The Influence of Frequency,Intensity, Volume and Mode of Strength Trainirg on Whole Muscle...

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The Influence of Frequency, Intensity,Volume and Mode of StrengthTrainirg on Whole MuscleCross-Sectional Area in HumansMathias Wernbom,r lesper Augustssonr,2 and Roland Thomeöl,21 Lundberg Laboratory for Human Muscle Function and Movement Analysis, Department of

Orthopaedics, Sahlgrenska University Hospital, Göteborg University, Göteborg, Sweden2 SportRehab Physical Therapy and Sports Medicine Clinic, Göteborg, Sweden

ConfenlsAbstrqct . . . . , . ,226l . Methods . . . . . . . . . .227

I. l L i lerotureSeorch . , . , ,2271.2 Clossificotion of Muscle Actions, Troining Methods ond Modolities . . .2281.3 Quontif icqtion of Exercise Frequency, Intensity ond Volume .........2291.4 Clossi f icol lon of Troining Stotus . . . . , . .230.l.5 Cqlculotion of Chonges ond Roteof Chonges in Muscle Cross-Sectionql Areq (CSA).......230

2. Resul tsPort l :Quqdr icepsStudies . . . . , . . .23. l2.1 Quodriceps Studies: Dynomic Externql Resislonce . . . . 231

2.1.1 Length of Troining Per iod, Averoge Increose in CSA ond CSA Per Doy., . , . . , .2322.1.2 RoteofGoininCSA: MenversusWomen . . . . . .2322.1.3 Frequency . . . . , . , , . . . .2322.1,4 Intensi ty . . , , . . , .2322.1.5 Volume . . , , . . , .232

2.2 QuodricepsStudies: Accommodot ing Resistonce.. . . . . . . . , .2332.2.1 Lengthof Troining Per iod,AverogelncreqseinCSAond CSAPerDoy.. . . . . . .2332.2,2 Frequency . . . . . . . . , . . .2332.2.3 Veloci ty . . . . . . . .2342.2,A Iotdte . . . . . , . . .23A2.2.5 Votume . . . . . . . .2g42,2,6 lotqlDurot ionPerSession . . . , . .2352.2,7 Time-Torque Producl PerSession . . . . . . ,235

2.3 Quodriceps Studies: lsometric Resistonce. . . . . 2352.3.1 Length of Troining Per iod,Averqge IncreoseinCSAqnd CSAPerDoy,. . . . . . .2352.3.2 Frequency.. . . . . . . . . . .2352.3.3 Intensi fy , . . . . . , .2352.3.4 Volume . . . . . . . .235

2.4 Quodriceps Studies: Combined Strength ond Enduronce Troining . . .2362.4.1 Rote of Goin in CSA: CombinedTroining versus PureStrengthTroining . . , . . . . .2362.4.2 Lengthof TroiningPeriodondlncreoseinCSA , . , . . , . ,236

2.5 Quodriceps Studies: All Voluntory Troining Modes . , . ,2362.5.1 Lengthof TroiningPeriodqndlncreoseinCSA . . . . . . . ,236

2.6 QuqdricepsStudies: StrengthTroiningoso Countermeosure Dur ing Unlooding.. . . . . . . . . . , .236

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The Influence of Frequency, Intensity,Volume and Mode of StrengthTrainirg on Whole MuscleCross-Sectional Area in HumansMathias Wernbom,r lesper Augustssonl,2 and Roland Thomeöl,21 Lundberg Laboratory for Human Muscle Function and Movement Analysis, Department of

Orthopaedics, Sahlgrenska University Hospital, Göteborg University, Göteborg, Sweden2 SportRehab Physical Therapy and Sports Medicine Clinic, Göteborg, Sweden

ConlenlsAbstroct . . . . . . .226l . Methods . . . . . . . . , .227

l . l L i lerotureSeorch . . . . .2271.2 Clossificotion of Muscle Actions, Troining Methods ond Modolities . . .2281.3 Quontif icqtion of Exercise Frequency, Intensity qnd Volume ...,,....2291.4 Clossi f icot ion of Troining Stotus . . . . . . .2301.5 Cqlculqtion of Chongesond Roteof Chongesin Muscle Cros-Sectionol Areo (CSA).......230

2. Resul tsPort l :Quodr icepsStudies . . . . . . . .2312.I Quodriceps Studiesl Dynomic Exlernol Resislonce . . . . 231

2. 1. l Lengthof TroiningPeriod,AverqgeIncreoseinCSAqndCSAPerDoy.. . . . . . .2322.1.2 Rote of Goin in CSA: Men versus Women . . . . . .2322.1.3 Frequency., . . . . . . . . . .2322.1,4 Intensi ty , . , . . . . .2322.1.5 Volume . . . . . . , .232

2.2 QuodricepsStudies: Accommodot ing Resistonce.. . . . . . . . . .2332.2.1 Lengrthof Troining Per iod,AverqgelncreoseinCSAond CSAPerDoy.. . . . . , .2332.2,2 Frequency . , . . . . . . . . . .2332.2.3 Veloci ty . . . . . . . .2342.2.4 loräue . . . . . . . . .2342.2.5 Votume . . . . . . . .2342.2.6 lotolDurot ionPerSession . . . . . .2352.2,7 l ime-IorqueProducl PerSession . . . . . . .235

2.3 Quodriceps Studies: lsometric Resistonce. . . . . 2352.3.1 Length of Troining Per iod,Averoge Increosein CSAond CSAPerDoy,. . . , . . .2352.3.2 Frequency . . . . . . . . . . . .2352.3.3 Intensi ty . . . , . . . .2352.3.4 Volume . . . . , . . .235

2.4 Quodriceps Studies: Combined Strength ond Enduronce Troining . , .2362.4.1 Rqte of Goin in CSA: Combined Troining versus Pure Strength Troining ...,,...2362.4.2 Lenglh of TroiningPeriodond IncreoseinCSA. . . . . . . .236

2,5 Quodriceps Sludies: All Voluntory Troining Modes . . . .2362.5.1 Length of Troining Per iod ond IncreoseinCSA . . . , . . . .236

2.6 QuqdricepsStudies: Strength Troining os o Countermeosure Dur ing Unlooding.. . . . . . , . . , . .236

Strength Training and Muscle Cross-Sectional Area 227

Strength training has become increasingly popu-lar in recent decades. Whereas previously strengthtraining had been used by a few selected athletes toimprove their strength and size, it is now an impor-tant component in training for most sports as well asfor injury prevention and rehabilitaliqn.tr-31 Quanti-fication of the dose-response relationships betweenthe training variables (e.g. intensity, frequency andvolume) and the outcome (e.g. strength, power andhypertrophy) is fundamental for the proper prescrip-tion of resistance training.tal Several meta-analy-sssta-8l sr6 numerous lsviswstl'3'e-lll have dealt withvarious aspects of optimising strength; however,with the exception of a paper by Fry,ttzl few system-atic reviews have focused on the issue of how totrain specifically for muscle hypertrophy. The re-view of Frytr2l discussed the role of training intensi-ty on hypertrophy as measured by increases in mus-cle fibre area (MFA).

Implicit in many articles in the literature are thefollowing assumptions: (i) training for strength andtraining for hypertrophy is essentially one and thesame thing; and (ii) the programme that yields thelargest increases in strength also results in the larg-est increases in muscle mass. These assumptions arenot necessarily true in all situations. For example,studies by Choi et al.tl3l and Masuda et al.llal showedsmaller increases in one repetition maximum (lRM)and isometric strength, but greater increases inquadriceps muscle area (as measured by magneticresonance imaging IMRII) and MFA after a typicalmoderate-load bodybuilding regimen when com-pared with a high-intensity powerlifting pro-gramme. Schmidtbleicher and Buehrletrsl showedgreater increases for triceps brachii muscle area (asmeasured by CT scanning) for a group that trainedwith 3 sets of 12 repetitions atTOVo of IRM whencompared with a group that trained with 7 sets ofl-3 repetitions at 90-l0OVo of lRM, while thestrength increases for the groups were similar. Thus,it is apparent from these and other studies that thetraining prescription for hypertrophy may differsomewhat from the prescription for maximumstrength. This observation has been taken into ac-count in various models of periodisation,tl6'17l *6"t"

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training periods or training sessions.aimed at stimu-lating maximum hypertrophy by high volume andmoderate loads are followed by periods or sessionsaimed at increasing maximum strength by moderatevolume and heavy loads. The latter type of workoutpresumably acts by optimising neural adapta-tions,trrl although marked hypertrophy can also oc-cur if the volume is sufficient.tl2'15'l8l

Scanning methods such as MRI and CT are re-garded as the gold standard for assessing wholemuscle size.tle'201 To our knowledge, no systematicreview has been published that has analysed theimpact of several important training variablessuch as frequency, intensity and volume on changesin muscle area or volume as measured by scanningmethods. Such a review could provide evidence-based guidelines for the prescription of strengthtraining for increasing muscle mass. Establishingefficient models of strength training for hypertrophyin humans could also be of value for the study of thephysiological mechanisms of the hypertrophy pro-cess. Therefore, the purpose of the present study wasto identify dose-response relationships for the devel-opment of muscle hypertrophy by calculating therates and magnitudes of increases in muscle cross-sectional area (CSA) or muscle volume induced byvarying levels of frequency, intensity and volume,as well as by different modes of strength training.

l. Melhods

l.l Literoture Seorch

Computer searches in the MEDLINE/PubMed,SportDiscus@ and CINAHL@ databases were per-formed for articles from 1970. when the first train-ing study using scanning techniques to evaluatechanges in anatomical muscle CSA was pub-lished.l2ll In addition. hand searches of relevantjournals and books as well as the reference lists ofarticles already obtained were performed. The datareviewed in this article was accumulated as a resultof literature searches conducted for this and otherprojects over a period of several years. The lastsearch was performed on 3 December 2006. As thesearch progressed, it quickly became apparent that

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228 Wernbom et al.

the quadriceps was by far the most studied musclegroup in humans undergoing strength training andthat the elbow flexors (biceps brachii and brachialis)were the second most studied muscle group. Cur-rently, these are probably the only muscle groupsthat allow for meaningful evaluation of dose-re-sponse trends. Therefore, the present review is fo-cused on the human quadriceps and elbow flexors.

Criteria for inclusion were as follows:l. Studies must have examined the effects ofstrength training on anatomical muscle area or mus-cle volume by a scanning method (i.e. MRI, CT orultrasound [UL]).2. Studies must have been conducted on healthy anduninjured participants between 18 and 59 years ofage.3. Sufficient data to calculate changes in muscle areaor volume must have been reported.4. Sufficient information regarding the training vari-ables (in particular: frequency, intensity and vol-ume) and the type and mode of exercise employedmust have been reported to allow for replication ofthe study.

Exclusion criteria were as follows:L The subjects received supplements (e.g. creatinemonohydrate, amino acids, proteins) or anabolichormones and/or growth factors that could poten-tially have influenced the neuromuscular adapta-tions to strength training. Such study groups (but notnecessarily other groups from the same study) wereexcluded from the current review.2. The subjects were in negative energy balance (i.e.on a weight-loss diet).3. The data from the study have been publishedbefore. However, sometimes it was necessary tocollect data from several different papers from thesame study.4. Only part of the muscle group (e.g. vastus lateral-is) was scanned. Alternatively, only data for the totalmuscle CSA of the limb (e.g. total thigh musclearea) was reported without specifying CSAs for theindividual muscles (e.g. quadriceps).

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1.2 Clossificotion of Muscle Actions, TroiningMethods ond Modolities

For the purposes of this review, the terminologyof Knuttgen and Komit22l was adopted for the classi-fication of muscle actions. Accordingly, exercisecan be classified as either static (involving isometricmuscle actions) or dynamic (involving concentricand/or eccentric muscle actions). During an isomet-ric muscle action, the muscle develops force but noexternal movement occurs and the length of themuscle-tendon complex does not change. During aconcentric action, the muscle produces force whileshortening. An eccentric muscle action refers to asituation where the muscle produces force whilelengthening.

In resistance exercise, training methods or mo-dalities are often classified according to the type ofresistance used. In his l98l review, arguably thefirst systematic look at strength training, tr1ftsteldivided the training modes into three main catego-ries: (i) isotonic; (ii) isokinetic; and (iii) isometric.Isometric training obviously involves isometric ac-tions. Isotonic training refers to dynamic exercise inwhich the muscle(s) exerts a constant tension.t22l Invarious textbooks of physiology, an isotonic muscleaction is often illustrated by an isolated muscle thatis shortening or lengthening against a constant load,thus developing a constant force. This is not true inthe intact muscle of a person performing an exercisebecause ofbiomechanical factors such as changes inthe lengths of the lever arms of the muscle and of theresistance. and also the accelerations and decelera-tions that occur during dynamic exercise. Thus, evenif the external resistance remains constant, the mus-cle will not develop a constant level of forae.l2z'231For this reason, the term 'isotonic' is often replacedby the term 'dynamic constant external resistance'(DCER).r2x In DCER exercise, the absolute load isconstant throughout the movement, as when lifting adumbell. Further examples of DCER would be sim-ple cable pulley systems with no lever arms andmachines with circle shaped cams. The term 'varia-ble resistance' is used when the resistance through-out the range of motion is varied, for example by anirregularly shaped camwheel or a lever nryl.tz3l 15"

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idea with variable resistance is to closely match theresistance with the strength of the subject through-out the range of motion.t24l However, because manydynamic training studies did not specify if the resis-tance was constant or variable, no distinction be-tween these subcategories was made in the presentreview. The overall category for both these subcat-egories is termed dynamic external resistance(DER).

In isokinetic training, muscle actions are per-formed at a constant angular velocity, which iscontrolled by the machine. Unlike dynamic externalresistance training, there is no set resistance to over-come; however, since the velocity is controlled, anyforce applied against the equipment results in anequal and opposite reaction force.t23lSince the sub-ject can freely vary the level of effort in the entiremovement to accommodate for pain or weakness incertain regions of the range of motion, the isokineticmode is very useful in rehabilitation.t24l Isokineticsare sometimes sorted into a category called 'accom-modating resistance'.[2s1 Also included in this cate-gory are devices in which the resistance is providedby hydraulic cylinders, which function by limitingthe flow through an adjustable aperture. Althoughnot providing a strictly isokinetic movement, theresistance setting on these machines can be adjustedto limit the velocity within relatively narrowranges.l2sl These devices are sometimes also re-ferred to as semi-isokinetic.t26l For the purposes ofthis review, the term 'accommodating resistance'was chosen for the main category. Another form ofstrength training uses the inertia of a flywheel forresistance. In this type ofergometer, the force exert-ed by the subject is transferred to a strap beingwound around the axle of a fixed flywheel.l271 4concentric muscle action unwinds the strap andovercomes the inertia of the flywheel, setting itspinning on low friction bearings. The rotating fly-wheel soon causes the strap to start winding upagain; therefore, the machine returns the stored en-ergy of the spinning flywheel via the strap and thesubject tries to resist the returning movement byperforming an eccentric muscle action. Caruso etal.t28l have used the term 'isoinertial' to describe this

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type of training, but Murphy and Wilsont2el haveused the exact same term to describe DCER training.With isoinertial flywheel ergometers, as withisokinetic training, the resistance is effort dependentfor each type of action. Therefore, this mode ofexercise will be included in the 'accommodatineresistance' category.

