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91:569-580, 2001. ;J Appl Physiol and Markku AlenKeijo Häkkinen, Arto Pakarinen, William J. Kraemer, Arja Häkkinen, Heli Valkeinenwomenand serum hormones during strength training in older Selective muscle hypertrophy, changes in EMG and force,

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Selective muscle hypertrophy, changes in EMG and force,and serum hormones during strength training in older women

KEIJO HAKKINEN,1 ARTO PAKARINEN,2 WILLIAM J. KRAEMER,3

ARJA HAKKINEN,4 HELI VALKEINEN,1,5 AND MARKKU ALEN5,6

1Neuromuscular Research Center and Department of Biology of Physical Activity, University ofJyvaskyla, 40351 Jyvaskyla; 2Department of Clinical Chemistry, University of Oulu,90220 Oulu, Finland; 3The Human Performance Laboratory, Ball State University, Muncie, Indiana47306; 4Department of Physical Medicine and Rehabilitation, Central Hospital, 40620 Jyvaskyla;5Department of Health Sciences, University of Jyvaskyla, 40351 Jyvaskyla; and 6Department ofPhysical Medicine and Rehabilitation, Kuopio University Hospital, 70211 Kuopio, FinlandReceived 12 January 2001; accepted in final form 5 March 2001

Hakkinen, Keijo, Arto Pakarinen, William J. Krae-mer, Arja Hakkinen, Heli Valkeinen, and Markku Alen.Selective muscle hypertrophy, changes in EMG and force,and serum hormones during strength training in olderwomen. J Appl Physiol 91: 569–580, 2001.—Effects ofstrength training (ST) for 21 wk were examined in 10 olderwomen (64 6 3 yr). Electromyogram, maximal isometricforce, one-repetition maximum strength, and rate of forcedevelopment of the leg extensors, muscle cross-sectionalarea (CSA) of the quadriceps femoris (QF) and of vastuslateralis (VL), medialis (VM), intermedius (VI) and rectusfemoris (RF) throughout the lengths of 3/12–12/15 (Lf) ofthe femur, muscle fiber proportion and areas of types I, IIa,and IIb of the VL were evaluated. Serum hormone concen-trations of testosterone, growth hormone (GH), cortisol,and IGF-I were analyzed for the resting, preexercise, andpostexercise conditions. After the 21-wk ST, maximal forceincreased by 37% (P , 0.001) and 1-RM by 29% (P ,0.001), accompanied by an increase (P , 0.01) in rate offorce development. The integrated electromyograms of thevastus muscles increased (P , 0.05). The CSA of the totalQF increased (P , 0.05) throughout the length of the femurby 5–9%. The increases were significant (P , 0.05) at7/15–12/15 Lf for VL and at 3/15–8/15 Lf for VM, at5/15–9/15 for VI and at 9/15 (P , 0.05) for RF. The fiberareas of type I (P , 0.05), IIa (P , 0.001), and IIb (P ,0.001) increased by 22–36%. No changes occurred duringST in serum basal concentrations of the hormones exam-ined, but the level of testosterone correlated with thechanges in the CSA of the QF (r 5 0.64, P , 0.05). An acuteincrease of GH (P , 0.05), remaining elevated up to 30 min(P , 0.05) postloading, was observed only at posttraining.Both neural adaptations and the capacity of skeletal mus-cle to undergo training-induced hypertrophy even in olderwomen explain the strength gains. The increases in theCSA of the QF occurred throughout its length but differedselectively between the individual muscles. The serumconcentrations of hormones remained unaltered, but a lowlevel of testosterone may be a limiting factor in training-induced muscle hypertrophy. The magnitude and timeduration of the acute GH response may be important

physiological indicators of anabolic adaptations duringstrength training even in older women.

aging; muscle; endocrine functions; resistance training; se-lective hypertrophy; electromyogram

