E I N E M A N NBr. J. Sp. Med., Vol. 29, No. 2, pp. 89-94, 1995

Elsevier Science LtdPrinted in Great Britain

0306-3674/95 $10.00 + 00

Eccentric activation and muscle damage:biomechanical and physiological considerationsduring downhill running

Roger G. Eston DPE, Jane Mickleborough MCSP MSct and Vasilios Baltzopoulos PhDtDivision of Health and Human Performance, University of Wales, Bangor UK and tDepartment of MovementScience and Physical Education, University of Liverpool, Liverpool, UK

An eccentric muscle activation is the controlled lengthen-ing of the muscle under tension. Functionally, most legmuscles work eccentrically for some part of a normal gaitcycle, to support the weight of the body against gravityand to absorb shock. During downhill running the role ofeccentric work of the 'anti-gravity' muscles - kneeextensors, muscles of the anterior and posterior tibialcompartments and hip extensors - is accentuated. Thepurpose of this paper is to review the relationship betweeneccentric muscle activation and muscle damage, particular-ly as it relates to running, and specifically, downhillrunning.

Keywords: downhill running, biomechanics, physiology,muscle damage

Mechanisms of muscle injuryRecent evidence indicates that skeletal muscle dam-age may be the primary mechanism contributing tomuscle soreness and strength loss after eccentricexercisel-5. However, the relationship betweenskeletal muscle damage, muscle soreness and loss ofmuscle force is unclear. Muscle soreness peaks wellbefore muscle damage indices and muscle weaknessappears to be at its worst immediately post-exercise.There is substantial evidence that eccentric contrac-tions cause more damage than other types ofcontraction" 2. Ultrastructural changes within skeletalmuscle fibres were first demonstrated by Friden et al.3following an exercise protocol of repeated stairdescents which caused severe delayed onset musclesoreness (DOMS). Post-exercise samples showedmyofibrillar disturbances consisting of Z-band disrup-tion and streaming.Two hypotheses, metabolic overload and mecha-

nical strain, have been suggested as causativemechanisms for muscle damage. As eccentric activa-tion causes most muscle damage, it suggests thathigh local muscle tensions are in some way moreimportant than extreme metabolic demand in theaetiology of DOMS injury6.

Appell et al.7 presented evidence to suggest thatthe mechanisms producing muscle damage after levelendurance running and downhill running were notthe same. A comparison was made of the histologicalstructure of the rat soleus muscle, subjected either toa level endurance run or a downhill run. The loss ofstriation pattern seen in 15% of fibres at 48 h werepredominantly in fibres which were glycogen de-pleted. This suggests a metabolic aetiology for thedamage. Glycogen depletion was present in 25% ofthe fibres immediately after level running andincreased to 33%, 48 hours later. There were similarlevels of lysosomes in the muscle fibres. This,combined with an immediate 16% loss of sarcomereorganization, suggested an autophagic response, dueto metabolic exhaustion and enzyme leakage. Incontrast, however, the downhill running muscle hadhigher disruption levels (33% of fibres with immedi-ate loss of sarcomere organization) but no glycogendepletion or lysosome occurrence in the fibres. Thislack of glycogen depletion and absence of autophagicresponse supports a mechanical origin of muscledamage8.

Strength lossPerhaps one of the more noticeable effects ofeccentric exercise induced by downhill running is theacute loss of strength which continues for some daysafter the damaging exercise9'2. Short-term strengthloss is also experienced after concentric and isometricexercise. The longer duration strength loss, associ-ated with eccentric exercise, has been attributed tosarcoplasmic reticulum damage. This latter theoryhas been postulated by Clarkson et al.9 on theassumption that, if the sarcoplasmic reticulum isdamaged, the restoration of normal calcium levelswould be delayed and the ability to generate normalforce levels would be impaired. Indeed, alteredsarcoplasmic reticulum function and consequentintracellular regulation of free calcium concentrationhas been reported after prolonged"3 and highintensity exercise14 in animals.An additional explanation for the loss of strength

after eccentric exercise has been put forward byClarkson et a19. They proposed that the sarcomeresare stretched out by performance of the lengthening

89

Address for correspondence: Dr R G. Eston, Division of Healthand Human Performance, Ffriddoedd Building, Victoria Drive,University of Wales, Bangor, LL57 2EN, UK

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from

Downhill running: physiological and biomechanical considerations: R. G. Eston et al.

action. Sarcomeres are shorter towards the end of themuscle fibres"5. If the lengthening action pulls someof the sarcomeres apart, the overlap between theactin and myosin filaments would be reduced whichwould reduce the number of cross bridges that couldform. However, they acknowledged that there are asyet no data to substantiate such a theory.