1.3 Quontificotion of Exercise Frequency,lntensity ond Volume

Regarding exercise intensity in dynamic externalresistance training, we chose to express intensity asa function of IRM in the exercise(s) performed forthe muscle group in question (e.g. SOVo of IRM inthe squat). In many of the studies, the authors pro-vided exact percentages or at least estimates of thepercentage. In cases where the intensity was ex-pressed only as a function of how many repetitionsthe subjects were able to perform (e.g. 8RM), weestimated the relative intensity based on data on therelationship between the number of repetitions per-formed and the IRM for the same or similar exer-cises.t2'30-331 For the squat, we used the RM tables ofWathan,t32l which have been shown to be accuratefor the squat in previously untrained subjects.t33l Forthe leg press, knee extension and arm curl exercises,we used data from Hoeger et al.t3ol The intensity forisometric training was quantified as a function of themaximum force achieved during a maximal volunta-ry isometric action (MVIA).

While the quantification of exercise intensity inconventional resistance training and isometric train-ing is relatively straightforward, how to express theintensity or load for isokinetic and other accommo-dating training modes is less obvious. The force-velocity relationship of skeletal muscle dictates thatas the velocity of the concentric muscle action in-creases, the maximum possible force decreases.[34'351Depending on the training status, the maximumtorque developed by the quadriceps during eccentricmuscle actions is slightly higher (trained subjects) ornot significantly higher (sedentary subjects) than themaximum isometric torque.t3sl In cases where thepeak torque during eccentric muscle actions exceedsthat of isometric muscle actions, the peak torque

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z5u Wernbom et al.

increases only marginally with increasing velocityand appears to reach a plateau at relatively lowvelocities.t35l The amount of force developed by themuscle is generally regarded as an important stimulifor muscle hypertrophy.t36l Since maximum effort(and therefore, recruitment of the greatest number ofmotor units possible) was used in most accommo-dating training studies, an estimate of the torquedeveloped in relation to the isometric maximumcould provide some insight into the level of forcenecessary to produce hypertrophy as a consequenceof accommodating resistance training. Therefore, inaddition to listing the training velocity, level ofeffort and type(s) of muscle action(s), we estimatedthe relative level of torque normalised to the maxi-mum isometric torque based on the peak torque datafor the quadriceps in untrained subjects fromAmiridis s1 al.t3sl For the elbow flexors, data fromHortobagyi and Katcht37l and Paddon-Jones et al.t38lwere used.

Training volume is a measure of the total amountof work (oules) performed in a given time peri-od.t23l In this review, training volume refers to asingle session. In a less strict sense, volume can beestimated by the sum of repetitionst23l or even by thenumber of sets performe6.t+t While simply statingthe number of sets may seem a crude measure ofvolume, several meta-analysest4-6'81 have shown sig-nificant differences in strength gains between train-ing with single and multiple sets in favour of multi-ple sets, particularly for trained subjects. Theoreti-cally, a given exercise volume can be distributed inmany different ways and as a consequence result indifferent adaptations. Therefore, several estimatesof volume (number of sets, total number of repeti-tions, total duration of work and total work) wereused in this review. However, instead of expressingthe total amount of work performed in joules, workwas calculated in arbitrary units (sets x repetitions xintensity;.tzsl If several exercises were performed forthe muscle group (e.g. leg presses and knee exten-sions for the quadriceps), the volumes for each ofthese were summed to yield the total volume for themuscle group. Regarding the training frequency, wehave chosen to report frequency as the number of

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sessions per muscle group per week, as opposed totraining days per week. For example, a traininggroup may have trained the quadriceps twice a day,three days a week. The frequency then is reported assix times per week. We are aware of the possibilitythat the physiological responses may differ betweentraining once a day six times per week and twice aday three times per week.

1.4 Clossificotion of Troining Stotus

In the majority of the studies, the subjects werereported as either untrained/sedentary or as physi-cally active. Physically active subjects generallyperformed some form of endurance training, but notany systematic strength training. Since many studiesreported varying levels of activity among the partici-pants and because endurance training induces littleif any muscle hypertrophy,l3el the categories 'un-trained' and 'physically active' were combined foranalyses. Deschenes and Kraemertaol made the fol-lowing classification of training status with refer-ence to resistance training: untrained, moderatelytrained, trained, advanced and elite. They suggestedthat the window of adaptation for strength becomesprogressively smaller as the subject progresses.However, because of the lack of studies involvingathletes ofdifferent training status, data from studieswith trained, advanced and elite athletes are dis-cussed together in the present review. In cases wherethe strength training status of the subjects was un-certain, information was sought regarding the CSAof the exercised muscles and comparisons weremade with data from previously untrained individu-alsl4l45l and resistance-trained subiects and strength61fle1es.lal,as-+71

L5 Colculotion of Chonges ond Rote ofChonges in Muscle Cross-SectionolAreo (CSA)

In most of the studies reviewed here, the authorsreported the changes in CSA or at least the pre- andpost-training values. Sometimes, figures were usedinstead of numerical data; in such cases the graphswere measured if possible. The relative changeswere calculated by simply dividing the post- with

Sports Med 2007j 37 (3)


the pre-training values. To allow for comparisonsbetween studies ofdifferent length, percent changesper day were calculated by dividing the change inarea with the length of the training period in days.Although some studiest43'481 have shown preferentialhypertrophy of individual muscles in a muscle groupand of different levels in the same muscle, no con-sistent pattern has yet emerged. Furthermore, datafrom other studiest44'4el suggest that changes in mus-cle CSA at the middle level and muscle volume aftera training period are of a similar magnitude. Inaddition, studies by Aagaard and co-workersts0l andTracy et al.t5ll have confirmed that quadriceps mus-cle volume can be accurately predicted from a singlescan at the middle level. Therefore, no distinctionwas made in this review between muscle volumeand CSA as indexes of muscle size. A further dis-cussion on the subject is provided by Tracy andcolleagues.ts2l

There are several reasons for focusing mainly onchanges in whole muscle CSA and not MFA. Asargued by Narici and colleaguest43l and D'Antona eta1.,t471 care should be taken when drawing conclu-sions concerning the whole muscle mass fromchanges occurring at a single biopsy site. In thestudy of Narici et al.,tarl 16" changes in mean fibrearea (2Vo increase in MFA) were not representativeof either the vastus lateralis at the same level as thebiopsy site (7.sEo increase in muscle CSA by MRI),or of the quadriceps as a whole (=l6Vo increase inmuscle CSA). Apart from the obvious risk of notdetecting hypertrophy because of sampling muscletissue from just a single site in a very large andarchitecturally complex muscle group such as thequadriceps, the lower limit for the increase in fibresize that can be detected is l0vo. Furthermore, thecoefficient of variation between repeated biopsies isquite large, =L5-2OVo (see Narici s1 al.ta3l for discus-sion). Thus, hypertrophic changes that are detecta-ble at the whole muscle level may go unnoticed ifonly fibre areas are measured. Finally, as discussedby McCall and colleagues,t5rl on" should be cau-tious in ruling out hyperplasia (an increase in thenumber of muscle fibres in a muscle) as a possible

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contributing mechanism for whole muscle hypertro-phv.

This is of course not to say that changes in fibrearea are irrelevant as an index of muscle mass.Ideally, a training study would include measure-ments at both the cellular level and at the wholemuscle level. Also, it should be noted that the rela-tive changes in mean fibre area are usually of alarger magnitude than the changes in anatomicalmuscle area.tal However, we feel that the focus onchanges in whole muscle CSA and volume, as mea-sured by scanning techniques, isjustified since theseare arguably the most sensitive and representativemeasures of whole muscle mass, even though theymay underestimate the changes at the cellular level.Regarding training issues where the evidence at thewhole muscle level is limited, we will discuss rele-vant studies, if any, which have measured MFAchanges.

2. Results Port l: Quodriceps Studies

2.1 Quodriceps Studies: DynomicExternol Resistonce

After application of the inclusion and exclusioncriteria, the literature search resulted in 44 originalafticlestl3'4346's4-e21 investigating quadriceps muscleCSA or volume before and after DER training.Because there were often more than one traininggroup or more than one limb that received training,these 44 articles yielded 65 datapoints for CSA. Fiveofthe articles (seven datapoints) involved trained toelite strength athletes. These were too few to allowfor any meaningful analysis and will be discussedbriefly in sections 4.1 and 4.6. Five studies dealtwith pure concentric and/or eccentric training, withfour datapoints for concentric training and three foreccentric training. Four datapoints from four differ-ent studies involved training where the subjects fin-ished each set with several repetitions in reserve.Since stopping well short of muscular failure hasbeen shown to yield modest hypertrophy in compar-ison with performing each set to muscular failure,lEsleven when the total volume is similar, these studygroups were excluded. As a result, except where

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ZJL Wernbom et al.

otherwise indicated, the analysis for DER deals withtraining using combined concentric-eccentric mus-cle actions (47 datapoints), with previously un-trained subjects.

2.1.1 Lenglh of lroining Peilod, Averdge lncrcq,sein CSA ond CSA Pet DoyThe average length of the training period was 79

days. The shortest study was 14 days and the longestlasted 6 months. The average increase in quadricepsCSA was 8.5Vo (range: l.l-17.37o). The averageincrease per day in CSA for training with combinedconcantric-eccentric muscle actions (47 datapoints)was 0.l2%o per day (range: 0.044.55Vo). If the studyof Abe et al.l841 is excluded as an 'outlier' because ofthe unusually high training frequency and rate ofgain, the average increase was O.llVo per day(range: 0.04-0.267o). For pure concentric training,the increase was O.06Vo per day and for pure eccen-tric training O.03Vo per day.

2.1.2 Rate ot Goin in CSA: Men versus WomenIn six studies, groups of men and groups of

women followed exactly the same training program-mes. The average increases in CSA per day in thesestudies were 0.l3%o for men and 0.l4%o for women.Because these differences were considered as negli-gible and because several studies contained groupsconsisting of both men and women, data from allstudies were pooled in the analysis for DER training(section 2. I ).

2.1.3 FrequencyThe mean training frequency was 2.8 times a

week. The most common frequency was three timesa week (22 of 47 datapoints), followed by two timesa week (17 datapoints). Frequencies between andabove these (2.3-4 times per week) were noted in afew cases. No studies were found that iirvolvedtraining at frequencies of more than two times perweek. A plot of frequency versus percentage in-crease in quadriceps CSA per day is shown in figure1. The highest rate of increase (O.55Vo per day) wasreported for the training studyts+l with the highestfrequency (12 times per week). For the frequency oftwo sessions per week, the average increase was0.11% per day (range: 0.034.21Vo); for three ses-

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sions per week, the increase was 0.ll%o per day(range: 0.04-0.267o).

2.1.4 IntensryThe mean peak intensity (the highest value

reached during a session, averaged over the entireperiod) wasT3Vo of lRM. The average intensity (themean of all training sets) was 66Vo of lRM. Inspec-tion of figure 2 reveals a tendency for greater ratesof increase for intensities >60Vo of 1RM when com-pared with intensities below this level; however, itshould be noted that only six datapoints involvedtraining with mean peak intensities <607o of lRM.The study of Abe s1 al.tsal is not shown because ofthe unusually high training frequency (12 times perweek) and very high rate of increase. The peakintensity in this study was 20Vo of lRM.

2.L5 VolumeThe mean number of sets was 6.1 and the mean

number of total repetitions was 60. The results areshown in figure 3. The study of Abe s1 61.t8+l was notincluded in the following analysis of volume. In-spection of the datapoints revealed four identifiable'clusters' in the range of total repetitions. Fourteendatapoints were found in the range of 2l-39 repeti-tions, 14 datapoints in the range of 40-60 repeti-tions, I I datapoints in the 66-90 repetition rangeand finally 6 datapoints in the range >100 repetitionsper session. The average rate ofincrease ofCSA foreach cluster was as follows: 2I-39 repetitions =O.l2% per day; 40-60 repetitions = O.l3Vo per day;66-90 repetitions = 0.087o per day; and >100 repeti-tions = 0.l2%o per day. No studies were found that

0 1 2 3 4 5 6 7 8 I 1011121314Number of sessions Der week

Fig. 1. Frequency of traihing vs percentage increase in cross-sec.tional area (CSA) per day of the quadriceps during dynamic exter.nal resistance training (number of study groups = 47).

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Sports Med 2007;37 (3)


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l r '0 10 20 30 40 50 60 70 80 90 100

Intensity (% of 1RM)Fig. 2. Peak intensity of training vs percentag€ Increas€ in cross-sectional area (CSA) per day of the quadriceps during dynamicexternal resistanco training (number of study groups = 46). RM =repetition maximum.

involved <21 repetitions per session on average. Forthe number of sets, the following groupings weremade: 3 sets (average CSA increase = O.O9Vo perday); 4 sets (0.1370 per day); 5-6 sets (O.l3Vo perday);7-9 sets (0.097o per day); and >10 sets (0.147oper day). No studies were found which involved <3sets. When training volume was expressed in arbi-trary units [sets x repetitions x intensity], no appar-ent relation was found between the volume andincreases in CSA per day (data not shown).

2.2 Quodriceps Studies:Accommodoting Resistonce

The literature search resulted in 17 original arti-clest2T'42'48'87'e3-1051 investigating quadriceps muscleCSA or volume before and after an accommodatingresistance-training programme. These 17 articlesyielded 2l datapoints for CSA. Of these, 14datapoints involved pure concentric training, threeinvolved pure eccentric training and four involvedtraining with combined concentric-eccentric muscleactions. Some of the studieste3'e5-e8l included sub-jects with strength training experience. Based onanthropometric and quadriceps muscle CSA data,they were considered as 'moderately trained' andare included in the analysis in sections 2.2.1-2.2.7,together with previously untrained and physicallyactive individuals.

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2.2.1 Lenglh of frolnlng Peilod, Avercge lncrcoseln CSA ond 6A Pet DdyThe average length of the training period was 52

days. The shortest study was l3 days and the longestlasted 84 days. The mean total increase in CSA was5,8Vo (range:2.5-l8.4%o) for all types muscle actioncombined. For pure concentric training, the meantotal CSA increase was 6.l%o (range: 2.5*18.47o),for pure eccentric training the mean increase was4.2Vo (range: 2.5-6.2Vo) and for combined concen-tric-eccentric training, the corresponding figureswere 6.0Vo (range: 4,1-7.47o). The mean CSA rn-crease per day for pure concentric training was0,l3%o (range:0.054.44Vo), for pure eccentric train-ing 0.067o (range: 0.044.09Vo) and for combinedconcentric-eccentric training 0.l6Vo (range:0.064.21Vo). The average CSA increase for all theaccommodating resistance modes combined was0.l3%o per day.