HUMAN MUSCLE MASS, STRENGTH, and power decrease dur-ing aging, especially from the sixth decade on in bothmen and women (36). The decline in muscle mass isthought to be mediated by a reduction in the sizeand/or number of individual muscle fibers, especially offast-twitch fibers (29). Age-related declines in strengthmay also be due to decreased maximal voluntary acti-vation of the agonist muscle and/or changes in antag-onist coactivation (14). The age-related decreases inmuscle mass and strength are not surprising, becauseaging is very often associated with a decline in thequantity and especially intensity of daily physical ac-tivities. Furthermore, with aging, blood concentrationsof circulating anabolic hormones and growth factors,e.g., testosterone, growth hormone (GH) and insulin-like growth factor I (IGF-I), are diminished, especiallyin women, suggesting that the decreasing basal level ofblood testosterone in aging women over the years maylead to decreasing anabolic effects on muscles associ-ated possibly with muscle atrophy and decreasedstrength (19).

However, progressive strength training not only inyoung and middle-aged adults but also in older menand women can lead to substantial increases instrength performance. This might primarily resultfrom considerable neural adaptations observed, espe-cially during the earlier weeks of training (16, 32), asindicated by large increases in maximal electromyo-graphic (EMG) activity of trained agonist muscles as-sociated with decreases in the coactivation of the an-tagonists especially in older women (16). It has alsobeen shown with sensitive techniques such as fiber

Address for reprint requests and other correspondence: K. Hakki-nen, Neuromuscular Research Center and Dept. of Biology of Phys-ical Activity, Univ. of Jyvaskyla, P. O. Box 35, 40351 Jyvaskyla,Finland.

The costs of publication of this article were defrayed in part by thepayment of page charges. The article must therefore be herebymarked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734solely to indicate this fact.

J Appl Physiol91: 569–580, 2001.

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area determination by muscle biopsy, or muscle cross-sectional area (CSA) determination by computed to-mography or magnetic resonance imaging (MRI) thatmuscle hypertrophy has accounted for the strengthgains not only in young and middle-aged adults butalso in older men and women (7, 13, 16–18, 37, 43). Thebasic requirements for training-induced hypertrophy,not only in older men, but also in older women, whousually show a large degree of muscle atrophy, are thatthe overall training intensity [the load in relation tothe 1-repetition maximum (1 RM) action] as well as theduration of the training period should be sufficient.

Training-induced hypertrophy in older men andwomen seems to take place in both fast- and slow-twitch muscle fibers. However, much less informationis available on training-induced hypertrophy of indi-vidual muscle fibers in older women (7, 17, 37), includ-ing also data of no training-induced hypertrophy (28).It is also important to point out that it has been shownin younger adults that training-induced muscle hyper-trophy (measured by use of MRI) can be nonuniformalong the belly of the muscle (33, 34). Until now, onlyone study, conducted by Tracy et al. (43), has examinedthe phenomenon of selective hypertrophy in olderwomen during strength training. The data indicatedthat strength training-induced muscle hypertrophywas greatest in the region of largest CSA (at midthigh)and the increases in CSA became progressively smallertoward the proximal and distal regions of the quadri-ceps femoris (QF). The authors concluded that thesingle-slice method may overestimate the true muscleCSA changes in other regions of the QF and may beprone to error. However, the authors reported the dataonly about the total QF muscle group and not about thetraining-induced selective hypertrophy taking placepossibly in each of the four individual muscles of theQF. Both the longitudinal shape with regard to theCSA and the overall CSA do differ largely betweenthe four individual muscles. Our interest was focusedon the examination of the degree of selective strengthtraining-induced muscle hypertrophy not only in thetotal QF but also in each of its individual muscles in agroup of older women.

