete measurement of the recovery oxygen volume,e.g. before the blood lactate concentration had returned to the controllevel following intermittent exercise (Table 3), cannot explain the higheroxygen cost of intermittent exercise as collection for a longer time would

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 491exaggerate the observed difference between intermittent and continuousexercise. Possible leakage of expired gas during the frequent switching inintermittent exercise would result in the gas exchange measurementsbeing smaller, not larger, than in continuous exercise.As a consequence of the higher total intake, whole body work efficiency

was lower in intermittent compared with continuous exercise (Table 4).Values for continuous exercise agree well with the figure of 29% foundexperimentally (calculated with reference to the loadless pedalling controlstate) and estimated on thermodynamic grounds (Whipp & Wasserman,1969). Higher values for heart rate, ventilation, oxygen intake, respiratoryexchange ratio and blood lactate concentration in intermittent exerciseagree with previous observations (Edwards, Melcher, Hesser, Wigertz &Ekelund, 1972). Heart rate and ventilation (and the respective totals)were similarly related to oxygen intake in all forms of exercise (Fig. 2).Heart rate, ventilation, respiratory exchange ratio and blood lactate con-centrations were increased in both forms of exercise to an extent whichwould be expected from the results of previous studies (referred to inEdwards, Jones, Oppenheimer, Hughes & Knill-Jones, 1969).The higher oxygen intake associated with intermittent exercise cannot

be attributed to the oxygen cost of the greater total number of heartbeats or higher total ventilation. The myocardial oxygen consumptionper stroke (MV02) is approximately given by the equation:

MV02 (ml.) = 0*36 x 10-3 (heart rate) + 04101(unpublished derivation supplied by the late Dr B. W. Lassers from studiesof human myocardial metabolism reported in 1971). Assuming that theheart beat totals associated with the different types of exercise (Table 4)have values for MU0 corresponding to the exercise heart rates given inTables 2 and 3, the amount of oxygen attributable to the difference inheart beat totals between intermittent and continuous exercise is 84-5 ml.at 25% Amax and 54 ml. at 50%%Wax Assuming an average oxygencost of breathing of 1.5 ml./l. of total ventilation (Agostoni, Campbell &Freedman, 1970) the additional oxygen intake associated with the higherventilation of intermittent exercise is 240 ml. at 25% Wmax and 285 ml.at 50% Wmax. The total oxygen cost of these changes combined amountsto about 10% of the difference in total oxygen intake between the twoforms of exercise (Table 4).

Since the recovery oxygen volume was a large proportion of the totaloxygen intake in intermittent exercise (Table 4) it is likely that the dif-ference in work efficiency between the two types of exercise was due todifferences in the aerobic recovery processes.

R. H. T. EDWARDS AND OTHERS

Aerobic recovery from exerciseFactors involved in aerobic recovery following exercise have been

recently reviewed (Harris, 1969). To be considered below are (i) repletionof oxygen stores, (ii) repletion of muscle phosphagen store, (iii) aerobicmetabolism of lactate, (iv) other influences.

(i) Repletion of oxygen storesThe possible importance of the oxygen stores has been considered in

previous studies of intermittent exercise. With 10 sec work periods and20 see (rest) recovery intervals, Astrand, Astrand, Christensen & Hedman(1960b) found an oxygen lag volume of 430 ml. per 10 sec work period.This volume was considered to be equal to the myoglobin oxygen store.Other possible factors, including a contribution from the venous bloodoxygen store and the sparing of oxygen by phosphagen break-down, werenot considered by these authors. In a study of alternating (equal) positiveand negative work periods of 2'25 and 4-1 see duration (so short that thecontributions of these two factors could be neglected) Hesser (1965)arrived at a much smaller figure (60 ml. or an estimated 3*0 ml. 02/kgactive muscle) for the myoglobin oxygen store. Saltin & Essen (1971),finding little or no resynthesis of phosphagen during 20 sec (rest) recoveryintervals, concluded that it was necessary to postulate the presence of anoxygen store in muscle which could be rapidly refilled during the re-covery intervals of intermittent exercise. But as the binding and releaseof oxygen by myoglobin and haemoglobin are reciprocal physiochemicalprocesses, the oxygen consumed in recovery should exactly match thatmissed during work (the oxygen lag volume) so that solely on this account,the work efficiency of continuous and intermittent exercise should beidentical. The explanation for the observed difference in work efficiencybetween the two forms of exercise must therefore be sought in differencesin the oxygen requirements of biochemical recovery processes.