In contrast to the rapid recuperation of strengthafter concentric exercise, the loss of strength aftereccentric exercise is much longer lasting. The lengthof time the muscle requires to regain full strengthdoes not appear to be established, as studies tend tomeasure only until around 10 days, where there isstill usually a significant reduction of strengthcompared to pre-trial values. Eston et al.'2 compareduphill and downhill running at similar exerciseintensity (80% of the maximal heart rate, %HRmax).They reported a decrease in the strength of the kneeextensors from 270(±40N m) to 115(± 34) immediate-ly following five 8-min bouts of downhill running at- 10% interspersed with 2 min rest periods. Strengthwas still lower (225 ±49N m) after 7 days. There wasno change in strength after running uphill at a similarmetabolic cost. Finney et al. 6 using a similar protocol,measured concentric and eccentric isokinetic strengthof the knee extensors. They reported similar strengthlosses for both concentric and eccentric strength, withvalues returning to normal after 4 days.The degree to which strength decreases appears to

be related to the relative length of the muscle duringeccentric exercise. For example, Newham et al.observed that when the elbow flexors were exercisedat long length, strength decreased to 75% of theinitial values immediately after exercise and at 24 hlater. Short length exercise produced much smallerchanges in strength.Muscle tenderness, which peaked at 48 h, was also

greatest in the muscles exercised at long length.Newham et al.17 therefore concluded that high forcegeneration was not the only explanation for theundesirable consequences of eccentric exercise. Itshould also be noted that forces generated at longlength are lower than forces generated at short length(100-250N long, 150-375N short)'7. Similarly, longlength isometric maximal voluntary contractions(MVC) produce greater low-frequency fatigue andpain, with relatively lower force than for MVC atshort length'8.Newham et al.17 therefore concluded that the

differences in strength, after exercise at long andshort length, were not just due to the magnitude ofthe force generated in the muscle. Changes instrength also appear to be related to the length atwhich the muscle is exercised. In downhill runningthe knee extensor muscle group is worked over agreater range than for uphill running, with morework at its longer length.

Soreness and tendernessTenderness, measured by pressure transducers (e.g.Penny and Giles Myometer, Christchurch, Dorset,UK) is greatest in the gluteus maximus, rectusfemoris, vastus medialis, vastus laterali, tibialisanterior, gastrocnemius and biceps femoris when

measured 2 days after downhill running'2. Thegreatest tenderness occurred at the distal myotendi-nous junction of the muscles. This corresponds withprevious investigations which have used differentprotocols of inducing damage'9-2'. The fact that thistenderness appears to be immediate'9 rather thandelayed may suggest that it originates in connectivetissue. Pain experienced during active extension isaccompanied by a decrease in resting angle'9, whichis perhaps due to tension on the damaged connectivetissue.

Creatine kinaseCreatine kinase is found in skeletal muscle, cardiacmuscle and the brain. Abnormally high circulatinglevels of enzymes such as creatine kinase are taken toreflect changes in the integrity of muscle fibremembranes - either damage to, or increasedpermeability, of the membrane to the enzyme.Eccentric activation of muscle has been widelyimplicated as the cause of large increases in plasmacreatine kinase (PCK) after exercised24There appears to be a quantitive difference in the

PCK response between high force, maximal eccentricexercise and downhill running. For example, aftermaximal eccentric exercise of the forearm flexors,Clarkson et al.9 observed that PCK levels started torise quickly after 2 days and peaked at 4 days at alevel of about 2500U-1' High intensity eccentricexercise in untrained men produced a mean peakPCK response of 2143 u l-l at 5 days25. Peak levels ofaround 1500-11 000 u-1l' were reported by Newhamet al.26 after maximal eccentric exercise. After high-intensity eccentric exercise of the knee extensors,PCK has also reached levels of 6988± 1913uu-I at thethird day after exercise27.