2.2.2 FrequencyThe mean frequency for concentric training was

3.4 times a week. Three sessions (nine datapoints)per week yielded an average increase in CSA of0.l3vo per day and 3.5-4 sessions per week (fourdatapoints) yielded an average increase in CSA ofO.l2Vo per day. Five sessions (one datapoint) perweek yielded an average increase in CSA of 0.22Voper day. The largest rate of CSA increase (O.44Vo perday) was noted in a studytlo4l using three sessionsper week. No concentric training studies were foundwith training frequencies below three sessions perweek or above five sessions per week. The frequen-

0.30.25

o.20.15

0.10.05

0

oo

aal

l '0 20 40 60 80 100 120 140 160

Total number of repetitions per sessionFig. 3. Total number of repetitions vs percentage increase in cross-sectional area (CSA) per day of the quadriceps during dynamicerlernal resistance training (number ot study groups = 45).

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234 Wernbom et al.

3 0.s- 0.45S o.oö 0.3soo 0.3u, 0.25? 0.2'ö o.tsfi o.tö 0.05Eo

0123456Numb€r of sessions per week

Fig. 4. Frequency of training vs percentage increase in cross-sec-tional area (CSA) per day of the quadriceps during accommodatingconcentric and/or eccentric training (number of study groups = 21 ).

cy for pure eccentric training was three times perweek in all studies (three datapoints). For the com-bined concentric-eccentric training regimens, thefrequencies were two (one datapoint), 2.3 (twodatapoints) and three (one datapoint) times perweek. The frequency plot for all categories com-bined is shown in figure 4. No relationship betweenthe frequency and the rate ofCSA increase is appar-ent from figure 4.

2.2.3 VelocityFor pure concentric training, the most common

velocities were 60o/s (seven datapoints, 0.l3Vo in-crease in CSA per day) and 120ols (four datapoints,0.16%o increase in CSA per day). Two studies used180'/s (0.147o increase in CSA per day) and onestudy used 90"/s (0.05Vo increase in CSA per day).The velocities for eccentric training and combinedconcentric-eccentric training were in the range be-tween 45 and 90o/s.

2.2.4 forqueData from Amiridis e1 al.t3sl on untrained subjects

suggests that the isokinetic concentric peak torqueof the quadriceps expressed as a percentage of maxi-mum isometric torque is =59Vo, 69Vo, 77Vo and 887oat the velocities of 180o/s, l2}ols,90o/s and 60o/s,respectively. When these percentage values wereapplied to the concentric training studies, no relationwas found between the level of torque developedand the rate of increase in CSA. The eccentric peaktorque of the quadriceps in relation to the maximumisometric torque is =lO4Vo, lO6Vo and l04Vo at thevelocities of 30o/s, 60o/s and 90"/s, respectively.

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When the percentage values for eccentric torquewere applied and all accommodating modes andtypes of muscle actions were combined, no relationwas found between the maximum torque developedduring training and the rate of increase in quadricepsCSA (see figure 5).

2.2.5 VolumeFor pure concentric training, the largest increases

occurred when the total number was between 50 and60 muscle actions (six datapoints,0.l9%o increase inCSA per day l0.l3%o increase in CSA per day with-out the studies of Akima et al.trO3] and Rafeeitrsll).Two datapoints were found in the interval of 3G40muscle actions (0.06Vo increase in CSA per day) andsix datapoints between 120 and 480 muscle actions(0.l0Vo increase in CSA per day). If studies withpure eccentric and combined concentric-eccentricmuscle actions are included in the analysis, theincreases still tend to reach their maximum in therange between 50 and 60 muscle actions per session(ten datapoints, 0.187o increase in CSA per day).See figure 6.

Regarding the number of sets for pure concentrictraining, one datapoint was found for 3 sets, one for4 sets, six for 5-6 sets, none for 7-9 sets and six for)10 sets. The highest increase occurred at 5-6 sets(O.l9Vo increase in CSA per day [O.l37o increase inCSA per day minus Akima et al.tro3l andRafeeitroall). The increase in CSA for >10 sets wasO.lOVo per day and the increase for 3-4 sets wasO.06Vo.If studies with pure eccentric and combined

0 20 40 60 80 100 120Torque (% ol MVIA)

Flg. 5. Torque vs percentage incraase in cross-sectional area(CSA) per day of the quadriceps during accommodating concentricand/or eccentric training (number of study groups = 21). MvlA =maximal voluntary isometric action.

- u.c;x

Fnooq 0.3o? o.'fr o.rgogo


Strength Training and Muscle Cross-Sectional Area

a 0.5;<

äooo

oo o3

?o,I otoco

! .:ro. . .

0 50 100 150 200 250 300 350 400 450 500Number of muscle aclions per session

Fig. 6, Number of muscle actions vs percentage increase in cross-seclional area (CSA) per day of the quadriceps during accommo-dating concentric and/or eccenlnc training (number of study groups= 211.

concentric-eccentric muscle actions are included inthe analysis, the results are as follows: 3 sets (twodatapoints) = O.08Vo increase in CSA per day; 4 sets(six datapoints) = g.12Eo increase in CSA; 5-6 sets(seven datapoints) = g.17qo increase in CSA (O.|lVowithout the studies of Akima et al.tr03l andRafeeitr0al); and >10 sets (six datapoints) = O.lOVoincrease in CSA per day.

2.2.6 fotol Durolion Per SessionFor pure concentric training, eight datapoints

were distributed between 37.5 and 75 seconds oftotal duration of muscle work. The average increasein CSA for these datapoints was 0.76Vo per day. Theother six datapoints were distributed between 170and 300 seconds. The average increase in CSA forthese datapoints was 0.09Vo per day. For the pureeccentric and combined concentric-eccentric train-ing groups taken together, the seven datapoints (av-erage of 0.l2%o increase in CSA per day) weredistributed between 40 and 84 seconds.

2.2.7 Time-Iorque Producl Per SesslbnThe time-torque product per session was calcu-

lated by multiplying the total duration with the esti-mated peak torque (with maximum isometric torqueassigned a value of 1) and is reported here in arbitra-ry units. No relation was found between the time-torque product and the rate of gain in CSA, regard-less of whether eccentric and combined concentric-eccentric training was included in the analysis or not(data not shown). For all types of muscle actionscombined, ten datapoints were in the interval be-

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tween 25 and 50 units (0.1470 increase in CSA perday), six between 50 and 100 units (0.l4%o increasein CSA per day) and five in the interval between 100and 265 units (0. l07o increase in CSA per day).

2.3 Quodriceps Studies: lsometric Resistonce

The literature search resulted in six original arti-clest55'lOGll0l investigating quadriceps muscle CSAor volume before and after an isometric resistancetraining programme, yielding nine datapoints forCSA.

2.3.1 Length of froining Peilod, Avercge lncreasein CSA ond CSA Per DoyThe average length of the training period was 84

days. The shortest study was 56 days and the longestlasted 98 days. The mean increase in total CSA afterthe training period was 8.9Vo (range: 4.8-l4.6Vo)and the average rate of CSA increase was 0. I I7o perday (0.06-0.26Vo).

2.3.2 FrequencyThree sessions per week (four datapoints) result-

ed in an increase in CSA of 0.127o per day and foursessions per week (five datapoints) resulted in anincrease in CSA of 0.ll%o per day. The largest rateof gain (0.26Vo increase in CSA per day) was report-ed in a studytloot using three sessions per week.

2.3.3 lnlensityThe most common intensity was 70Vo of MVIA

(seven datapoints), the intensity in the other twocases was 80Vo and 1007o, respectively. The largestrate of CSA increase (O.26Vo per day) was found inthe studyttoot that used the highest training intensity(lO0Vo of MVIA).

2.3.4 VolumeThe total number of repetitions ranged between 4

and 150. The time each repetition was held rangedbetween I and 30 seconds, while the total durationof muscle work per session was between 80 and 150seconds. No relation was found between the numberof repetitions and the increase per day in CSA.Similarly, when volume was expressed as the totalduration per sessio4 and as the product of intensityand total duration, no apparent relation betweenvolume and rate of increase in CSA was observed.


Wernbom et al.

although the highest rate of increase in CSA (0.267oper day) was observed for the training studytl06l withthe largest product of intensity and duration.

2.4 Quodriceps Studies: Combined Strengthond Enduronce Troining

The literature search resulted in seven originalaltislestTT'78'86'e6'lll-ll3l investigating quadricepsmuscle CSA or volume before and after a combinedtraining programme, yielding ten datapoints. Someof the studies included groups that performed onlystrength training, these have been included in sec-tions 2.1 and 2.2. Because of the limited data anddifferent modes of endurance training (rowing, run-ning and cycling), as well as the different modes ofstrength training, no analysis was performed regard-ing frequency, intensity and volume.

2.4.1 Pote ol Goin in CSA: Combined frclnlngvercus Purc Strenglh TrciningIn four of seven studies,tTT'78'e6'llll comparisons

were made between pure strength training and com-bined training regarding increases in quadricepsCSA. If these are summarised, the resulting averageincreases are as follows: pure strength training =O.09Vo increase in CSA per day; and combinedtraining = O.ll%o increase in CSA per day. If thecombined training groups of the other three stud-iesl86'll2'1131 are included, the average rate of CSAincrease for combined training becomes 0.l2Vo perday.

2.4.2 Length of fraining Period and lncraosein CSAThe shortest study was 70 days and the longest

lasted 168 days. The mean total increase in CSAafter the training period was l1.l%o. The largestincrease in CSA was 347o (0.24Vo per day) and thesmallest was 3.9Vo (0.O5Vo per day).

2.5 Quqdriceps Studies: All VoluntoryTroining Modes

2.5.1 Length ol lrclning Period and lncrcosein CSALonger training periods generally tended to result

in larger increases in CSA. Accordingly, the greatest

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increase in quadriceps CSA (347o) was noted in oneof the longer studies,tll2l afrcr 20 weeks of training(see figure 7). There was also an apparent tendencyfor the rate of increase in CSA to decrease withincreasing lengths of the training period (figure 8). Ifone regards the studies of Abe et al.tsal andRafeeitloalas outliers because oftheir unusually highrates of increase, the slope becomes less steep.

2.6 Quodriceps Studies: Strength Troining oso Countermeosure During Unlooding

The literature search resulted in eight originalafticlestl l4-l2ll investigating quadriceps muscle CSAor volume before and after a resistance trainingprograrnme as a countermeasure during otherwiseunloaded conditions (bed rest or limb suspension).These eight papers yielded nine datapoints for CSAfor the training groups and nine datapoints for thecontrol groups, which performed no training. Onestudy (one datapoint) used isometric training as acountermeasure, one study (one datapoint) used vi-bration combined with isometric training, four stud-ies (five datapoints) used dynamic external resis-tance with coupled concentric-eccentric muscle ac-tions and two studies (two datapoints) usedaccommodating resistance with coupled concentric-eccentric muscle actions.

2.6.1 Unloading versus Unloading andExerclse CountetmeosweThe average length of the training and unloading

period was 49 days (range: 20-ll9 days). The meandecrease in quadriceps CSA for unloading was

o 20 40 60 80 100 120 140 160 180 200Length of traning period (days)

Fig.7. Traning period vs tbtal percentage increase in cross-section-al area (CSA) ot the quadriceps during all types of voluntarystrength training (number of study groups = 91).

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SDorts Med 2m7;37 (3)


g o'u6 u.c

E o.a9? 0.3c6 0.2

ü o.ro

0o 20 40 60 80 100 120 '140 160 180 200

Length of laining period (days)Flg. 8. Training period vs percentage change in cross-sectionalarea (CSA) per day of the quadriceps during all types of volunlarystrength training (number of study groups = 91).

-ll.lVo and the mean rate of decrease was 43070per day. The degree of loss appeared to be related tothe length of the unloading period, as the largestdecrements in CSA were found in the studies withthe longest unloading period. However, the rate ofloss in CSA seemed to decrease with the length ofthe unloading period, so that the longer studiesshowed lower average rates of change. For the un-loading plus strength training countermeasure, theCSA increased by an average of l.3%o (0.03Vo perday). If the isometric training and the vibrationtraining groups are excluded, the increase in CSAbecomes 2.7Vo (0.O9Vo per day). The largest totalCSA increase was 7.l%o (0.22V0 per day) and thelargest rate of gai n w as 0.3OVo per day (6.0Vo in totalCSA). The greatest total CSA decrement was-3.8Vo(4.l9vo per day) for the isometric countermeasure.The greatest total CSA decrease for the dynamicgroups was-l.9Vo (4.O2Vo per day). Because of thelimited data and differences in both training modesand unloading models, no analysis was performedregarding frequency, intensity and volume. Thelowest training frequency was every third day (2.3times per week) and the highest was twice a day (14times per week).

2.7 QuodricepsStudies: Electromyostimulotion

The literature search resulted in three originalnllislsstee'122'1231 investigating quadriceps muscleCSA in healthy uninjured subjects before and after aresistance training programme using electromyos-

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timulation to evoke muscle actions. In the first ofthese,teel previously untrained subjects performed3-5 sets of l0 unilateral combined concentric andeccentric actions in an isokinetic dynamometer at avelocity of 75'ls, for two sessions per week for 9weeks. The increase in quadriceps CSA was l0.l7o(0.16%o per day). In the second study,t1221 from thesame research group, recreationally resistance-trained subjects performed an identical protocol tothat in the first study, for two sessions per week for 8weeks. These subjects continued their normal resis-tance-training regimens during the study, includingexercises for the quadriceps of both sides. The in-crease in CSA was 9.87o (0.l8%o per day). Thecontrol limb that performed only regular resistanceexercise showed no increase in quadriceps CSA.Another group performed exactly the same pro-grarnme but also received creatine supplementation.This group increased the CSA with l2.l%o (O.22Voper day) but this was not significantly greater thanthe other (placebo) group. The control limb thatperformed regular resistance exercise only showed aslight increase (SVo) in quadriceps CSA. In the thirdstudy,ttz3l electromyostimulation was used to evoke40 isometric muscle actions per session, four ses-sions a week for 8 weeks. The increase in CSA was6Vo (O.ll%o per day).

3. Resulls Porl2: Elbow Flexor Studies

3..| Elbow Flexor Studies: DynomicExternol Resistonce

The literature search resulted in 16 original arti-cles[25'53'124-1371 investigating elbow flexor (bicepsand brachialis) muscle CSA or volume before andafter a DER training programme with specific exer-cises for the elbow flexors. These papers yielded 36datapoints for CSA. Three of the papers (sevendatapoints) included highly-trained subjects, whileone paper included recreationally-trained subjects(one datapoint), who had previously trained withoutany structured programmes or specific goals. Basedon strength and CSA data, the latter group wasregarded as 'moderately trained' and included in theanalysis of'untrained' and 'physically active' sub-

" i . l ' ,;r l l l3 i', '. t

a

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Sports Med 2m7j 37 (3)

238 Wernbom et al.

jects in sections 3.1.1-3.1.4. Four groups (fourdatapoints) from three other studies were excludedbecause they either performed only non-specificexercises for the biceps and brachialis muscles (e.g.latissimus pulldown, dumbell row) or they did notperform their elbow flexor exercises with near maxi-mal effort or near muscular failure in any set. Onegroup from another study was excluded because theeccentric phase was performed in a plyometric man-ner with the resistance building up momentumbefore the subject started to resist it, making it verydifficult to estimate the actual intensity. As a result,the analysis in sections 3.1.1-3.1.4 for the variablesof frequency, intensity and volume is based on 24datapoints for training with previously untrained tomoderately trained subjects. All studies involvedtraining with combined concentric-eccentric muscleactions, but in one study the eccentric phase wasoverloaded with =1807o of lRM.