(ii) Repletion of muscle phosphagen storeRecovery oxygen intake initially falls with an exponential half time of

about 25 sec. This component was first attributed to phosphagen resyn-thesis by Margaria, Edwards & Dill (1933) and recently experimentalsupport for this hypothesis has been provided from studies in dog muscle(Di Prampero & Margaria, 1969). In studies of intermittent exercise with30 see (rest) recovery intervals, Margaria et al. (1969)- attributed theoxygen lag volume per 10 see work period exclusively to phosphagenutilization but made no measurements of muscle phosphagen.

Studies of the rate of resynthesis following depletion of the phosphagen

492

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 493

store in human muscle (Edwards, Harris, Hultman & Nordesj6, 1972;Hultman, 1973) indicate that muscle phosphagen is half restored in about20-30 sec. Phosphagen resynthesis does therefore appear to be sufficientlyrapid (despite the contrary report by Saltin & Ess6n 1971) to play animportant role in energy supply during intermittent exercise. In anattempt to keep the total number of biopsies to a minimum we did notsample muscle at the start and end of consecutive work and recoveryperiods. However the finding that mean phosphagen (ATP+phospho-creatine) contents tended to be higher (Tables 2 and 3) in sample bobtained 30 see after the final work period, than in those taken imme-diately at the end of a burst of activity earlier in the work a suggeststhat phosphagen resynthesis was probably occurring in the recoveryintervals.

(iii) Aerobic metabolism of lactateThe slow component of the recovery oxygen intake curve (exponential

half time about 15 min) has long been attributed to aerobic metabolismof lactate (Margaria et al. 1933; Davies & Crockford, 1971). But the factthat oxygen debt is not repaid during prolonged submaximal exercise(Schneider, Robinson & Newton, 1968; Knuttgen, 1970), though theblood lactate concentration may return to resting levels during con-tinuous submaximal exercise (Bang 1936; Saiki, Margaria & Cuttica,1967; Knuttgen, 1970) would appear to be evidence against aerobiclactate metabolism being a primary determinant of the recovery oxygenvolume. Recent studies employing radioactively labelled lactate in dogs(Depocas, Minaire & Chatonnet, 1969) and in man (Hubbard, 1973) haveshown that lactate production is sustained throughout continuous sub-maximal exercise, even when blood lactate concentration has fallen almostto the resting level. The finding of a gradient for lactate between muscleand blood (Fig. 4) appears to support the possibility of continuing lactateproduction in the present study. Clearly a continuing lactate productionduring exercise and a concentration gradient for lactate between muscleand blood would invalidate any calculation of the size of the lactate poolfrom blood measurements thus making it impossible to estimate quanti-tatively the lactacid contribution to the recovery oxygen volume.

(iv) Other influencesA very slow component of the oxygen uptake curve in recovery (time

course lasting several hours) has been attributed to a disturbance in basalmetabolism (Hill, Long & Lupton, 1924). A rise in body temperature wouldbe expected to result in such a disturbance (Brooks, Hittelman, Faulkner& Beyer, 1971) though this is unlikely to be of any importance in the

R. H. T. EDWARDS AND OTHERS

present study as the observed rise in rectal temperature was small (0. 3 C),and not significantly different in the two forms of exercise.