In contrast, PCK levels after downhill runningseem to peak much earlier, at a much lower level.Examples of this are levels of 339±379.6u'1-1,observed by Byrnes et al. at 24 h28, and a peak at 24 hof between 425-460 u1-1 observed by Schwane etal.29'3'. Studies from our laboratory showed peaklevels of 400-580 u1-1 occurring 2 to 4 days afterdownhill running at 10% gradient'2 16. PCK levels fordownhill walking seem to reflect the relative intensityand duration of maximal eccentric exercise, withlevels of between 700-1500 u -1 between 4-7 days24.There is a large difference in the working muscle

mass of forearm flexors compared to the eccentricallyworking leg muscles in downhill running, whichmakes these contrasts even more striking. There is asyet no explanation for the difference in time course ormagnitude of PCK levels between high force eccentricexercise and downhill running exercise9. Perhaps thereason for the disparity in magnitude is that highforce eccentrics involve higher forces maintainedthrough a longer strain range than downhill running.

Oxygen drift during downhill runningDespite its relative metabolic efficiency, a number ofstudies have shown a steady upward driftof V12 during downhill runningll"28,31-33. Sergeantand Dolan"l observed that oxygen uptake rose

90 Br J Sp Med 1995; 29(2)

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from

Downhill running: physiological and biomechanical considerations: R. G. Eston et al.

progressively from 45% of VO2ma,, after 10 min to 65%VO2max at the end of a downhill running exercise.Pierrynowski et al.32 also observed an upward drift ofV02 during downhill running and downhill trainingat a constant stride frequency, compared with a stableVo2 during uphill training.

Iverson and McMahon 4 found that the oxygendemand at a steady 3m/sec-1 reduced with increas-ing downhill gradient, until near -0.10 rad, and thenincreased as the downhill angle grew steeper. At theangle of -0.10 rad, the normal foot reaction force wasfound to be maximal. It is suggested that this gradientis the most efficient in terms of energy expenditure,making greater use of the stored elastic energy of themusdes, while causing most stress to the legs andfeet.Dick and Cavanagh31 compared the V02 of experi-

enced runners, over two same-speed runs, 2 daysapart, on the level and downhill. For the level runthere were no differences in 02 consumption,integrated EMG (vastus lateralis and vastus medialis)or stride length after 10 and 40 min. However, in thedownhill run, there was a 10% increase in 02consumption and a 23% increase in EMG activity inthe same time period. It was hypothesized that theupward drift in V02 and EMG increase were a resultof increased motor unit recruitment in the eccentrical-ly activated muscles, caused by muscle/connectivetissue damage and local muscle fatigue. However,Westerlind et al.' have contradicted this argument.They observed increases in Va2, heart rate andventilation during two downhill runs at 40% peakV02. Upward drift of Vo2 over time was similar forthe two downhill runs (15.6% and 14.7% respective-ly). Serum CK activity or perceived muscle sorenesshowever was reduced during the second run. It wastherefore suggested that the V62 drift increase duringdownhill running is not related to muscle damage.

Adaptation and trainingPrevious training reduces the muscle soreness re-sponse and reduces morphological changes, perform-ance changes and PCK activity in theblood'~t . Soreness is reduced by trainingthat involves eccentric contractions2' as concentrictraining does not reduce DOMS in subsequenteccentric exercise42. Similarly, in animals, the muscledamage that occurs during downhill running isprevented by downhill and level training, but not byuphill traininge. The protective effect of a prior boutof exercise, that in itself may only produce minimalsoreness, lasts for prolonged periods. Byrnes et al.28observed that the muscle soreness response todownhill running was reduced by up to 6 weeksfollowing an initial bout of downhill running.Similarly, Pierrynowski et al.32 found that as little astwo 12 min bouts of downhill running at a gradient of10% were sufficient to protect against the occurrenceof DOMS in a subsequent downhill run 3 days later,which had produced DOMS in the control group.However, they also noticed that this training was notsufficient to prevent a 2-3 day reduction in muscularstrength, suggesting that strength loss and DOMSmay have different physiological origins.