3.1.1 Lenglh of froining Period, Average lncrcasein CSA ond CSA Per DoyThe average length of the training period was 9l

days. The shortest study was 30 days and the longestlasted 6 months. The average increase in flexor CSAwas 15.87o and the average increase per day in CSAwas O.20Vo. The highest increase in elbow flexorCSA (337o) was noted in the longest study, after 6months of training,tl3Ol although an almost equalincrease (32.64o) was observed in another studyafter l l weeks.tl25l

3.L2 FrequencyThe results are shown in figure 9. The mean

training frequency was 2.9 times a week. The mostcommon frequency was three times a week(l'l of 24datapoints), followed by two times a week (sixdatapoints). The highest frequency was four timesper week. No studies were found that involved train-ing at frequencies of less than two times per week.The highest rate of CSA increase (0.597o per day)was noted for a training studytl28l with a frequencyof four times per week. For the frequency of threesessions per week, the average CSA increase wasO.l8Vo per day and for two sessions per week, theCSA increase was 0. l87o per day.

@ 2007 Adis Doto Informolion BV. All righls reserved.

3.1.3 lnlensityThe mean peak intensity (the highest value

reached during a session, averaged over the entireperiod) wasl2Vo, which was the same as the averageintensity (the mean of all training sets), since nostudy reported using different loads during one andthe same session. The highest mean intensity report-ed was 1807o of lRM, in a studytr26l that usedeccentric overload, in addition to performing theconcentric phase with a lower resistance. This wasalso the only study that used such overload; theothers used the same resistance in both types ofmuscle actions. The lowest resistance reported in astudy was 107o. When the intensity was plottedagainst the rate of increase, a tendency was foundfor the rate to increase with increasing intensity. Thehighest rates of increase tended to occur aroundT 5Voof IRM (see figure l0).

3.1.4 VolumeThe results for the number of repetitions versus

CSA per day are shown in figure 11. The meannumber of sets was 5.4 and the mean number of totalrepetitions was 47. Three clusters of datapoints wereidentified as follows: (i) 7-38 repetitions (tendatapoints); (1i) 42-66 repetitions (nine datapoints);(iii) and 74-120 repetitions (five datapoints). Themaximum rate of CSA increase was found in theinterval between 42 and 66 repetitions (0.267o perday). For 7-38 repetitions, the CSA increase wasO.lSVo per day, and for 74-l2O repetitions, the ratewas 0.1870 per day. For total sets, the rate of CSAincrease appeared to peak between 4 and 6 sets (nine

01234Number of sessions per week

Flg. 9. Frequency of training vs percentage increase in cross-sec-tional area (CSA) per day of the elbow flexors during dynamicexternal resislance training (number of study groups = 24).

g 0.,ä 0.6

b 0.s

< 0.4U'? o.'E 0.2GE 0.1o-0



g 0'tä 0.6

b 0.s< 0.4g)

? o.3 0.2GE 0.1

0o 20 40 60 80 100 120 140 160 180 200

Inlensity (% of l RM)Flg. 10. Peak intensity of training vs percentage increase in cross-sectional area (CSA) per day of the elbow llexors during dynamicexternal resistance training (number ot study groups = 24). RM =repetition maximum.

datapoints, 0.247o increase in CSA per day). For3-3.5 sets (ten datapoints), the CSA increase was0.177o per day and for >9 sets (five datapoints) theCSA increase was 0.187o per day.

3.2 Elbow Flexor Studies:Accommodoting Resistonce

The literature search resulted in three original311isls5t25'48'1381 investigating elbow flexor muscleCSA before and after an accommodating resistancetraining programme, yielding four datapoints forCSA. Of these, two datapoints involved pure con-centric training and two involved pure eccentrictraining. The longest study was 140 days and theshortest was 56 days. The mean CSA increases perday were O.l6Vo and O.l27o for concentric and ec-centric training, respectively. Both the largest in-crease in total CSA (16.3Vo, O.l27o per day) and thehighest rate of CSA increase (O.2OVo per day, ll%ototal increase in CSA) was noted for concentrictraining. Because of the lack of data involving pureconcentric training, combined concentric-eccentricand pure eccentric training, no formal analysis con-cerning the effects of frequency, intensity and vol-ume was performed. The frequency was three timesa week for all studies. The number of sets andrepetitions per set was 4.6 and 10, respectively. Theaverage total duration of contractile activity was84.8 seconds (range: 13.9-146.2 seconds),

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3,3 Elbow Flexor Studies: lsometric Resistonce

The literature search resulted in three originalarticlest2l'|24'l3el investigating elbow flexor muscleCSA before and after an isometric resistance train-ing programme, with a total of three datapoints forCSA. The mean CSA increase per day was O.l4Vo.The largest total increase in CSA (23.0Vo) was notedfor the longest study,tztl which lasted 100 days. Thefrequency was six times a week for two sludlest2l'l2al(O.23Vo average CSA increase per day and O.06Voper day, respectively) and three times per week forthe third studylt3el (OJ3Vo per day). The intensity inthe three sludisst2l'l24'l3el wäs l00%o,67Vo andSOVoof MVIA, respectively. The number of total repeti-tions was 3-24. The total duration of contractileactivity was 30 seconds in two studiesl2l'1241 and 96seconds in the third study.tl3el

4. Discussion

4,1 Frequency

For quadriceps training with dynamic externalresistance, the largest rate of gain in CSA (0.557oper day) was noted in the studyt8al with the greatesttraining frequency (12 sessions per week). Howev-er, it should be noted that (i) this study lasted foronly 2 weeks; (ii) the intensity was 2OVo of IRM;and (iii) the training was performed in combinationwith partial vascular occlusion. Therefore, the re-sults from this study should be viewed with cautionwhen considering the application of extremely high

soEoCL

o

;Eoc

0.70.60.50.40.3o.20.1

00 20 40 60 80 100 120 140

Number ot repetitions per sessionFlg. 11, Total number of r€petitions vs percentage increase incross-sectional area (CSA) per day ol the elbow flexors duringdynamic eliternal resistance training (number ol study groups = 24).

o 20 40 60 80 100 120 140 160 180


Wernbom et al.

frequencies in more conventional training. Further-more, it is interesting to note that there was nodifference in the mean rates of increase in CSAbetween two and three sessions per week for DERquadriceps training (O.llVo vs 0.l l%o per day, re-spectively). For accommodating resistance trainingand isometric quadriceps training, it is difficult toevaluate any trend because of the limited number ofstudies and the smaller range of frequencies. Thehighest rate of CSA gain in the isometric category(0.267o per day) was achieved in a studytro6l inwhich the subjects trained three times per week;however, this was also the study with the highesttraining intensity (l00Vo of MVIA) and the highestproduct of intensity and total duration. The highestrate of CSA increase for accommodating resistancetraining (O.44Vo per day) was noted in a studytto+tthat used a frequency of three sessions per week,followed by a studytlorl that used a frequency of fivetimes per week (0.22Vo increase in CSA per day).High rates of CSA increase (O.l74.2l%o per day)were also observed in three s1udis5t27'87'1051 in whichtraining was performed two to three times per week.

For the unloading plus resistance exercise coun-termeasure studies, the highest rate of CSA gain(O.3OVo per day) was noted for the studytr rsl with thegreatest training frequency (14 sessions per week),although a high rate of CSA increase (0.22Vo perday) was also noted in a studyttl8l with a frequencyof every third day. However, caution is warrantedwhen comparing the results of these studies becauseof possible differences in the effects of the differentmodels of unloading and,/or the exercise regimens.For example, Tesch and co-workerstll8l employedlimb suspension for unloading and knee extensionsfor the exercise countermeasure and showed amarked hypertrophic response in the quadriceps ofthe unloading plus exercise limb. In a different studyby Alkner and Tesch,tllel when using bedrest forunloading and horizontal squats, but with the exactsame dosage of training as in their other study,tll8lthe exercise resulted in no hypertrophy but stillmanaged to completely counteract the atrophy thatwas evident in the pure bedrest group. Also notableis that in one bedrest 51udy.tll+l which used isometric

@ 2007 Adis Doio Informoiion BV. All righis reserued.

training at l0o7o of MVIA as a countermeasure,training once a day was insufficient to prevent all theatrophy. In yet another bedrest study,tltzl trainingonce a day using a leg press, with coupled concen-tric-eccentric actions at 90Vo of I RM, preserved themuscle volume but failed to induce significant hy-peruophy. Further research is obviously needed toaddress the effects of different exercise modes andregimens (e.g. different frequencies and distribu-tions of the total training volume), as well as theimpact of the unloading model employed.

For elbow flexor training with dynamic externalresistance, the greatest rate of increase in CSA(O.59Vo per day; 17.1Vo total increase in CSA) wasobserved in a studytl2sl with a frequency of fourtimes a week. The second, third, fourth highestincrease in CSA rates noted were0.42Vo,0.38Vo andO.32Vo per day, respectively. These three stud-iestl25'126'1321 used a frequency of three times perweek. However, with the exception of these threestudies, the average values suggest that there isrelatively little difference between training the el-bow flexors two or three times per week, in terms ofthe rate of increase in CSA (0.18%o per day for bothfrequencies). However, the highest increase in CSAthat was noted for two times per week was O.24Voper day, compared with 0.42Vo per day for threetimes per week. As noted in section 3.2, all accom-modating resistance training studies involving theelbow flexors used a frequency of three times aweek. Regarding frequency for isometric elbowflexor training, the highest rate of CSA increase(0.23Vo per day) was noted for a studyt2rl with afrequency of six times per week, but this was alsothe study that had the highest intensity (I00Vo ofMVIA). Remarkably, this regimen consisted of onlythree isometric actions per day, each lasting l0seconds, thus resulting in a total of 30 seconds ofmaximal isometric activity each day.

While a higher than normal training frequency(four or more times per week) can result in rapidhypertrophy in the initial stage, it should also benoted that several of these sludisstsa'lls'1281 lastedonly between 2 and 4 weeks. It is uncertain iftraining at these high frequencies would continue to


Strength Training and Muscle Cross-Sectional Area ai1

yield very high rates ofincreases in CSA or perhapsresult in diminishing returns or even overtrainingafter a longer period. Inspection ofthe data from thestudy of Abe et al.tsal suggests that the rate ofincrease in CSA was considerably slower during thesecond week compared with the first week, drop-ping from a maximum of =l%o per day to =0.257oper day. Using a frequency of three times a week anda protocol of 4 sets of 7 maximal effort concentric-eccentric actions, Seynnes s1 3l.tlOsl showed a rate ofincrease of only =0.72Vo per day during the first l0days, but =0.25Vo per day during the last 25 days of atraining period that lasted 35 days. Thus, there is apossibility that training with a frequency of two tothree times per week may start to produce a high rateof increase after the first two weeks; because of thisand the paucity ofdata regarding long-term trainingwith high frequencies, it is not possible to say whichfrequency is more optimal in the long run. Neverthe-less, a high frequency (four or more times per week),in combination with relatively non-damaging low-to-moderate volume training, may be a good way to'kick-start' the hypertrophy process. For longer-term training, the studies included in this reviewshow that frequencies between two and four times aweek can result in CSA gains for periods of up to 6months. For previously untrained subjects, no studywas found with a training frequency of less than twosessions per week.

Regarding the impact of training frequency inmore advanced trainers, we found nine stud-ies[45,46,s6,61,?6,7e,133,t34,r37] using Scanning methods tOmonitor changes in CSA in the quadriceps and/orelbow flexors as a result of training in strength-trained subjects and strength"/power athletes. In twopreliminary reports,tTe'I34] different frequencies oftraining were directly compared. Vikne and co-workerstTel investigated the effects of squat trainingwith an eccentric overload on quadriceps CSA insubjects that trained one, two and three times a weekfor 12 weeks. All groups performed 5 sets of 4repetitions in each session using a squat machine,which was loaded to 50Vo of IRM in the concentricphase and to llo-1357o of lRM in the eccentricphase. The groups that trained two and three times

o 2007 Adis Dofo Informotion BV. All righls reserued.

per week gained significantly more in lRM strengthand quadriceps CSA (5.99% and 6.75Vo, respective-ly) than the group that trained once a week (3.17oincrease in CSA). There was no difference betweentraining two and three times per week. Wirth andcolleaguestl3al investigated the effects of frequencyon elbow flexor CSA in subjects that trained once,twice and three times a week for 8 weeks. All groupsperformed several types of arm curls for a total of 5sets of 8-12 repetitions in each session. The groupsthat trained two and three times per week gainedsignificantly more in elbow flexor CSA (6.6% andT.4Vo,respectively) than the group that trained oncea week (3.9Vo).

The results of Vikne e1 sl.tTel and Wirth s1 al.tl3+lare remarkably similar despite using different mus-cle groups and training modes. In both reports, twoand three sessions per week yielded almost twice theincrease in muscle CSAwhen compared with onesession, with no apparent further advantage for threeversus two sessions. This seems logical in view ofthe typical pattern of changes in muscle proteinsynthesis after a resistance training session, withpeak synthesis rates observed between 3 and 24hours, and with elevated rates sometimes lastingbetween 48 and 72 hours after exercise.t140-1431 How-ever, it cannot be excluded that larger volumes and/or different modes of training would yield differentresults. Furthermore, the total weekly volumes werenot matched between the groups in the studies ofVikne et al.t?el and Wirth et al.tr3aj Also, it should benoted that most studies on muscle protein synthesisin humans after resistance exercise have only stud-ied a time span of up to 48 hours post-exercise.

Anecdotally, many bodybuilders and otherstrength athletes only train each muscle group spe-cifically between one and two times per week,sometimes even less often. On the other hand,weightlifters are known to perform exercises involv-ing their quadriceps for several sessions per trainingday.tt+el Teschtl45l has remarked that it is not knownif bodybuilding regimens are superior to the trainingregimens performed by powerlifters and olympiclifters. Training each muscle group once a week hasbeen shown to result in increases in muscle

Sports Med 2@7:37 (3)

242 Wernbom et al

csAt7e,r34,r46l and lean body mass.tla6,laTl However,the results of Wirth et al.tl34l and Vikne et al.tTel aresupported by data from Mclester et al.,tla7l whousing experienced subjects showed superior in-creases in lean body mass for three training sessionsper week versus only one per week per musclegroup, even when the total weekly volume remainedthe same for the two groups.

Häkkinen and Kallinent6rl also investigated theeffects of different distributions of the same totalvolume, in a group of trained female subjects ofwhich some were competitive strength athletes.These subjects underwent two three-week periods ofstrength training for the quadriceps, with 3 trainingdays per week. During one period, the subjectstrained once each training day and during the secondperiod the same subjects trained with the same totaldaily volume but separated into two sessions. Dur-ing the first training period, the subjects did not gainin either strength or quadriceps CSA, but during thesecond period, the subjects increased significantly inboth maximum static strength and CSA (4.0Vo andO.l9Vo per day, respectively). Although some inter-esting trends can be discerned from the data dis-cussed in this section, there is clearly a need forfurther research on training frequency in both high-ly-trained and less-trained subjects.