Heavy-resistance exercise is well known to be a po-tent stimulus for acute increases in circulating ana-bolic hormones in younger men. However, the magni-tude of hormonal response is lowered in older men (8,21, 25). In women, the acute response in serum testos-terone and GH is lower than in men, whereas noresponse at all is necessarily observed in older women(21, 22). During strength training, no systematicchanges have been reported to take place in basal bloodconcentrations of circulating anabolic hormones eitherin older men (8, 22, 35) or in older women (20, 22).Because of the pulsatile nature of GH secretion, theinterpretation of single measures must be done cau-tiously, but the data available indicate that the re-sponse of GH to the same relative heavy-resistanceworkload is greatly lowered in older women at the ageof 67 yr, and they remained nonresponsive also afterthe 6-mo strength-training period (22). However, the

acute responsiveness of serum GH to heavy-resistanceexercise in older women needs further investigation.Second, because of large interindividual variationamong older women, the physiological role of the acuteGH response or lack of it for the trainability of an olderindividual during prolonged strength training waswithin our special interest.

We hypothesized that systematic strength training,even in older women, would lead to significant hyper-trophy of the trained muscles, but we were specificallyinterested to examine the phenomenon of selectivehypertrophy over the entire length of the thigh withregard to the total QF and to each of its individualmuscles. Second, because blood concentrations of cir-culating anabolic hormones and growth factors areknown to diminish with aging women, we wanted toexamine the underlying endocrine mechanisms relatedto muscle hypertrophy by studying the possible effectsof strength training 1) on basal concentrations and 2)acute responses of serum hormones as well as 3) theirpossible interrelationships with the overall degree ofmuscle hypertrophy and strength development in thisspecial group of subjects (older women) during a pro-longed strength-training period of 21 wk.

METHODS

Subjects

Ten healthy older women (64 6 3 yr; n 5 10) (mean 6 SD)volunteered for the study. The subjects were carefully in-formed about the design of the study with special informationas to possible risks and discomfort that might result. There-after, the subjects signed a written consent form beforeparticipation in the project. The study was conducted accord-ing to the declaration of Helsinki and was approved by theEthics Committee of the University of Jyvaskyla, Finland.

The subjects were healthy and habitually physically ac-tive. To keep themselves fit, they had taken part in variousrecreational low-intensity physical activities such as walk-ing, jogging, cross-country skiing, aerobics, or biking, butnone of the subjects had any background in regular strengthtraining. Subjects were recruited through advertisementsand were medically screened by a medical doctor. None of thesubjects had contraindications to perform rigorous resistanceexercise. No medication was being taken by the subjects thatwould have been expected to affect physical performance.

Experimental Design

The experimental period of 25 wk consisted of a 4-wkcontrol period followed by a 21-wk resistance-training period.The subjects were tested on five different occasions usingidentical protocols. The first month of the study (between themeasurements at week 24 and at week 0) served as a controlperiod during which time no strength training was carriedout but the subjects maintained their normal low-intensityrecreational physical activities. The subjects were testedbefore and after this control period. Thereafter, the subjectsstarted a supervised experimental strength-training periodfor 21 wk. The measurements were repeated during theactual experimental training period at 7-wk intervals (i.e.,weeks 0, 7, 14, and 21).

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Testing

The subjects were carefully familiarized with the testingprocedures of voluntary force production of the leg musclesduring several submaximal and maximal performances ;1week before the measurements at week 24. Second, duringthe actual testing occasion, several warm-up contractionswere performed before the maximal test actions.

Isometric force-time curves, maximal isometric force, andmaximal rate of isometric force development (RFD) of thebilateral leg extensor muscles (hip, knee, and ankle exten-sors) were measured on an electromechanical dynamometer(14, 16). In this test, the subjects were in a sitting position sothat the knee and hip angles were 107 and 110°, respectively.The subjects were instructed to exert their maximal force asfast as possible during a period of 2.5–4.0 s. A minimum ofthree trials was completed for each subject, and the bestperformance trial with regard to maximal peak force wasused for the subsequent statistical analysis.