We have examined the effect of a prior bout ofmaximal isokinetic eccentric exercise on DOMS,strength loss and serum CK'6 following a downhillrun in 10 male students. The experimental groupperformed 100 maximal, isokinetic eccentric activa-tions at 0.52rads-l. Two weeks later the downhillrun was performed on a motor driven treadmill. Thisconsisted of five bouts of 8 min at a gradient of -10%at a speed corresponding to 80% of the maximumheart rate. The control group performed the downhillrun as above but without the prior isokinetic session.After isokinetic exercise, peak torque decreased by10% (358.6±38.8 to 323.0±26.9N m) immediatelypost-exercise and returned to baseline levels by day 4.Serum creatine kinase activity increased by 403%(86±22 against 345±234uP1-1) and rating ofperceived soreness (RPS) increased from 0 to 4.8±2.8by day 4. Following the downhill run, post-exercisestrength loss was lower in the trained group (p<0.05)at both eccentric speeds (7N m against 68N m at 0.52rads-1 and 37N m against 87N m at 2.83 rad-s' forthe trained and untrained groups, respectively) andat the slower concentric speed (22N m against 64N mfor the trained and untrained group, respectively).There was less soreness and tenderness (p<0.05) inthe trained knee extensor muscle group. Strengthalso returned to baseline measures earlier for thetrained group. Serum creatine kinase activity peakedon day 4 for the trained group (319± 109 u*l ) and onday 2 for the untrained group (578±269u'1-1)(p<0.05). For the untrained group tenderness wasgreatest (p<0.05) in the distal musculotendinousjunction, whereas it was greatest in the muscle bellyfor the trained group. There were no significantdifferences in tenderness measurements for thegluteus maximus, anterior tibialis and gastrocnemiusmuscles between the two groups. The results suggestthat a prior bout of isokinetic eccentric trainingreduces the severity of muscle damage, reduces theamount of strength loss and decreases the sensationof soreness and tenderness after downhill running.

Ebbeling and Clarkson4 suggested that the musclerepairs itself after the first bout of damage-inducingexercise and that adaptations within the musdesurrounding connective tissue were the reasons forthe rapid training effect after one eccentric exercisebout. However, Clarkson et al.9 have now suggestedthat this theory is unlikely, as over time periods of 6months, with the constant turnover of cellularcomponents, the 'conditioned' fibres were unlikely toretain their adaptations. They hypothesized that thefirst bout of eccentric exercise adapts the motor-unitrecruitment pattern over the movement range, tomore equally distribute the force between the musclefibres, reducing the chance of severe damage to anyone motor unit. Motor skills are 'stored' for a longtime, giving credence to this neurological theory;along with a cellular response as the reason for thelong training effect.

Biomechanics of downhill runningDuring normal locomotion (walking and running) theextensor muscles in the lower limbs perform eccentriccontraction during each stride to decelerate the centre

Br J Sp Med 1995; 29(2) 91

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from

Downhill running: physiological and biomechanical considerations: R. G. Eston et al.

of mass after the foot touches the ground'.Following downhill running, greater DOMS isproduced in the gluteal muscles, the quadriceps, andthe anterior and posterior tibial muscles, than for anequivalent bout of level running'2.Armstrong et al.2 suggested that it is primarily the

eccentric contraction phase that causes muscledamage during normal level running since thehighest tensions in the leg extensor muscles areproduced whilst the muscles are lengthening afterthe foot touches the ground and the centre of mass isdecelerating.Few studies have examined the kinematic differ-

ences between downhill and level running andhighlighted the differences in the knee angle betweenfootstrike and peak flexion angle45 46. The overallchange in angle is greater in downhill running, withpeak flexion angle significantly greater. This meansthat the muscle is working eccentrically at a greaterlength during downhill running. As alluded toearlier, there appears to be a length-dependantcomponent in the production of muscle damage"7. Indownhill running the knee extensor muscle group isworked over a greater length, with more work at itslonger length. This is exemplified from the followingkinematic data.During downhill running the overall change in