ConclusionIt is not possible on the available evidence to assess which of the

aerobic recovery processes is responsible for the larger total oxygen intakein intermittent exercise. Though at first sight unlikely, there exists thepossibility that the delayed aerobic resynthesis of phosphagen in this typeof exercise could be inefficient. Piiper & Spiller (1970) reported measure-ments of the rate of phosphagen resynthesis in relation to the time courseof oxygen consumption following exercise in the perfused gastrocnemiusmuscle of the dog. The lactacid contribution to the recovery oxygenvolume was considered to be negligible in these experiments. Notablefindings were (i) oxygen recovery volume was twice the oxygen lagvolume, and (ii) the calculated P:0 ratio for phosphagen resynthesis(after making allowance for restoration of oxygen stores) was 1-7. The P:0ratio was still less than 3 0 after partitioning the time course of aerobicrecovery into fast and slow components. This prompted the authors tosuggest that the observed low P: 0 ratio was due to a 'limited energeticeconomy of the oxygen debt repayment or to oxygen requirement ofrestoration processes other than resynthesis of high energy phosphates'.The present finding of a similar sized difference between the total oxygencost of intermittent and continuous exercise at both 25% V4VaX and,50% "Vax (when, from the measured lactate concentrations in muscleand blood, the lactate production might be expected to be less than at50%l'Umax) is compatible with the possibility of a 'limited energeticeconomy' in the resynthesis of phosphagen in muscle. Recent studies inman have shown that muscle lactate content rises in the first fewseconds of muscular activity, before depletion of the phosphagen store iscomplete (Bergstr6m, Harris, Hultman & Nordesj6, 1971; Karlsson,1971). Phosphagen depletion during the brief bursts of activity in inter-mittent exercise is therefore likely to have been accompanied by anaerobicglycolysis. Aerobic metabolism of the larger lactate yield in recoverywould thus account for the greater total oxygen cost of this type ofexercise. The finding of a larger total oxygen cost in intermittent exercisein this study thus entirely supports the conclusions reached in severalearly studies (Simonson & Hebestreit, 1930; Simonson & Sirkna, 1934;Assmussen, 1946; Christensen & Hdgberg, 1950) which showed reducedaerobic efficiency of single, brief periods of exercise.A practical conclusion shown by the results of the present study is

that if the aim is to keep the physiological cost of exercise to a minimum,a given amount of work is better performed continuously at a low power

494

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 495output. If the aim is to stress adaptive mechanisms then intermittentexercise is preferable. In fact intermittent exercise in the form of intervaltraining is widely used in athletics (Astrand & Rodahl, 1970).R.H.T.E. was in receipt of a Swedish Wellcome Travelling Research Fellowship

during leave of absence from the Royal Postgraduate Medical School, London. Theseexperiments were supported by Swedish Medical Research Council Grants, nos.B71-40X-682-06, B70-19X-1002-05B, B70-19X-2647-02B and K70-19X-2647-02BK.

REFERENCES

AGosToNI, E., CAMPBELL, E. J. M. & FREEDMAN, S. (1970). Energetics. In The Re-spiratory Muscle8, ed. CAMPBELL, E. J. M., AGOSTONI, E. & NEWSOM DAVIS, J.,pp. 115-137. London: Lloyd Luke.

ASMUSSEN, E. (1946). Aerobic recovery after anaerobiosis in rest and work. Actaphysiol. scand. 11, 197-210.

ASTRAND, I., ASTRAND, P-O., CHRISTENSEN, E. H. & HEDMAN, R. (1960a). Inter-mittent muscular work. Acta physiol. scand. 48, 448-453.

ASTRAND, I., ASTRAND, P-O., CHRISTENSEN, E. H. & HEDMAN, R. (1960b). Myo-hemoglobin as an oxygen store in man. Acta physiol. scand. 48, 454-460.

ASTRAND, P-O. & RODAHL, K. (1970). Textbook of Work Physiology, pp. 352-387.New York: McGraw-Hill.

BANG, 0. (1936). The lactate content of the blood during and after muscular exer-cise in man. Skand. Arch. Physiol. 74, suppl. 10, 51-82.