4.2 Intensity

The studies reviewed in this article show thatthere is a remarkably wide range of intensities thatmay produce hypertrophy. Still, there seems to besome relationship between the load (or torque) andthe rate of increase in CSA, at least for dynamicexternal resistance training, but this relationship isnot a straightforward one. In figure 2 and figure 10,it can be seen that the rates of increase are generallyhigher for intensities >6OVo of IRM than for those<60V0 of lRM, although caution is warranted be-cause of the few datapoints <6OVo of lRM. Howev-er, it appears that intensities of =70-85V0 of IRMare sufficient to induce high rates of increase andthat even heavier loads do not necessarily result ingreater CSA gains. In the categories of accommo-dating resistance, where the effort is usually maxi-

o 2007 Adis Dqto Informotion BV. All righls reserued.

mal from the first repetition, there was no relationbetween the torque developed and the rate of gain inCSA, regardless of whether eccentric muscle actionswere included in the analysis or not. This was truefor both the quadriceps (figure 5) and the elbowflexors (data not shown). This is contradictory tosome of the studies in the literature,[48-lsll but con-sistent with other reports.[5s'62'68'6e] It should be not-ed that no accommodating training study was foundin which the level of torque was <6OVo of MVIA.

In contrast, the study of Farthing andChilibecktlsll seems to confirm the importance ofthe force developed during training for the hyper-trophic response. In their study, subjects trainedtheir elbow flexors in an isokinetic dynamometer,with concentric actions for one arm and eccentricactions for the other arm. One group trained withfast (180'/s) and another group trained with slow(30'/s) speed, with all groups training three timesper week and progressing from 2 to 6 sets of 8repetitions over the course of the training period,which lasted 8 weeks. The hypertrophic responsewas evaluated with measurements of muscle thick-ness by ultrasound. The greatest increase in thick-ness (=13Eo at the middle level) was found in the fasteccentric group, followed by the slow eccentricgroup (=1Vo), the slow concentric group (=57o) andthe fast concentric grovp (=2Eo). The authors inter-preted their results as a confirmation of the theorythat greater force production leads to greater hyper-trophy.

This interpretation may be premature since theprotocols differed greatly in terms of torque-timeintegral and in the volume of work performed. Fur-thermore, it is possible that a local overtrainingresponse was developing in the slow eccentricgroup. Support for this possibility comes from anearlier study by Paddon-Jones and colleagues,t3slwho used very similar eccentric training regimens tothose in the study of Farthing and Chilibeck.tr5rlTheir results generally showed increases in elbowflexor torque for both fast and slow eccentric train-ing after 5 weeks _of training, but at l0 weeks thetorque values of the slow group were either halted oreven back to the baseline values while the fast group

Sports Med 2ü7:37 (3)


continued to gain. The authors suggested that thegreat cumulative stress of the slow protocol hadcaused an overtraining-like response. The results ofShepstone et al.lr38l confirmed the findings of Far-thing and Chilibecktrsrlregarding the superiority offast versus slow eccentric training for the hyper-trophic response of the elbow flexors. However, thisstudy is open to the same interpretation regardingthe possibility of a local overtraining response in theslow eccentric group, since the difference in torque-time integral between the fast and slow protocol waseven greater (>1O-fold) than in the preceeding stud-ies. Moreover, the slight differences in peak torquebetween the fast and the slow eccentric velocities inthe studies mentioned here argues against the levelof torque as the primary explanation for the differ-ences observed in the hypertrophy of the elbowflexors. Recruitment differences between fast andslow eccentric velocities cannot be excluded as acontributing factor; however, at present there is notenough evidence to support that this occurs. Never-theless, the considerable difference in hypertrophybetween fast eccentric and both fast and slow con-centric training in the study of Farthing andChilibecktl5rl lends support to the hypothesis thatthe force developed by the muscle during training isan important factor for hypertrophy.

At present, there are no accommodating resis-tance training studies that have investigated the im-pact of different eccentric velocities and/or differentlevels of torque development during eccentric mus-cle actions on the CSA of the human quadriceps asmeasured by scanning methods. There is also a lackof direct comparisons using accommodating con-centric training at different velocities and/or differ-ent levels of torque development. The studies re-viewed in this article suggest that hypertrophy canbe induced with a range of concentric velocities. Theupper limit of concentric velocity that is still capableof inducing hypertrophy is not known, but type Ifibre hypertrophy has been observed after training at2400lsttsz) and type 2fibre hypertrophy after trainingat velocities as high as 300o/s.tls3l While being quitehigh compared with the cadence of conventionalresistance training, these velocities are still well be-

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low the reported maximum velocity of unload-ed knee extensions, which may reach values of=JQQo/5.tlsal

In support of the use of moderately fast concen-tric training, an early study by Thomed s1 al.lrssishowed a clear trend (but not significant) for hyper-trophy of type 2 muscle fibres (=30-35V0) in thevastus lateralis in both the healthy and the injuredlimbs in individuals undergoing moderately fast(180'/s) isokinetic concentric training after recon-struction of the anterior cruciate ligament (ACL).No such trend was apparent in either limb in thegroup that trained at a low velocity (60'/s). Thetraining was carried out three times per week for 8weeks, with the slow velocity group progressingfrom 3 sets of l0 repetitions to l0 sets of l0 repeti-tions and the fast group from 3 sets of 15 repetitionsto l0 sets of l5 repetitions during the time course ofthe study. A CT scan was also performed of thequadriceps and vastus lateralis at mid-thigh level,but unfortunately too few scans were available dueto problems with the scanner, thus making it impos-sible to confirm or reject the trend ofthe fibre CSAdata at the whole muscle level. However, a study byFroböse and colleaguestl56l also supports the use ofmoderately fast concentric training for the quadri-ceps, at least in the rehabilitation setting. Theseauthors investigated the effects of isokinetic concen-tric training in patients that had undergone recon-struction of the ACL and they showed hypertrophyof the quadriceps in response to moderate (150'/s)and fast (240"|s) protocols, which was at least equalto that of the slow protocol (60'/s). Thus, it appearsthat hypertrophy can be induced in the human quad-riceps as a result of concentric training at velocitiesof up to at least 24o"ls and torque levels as low as=50Vo of MVIA.

However, the largest increase (=l\Vo at mid-thigh level), as well as the by far highest rate ofincrease in quadriceps CSA (0.447o per day) foraccommodating training, was noted in the study byRafeei,troal who trained subjects with 5 sets of 10concentric muscle actions at 9OVo of the maximumtorque at 60o/s, three times per week for 6 weeks. Aninteresting feature of the study of Rafeeitl0al was that


244 Wernbom et al.

the subjects trained at the same absolute torquethroughout the study. Another notable feature wasthe generous rest periods, with 5 seconds betweeneach concentric action and 120 seconds betweeneach set. The level of effort was probably highenough to recruit most of the motor units, while thehigh but not maximal force level and the generousrest periods may have minimised muscle damageand fatigue of fast fibres, thus allowing the muscleto hypertrophy already in the initial stages of train-ing.

Regarding dynamic external resistance training,the range of intensities that can produce hypertrophyis even more remarkable than in the case of accom-modating resistance. 5g6i"rt83'8al have shownmarked increases in CSA in response to loads as lowas 20Vo of IRM when the exercise has been com-bined with partial restriction of the blood flow bymeans of thigh torniquets. Even so, consideration ofthe recruitment of motor units during fatiguing exer-cise with low loads reveals that the results of thestudies of Takarada et al.t83l and Abe et al.t8al do notnecessarily disprove the theory that tension is amajor determinant of the hypertrophic response. Astudy by Greenhaff and co-workerstlsTl showed agreatly increased rate of glycogenolysis in type Ifibres and a marked decline in force and near totaldepletion of phosphocreatine in both fibre typesduring intermittent electrical stimulation of thequadriceps with the blood flow occluded. In con-trast, the decline in force during the same protocol ofstimulation but with intact circulation was ascribedalmost solely to fatigue in type 2 fibres. AlthoughGreenhaff et al.tl571 used electrical stimulation in-stead of voluntary activation, their findings are ofrelevance for the development of fatigue under cir-cumstances where the blood supply to the workingmuscle is limited, for example by a tourniquet and/or by the raised intramuscular pressure during thecontinuously performed coupled concentric-eccen-tric muscle actions that conventional resistancetraining usually consists of. With a decline in forcein type I fibres, more type 2 fibres would have to berecruited and towards the end of each set. the re-maining force-producing fibres could be exposed to

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relatively high tensions. It is also possible that somefast fibres are preferentially recruited during eccen-tric actions and that this may occur at loads as low as25Vo of MYlA.tr58l 16ut, it may be too simplistic toestimate the stress imposed on each muscle fibremerely by the magnitude of the external load.

In summary, although there may well exist alevel oftension below which no hypertrophy occurs,the relationship between the training load and thehypertrophic response is complex. Achieving re-cruitment of the greatest possible number of motorunits in the target muscle(s) and making these motorunits fire at high rates and for sufficient lengths oftime are obvious prerequisites for inducing signifi-cant hypertrophy. Still, it appears that maximalloads are not necessary to ensure that these condi-tions are met providing that the training is per-formed with close to maximum effort in at least oneof the sets. Thus, the results of this review supportthe typical recommendations with intensity levels of70-85V0 of maximum when training for muscle hy-pertrophy, but also show that marked hypertrophy ispossible at both higher and lower loads. However,placing high mechanical stress on the working mus-cle may result in local overtraining if the duration ofwork is long. Some of the possible interactionsbetween the level of tension, duration of exercise,mode of exercise and muscle damage will be dis-cussed in section 4.6. The impact of intensity inmore advanced athletes remains poorly defined dueto the lack of objective scientific data.

4.3 Volume

A notable trend in the several types and modes ofstrength training reviewed in this article was theoccurrence of a plateau in the hypertrophic adapta-tions after a certain point of volume or duration ofwork had been reached. In some of the results, thereis even a suggestion of a decline when the volume orduration is extended beyond the point of the plateau.Again, it must be noted that no studies were foundthat investigated the effects of I or 2 sets on muscleCSA or muscle volume of the quadriceps or elbowflexors. That said, figure I l, for the total repetitionsfor DER training of the elbow flexors, suggests a



dose-response curve where greater gains in musclemass are noted initially with increasing volume (orduration) of work, but with diminishing returns asthe volume increases further. Overall, moderatevolumes (=30-60 repetitions per session for DERtraining) appear to yield the largest responses.

However, two notable exceptionstl25'1261 also ap-pear in figure 11, which demonstrate that high ratesof growth can be achieved with a relatively smallnumber (=12-14) of repetitions per session undersome circumstances. In the first of these s1udiss,ll25lvery high loads (=90-l00Vo of IRM) were used forboth the concentric and the eccentric phases and in .the other study,ttz6l extremely high loads (progress-ing from 130 to 230Vo of IRM) were used for theeccentric phase. As can be seen in figure 10, themajority of the other datapoints were distributedbetween 60 and 9OVo of lRM. A further exampledemonstrating that significant hypertrophy can beinduced with a surprisingly small number of muscleactions at very high loads, at least in previouslyuntrained subjects, can be found in a study by Haw-kins et al.,tl48l who showed that a total of 9 maximaleccentric muscle actions was sufficient to inducesignificant increases in thigh lean mass, while 12maximal concentric actions was not. Thus, the rela-tionship between volume and the hypertrophic re-sponse may differ between different levels of torqueand/or types and modes of strength training. Thediscrepancy between different studies in terms of thevolume needed to induce hypertrophy may, in part,be related to differences in the total duration ofmuscle activity per session. In many studies, neitherthe velocity nor the duration ofeach repetition werereported.

To date, relatively few studies have directly com-pared the effects of different volumes of work on thehypertrophic response as measured by scanningmethodology. These few studiestl6'l5e-l6ll used lessaccurate measures of muscle mass rather than mus-cle CSA or volume, or scanned only parts of themuscle groups, and it is therefore difficult to com-pare these with studies in which whole muscle scanswere performed with MRI, CT or UL. However, intwo of these studies,tl5e'1601 significant increases in

O 2m7 Adis Doto lnformotion BV, All rights reserued.

muscle thickness were demonstrated after as little asI set of 8-12 repetitions of specific exercise permuscle group. Because of this and given the relativepaucity of data, especially regarding the early part ofthe volume continuum (i.e. l-20 total repetitions),there is clearly a need for further research on theimpact of training volume on whole muscle CSA.This appears to be true for both previously untrainedand well-trained individuals.

However, recent data from Ronneshd s1 al.tt6zlprovide further support to the notion of a dose-response relationship between the training volumeand the hypertrophic response of the quadriceps.These authors reported superior increases in quadri-ceps CSA for a total of 6 sets (ll3qo) versus 2 sets(7 ,6Vo) of quadriceps exercise (two exercises of I or3 sets each at 7-l0RM) at an exercise frequency ofthree times per week for I I weeks. It deserves to benoted that the subjects in this study received a prote-in supplement prior to each workout. Because it iscurrently unknown how protein supplementation in-teracts with training volume, these results may notnecessarily apply to strength training that is per-formed without supplementation.

4,4 Mode of Troining ond Type ofMuscle Action

In the scientific literature relating to the area ofresistance training, one sometimes finds categoricstatements such as 'eccentric training produces thegreatest muscle hypertrophy'. This review demon-strates that given sufficient frequency, intensity andduration of work, all three types of muscle actionscan induce significant hypertrophy at impressiverates and that at present, there is insufficient evi-dence for the superiority of any mode and/or type ofmuscle action over other modes and types of train-ing in this regard. Using dynamic external resistancetraining as an example, one would be tempted toconclude that, if anything, pure eccentric training isactually inferior to both concentric and concentric-eccentric training, as judged by the degree and rateof hypertrophy observed in the studies included inthis review. If one instead considers concentric andeccentric training with accommodating resistance,


Wembom et al.

maximal eccentric training has been slightly moreeffective than maximal concentric training in thefew studies that have directly compared these twotypes of training. However, the hypertrophic re-sponse has been modest in many of the studiescomparing the effects of pure concentric versus pureeccentric training and this appears to be true both foraccommodating resistance and dynamic external re-sistance training studies. Thus, the protocols thathave been compared may not have been the best ofeach type. Again, it is noteworthy that both thelargest total increase in CSA (l8.4Vo) and the high-est rate of increase in CSA (O.44Vo per day) for thequadriceps for the category of accommodating train-ing was noted for a pure concentric traininggroup.tlo4l This was also the second highest rate ofincrease for any mode of quadriceps training, sur-passed only by the shorter study of Abe et al.t84l Thefindings of Rafeei,tr@l of greater hypertophy at thewhole muscle level as well as at the muscle fibrelevel for near maximal concentric versus submax-imal eccentric training, expanded on an almost iden-tical study from the same research group,tto3l inwhich greater fibre hypertrophy was found for con-centric training when compared with eccentric train-ing when both regimens were performed at the sametorque level.