A David 210 dynamometer (David Fitness and Medical)was used to measure maximal bilateral concentric force pro-duction of the leg extensors (hip, knee, and ankle extensors)(14, 16). The subject was in a seated position so that the hipangle was 110°. On verbal command, the subject performed aconcentric leg extension starting from a flexed position of 70°trying to reach a full extension of 180° against the resistancedetermined by the loads chosen on the weight stack. In thetesting of the maximal load, separate 1-RM contractions wereperformed. After each repetition, the load was increased untilthe subject was unable to extend the legs to the requiredposition. The last acceptable extension with the highest pos-sible load was determined as 1 RM.

The force signal was recorded on a computer (486 DX-100)and thereafter digitized and analyzed with an Codas TMcomputer system (Data Instruments). Maximal peak forcewas defined as the highest value of the force (N) recordedduring the bilateral isometric leg extension. The force-timeanalysis on the absolute scale included the calculation ofaverage force (N) produced during 100-ms epochs from thestart of the contraction up to 500 ms (14, 16). The RFD (N/s)was also analyzed and defined as the greatest increase inforce in a given 50-ms time period.

EMG activity during the bilateral extension actions of theleg muscles was recorded from the agonist muscles of thevastus lateralis (VL) and vastus medialis (VM) of the rightand left leg separately. Bipolar (20-mm interelectrode dis-tance) surface EMG recording (Beckman miniature-sizedskin electrodes 650437) was employed. The electrodes wereplaced longitudinally on the motor point areas determined byan electrical stimulator. EMG signals were recorded tele-metrically (Glonner, Biomes 2000). The positions of the elec-trodes were marked on the skin by small ink tattoos (16).These dots ensured the same electrode positioning in eachtest over the 25-wk experimental period. The EMG signalwas amplified (by a multiplication factor of 200; low-passcutoff frequency of 360 Hz/3 dB) and digitized at the sam-pling frequency of 1,000 Hz by an on-line computer system.EMG was full-wave rectified, integrated (iEMG, in mV zs),and time normalized for 1 s in the following phases: 1) in theisometric actions for the periods of 100–500 ms to obtain aniEMG-time curve from the start of the contraction, 2) in themaximal peak force phase of the isometric contractions (500–1,500 ms) to calculate maximal iEMG, and 3) in the concen-tric action of the 1-RM performance for the entire range ofmotion (14, 16).

Muscle biopsies were obtained before and after the exper-imental training period. The samples were obtained from the

superficial portion of the VL muscle of the right leg (at thelower third portion of the thigh) utilizing the percutaneousneedle biopsy technique of Bergstrom (4). Special care wastaken to extract tissue from the same location (close to theprebiopsy scar) and depth each time. Muscle tissue sampleswere frozen in isopentane cooled with liquid nitrogen andstored at 280°C until analyzed. Serial cross sections (10 mmthick) were cut on a cryostat at 220°C for histochemicalanalyses. Histochemical staining for myofibrillar ATPasewas used to classify the fibers as I, IIa, IIb, and IIc (on thebasis of the stability of their ATPase activity at pH 4.2, 4.6,and 10.3 in the preincubation medium) according to Brookeand Kaiser (5). IIc fibers were, however, so rare that theywere not included in the final statistical analyses. Fiber-typepercentages were calculated from the mean number of fibers(at pre- and posttraining) of 481 6 250 and 356 6 124,respectively. For the calculation of mean fiber areas, anaverage number of fibers analyzed were 117 6 41 and 85 629, respectively. A loaded image of stained cross sections wasanalyzed by Tema Image-Analysis System (Scan Beam). Avideoscope consisting of a microscope (Olympus BX 50) andcolor video camera (Sanyo High Resolution CCD) was used tocalculate the mean fiber areas of each fiber type.