knee angle from footstrike to peak flexion angle ismuch greater than in level running. Values cited inthe literature for downhill and level running are0.52 rad (30.90) at a gradient of -8.3% against 0.34 rad(19.3°)45, 0.61 rad (35.1M at a gradient of -10%against 0.47rad (27.2°) , and 0.57rad (32.50) at agradient of -9% against 0.36 rad (20.50) (results fromour laboratory). This movement takes place in thefirst half of the stance phase of gait, with peak flexionangle occurring significantly later (40.7% and 33.6%of stance), for downhill and level running respective-ly45. Values from our laboratory are 50.0% against47.6% of the stance phase for downhill and levelrunning respectively. This appears to be the majorphase of negative or eccentric work for the kneeextensors, which control knee flexion and absorbshock. The initial knee flexion angle at footstrike isless in downhill compared to level running 0.30rad(17.00) against 0.43 rad (24.60) and the peak flexionangle is greater 0.84 rad (47.90) against 0.77 rad(43.90)45. Corresponding values for the initial kneeflexion angle at heelstrike from our laboratory are0.12rad (7.10) at -9% gradient and 4m s-1, against0.30rad (17.40) for the level running. Despite thesedifferences the angle between leg and the verticaldoes not change during downhill running34.

In downhill running, the knee extensor musclegroup is being actively strained to a greater degreethan in level running, while undergoing a simul-taneous contraction. Leiber and Friden's47 workdemonstrated that it is the degree of active strain on acontracting muscle, independent of the relative forceexerted by the muscle, that produces the characteris-tic signs and symptoms of musde damage, not foundin level running.The timing of maximum dorsiflexion is also later as

a percentage of stance in downhill compared to levelrunning (49.3% against 45.0%). Peak dorsiflexion

velocity is the same for both downhill and levelrunning, but there are significant differences in thetiming, with peak values occurring later in stance(28.6% against 21.4%)45.However, there is no difference in the peak

dorsiflexion angle at the ankle. This may explain whythere is no greater incidence of muscle damage in theposterior calf muscles during downhill running. Moststudies of downhill running and muscle damage haveconcentrated on the quadriceps group, with verylittle mention of posterior calf pain. The ankle is a lessmobile joint than the knee, with dorsiflexion fromneutral restricted to less than 0.44 rad (250)48. Thislack of range of movement may explain the finding ofWinter49 that the ankle is a net generator of force,while the knee is a net absorber in level jogging.There may not be sufficient range in the ankle to letthe calf muscles act efficiently as absorbers of force.Because of the functional position of the ankle, theposterior calf muscles may simply be more adapted toworking at their long length, protecting them frommuscle damage in downhill running. Power genera-tion/absorption is the product of joint moment andjoint angular velocity and is either a positive ornegative quantity, depending on the directions ofjoint moment and angular velocity. Buczec andCavanagh45 reported a much greater total of negativework in both knee and ankle in downhill, comparedto level, running. Values for absorption at the kneewere about twice those for the ankle in both downhilland level running. Specifically, the negative (absorp-tion) work of the knee extensors in stance phase was58 J and 30 J for downhill and level running,respectively. Negative work done on extensor mus-cles at the ankle was 26.1 J for downhill runningcompared to 12.6J for level running. It was proposedthat it was the higher power absorption require-ments, rather than the greater range of jointmovement in downhill running that caused themuscle damage and soreness. Overall in levelrunning, it has been shown that the knee extensorsabsorb 3.5 times as much energy as they generate(69.2J against 19.6 J), with the ankle plantarflexorsgenerating 3 times more energy than they absorb(59.0J against 19.6J)49.At the knee, the negative work period as a

percentage of total stance time is significantly greaterfor downhill running (42.1% against 35.7%), with nosignificant difference in the duration of stance phasebetween downhill and level running. In the ankle thenegative work period is also significantly greater fordownhill running (43.6% against 28.6%)45.

In the lower leg, the plantarflexors of the anklesoleus and gastrocnemius - work eccentrically tocontrol the forward momentum of the leg over thefoot in early stance phase and facilitate heel lift. Theankle extensors (dorsiflexors) tibialis anterior, exten-sor hallucis longus and extensor digitorum longus,also have a considerable eccentric work component ingait to control the descent of the forefoot48.