The divergence in the results of concentric versuseccentric training between different modes (DER vsaccommodating resistance) may be due to differ-ences in the characteristics ofthe resistance for eachmode. As discussed in the introduction, when usingexternal resistance (e.g. free weights, weight ma-chines), the torque is not necessarily optimallymatched throughout the movement to the individu-al's strength curve. Herzog et al.tto+l calculated thatthe internal forces ofthe three vastus muscles ofthequadriceps are at their highest at knee angles of=60-80o of flexion (full extension is defined here as0o of flexion), whereafter the forces drops to lowerlevels with decreasing angles of flexion. At 0-20'offlexion, the forces are low, only =2040Eo of maxt-mum. Similarly, Ichinose s1 3l.tr6sl reported that theforce of the vastus lateralis was maximal at 70o offlexion.

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If force is an important stimuli in resistance trarn-ing, it follows that a certain level of torque must bereached for some minimum duration for significanthypertrophy to occur. In the pioneering study ofJones and Rutherford,t55l who compared pure con-centric and eccentric regimens using a variable re-sistance knee extension device, the authors notedthat the subjects activation of the quadriceps washigh only near the position of full knee extension.Further inspection of their electromyogram datasuggests that the eccentric training was accompa-nied by slightly less activation than the concentrictraining and also that the duration of high activitywas shorter. Thus, it is possible that less than opti-mal internal force production and short total dura-tions of high activity contributed to the finding of nodifference between the eccentric and concentrictraining, and to the modest hypertrophy for bothprotocols in their study. The eccentric and concen-tric exercise regimens in the studies of Housh etal.t68'6el may have shared the same problem, as theresistance in their device was greatest near full ex-tension. Nonetheless, the studies of Jones and Ruth-erford,ts5l Smith and Rutherfordt62l and Housh etal.t68'6el show that at least for the mode of dynamicexternal resistance training, the greater loads that arepossible with eccentric training (compared withconcentric training) do not necessarily translate intogreater gains in muscle size.

Among the accommodating modes, the isoiner-tial flywheel knee-extension model of Tesch andcolleaguest2T'87'105'll8l has so far consistently inducedhypertrophy of the quadriceps CSA at high rates(0.174.22Vo per day). It is not immediately obviouswhy this mode seems to be more effective than mostof the isokinetic regimens that have also used maxr-mal eccentric actions. In the flywheel study of Teschet al.,Iz1l the subjects were instructed to resist onlygently during the first part of the eccentric actionand then apply maximum force. The torque-anglecurves in the same studytzrt show that high eccentricforces were reached only during a rather short arc of=20-25", from =65-90o offlexion. In contrast, dur-ing isokinetic eccentric exercise, maximum effort isusually applied from the start and dn16ll66't671 gsl-



lected at similar average velocities show that higheccentric forces can be achieved through an arc ofatleast 40o. However, maximum eccentric efforts atextended knee angles are often perceived as uncom-fortable.lr68l In the isokinetic study of Seger etal.,tlO2l four of five subjects in the eccentric traininggroup had frequent complaints of knee pain duringthe training, which may have affected the hyper-trophic adaptations. Interestingly, Holder-Powelland Rutherfordt168l showed that much of the discom-fort associated with maximum isokinetic eccentricexercise could be avoided if the subjects started toresist later in the arc of motion, from =45o of flexioninstead of 15" of flexion. Also, the eccentric peaktorque was significantly higher when the range ofmotion was 45-95o, compared with l5-95o of flex-ion. It could be that the relatively low volumes andshort ranges of high-force eccentric exercise in theflywheel studies worked in favour of producinghypertrophy, whereas the isokinetic-eccentric proto-cols may have resulted in too much stress and strainon the tissues.

Other factors to consider when comparing theisokinetic and flywheel modes are the accelerationsand decelerations that occur in the latter mode but bydefinition not in the former. It has been hypothesisedthat accelerative and decelerative forces are impor-tant components of the stimulus for muscle hyper-trophy in resistance training.tl0el To date, there islittle evidence to support this hypothesis. Collective-ly, the successes of both the dynamic, isokinetic andisometric modes in producing muscle hypertrophydoes not appear to support accelerations and/or de-celerations as being particularly important for thehypertrophic response. However, although the angu-lar velocity in isokinetic training is controlled, thefascicle velocity in the working quadriceps variesmarkedly through the range of motion.tlT0l Further-more, isokinetics usually involve a brief build up ofspeed before the isovelocity phase is reached and ashort braking period after the isovelocity phase.tlT0lThus, from a muscle point-of-view, accelerationsand decelerations occur even during 'isokinetic' ex-ercise. It should also be noted that with weight-based resistance training, accelerations and deceler-

@ 2m7 Adis Dsto Infomotion BV. All rights reserued.

ations can result in far greater peak loads than thenominal load.tl2el The significance, if any, of thesevery high but momentary forces for the hypertrophicresponse remains to be explored. We speculate thatdifferences in torque profile, torque-time integraland motor unit recruitment account for some of thedifferences in the hypertrophy observed betweenstudies where the training variables have been nomi-nally similar. Also, if strenuous eccentric training isperformed at a high frequency, the hypertrophicresponse may become compromised. These interac-tions will be discussed in sreater detail in section4.6.

In summary, all modes reviewed here seem capa-ble of inducing marked hypertrophy, at least in theshort term. This is not to say that some method orcombination of modes will not emerge as superior inthe long term. The ideal proportions between thedifferent types of muscle actions are still a subject ofdebate rather than a scientific certaintv.

4.5 Rest Periods ond the Role of Fotigue

Because too many studies did not report the restperiods between sets (and repetitions), we opted notto try to evaluate any trends. However, some elabo-ration regarding the potential impact of rest periodsis possible. Closely associated with rest periods rsthe role of fatigue in strength training. Regardingstrength, some studiestlTl'1721 have shown that shortrest periods between sets and/or repetitions are supe-rior to longer ones, whereas other studiestlT3l haveconcluded that longer periods are superior to shorterones, while yet other studiestlTal have reported nodifference. Upon closer examination, it appears thatwhen maximal or near-maximal efforts are used, it isadvantageous to use long periods of rest. This islogical in light of the well known detrimental effectsof fatigue on force production and electrical activityin the working muscle. If high levels of force andmaximum recruitment of motor units are importantfactors in stimulating muscle hypertrophy, it makessense to use generous rest periods between sets andrepetitions of near-maximal to maximal efforts.

It is interesting that for the accommodating andisometric categories, the studies in which the highest


248 Wernbom et al

rates of muscle growth were foundtl04'1061 did in-clude long rest periods. Furthermore, in the DERtraining studytezl that reported the highest rate ofCSA increase (O.26Vo per day), very long rest peri-ods (10 minutes) between working sets were used,but in this study the volume was periodised, whichmay also have impacted on the results. It is alsoworth noting that maximum isokinetic-concentricexercise performed with little rest between eachmuscle action is associated with a marked decline inpeak torque during each working set, whereas littleor no decline occurs during maximum eccentricexercise.tlT5-1771 Hence, it can be hypothesised that ifthe rest periods are too short during near-maximalconcentric exercise, the training effects will be com-promised.

Although eccentric exercise generally produceslittle acute fatigue, it appears that it is dependent onthe training velocity (and probably also the work-to-rest ratio), with faster eccentric velocities producingless fatigue than slower velocities (see Tesch etal.lr75l for a discussion). The difference in acutefatigue development between concentric and eccen-tric muscle actions and also between fast and sloweccentric muscle actions have obvious implicationsfor comparisons between these modes in regard totraining effects. On the other hand, when usingsubmaximal resistance, the size principle dictatesthat motor unit recruitment and firing rates are prob-ably far from maximal until the muscle is nearfatigue or unless the repetitions are performed withthe intention to execute the movement very quickly.

The importance of exercising with near-maximaleffort when using submaximal resistance in conven-tional strength training has been elegantly demon-strated by Goto and co-workers.l85l In their study,two groups of untrained subjects performed 5 sets ofl0 repetitions of dynamic knee extensions at a loadof lORM (=75Vo of IRM), two times per week for l2weeks. One group performed all l0 repetitions ineach set in a continuous manner to muscular failure,while the other group performed 5 repetitions andthen rested for 30 seconds before performing theremaining 5 repetitions. Thus, although the volumewas matched between the groups, the subjects of the

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latter group trained with considerably less effort incomparison to the first group. The results showed adramatic difference in the extent of hypertrophy infavour of the group that trained in a continuousmanner (l2.9%o increase in quadriceps CSA), versusthe group that rested in the middle of each set (4.0Voincrease in quadriceps CSA). The authors speculat-ed that both increased recruitment of motor unitsand a greater acute hormonal response could havecontributed to the greater hypertrophy seen after thecontinuous protocol. However, along with the rn-creased stress on the muscle with shorter rest peri-ods at submaximal resistance, the potential for over-training may also increase. In a study by Folland andcolleagues,tlTal conventional resistance training withmultiple sets to muscular failure and very short restperiods (30 seconds) led to considerable delayedonset muscle soreness during the first week of train-ing. With this type of training, caution with thetraining frequency and volume appears to be war-ranted.

The impact of rest periods may extend beyondthe effects on fatigue and motor unit recruitment.Using a rat muscle model, the research group ofFaulkner has, in a series of studies,llT8-1801 investigat-ed the effects of electrical stimulation against thedeleterious effects of denervation on muscle mass.They showed that denervated muscle is sensitive toboth the total number of muscle actions and thedistribution of loading. For example, 100 muscleactions per day generated at a constant interval over24 hours was sufficient to maintain muscle mass andforce, but the same number of muscle actions dis-tributed over just 4 hours per day (and consequently20 hours of rest in between) failed to maintain massand force. Although these findings may not necessa-rily extrapolate to intact innervated human muscle,they show that skeletal muscle, at least under somecircumstances, is sensitive to both the total numberof muscle actions and the distribution of them. Fu-ture studies should examine the potential impact ofboth shorter (seconds) and longer (minutes, hours)rest periods on skeletal muscle hypertrophy andhypertrophic signalling in this light.

Soorts Med 2m7;37 (3)


4.6 Interoctions Between Frequency,Intensity, Volume ond Mode

After acknowledging that the training volumeseems to influence the hypertrophic response to acertain extent, the question arises of what aspect ofvolume is the most important determinant of thisresponse? Is it the total mechanical work performedor is it the time-tension integral of the activity?Based on the available evidence, we suggest that thetime-tension integral is a more important parameterthan the mechanical work output (force x distance).

The elbow flexor eccentric training studies ofRefsnes,tl261 Paddon-Jones et a1.,1381 Farthing andChilibecktr5rl and Shepstons s1 4l.tl38J provide in_sight into some of the complex interactions thattakes place between the training variables of fre-quency, intensity, volume and mode of resistancetraining. If one considers the last two of these stud-ies, one finds that the external work output (ex-pressed as total number of repetitions x the torquedeveloped) was likely to be similar between theslow and fast eccentric groups because of the margi-nal difference in maximum torque between the slowand the fast velocities. In contrast, the total durationand the torque-time integral between the groupswere vastly different, =6-10-fold greater for theslow groups compared with the fast groups. Thestudies of Farthing and Chilibecktrsrl and Shepstoneet al.tl38l are difficult to compare with each other interms ofthe degree ofhypertrophy achieved becausedifferent measures of muscle mass were used (mus-cle thickness vs muscle CSA). Still, the hypertrophicresponse noted for the fast eccentric group appearsto be larger in the Farthing and Chilibeck studyttstJ(=l3Vo increase in muscle thickness) than the 8.57oincrease in CSA reported by Shepstone s1 3l.tl38lBecause thickness measures only one dimension ofthe muscle, the increase in elbow flexor CSA waslikely to be greater than l3vo. If the muscle grewequally in width as it did in thickness, the resultwould be an increase in CSA of 27 .1Vo. This scena-rio seems unlikely, because a triceps training studyby Kawakami et al.tlsu showed that an increase of3l.7Vo in elbow extensor area was accompanied byan increase in thickness of 27.OVo.If the same ratio

o 2007 Adis Dolo Informotion BV, All rlghls reseNed.

of =1.17 between the increase in CSA and thicknessis applied to the elbow flexors in the study of Far-thing and Chilibeck,tl5ll one arrives at an estimatedincrease in CSA of =157o for the fast eccentrictraining group.

The training groups of Farthing and Chilibecktrsrlprogressed from2 sets of 8 repetitions to 6 sets of 8repetitions, resulting in an average total duration ofmuscle activity per session of 22 and 132 secondsfor the fast and slow eccentric groups. respectively.In the study of Shepstone et al.,tl38l the progressionwas from I set of l0 repetitions to 4 sets of l0repetitions and the corresponding average totaldurations of muscle activity per session were 14 and146 seconds for the fast and slow eccentric groups,respectively. We suggest that the slightly greatertotal duration for the fast group in Farthing andChilibecktlsll versus Shepstone et al.tl38l was re-sponsible for the greater hypertrophic response inthe former study. On the other hand, with the slow-velocity protocols, the cumulative damaging effectsof the long durations of maximum eccentric exerclsemay have counteracted the hypertrophy so that thisbecame less in comparison with the fast training.The study of Refsnes,l126l using a dynamic constantresistance training model in which the eccentricphase was overloaded (progressing from 1307o to=230Vo of IRM during the time course of the study)also attests to the effectiveness of short durations ofmaximum eccentric exercise for inducing increasesin elbow flexor CSA. In this study, the volume wascarefully progressed from 2 sets of 2 repetitions to 5sets of 4 repetitions during the 8 weeks of the study,resulting in a maximum duration of =14-16 secondsof near-maximal eccentric work. The velocity in theeccentric phase was moderate, =8G-90"/s. The con-centric phase was loaded with only 307o of lRM,and the contribution of the concentric phase to thehypertrophic response was therefore probably small.The subjects increased their elbow flexor CSA by2l.5Vo (0.38Vo per day), an impressive increase es-pecially when considering the very briefduration ofwork.

The risk for overtraining with long durations ofhigh-force eccentric exercise is supported by a study

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250 Wernbom et al

by Amiridis et al.,tr82l who compared differentmodes of training in a group of young elite femalebasketball players after a period of very strenuoustraining for the knee extensors. During the first 12weeks, all subjects performed 8 sets of 8 concentricrepetitions at10%o of lRM and 8 sets of 8 eccentricrepetitions at llo%o of IRM in the leg press, 4sessions per week. At 12 weeks, the subjects hadsignificantly reduced performances in both the legpress and the countermovement jump, indicatingthat they were overtrained. During the second 12weeks of training, the subjects were divided intothree groups that performed different modes of re-covery training, 4 sessions per week. The first grouptrained with 8 sets of 8 concentric repetitions atTOVoof lRM; the second group completed 4 sets of 8concentric repetitions at 7 }Vo of I RM and 4 sets of 8eccentric repetitions at llo%o of IRM; and the thirdgroup performed 8 sets of 8 eccentric repetitions atllo%a of lRM. Compared with values from the first12 weeks overtraining, all groups increased theirperformance in the leg press and the countermove-ment jump, but only the pure concentric group notedsignificant increases in leg-press strength (39Vo),isokinetic strength (ll43Eo) and vertical jump(l1vo) in comparison with the pre-training values.Although no morphological data was presented inthis study, it is likely that some degree of overtrain-ing at the muscle level was responsible for the poorperformance at 12 weeks. It is also interesting tonote that despite reduced total volume in compari-son with the first 12 weeks, neither the pure eccen-tric nor the combined concentric-eccentric groupsexperienced any supercompensation in perform-ance, whereas the pure concentric group did. Thus, itwould appear that moderate-force concentric train-ing was better tolerated than high-force eccentrictraining, at least for the moderately high volumesand the rather high training frequency used in thisstudy. Taken together, the results of these studiessupport the common recommendation of usingsomewhat lower frequencies and volumes for high-force eccentric exercise than for conventional resis-tance training.