The muscle CSA of the right QF was assessed before andafter the 21-wk strength training by using MRI (PhilipsGyroscan ACS-NT Scanner, 1.5 T) at the Keski-SuomenMagneettikuvaus, Jyvaskyla, Finland. Once the subject waspositioned within the magnet, the thighs of both legs werekept parallel to the MRI table, and the feet were strappedtogether to prevent rotation. The lengths of the femur (Lf),taken as the distance from the intercondular notch of thefemur to the inferior corner of the femoral head, was mea-sured on a coronal plane. Subsequently, 15 axial scans of thethigh interspaced by a distance of 1/15 Lf were obtained fromthe level of 1/15 Lf to 15/15 Lf as also done in our laboratory’sprevious study (17). Great care was taken to reproduce thesame, individual Lf each time by using the appropriate ana-tomical landmarks. In addition, one scan was taken at thesite (marked on the skin by the ink tattoo) of the musclebiopsy of the VL muscle. All MRI images were then ported toa Macintosh computer for the calculation of muscle CSA. Foreach axial scan, CSA computation was carried out on the QFas a whole and, individually, on the VL, VM, vastus inter-medius (VI), and rectus femoris (RF). For the final calcula-tion of the CSA, slices 3/15-12/15 were used (slice 3 beingcloser to the knee joint of the thigh) for all muscles examinedexcept for the RF, which was analyzed only for the slices5/15-12/15. CSA (measured as cm2) was determined by trac-ing manually along the border of each muscle of the QF.

The percentage of fat in the body was estimated fromthe measurements of skinfold thickness from four differentsites (9).

Experimental Strength Training

The supervised 21-wk periodized strength-training pro-gram of the subjects was a total body (low-volume) programcut into a 2 day/wk format (the typically recommended fre-quency for recreational training purposes). A minimum of 2days of rest was required between the two sessions of eachweek. Each training session included two exercises for the legextensor muscles: the bilateral leg press exercise and thebilateral and/or unilateral knee extension exercise on theDavid 200 machine. We chose these exercises because 1) theyare probably the most common ones used in strength trainingfor the thigh musculature, 2) they are easy to perform by anysubject at all ages, 3) the thigh muscles can be “maximally”

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activated throughout the range of motion by using thepresent knee-extension exercise, and 4) the biomechanicalnature of the bilateral leg press exercise is very similar tothat of the testing action used in the present strength mea-surements. In addition, each training session included four tofive exercises for the other main muscle groups of the body(the bench press and/or the triceps push-down and/or lateralpull-down exercise for the upper body; the sit-up exercise forthe trunk flexors and/or another exercise for the trunk ex-tensors; and the bilateral/unilateral elbow and/or knee flex-ion exercise and/or leg adduction/abduction exercise). All theexercises were performed using concentric muscle actionsfollowed by eccentric actions during the “lowering” phase ofthe movement. The loads were determined during the train-ing sessions throughout the 21-wk training period accordingto the maximum-repetition method.

During the first 7 wk of the training, the subjects trainedwith loads of 40–70% of the 1 RM. The loads of 40–60% wereused during the first 4 wk and those of 50–70% during thelast 3 wk. The subjects performed 15–20 repetitions per setat loads of 40%, 12–15 repetitions at loads of 50%, 10–12repetitions at loads of 60%, and 8–10 repetitions at loads of70%. Three sets were performed in each exercise duringweeks 1–4 and three to four sets during weeks 5–7. The loadswere 40–50% and 60–70% of the maximum by week 11 and50%, 60–70%, and 70–80% by week 14. In the two exercisesfor the leg extensor muscles, the subjects now performedeither 10–12 repetitions per set at loads of 40% and 8–10repetitions at loads of 50% (loads of 40 and 50% for rapidmuscle actions) or 10–12 repetitions per set at loads of 60%,8–10 repetitions at loads of 70%, and 5–8 repetitions at loadsof 80%. Three to four sets were performed by week 11, andfour to five sets by week 14. In the other four exercises, thesubjects performed 10–12 repetitions per set at loads of 60%and performed 3–4 sets by week 11 and 4–5 sets by week 14.During the last 7 wk of training (weeks 14–21), the subjectsperformed the two exercises for the leg extensor muscleseither 8–10 repetitions per set with loads of 70% and 5–8repetitions per set with loads of 80% of the maximum or10–12 repetitions per set with loads of 40% and 8–10 repe-titions per set with loads of 50% (loads of 40 and 50% forrapid muscle actions). Five to six sets were performed duringweeks 14–18 and four to five sets during weeks 19–21. In theother four exercises, 8–12 repetitions per set (10–12 repeti-tions per set at loads of 60% and 8–10 repetitions per set atloads of 70%) were performed for four to five sets duringweeks 14–18 and three to four sets during weeks 19–21.