In a study of ground reaction forces during leveland downhill running, support time was againalmost identical between conditions50. Vertical im-pact peak force was 14% higher for downhillcompared to level running. The anteroposterior

92 Br J Sp Med 1995; 29(2)

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from

Downhill running: physiological and biomechanical considerations: R. G. Eston et al.

braking impulse in downhill running was almostdouble that of the propulsive impulse. In levelrunning, these two impulses were not significantlydifferent. The peak impact vertical force duringdownhill running at -12% gradient is approximately1800N or 2.8 times body weighte4.

Anterior compartmentFriden and colleagues have concentrated on theeffects of eccentric muscle action on the anteriorcompartment of the lege"~. This compartment hasnon-elastic fascial sheaths and may be predisposed toanterior tibial compartment syndrome with repeateddownhill running.

Eccentric exercise causes a significant increase inintramuscular pressure in a non-compliant compart-ment, compared with concentric exercise. Musclefibre swelling is a predominant feature after eccentricexercise. This was thought to be a factor in thedevelopment of DOMS in a tight compartment51.However, intramuscular pressure is raised immedi-ately after eccentric exercise, before the musclesbecome painful. Once pain starts there are still thesame raised pressures. Newham and Jones' work52on DOMS in the biceps, found there was nodetectable difference in pressure between sore andcontrol arms. It appears therefore that eccentricexercise may cause an increase in pressure innon-compliant compartments (with the possibility ofcompartment syndrome) but is not directly associatedwith DOMS pain51.

It has been reported53 that anterior compartmentsyndrome develops mainly in runners, while soccerplayers and cyclists develop posterior compartmentsyndrome. Perhaps there is a connection between theeccentric work done in the anterior compartmxent inrunners, to control forefoot loading. This movementis not found in cyclists. In downhill running theremay be more eccentric work done by these muscles,which may contribute to a higher incidence ofcompartment syndrome.

SummaryThere are striking differences in the timing of eventsin stance phase between downhill and level runningalthough contact phase is independant of downhillangle . Peak knee flexion angle, peak flexionvelocity, maximum ankle dorsiflexion and peakdorsiflexion velocity all occur significantly later instance phase in downhill running'5. Possibly becausethere is a longer period of negative work for the kneeextensors and ankle flexors, there is more resultantmuscle damage.Variation in intensity of the eccentric exercise may

be the reason for the differences in both time courseand magnitude of PCK response between downhillrunning and high intensity eccentric exercise. Mostprotocols using high-intensity eccentric exercise werecareful to eliminate all concentric components fromthe tests. In contrast, downhill running is a muchmore functional activity, combining concentric andeccentric exercise. The physiological consequences ofdownhill running seem to be closer to normal

reactions to muscle damage with moderate PCKincreases. There is evidence to suggest that a priorbout of eccentric exercise does reduce decrements instrength, severity of muscle damage and perceivedmuscle soreness after a subsequent bout of downhillrunning.

References1 Newham DJ, McPhail G, Mills KR, Edwards RHT. Ultrastruc-

tural changes after concentric and eccentric contractions inhuman muscle. I Neurol Sci 1983; 61: 109-22.

2 Armstrong RB, Ogilvie RW, Schwane JA. Eccentric exercise-induced injury to rat skeletal muscle. I Appl Physiol 1983; 54:90-3.

3 Friden J. Sjostrom M, Ekblom B. A morphological study ofdelayed onset muscle soreness. Experientia 1981; 237: 506-7.

4 Friden J, Seger J, Ekblom B. Sublethal muscle fibre injuriesafter high-tension anaerobic exercise. Eur I Appl Physiol 1988;57: 360-68.

5 Friden J. Changes in human skeletal muscle induced by longterm eccentric exercise. Cell Tissue Research 1984; 236: 365-72.

6 Armstrong RB. Muscle damage and endurance events. SportsMed 1986; 3: 370-81.

7 Appell HJ, Soares JM, Duarte JA. Exercise, muscle damageand fatigue. Sports Med 1992; 13: 108-15.

8 Armstrong RB, Warren GL, Warren JA. Mechanisms ofexercise induced muscle fibre injury. Sports Med 1991; 12:184-207.

9 Clarkson PM, Nosaka K, Braun B. Muscle function afterexercise-induced muscle damage and rapid adaptation. MedSci Sports Exerc 1992; 24: 512-20.