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On the other hand, studies by LaStayo and col-leaguesll83'ta+l using eccentric cycling at submax-imal intensities for long durations (=20-30 minutes)have shown very rapid and large gains in MFA(=5U60Vo). Recently, a case reporltl8sl was pub-lished that showed that marked hypertrophy is evi-dent also at the whole muscle level after this type oftraining. In these regimens, up to =100G-2000 ec-centric muscle actions were performed during eachtraining session, three times per week. The absoluteintensity level was reported in watts, so it is difficultto quantify the forces in terms of percentage ofMVIA. Nevertheless, these studiesl183-1851 show thatgiven careful and gradual progression of exerciseintensity and duration, human skeletal muscle cantolerate and adapt to prolonged submaximal-eccen-tric exercise.

Overall, we feel that the trends observed in thisreview are consistent with the model for training-overtraining continuum proposed by Fry,tt8el *6"r"the optimal training volume and also the volumethreshold for overtraining decreases with increasingintensity. The study of Abe s1 3l.t8al is especiallyintriguing in this context because of the combinatronof very low intensity and extremely high frequency.To the best of our knowledge, no studies to datehave investigated the effect of performing twostrength training sessions during the same day onskeletal muscle protein synthesis, so it is not knownwhether there is any additional benefit in doing socompared with performing just a single session. Ifthe sensitivity of skeletal muscle protein synthesis tomechanical stimuli is regained during the same dayand if there is room for further elevations of the netprotein synthesis, then it would make sense to per-form more than one session per day. This couldexplain the results of Häkkinen and Kallinen,l6llalthough the effects of tapering down the volume(and hence, the total stress per session imposed onthe muscle) also remain a possibility. As pointed outin the discussion concerning rest periods (section4.5), mechanistic investigations concerning the ef-fects of different _distributions of loads and restperiods on skeletal muscle mass and/or intracellularhypertrophic signalling are largely lacking. It is also

Spods Med 2ü7:37 (3)


uncertain whether the mechanosensitivity of skeletalmuscle decreases with long periods of strength train-ing. Until these and other dose-response relation-ships become more fully characterised, it will re-main difficult to prescribe a proper 'dosage' oftraining for each mode of training and type of mus-cle action for the specific purpose of inducing hy-pertrophy.

Regarding training for hypertrophy in alreadyhighly-trained individuals, there is at present insuffi-cient data to suggest any trends in the dose-responsecurves for the training variables, It has been suggest-ed by some authorstl8Tl that the volume needed toinduce optimal gains in strength, increases withtraining status, so that advanced trainers and eliteathletes will have to perform far more sets (>10 setsper muscle group) than untrained and recreationallifters (={-5 sets per muscle group). Other authorsemphasise the importance of load and the type ofmuscle action. Refsnestls8l has reported preliminaryfindings from unpublished studies, which indicatethat very well-trained athletes respond to eccentricoverload training with greater hypertrophy than af-ter conventional training. Recently, a study byVikne and colleaguestl3Tl demonstrated significantlylarger increases in elbow flexor area in well-trainedindividuals after pure eccentric training (ll%o in-crease) than after concentric training (3% increase).It should be noted that the volume was not equalisedbetween the groups and it also seems likely that thetotal duration of work was markedly longer for theeccentric group, thus resulting in large differences intime-tension integral between the protocols. Hence,although the results suggest a clear superiority ofpure eccentric exercise versus pure concentric exer-cise for inducing hypertrophy in well-trained sub-jects, other variables cannot be ruled out as contrib-uting factors. Seemingly at odds with the observa-tions of Refsneslls8l and Vikne et al.,t l37]Brandenburg and Dochertytl33l showed no differ-ence in muscle CSA after eccentric-overload train-ing for the elbow flexors and the elbow extensorscompared with conventional training. In theirstudy,tl33l coupled concentric-eccentric repetitionswere performed in both groups and the total volume

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was similar between the groups. Needless to say,more research is needed regarding interactions be-tween variables in both trained and untrained sub-jects.

Finally, a comment on the interactions betweenstrength and endurance training is warranted. It hasbeen recommended that both strength and endur-ance training should be included in a well-roundedtraining programme.tlsel The additive effects ofstrength and endurance training on various parame-ters of health status have been shown in severalstudles.lleo-le2l Recently, it has been demonstratedthat while strength training by itself can lead toincreased arterial stiffness, this negative effect canbe offset if endurance training is performed concur-rently.tte3l From a strength training point of view,there is an interest in how to train concurrentlywithout affecting strength and hypertrophy nega-tively. It has been suggested that strength trainingshould be performed first, in order not to compro-mise the quality of the strength-training session.trealHowever, this order may not necessarily be the bestchoice for inducing increases in muscle mass.Deakintre5l investigated the impact of the order ofexercise in combined strength and endurance train-ing and reported that gene expression associatedwith muscle hypertrophy responded more stronglywhen cycling was performed before strength train-ing, instead of vice versa. Interestingly, in the studyof Sale et al.,tr I rl performing cycling first seemed toinduce the greatest increase in muscle area. Still,because the lack of studies investigating the effectsof the order of exercise in concurrent training onhypertrophy, no firm conclusions can be drawn onthis issue.

4,7 Time Course of Muscle Hypertrophy

Strength gains as a result of a period of resistancetraining are usually attributed to two major factors:(i) neural adaptations; and (ii) hypertrophy.tre6l Untilrecently, the prevailing opinion has been that neuraladaptations play the dominant role during the first6-7 weeks of training, during which hypertrophy isusually minor. However, as noted by Staron and co-workerstle6l and by Sale,tleTl it appears that the hy-

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Wernbom et al.

pertrophy process begins earlier than this, as trendsfor increased fibre CSAs can be observed at 2 weeksinto the training period. In the studies of Mayhew etal.tl631 and Rafeei,tl0al significant increases in fibreCSA (type | = l2-l4%o; type 2 = 26-28Vo) wereobserved for the concentric training groups as earlyas 4 weeks into the training. In the latter study,llO4lfurther hypertrophy had occurred at 6 weeks, whichwas also manifested at the whole muscle level(=l8Vo increase in quadriceps CSA at mid-thighlevel). In the study of Abe et a1.,t841 significantincreases in muscle volume were noted after just 2weeks and several other investiga-1isnst13,27,54,87.105.118,1281 have also demonstrated sig_nificant hypertrophy at the whole muscle level aftershort periods of training (3-5 weeks). Thus, there isnow plenty of evidence that significant hypertrophycan take place early on given proper frequency,intensity and volume of training.

Based on the observation of positive muscle-protein balance after an isolated session of resis-tance exercise, Phillipstle8l has proposed that a gainin active force-producing myofibrillar proteinscould occur after a single strength-training sessionand that this increase may take place without achange in fibre CSA. In line with this idea, Wil-loughby and Taylorlleelreported an increase in my-ofibrillar content in muscle biopsies obtained frompreviously untrained young men after just threestrength-training sessions, with sessions separatedby 48 hours of rest. As argued by Phillips,tle8l theidea that early gains in strength are due exclusivelyto neural adaptations seems doubtful. Judging fromthe studies included in this review, the hypertrophyprocess actually seems to be most rapid during thefirst 6 weeks, after which the rate declines slowly.Because the majority of studies have only investi-gated a time period of up to 12 weeks, it is difficultto assess how the rate of protein accretion is affectedby longer periods of training. A study by Sale etal.tll2l suggests that relatively high rates of increasein muscle CSA (0.22-0.24Vo per day) may be possi-ble to maintain for periods of up to 20 weeks, butunfortunately no mid-point data were available fromthis investigation. Therefore, it cannot be excluded

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that the majority of the increase took place duringthe first l0 weeks of training.

Little is also known about how different trainingvariables and modes interact with the length of thetraining period. In some strength-training studies,the increase in muscle volume is delayed, while inothers, the rate of growth is rapid. We speculate thatless-damaging training modes may allow the hyper-trophy response to start earlier. Regimens that in-clude eccentric muscle actions, especially those in-volving maximal effort, appear to require a carefulinitiation and progression of training to avoid mus-cle damage and muscle protein breakdown. In linewith the results of Foley et a1.,t2001 who noted a long-lasting decrease in elbow flexor muscle volume afteran acute session of high-force eccentric exercise,Willoughby e1 al.t2orl found decreased myofibrillarprotein content in muscle biopsies taken from thevastus lateralis after an acute session of 70 near-maximal eccentric actions for the knee extensors.This decrease was accompanied by increases in cas-pase 3 activity and in the expression of ubiquitin,which the authors interpreted as indicating thatapoptosis and increased proteolysis had occurred inthe exercised muscle. They also reported a repeatedbout effect for most of the parameters after a secondsession ofan identical eccentric protocol. Neverthe-less, a trend towards decreased myofibrillar contentwas evident even after the second session, althoughthis was not significant and certainly of a smallermagnitude than after the first session. In contrast, inthe study of Willoughby and Taylor,treel where aconventional resistance-training model for the quad-riceps was employed, the myofibrillar content ap-peared to increase from the very first workout,reaching significance after the second session.Clearly, more research into the time course of thehypertrophic process is needed, especially with ref-erence to the effects of different resimens andmodes.

4.8 Hypertrophic Response of theQuodriceos versus the Elbow Flexors

It has long been recognised that some muscles arevery responsive to the stimulus of strength training,

Sporls Med 2m7;37 (3)


while others seem more stubborn. One explanationto this phenomenon could be that muscles that arefrequently used in everyday activities are already ina trained state, thus leaving less room for improve-ments in strength and size. For example, the soleusmuscle appears to be relatively unresponsive to re-sistance exercise in comparison with the vastuslateralis and the biceps brachii.t2@l Regarding thelatter two muscles, it is commonly held that theelbow flexors are in a less-trained state than thequadriceps.tl28'2031 Südies where the hypertrophicresponse of the quadriceps and the elbow flexors tosimilar training regimens have been directly com-pared tend to support this theory.ta8'6'2sl The trendsreported in this review for conventional resistancetraining for the quadriceps versus the elbow flexorslend support to this observation, as the CSA of theelbow flexors tended to increase at a greater rate(0.2OVo per day) than the quadriceps (O.ll7o perday). Further support comes from a study by Turnerand co-workers,t2o3l who found marked hypertrophyin the elbow flexors (24Vo increase in CSA) inresponse to endurance training for the upper limb(arm cycling to exhaustion for 30 minutes, fivetimes per week for 6 weeks), while leg cycling at thesame relative intensity and duration had negligibleeffects on the mass of the lower limb. Notably, therate of CSA hypertrophy for the elbow flexors ob-served in this study (0.57Vo per day) surpasses allstrength-training studies included in this review,except that of Narici and Kayser.tl2sl The differencesbetween various muscle groups in the physiologicalresponse to similar training regimens warrants somecaution in generalising findings from one musclegroup to another. Future investigations should studywhether the dose-response relationships differ be-tween the elbow flexors and the quadriceps in regardto the major training variables.

4.9 The Stimulus for Muscle Hypertrophy inStrength Troining

It is beyond the scope of this article to discuss inany detail the pathways or networks of intracellularsignals leading to hypertrophy as a result ofa periodofincreased loading ofthe muscle(s) involved. Sev-

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eral excellent levievv5[205-2081 and original investiga-donstel'20e-2131 on various aspects of this topic areavailable. However, a brief discussion of some ofthe physiological stimuli occurring during resistancetraining that may trigger the hypertrophic pathwaysis relevant. Over 30 years ago, it was suggested byGoldberg and co-workersl2l4l that increased tensiondevelopment (either passive or active) is the criticalevent in initiating compensatory growth. MacDou-galltzr5l noted that the loading of the muscle must bevery high in order to result in hypertrophy, but thatthe total duration during which the muscle developstension also affects the magnitude of the hypertro-phy response. He supported this observation withthe results of the study of Sale and colleagues,tl2slwho showed a tendency for training with 6 sets oflO-l2RM to result in larger increases in elbowflexor muscle CSA than trainins with 6 sets ofl-3RM (33Vo vs247o).

Two studies by Martineau and Gardinert2l6'2171have provided insight into how different levels offorce and different durations of tension may affecthypertrophic signaling in skeletal muscle. Using ratmuscle preparations, these authors noted thatmechanically sensitive pathways reacted in a dose-dependent manner to the level of force, so that largerincreases in intracellular signaling were seen aftereccentric actions when compared with isometric andconcentric actions.t2l6l In a follow-up study,l2rTl theyshowed that the same pathways were also sensitiveto the time-tension integral in a dose-dependentmanner. Interestingly, this was the case regardless ofwhether the total duration was distributed into a fewlong durations of stretch or many short ones. Also,the rate of stretch had no effect on these pathways.In the latter study,t2l7l they remarked that both peaktension and time-tension integral must be includedin the modelling of the mechanical stimulus re-sponse of skeletal muscle. Some of the pathwaysthat are now recognised as crucial for the hyper-trophic response were not assessed in the studies ofMartineau and Gardiner,l2 t6'2t'1 1 and little is currentlyknown about the response of these pathways to thevariables of peak tension and time-tension integral.One of these is the phosphatidylinositol-3 kinase/

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Wernbom et al

protein kinase B/mammalian target of rapamycinPathway,t20s-2081 which has several downstreamtargets, among them the signaling molecule p70 56kinase (p70S6K). A recent study by Eliasson etal.t2r8l showed that the phosphorylation of p70S6Kin the human quadriceps 2 hours after resistanceexercise was greater after a total of 24 maximal-eccentric actions compared with 24 maximal-con-centric actions and to 24 submaximal eccentric ac-tions. However, this was in the absence of nutrition-al supply. In contrast, Cuthbertson and col-leaguestzlel demonstrated similar increases inp70S6K and muscle protein synthesis after eccentricand concentric exercise. Importantly, in this studythe subjects received protein and carbohydrate sup-plementation immediately post-exercise. Anotherdifference is that a much greater volume of workwas performed compared with the study of Eliassonet al . l2 l8 l