The strength training utilized was a combination of heavyand explosive resistance-training programs so that a volumeof ;20% of the total volume of the leg extensor exercises (legpress and knee extension) with light loads (40% of the max-imum for 10–12 repetitions per set and that of 50% for 8–10repetitions per set) was performed according to the principleof explosive strength training (16). These repetitions wereexecuted as explosively as possible (i.e., rapid muscle actions)throughout the range of motion. The overall amount of train-ing was progressively increased (in terms of number of setswithin the range limits described) until the fifth month, atwhich point it was slightly reduced for the final 3 wk of the21-wk training period. During the 21-wk experimental train-ing period, the subjects continued taking part in recreationallow-intensity physical activities such as walking, jogging,swimming, biking, or gymnastics one to three times per weekin a similar manner to what they were accustomed to beforethis experiment.

Heavy-Resistance Protocol for the Examinationof Acute Hormone Responses

The heavy-resistance protocol at week 0 before the trainingperiod as well as at week 21 after the 21-wk strength-trainingperiod included the bilateral leg press exercise on a machine(David 210, David Fitness and Medical). In the exercise, thesubject started from the flexed-knee position (70°) and ex-tended the knees concentrically to a full extension (180°) andthereafter lowered the load eccentrically back to the startingposition. The actual loads were always the repetition maxi-mums for each subject so that the subjects performed 10repetitions per set with the maximal load possible for a totalof 5 sets (5 3 10 repetition maximums). The recovery timebetween the sets was 2 min. The loads were adjusted duringthe course of the session due to fatigue so that each subjectwould be able to perform 10 repetitions at each set. If the loadhappened to become too heavy, the subject was assistedslightly during the last one to three repetitions of the set,while she maintained her maximum performance, so that therequired number of repetitions could be reached and thesubjects would also maintain the same contraction time.

Blood Samples During the Heavy-ResistanceLoading Protocol

The control samples. To examine acute hormone responsesto the heavy-resistance loading, the control blood sampleswere drawn from the antecubital vein of each subject twice(two control samples within 1 h of each other) during thecontrol day at week 0. The corresponding two control sampleswere also drawn twice (two control samples within 1 h of eachother) during the second control day after the training atweek 21.

The loading samples. Blood samples were drawn fourtimes during the two heavy-resistance exercise days (pre-and postloading samples within ;1 h as well as 15 min and30 min after termination of the training session) at week 0and at week 21. The heavy-resistance protocol was performedbetween 8:00 AM and 6:00 PM but always at the same timeof day for each subject (at the corresponding time of the dayas the blood sampling during the control days) before andafter the 21-wk training period. The subjects were instructedto maintain their normal food intake before the heavy-resis-tance exercise protocol and to have their last light mealduring that day no later than 2 h before the session.

Basal Blood Samples During the 4-wk Control Periodand 21-wk Strength Training

To examine the basal concentrations of serum hormones,blood samples were drawn from the antecubital vein of eachsubject after 10 h of fasting and ;8 h of sleep in the mornings(between 7:30 AM and 8:30 AM) during the 1-mo controlperiod (at week 24 and week 0) as well as during the 21-wktraining period (at weeks 7, 14, and 21).