BERGSTROM, J. (1962). Muscle electrolytes in man. Determined by neutron activa-tion analysis on needle biopsy specimens. A study on normal subjects, kidneypatients, and patients with chronic diarrhoea. Scand. J. clin. Lab. Invest. 14,suppl. 68, pp. 11-14.

BERGSTROM, J., HARRIS, R. C., HULTMAN, E. & NORDESJO, L.-O. (1971). Energyrich phosphagens in dynamic and static work. In Muscle Metabolism duringExercise, ed. PERNOW, B. & SALTIN, B., pp. 341-355. New York: Plenum.

BROOKS, G. A., HITTELMAN, K. J., FAULKNER, J. A. & BEYER, R. E. (1971). Tem-perature, skeletal muscle, mitochondrial functions and oxygen debt. Am. J.Physiol. 220, 1053-1059.

CHRISTENSEN, E. H. & HOGBERG, P. (1950). The efficiency of anaerobical work.Arbeitsphysiol. 14, 249-250.

CHRISTENSEN, E. H., HEDMAN, R. & HOLMDAHIL, I. (1960). The influence of restpauses on mechanical efficiency. Acta physiol. scand. 48, 443-447.

CROWDEN, G. P. (1934), The effect of duration of work on the efficiency of muscularwork in man. J. Physiol. 80, 394-408.

DAVIES, C. T. M. & CROCKFORD, G. W. (1971). The kinetics of recovery oxygenintake and blood lactic acid concentration measured to a baseline of mild steadywork. Ergonomics 14, 721-731.

DEPOCAS, F., MINAIRE, Y. & CHATONNET, J. (1969). Rates of formation and oxida-tion of lactic acid in dogs at rest and during moderate exercise. Can. J. Physiol.Pharmacol. 47, 603-610.

DI PRAMPERO, P. E. & MARGARIA, R. (1969). Mechanical efficiency of phosphagen(ATP + CP) splitting and its speed of resynthesis. Pfliiger Arch. ges. Physiol.308, 197-202.

EDWARDS, R. H. T. (1971 a). Peripheral factors influencing effort tolerance inpatients with chronic obstructive bronchitis. Scand. J. resp. Dis. suppl. 77, 107-111.17 PH Y 234

496 R. H. T. EDWARDS AND OTHERSEDWARDS, R. H. T. (1971 b). Percutaneous needle-biopsy of skeletal muscle in

diagnosis and research. Lancet ii, 593-596.EDWARDS, R. H. T., JONES, N. L., OPPENHEIMER, E. A., HUGHES, R. L. & KNILL-JoNEs, R. P. (1969). Inter-relation of responses during progressive exercise intrained and untrained subjects. Q. Jl exp. Physiol. 54, 385-396.

EDWARDS, R. H. T., HARRIS, R. C., HULTMAN, E., KAIJSER, L., KOH, D. &NORDESJ6, L.-O. (1972). Effect of temperature on muscle energy metabolismand endurance during successive isometric contractions, sustained to fatigue, ofthe quadriceps muscle in man. J. Physiol. 220, 335-352.

EDWARDS, R. H. T., HARRIS, R. C., HULTMAN, E. & NORDESJ6, L.-O. (1972).Phosphagen utilization and resynthesis in successive isometric contractions, sus-tained to fatigue of the quadriceps muscle in man. J. Physiol. 224, 40-41 P.

EDWARDS, R. H. T., MELCHER, A., HESSER, C. M., WIGERTZ, 0. & EKELUND,L.-G. (1972). Physiological correlates of perceived exertion in continuous andintermittent exercise with the same average power output. Eur. J. clin. Invest.2, 108-114.

EKBLOM, B., GREENLEAF, C. J., GREENLEAF, J. E. & HERMANSEN, L. (1971). Tem-perature regulation during continuous and intermittent exercise in man. Actaphysiol. sand. 81, 1-10.

HARRIS, P. (1969). Lactic acid and the phlogiston debt. Cardiovasc. Res. 3, 381-390.HESSER, C. M. (1965). Energy cost of alternating positive and negative work. Acta

physiol. scand. 63, 84-93.HILL, A. V., LONG, C. N. H. & LUPTON, H. (1924). Muscular exercise, lactic acidand the supply and utilization of oxygen. Parts IV to VI. Proc. R. Soc. B 97,155-176.