Based on the data reviewed in this paper, wespeculate that hypertrophic signalling in humanskeletal muscle is very sensitive to the magnitude oftension developed in the muscle. Hence, for veryshort durations of work, the increase in muscle sizewill be greater for maximal-eccentric exercise thanfor maximal-concentric exercise of similar dura-tions, as in the studies of Farthing and Chilibecktr5rland Hawkins et al.tl48l The response is presumablyalso dependent on the total duration of work andincreases initially with greater durations. Thus, bothshort durations of maximal eccentric exercise andsomewhat longer durations of concentric, isometricand conventional dynamic resistance exercise canresult in impressive increases in muscle volume.However, especially with maximal eccentric exer-cise, damage also seems to come into play as theduration of work increases even further and theacute and/or cumulative damage may eventuallyoverpower the hypertrophic process. This could bean explanation for the modest hypertrophy reportedin several isokinetic training studies where the ec-centric component has been maximal and of moder-ate-to-long total durations. As discussed by Rennieand colleaguest2osl and Jones and Folland,t22ol otherphysiological events associated with muscle activa-

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tion (e.g. temporarily increased Ca2+ levels in thecytosol, metabolite accumulation, ischaemia andacute hormonal changes) may also act as signals foradaptation and interactions between these andmechanically-induced signaling seem plausible. Thepotential role of acute hormonal responses has beenreviewed by Kraemer and Ratamess.t22ll

Apart from mechanical forces, growth factorsand hormones, another exercise-related stimuli thathas been shown to affect the hypertrophic signalingin skeletal muscle (as assessed by phosphorylationof p70S6K) is heat stress.t222l Interestingly, both incultured muscle cells and in skeletal muscle, heatstress and mechanical stretch has been shown tointeract so that protein expression and concentrationis higher after a combination of the two stimuli thaneither alone.tz23'2241 These authors suggested that astress-induced heat-shock response may modulatethe exercise-induced adaptations of skeletal mus-cles, for example when combining vascular occlu-sion with resistance exercise. If an interaction be-tween heat stress and mechanical stimuli occursduring strength training with restricted blood flow, itcould, at least in part, explain the success of low-to-moderate intensity training during these conditionsin inducing hypertrophy,[83'84'r3rl even in highly-trained athletes.tT6'2251

4.10 Suggestions for Future Reseorch

The trends observed in this review could serve asa starting point for experiments aiming to establishefficient models of training for the purpose of gain-ing and/or preserving muscle mass. Major chal-lenges for future research are to isolate the impact ofeach of the resistance training variables and to in-vestigate the interactions between them, as well asthe effects of various training strategies (e.g. perr-odization, tapering, changes in type and mode ofexercise in order to 'shock' the muscles). We alsorecommend that future investigations should de-scribe the exercise protocols in greater detail thanhas generally been the case up until recently. Conse-quently, variables Euch as speed, range and durationof each repetition and rest periods between repeti-tions and sets should also be reported in addition to

Sports Med 2m7; 37 (3)


the commonly recognised variables of frequency,intensity, volume and mode of exercise.

To date, the vast majority of the research con-cerning the effects of manipulating training vari-ables have been carried out using DER training. Forexample, we were unable to locate any accommo-dating training study that directly compared the ef-fects of different volumes on the hypertrophic re-sponse. Because the accommodating training modescan induce hypertrophy at rates comparable to thoseof conventional weight training, and because thetraining parameters are easily standardised, thesemodes are well suited for experiments designed toprovide insight into the nature of the dose-responserelationships.

In humans, electromyostimulation (EMS) hasbeen proven to result in increases in muscle volumecomparable to those seen after voluntary strengthtraining. Since EMS bypasses the CNS, the level ofactivation of a particular muscle group can bestandardised. Combining EMS with isokinetic dyna-mometry could provide an opportunity to gain fur-ther insight into many of the issues discussed in thisreview, such as the effects of the level of torque, thetype of muscle action (concentric vs isometric vseccentric) and the total duration of activity. Howev-

er, because EMS involves motor-unit firing patterns,which are usually very different from those occur-ring in voluntary exercise, findings from such stud-ies may not necessarily apply to voluntary strengthtraining.

As noted in section 2.1, investigations concern-ing very well-trained individuals are largely lacking,as are studies extending for longer than the typical8-12 weeks. Because of this, the knowledge regard-ing the dynamics of the hypertrophy process pastthis point is limited. In short-term studies, largeincreases in the training loads for lower-body exer-cises such as squats, leg presses and knee extensionsare often reported, sometimes on the order of100-200%o.18'55,re61 Since the gain in quadricepsmuscle volume during the same time period rarelyexceeds =l1%o, the stress per unit of muscle areashould increase by almost as much as the increase intraining weight. The significance of the large in-crease in the stress on the muscles and its interac-tions with the volume and frequency of training interms of the hypertrophic response and the risk forovertraining remains to be explored. Although notdiscussed in this article, the issue of dose-responseeffects needs to be adressed in the trainine of other

Table l. Recommendations for dynamic extemal resistance training (e.9. weight-based resistance) for hypertrophy

Moderate load slow-speed training Conventional hypertrophy training Eccentric (ecc) overload trainingMuscle actionExerciseLoad

RepetitionsSets

Velocity and durationper repetition

Resl between setsFrequency

Comments

Con and eccSingle and/or multiple joint

-50% of 1RM

8-14 to muscular failure1-3 per exercise

total per muscle groupSlowEcc = 2-3 secondsCon = 2-3 seconds3H0 seconds

Suitable training method lorbeginners and individuals whocannot tolerate high forces

Con and €ccSingle and/or multiple joint8-1oRM (range: ö-12)=75-80% of 1 RM8-10 to muscular failure or near 4-€

in total per muscle groupModerateEcc = 1-2 secondsCon = 1-2 seconds60-180 seconds

These recommendations are fornovice to moderately trainedindividuals. Well trained athletesmay need increased variation inintensity and volume

Ecc (con = optional)Single and/or multiple jointEcc = >105% of lRMCon = 60-75% of lRM

total per muscle groupSlow/moderateEcc = 24 secondsCon = 1-2 seconds120-180 seconds

Mainly for advanced to elite athletes.Progressive but careful increase ofthe load and volume for the eccentricohase

1-3 Der exercise 1-5 per exerciseProgression from 1 to 3-4 sets in Progression from 1-2 to $-6 sets Progression kom 1-2 to 3-5 sets in

2-3 sessions per muscle group/ 2-3 sessions per muscle group/ 1-3 sessions per muscle group/weekweek week

Con = concentric: RM = repetition maximum.

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Wernbom et al

Table ll. Recommendations for accommodating training lor hypertrophyModerately fast concentric (con) Slow concentric trainingtraining

Accommodating eccentric (ecc)overload

ModeMuscle actions

ExerciseEttorta

RepetitionsSets

VelocityRest between repetitionsand sets, respectivelyFrequency

lsokinetic or hydraulicCon

Single and/or multiple joint90-100%

10-15H per exerciseProgression from 3 to rre sets intolal per muscle group12o-24o"ls1-2 seconds,60-120 seconds3-5 sessions per muscle group/weeK

lsokinetic or hydraulicCon

Single and/or multiple joint90%

103-5 per exerciseProgression from 3 to 5 sets intotal per muscle group4ffio"/s5 seconds,'120 seconds3 sessions per muscle group/week

lsokinetic or isoinertial tlywheelEcc and con (con is optional inisokinetics)Single and/or multiple jointEcc = up to 100%Con = up to 100%6-81-5 per exerciseProgression from 1-2 to 4-5 setsin total per muscle group4H0'/s0-5 seconds,120 seconds2 sessions per muscle group/week

a indicates level ol torque in relation to the maximum possible torque at the specified velocity.

populations, such as the elderly and individuals re-covering from sports injuries.

4..| i Limitotions

We recognise that it is obviously very difficult toseparate the impact of each training variable fromthe effects of the other training variables. For exam-ple, if one increases the training load (percentage ofIRM) in conventional weight training, it will alsoaffect the volume of training, unless this is compen-sated for by increasing the number of sets per-formed. Furthermore, we acknowledge that the mainobjective of many of the studies included in thisreview was not necessarily to maximise the hyper-trophic response and that the motivational level ofthe subjects may well have differed considerablybetween different studies. Closely associated withmotivation is whether the training is performedunder supervision or not. Direct supervision of theworkout has been shown to result in superior in-creases in strength when compared with un-supervised training.tzz6l The level of supervisionduring training varied among the studies included inthis review.

Apart from the training regimen, the trainingstatus is also likely to have an impact on the hyper-trophic response. Theoretically, a muscle that isalready somewhat hypertrophied has less potential

@ 2007 Adis Dsto Infomotion BV. All rights reserued.

to hypertrophy further in relative terms than a previ-ously untrained muscle. Conversely, a muscle thathas atrophied because of disuse or detraining has alarge growth potential and merely getting it back toits previous level will represent an increase in mus-cle volume if the atrophied state is taken as a base-line. Thus, even slight variations in training statusmay affect the hypertrophic response to a givenresistance training regimen. Also, the method ofmeasuring muscle volume or CSA may influencethe results. With earlier scanning techniques, theanatomical CSA of the muscle was measured with-out correcting for intramuscular fat. Recent methodsof MRI and CT allow for measurements of intersti-tial fat, as well as muscle, and consequently forcalculation of adipose tissue-free muscle.l227l Inyoung healthy subjects, the anatomical muscle areais only slightly larger than adipose tissue-free mus-cle area.tz21l Hence, any increase in muscle volumeas a result of strength training will mainly reflect anincrease in adipose tissue-free muscle mass. There-fore, the data from the studies included in this re-view were pooled irrespective of the muscle-scan-ning method used. However, because of the factorsdiscussed here and the many other confoundingfactors that inevitably are present when summaris-ing and comparing the results of many differentstudies, the dose-response trends and recommenda-



tions outlined in the present review should be re-garded as tentative.

4.12 Troining lmplicotionsond Recommendotions

Preliminary recommendations for each mode aregiven in table I, table II and table III. These arebased on the evidence outlined in this article, as wellas on training protocols that have been shown toincrease muscle mass. However, the tables shouldnot be interpreted as stating that all modes andmethods are equally effective in increasing musclemass. Rather, the aim is to summarise differentmethods that may be suitable in different situationsand for specific populations. For example, fatiguing,low-to-moderate load, slow-speed resistance train-ingtTs'88'e2'llo; has potential applications for the reha-bilitation of patients for whom the high forces ofconventional heavy-resistance exercise are contrain-dicated. For patients who can tolerate relatively highforces, but for whom the metabolic and cardiovascu-lar demands of traditional strength training are toosevere, pure eccentric exercise may be an alternativebecause of the low energy demands of this type ofexercise.tls3l Our recommendations for conventionalhypertrophy training are similar to those presentedin the American College of Sports Medicine posi-

Table lll. Becommendations for isometric training lor hypertrophy

tion standt3l and by Kraemer and Ratamess.trl Wealso agree with these authors on the importance ofprogression and individualisation of the exerciseprescription. Regarding progression, we recommendlow volumes (e.9. l-2 sets) in the initial stages oftraining, when performing eccentric-muscle actions,because low volumes have been shown to be suffi-cient to induce hypertrophy in the early stages oftraining and because exercise adherence may beimproved if the workout is relatively brief. Also,avoiding unnecessary damage may allow hypertro-phy to take place earlier. As the individual adapts tothe stimulus of strength training, the overall volumeand/or intensity may have to be gradually increasedto result in continued physiological adaptations andother strategies (e.g, periodisation) can also be intro-duced if even further progress is desired.

In this context, it is essential that the trainer ortherapist is aware of possible interactions betweenthe training variables and how these, in turn, interactwith the exercise tolerance of the individual. Forexample, a training volume that is appropriate at afrequency of two sessions per muscle group perweek may become excessive at three sessions perweek. Conversely, a volume that is sufficient atthree sessions per week may be less than optimal attwo sessions per week. The workout structure (e.g.

Low-intensity isometric training High-intensity isometric training Maximum-intensity isometrictraining

Exercise selectionTorque levelRepetitionsSets

Duration per repetition

Rest between repetitionsand sets, repectivelyFrequency

Comments

Single and/or multiple ioint30-50% of MVIAI

2-€ per exerciseProgression from 2 to 4-€ sets intotal per muscle group4H0 seconds, and to muscularfailure during the linal 1-2 sets3m0 seconds

3-4 sessions per muscle group/weeKSuitable for individuals who cannottolerate high forces and withrestricted range of movement dueto pain and/or injury

Single and/or multiple joint7H0o/o ol MVIA12-6 per exerciseProgression from 2 to 4-6 setsin total per muscle group15-20 seconds, and lo muscularfailure during the tinal 1-2 sets3H0 seconds

H sessions per muscle group/weekSuitable lor individuals whocannol tolerate near-maximalforces

Single and/or multiple joint100o/o of MVIA101-3 per exerciseProgression kom 1 to 3 sets intotal per muscle group3-5 seconds

25-30 seconds,60 seconds3 sessions per muscle group/week

Care should be taken to avoidexcessive breath-holding and veryhigh blood pressures

MVIA = maximal voluntary isometric action.

o 2007 Adis Doto Informollon 8V. All rights reserved. Sports Med 2m7;37 (3)

258 Wernbom et al.

whole-body workout versus single muscle-grouptraining) also has a direct bearing on the appropriatedosage of training. Table I, table II and table II areintended as guidelines for single muscle-grouptraining. If whole-body workouts are performed, thevolume of specific work per muscle group may haveto be reduced so that the overall volume does notbecome excessive. For further discussion on thetopic of workout design, we refer to the paper ofKraemer and Ratamess.tll

5. Conclusions

This review demonstrates that several modes oftraining and all three types of muscle actions caninduce hypertrophy at impressive rates and that, atpresent, there is insufficient evidence for the superi-ority of any mode and/or type of muscle action overother modes and types of training. That said, itappears that exercise with a maximal-eccentric com-ponent can induce increases in muscle mass withshorter durations of work than other modes. Someevidence suggests that the training frequency has alarge impact on the rate of gain in muscle volume forshorter periods of training. Because longer studiesusing relatively high frequencies are lacking, it can-not be excluded that stagnation or even overtrainingwould occur in the long term. Regarding intensity,moderately heavy loads seem to elicit the greatestgains for most categories of training, although ex-amples of very high rates were noted at both verylow and very high intensities when the sets wereperformed with maximum effort or taken to muscu-lar failure. Thus, achieving recruitment of the great-est number of muscle fibres possible and exposingthem to the exercise stimulus may be as important asthe training load per se. For the total volume orduration of activity, the results suggest a dose-re-sponse curve characterised by an increase in the rateof growth in the initial part of the curve, which isfollowed by the region of peak rate of increase,which in turn is followed by a plateau or even adecline.

It is recognised that the conclusions drawn in thispaper mainly concern relatively short-term trainingin previously untrained subjects and that in highly-

@ 2007 Adis Doto Infotmotion BV. All righls reserved.

trained subjects or for training studies extending forseveral months, the dose-response trends and thehypertrophic effects of different modes and types ofstrength training may be very different. The samemay well be true for other populations, such aselderly and injured individuals.

AcknowledgementsNo sources of funding were used to assist in the prepara-

tion of this review. The authors have no conflicts of interestthat are directly relevant to the content of this review.

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Correspondence and offprints: Mathins W ernbom, LundbergLaboratory for Human Muscle Function and MovementAnalysis, Department of Orthopaedics, Sahlgrenska Uni-versity Hospital, Gröna Sträket 12, Göteborg, SE4f3 45,Sweden.E-mail: mathias.wembem@orthop. gu.se

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