10 Clarkson PM, Tremblay I. Exercise-induced muscle damage,repair and adaptation in humans. J Appl Physiol 1988; 65: 1-6.

11 Sargeant AJ, Dolan P. Human muscle function followingprolonged eccentric exercise. Eur I Appl Physiol 1987; 56:704-11.

12 Eston RG, Critchley N, Baltzopoulos V. Delayed-onsetmusde soreness, strength loss characteristics and creatinekinase activity following uphill and downhill running. I SportsSci 1994; 12: 135.

13 Fitts RH, Courtwright JB, Kim DHK Witzmann FA. Musclefatigue with prolonged exercise: contractile and biochemicalalterations. Am I Physiol 1982; 242: C65-73.

14 Byrd SK, McCutcheon LJ, Hodgson DR, Gollnick PD. Alteredsarcoplasmic reticulum function after high intensity exercise.I Appl Physiol 1989; 67: 2072-77.

15 Jones DA, Round JM. Skeletal Muscle in Health and Disease: Atextbook of muscle physiology. Manchester, UK: ManchesterUniversity Press. 1990; 158-74.

16 Finney S, Eston RG, Baltzopoulos V. Muscle soreness andstrength loss changes after downhill running following aprior bout of isokinetic eccentric exercise. J Sports Sci 1994; (inpress).

17 Newham DJ, Jones DA, Ghosh G, Aurora P. Muscle fatigueand pain after eccentric contractions at long and short length.Clinical Science 1988; T4: 553-7.

18 Jones DA, Newham DJ, Torgan C. Mechanical influences onlong-standing human muscle fatigue and delayed-onset pain.J Physiol 1989; 412: 415-27.

19 Cleak MJ, Eston RG. Muscle soreness, swelling, stiffness andstrength loss after intense eccentric exercise. Br J Sports Med1992; 26: 267-72.

20 Edwards RHT, Mills KR. Newham DJ. Measurement ofseverity and distribution of experimental muscle tenderness. JPhysiol 1981; 317: 1-2P.

21 Newham DJ, Mills KR, Quigley BM, Edwards RHT. Pain andfatigue after concentric and eccentric muscle contractions.Clin Sci 1983; 64: 55-62.

22 Friden J, Sfakianos PN, Hargens AR. Blood indices of muscleinjury associated with eccentric muscle contractions. J OrthopRes 1989; 7: 142-45.

23 Jones DA, Newham DJ, Round JM, Tolfree SE. Experimentalhuman muscle damage: morphological changes in relation toother indices of damage. I Physiol. 1986; 375: 435-48.

24 Newham DJ, Jones DA, Edwards RHT. Plasma creatinekinase changes after eccentric and concentric contractions.Muscle-Nerve 1986; 9: 59-63.

Br J Sp Med 1995; 29(2) 93

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from

Downhill running: physiological and biomechanical considerations: R. G. Eston et al.

25 Evans WJ, Meredith CN, Cannon JG, Dinarello CA, FronteraWR, Hughes VA, Jones BH, Knuttgen HG. Metabolic changesfollowing eccentric exercise in trained and untrained men. JAppl Physiol 1986; 61: 1864-68.

26 Newham DJ, Jones DA, Clarkson PM. Repeated high-forceeccentric exercise: effects on muscle pain and damage. I ApplPhysiol 1987; 63: 1381-86.

27 Costill DL, Pascoe DD, Fink WJ, Robergs RA, Barr SI, PearsonD. Impaired muscle glycogen resynthesis after eccentricexercise. J Appl Physiol 1990; 69: 46-50.

28 Byrnes WC, Clarkson PM, White JS, Hsieh SS, Frykman PN,Maughan RJ. Delayed onset muscle soreness after repeatedbouts of downhill running. J Appl Physiol 1985; 59: 710-15.

29 Schwane JA, Williams JS, Sloan JH. Effects of training ondelayed muscle soreness and serum creatine kinase activityafter running. Med Sci Sports Exerc 1987; 19: 584-90.

30 Schwane JA, Johnson SR, Vandenakker CB, Armstrong RB.Delayed-onset muscle soreness and plasma CPK and LDHactivities after downhill running. Med Sci Sports Exerc 1983; 15:51-6.