Analytical Methods

Serum samples for the hormonal analyses were kept fro-zen at 220°C until assayed. Serum testosterone concentra-tions were measured by the Chiron Diagnostics ACS:180automated chemiluminescence system using a ACS:180 an-alyzer. The sensitivity of the testosterone assay was 0.42nmol/l, and the intra-assay coefficient of variation was 6.7%.The concentrations of serum free testosterone and dehydro-epiandrosterone sulfate (DHEAS) were measured by radio-immunoassays using kits obtained from Diagnostic Products(Los Angeles, CA). The sensitivity of the free testosterone




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assay was 0.52 pmol/l, and the intra-assay variation was3.8%. The respective values were 0.06 mmol/l and 4.5% for theDHEAS assay. The assays of serum cortisol were carried outby radioimmunoassays. The sensitivity of cortisol assay was0.05 mmol/l, and the coefficient of the intra-assay variationwas 4.0%. Serum sex hormone-binding globulin (SHBG) con-centrations were measured by two-site fluoroimmunometricmethods with kits obtained from Wallac (Turku, Finland)using the 1235 AutoDELFIA automatic immunoassay sys-tem. The sensitivity of the SHBG assay was 0.5 nmol/l, andthe intra-assay variation was 4.4%. Concentrations of GHwere measured by use of radioimmunoassay kits from Phar-macia Diagnostics (Uppsala, Sweden). The sensitivity of theGH assay was 0.2 mg/l, and the intra-assay variation was2.5–5.1%. Serum IGF-I concentrations were measured byradioimmunoassays using reagent kits from DiaSorin (Still-water, MN). The method included an octadecylsiyl-silica ex-traction procedure for the serum samples. The sensitivity ofthe IGF-I assay was below 2.0 nmol/l, and the intra-assayvariation was 9.2%. All samples for each test subject wereanalyzed in the same assay for each hormone.

Statistical Methods

Standard statistical methods were used for the calculationof means, SD, SE, and Pearson product moment correlationcoefficients. The data were then analyzed by utilizing multi-variate analysis of variance with repeated measures. Proba-bility-adjusted t-tests were used for pairwise comparisonswhen appropriate. The P , 0.05 criterion was used for estab-lishing statistical significance.

RESULTS

Physical Characteristics

Body mass (from 70.5 6 6.1 to 70.9 6 5.1 kg) andbody height (from 160.1 6 5.9 to 160.4 6 6.1 cm)remained statistically unaltered, but the percentage ofbody fat decreased (from 38.7 6 1.6 to 38.1 6 1.7%; P ,0.001) during the 21-wk strength-training period.

Maximal Isometric Leg Extension Force, Force-Time,and iEMGS

Maximal isometric bilateral force remained unal-tered during the 4-wk control period (from week 24 toweek 0) (Fig. 1). A large increase of 37% took place inmaximal force during the 21-wk training period from

1,435 6 345 to 1,970 6 410 N (P , 0.001). The averageforce produced in 500 ms remained unaltered duringthe control period but increased during the 21-wktraining period from 550 6 319 to 846 6 402 N (P ,0.01). The RFD values remained unaltered during thecontrol period but increased significantly during the21-wk training period from 4,450 6 2,670 to 6,880 63,413 N/s (P , 0.01).

No significant changes occurred during the controlperiod in the maximum iEMGs of the VL and VMmuscles of the isometric actions (Fig. 2). During thecourse of the 21-wk training, significant increases wereobserved in the iEMGs of the VL and VM muscles ofthe right (P values between ,0.001 and ,0.05) and leftleg (P values between ,0.001 and ,0.05). The iEMGsof the VL and VM muscles during the first 500 ms ofthe isometric action increased (P , 0.05) during thetraining.

1-RM Leg Extension Values and Maximum iEMGs

The 1-RM bilateral leg extension values remainedstatistically unaltered during the control period (Fig.3). During the 21-wk training, the 1-RM values im-proved by 29% from 106 6 23 to 137 6 23 kg (P ,0.001).