HUBBARD, J. (1973). The effect of exercise on lactate metabolism. J. Physiol. 231,1-18.

HULTMAN, E. (1973). Energy metabolism in human muscle. Clin. Sci. 44, 12-13P.KARLSSON, J. (1971). Lactate and phosphagen concentrations in working muscle ofman with special reference to the oxygen deficit at the onset of work. Acta physiol.scand. 81, suppl. 358, 1-72.

KNUTTGEN, H. G. (1970). Oxygen debt after submaximal physical exercise. J. apple.Physiol. 29, 651-657.

LASSERS, B. W. (1971). Myocardial lipid and carbohydrate metabolism in healthyman. Acta Univ. Upsaliensis 109, 1-35.

LINDBORG, B., ODMAN, T. & WIGERTZ, 0. (1969). A beat-to-beat heart rate meterwith digital read out and linear analog output. Report Lab. Aviat. Naval Med.,Karol. Inst., Stockholm.

LUNDHOLM, L., MOHME-LUNDHOLM, E. & VAMOS, N. (1963). Lactic acid assay withL(+)-lactic acid dehydrogenase from rabbit muscle. Acta physiol. scand. 58,243-249.

MARGARIA, R., EDWARDS, H. T. & DILL, D. B. (1933). The possible mechanism ofcontracting and paying the oxygen debt and the role of lactic acid in muscularcontraction. Am. J. Physiol. 106, 689-715.

MARGARIA, R., OLIVA, R. D., Di PRAMPERO, P. E. & CERRETELLI, P. (1969). Energyutilization in intermittent exercise of supramaximal intensity. J. appl. Physiol.26, 752-756.

PIIPER, J. & SPILLER, P. (1970). Repayment of 02 debt and resynthesis of highenergy phosphates in gastrocnemius muscle of the dog. J. appl. Physiol. 28, 657-662.

PUGH, L. G. C. E. (1958). Muscular exercise on Mount Everest. J. Physiol. 141, 233-261.

SAIKI, H., MARGARIA, R. & CUTTICA, F. (1967). Lactic acid production in submaxi-mal work. Int. Z. agnew. Physiol. 24, 57-61.

AEROBIC RECOVERY AFTER MUSCULAR ACTIVITY 497SALTIN, B. & ESSEN, B. (1971). Muscle glycogen lactate ATP and CP in intermittent

exercise. In Muscle Metabolism during Exercise, ed. PERNOW, B. & SALTIN, B.,pp. 419-424. New York: Plenum.

SCHNEIDER, E. G., ROBINSON, S. & NEWTON, J. L. (1968). Oxygen debt in aerobicwork. J. appl. Physiol. 25, 58-62.

SIMONSON, E. & HEBESTREIT (1930). Zum verhalten des Wirkungsgrades bei korper-licher Arbeit. Pflugers Arch. ges. Physiol. 225, 498-532.

SIMONSON, E. & SIRKNA, G. (1934). Wirkungsgrad und Arbeitsmaxim. Int. Z.angew. Physiol. 7, 457-474.

TORNVALL, G. (1963). Assessment of physical capacities with special reference to theevaluation of maximal voluntary isometric muscle strength and maximal workingcapacity. Acta physiol. scand. 58, suppl. 201, 62-70.

WHIPP, B. J. & WASSERMAN, K. (1969). Efficiency of muscular work. J. apple.Physiol. 26, 644-648.

WHIPP, B. J., SEARD, C. & WASSERMAN, K. (1970). Oxygen deficit-oxygen debtrelationships and efficiency of anaerobic work. J. appl. Physiol. 28, 452-456.

WIGERTZ, 0. (1970). Dynamics of ventilation and heart rate in response to sinu-soidal work load in man. J. appl. Physiol. 29, 208-218.

17-2