31 Dick RW, Cavanagh PR An explanation of the upward driftin oxygen uptake during prolonged sub-maximal downhillrunning. Med Sci Sports Exerc 1987, 19: 310-17.

32 Pierrynowski MR, Tudus PM, Plyley MJ. Effects of downhillor uphill training prior to the downhill run. Eur J Appl Physiol1987; 56: 668-72.

33 Westerlind KC, Byrnes WC, Mazzeo RS. A comparison of theoxygen drift in downhill vs. level running. J Appl Physiol 1992;72: 796-800.

34 Iverson JR, McMahon TA. Running on an incline. J BiomechEng 1992; 114: 435-41.

35 Komi PV, Buskirk ER Effect of eccentric and concentricmuscle conditioning on tension and electrical activity ofhuman musde. Ergonomics 1972; 15: 417-34.

36 Schwane JA, Armstrong RB. Effect of training on skeletalmuscle injury from downhill running in rats. I Appl Physiol1983; 55: 969-75.

37 Friden J, Seger J, Sjostrom M, Ekblom B. Adaptive responsein human skeletal muscle subjected to prolonged eccentrictraining. Int J Sports Med 1983; 4: 177-83.

38 Jones DA, Newham DJ. The effect of training on humanmuscle pain and muscle damage. J Physiol. 1985; 365: 76P.

39 Byrnes WC, Clarkson PM. Delayed onset muscle sorenessand training. Clin Sports Med 1986; 5: 605-14.

40 Clarkson PM, Byrnes WC, Gillison E, Harper E. Adaptationto exercise-induced muscle damage. Clin Sci 1987; 73: 383-86.

41 Miller G, Wilcox A, Schwenkel J. The protective effect of aprior bout of downhill running on delayed onset musclesoreness (DOMS). Med Sci Sports Exerc 1988; 20: S75.

42 Sforzo GA, Lamb DR Muscie soreness after exercise: effectsof early training with concentric contraction. In: Dotson CO,Humphrey JH, eds. Exercise Physiology: current selected research.New York, USA: AMS Press, 1985; 171-79.

43 Ebbeling CB, Clarkson PM. Muscle adaptation prior torecovery following eccentric exercise. Euro I Appl Physiol 1990;60: 26-31.

44 Walmsley B, Hudgson JA, Burke RE. Forces produced bymedial gastrocnemius and soleus muscles during locomotionin freely moving cats. J Neurophysiol 1978; 41: 1203-16.

45 Buczec FL, Cavanagh PR Stance phase knee and anklekinematics and kinetics during level and downhill running.Med Sci Sports Exerc 1990; 22: 669-77.

46 Milliron MJ, Cavanagh PR Saggital plane kinematics of thelower extremity during distance running. In: Cavanagh PR(ed) Biomechanics of Distance Running, Champaign, IL USA:Human Kinetics Publishers, 1990.

47 Leiber RL, Frid~n J. Muscle damage is not a function ofmuscle force but active strain. J Appl Physiol 1993; 74: 520-26.

48 Root ML, Orien WP, Weed JH. Normal and Abnormal Functionsof the Foot. Clinical Biomechanics Vol 2. Los Angeles, USA:Clinical Biomechanics Corporation, 1977.

49 Winter DA. Moments of force and mechanical power injogging. J Biomech 1983; 16: 91-7.

50 Dick RW, Cavanagh PR A comparison of ground reactionforces (GRF) during level and downhill running at similarspeeds. Med Sci Sports Exerc 1987; 19: S12.

51 Frid~n J, Sfakianos PN, Hargens AR Muscle soreness andintramuscular fluid pressure: comparison between eccentricand concentric load. I Appl Physiol 1986; 61: 2175-79.

52 Newham DJ, Jones DA. Intra-muscular pressure in thepainful human biceps. Clin Sci 1985; 69: (Suppl): 27.

53 Styf J. Chronic exercise-induced pain in the anterior aspect ofthe lower leg. An overview of diagnosis. Sports Med 1989; 7:331-39.

94 Br J Sp Med 1995; 29(2)

on October 2, 2020 by guest. P

rotected by copyright.http://bjsm

.bmj.com

/B

r J Sports M

ed: first published as 10.1136/bjsm.29.2.89 on 1 June 1995. D

ownloaded from