Fig. 1. Mean 6 SD maximal voluntary isometric force of the bilateralleg extension in older women during the 4-wk control period andduring the course of the 21-wk strength-training period.

Fig. 2. Mean 6 SE maximal integrated electromyographic activity[iEMG, averaged for the vastus lateralis (VL) and medialis (VM)muscles of the left leg] in the voluntary maximal bilateral isometricleg extension action in older women during the 4-wk control periodand during the course of the 21-wk strength-training period.

Fig. 3. Mean 6 SD maximal voluntary concentric 1-repetition max-imum (1-RM) strength of the bilateral leg extension action in olderwomen during the 4-wk control period and during the course of the21-wk strength-training period.




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No statistically significant changes occurred duringthe control period in the iEMGs of the VL and VMmuscles of the 1-RM actions, but the iEMG valuesincreased during the 21-wk training both in the left (Pvalues between ,0.01 and ,0.05) and right leg (Pvalues between ,0.01 and ,0.05).

Muscle CSA

The CSA of the QF increased during the 21-wktraining period significantly (P , 0.05–0.01) through-out the length of the quadriceps from 4/15 to 12/15 Lf(Fig. 4). The mean relative increase at different Lf of

the QF was 7.5% ranging from 6 to 11% but did notdiffer significantly from each other. However, for indi-vidual muscles, the CSA of the VL increased during the21-wk training significantly (P , 0.01 and ,0.05) at7–12/15 Lf (by 9–14%) but not at 3–6/15 Lf (Fig. 5),whereas the corresponding increases of the VM weresignificant (P , 0.05 and 0.01) at 3–8/15 (by 6–12%)but not at 9–12/15 Lf (Fig. 5). The increases of theCSAs of the VI were significant (P , 0.05) at 5–9/15and 11–12/15 (by 4–11%) (Fig. 5), and the only signif-icant increase (P , 0.05) in the case of the RF wasobserved at 9/15 (by 8%) (Fig. 5). The increases of theCSAs of the muscles measured at the length of themuscle biopsy site were significant for the VL (P ,0.01) and VM (P , 0.05) and for the whole QF (P ,0.05) but not for the VI or RF (Fig. 6).

Muscle Fiber Characteristics

The percent values for the muscle fiber distributionof the VL muscle did not differ significantly before orafter the training period (Table 1). The mean fiberareas of type I as well as those of types IIa and IIbincreased after the 21-wk training period (P , 0.05 andP , 0.001) (Table 2). The relative increases for type Iarea and the average area of type II were 22 6 25% and36 6 20%, respectively.

The individual mean fiber areas of type II correlatedsignificantly with the individual CSAs of the VL mus-cle (at the length of the biopsy site) both before (r 50.94; P , 0.001) and after the 21-wk training period(r 5 0.81; P , 0.01). The correlation coefficients be-

Fig. 4. Mean 6 SD cross-sectional areas (CSAs) of the total quadri-ceps femoris (QF) muscle group at the lengths of the femur (Lf ) from3/15 to 12/15 in older women before and after the 21-wk strength-training period (*P , 0.05; **P , 0.01).

Fig. 5. Mean 6 SD CSAs of the individual muscles of the VL (A), VM (B), vastus intermedius (VI) (C), and rectusfemoris (RF) (D) of the QF muscle group at Lf from 3/15 to 12/15 in older women before and after the 21-wkstrength-training period (*P , 0.05; **P , 0.01; ***P , 0.001).




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tween the changes in the individual fiber areas and thechanges in the CSA variables during the 21-wk train-ing period were not significant.

Serum Hormones

Table 3 depicts the basal serum hormone concentra-tions at weeks 24, 0, 7, 14, and 21. No statisticallysignificant changes took place in the serum concentra-tions of total and free testosterone, GH, DHEAS, IGF-I,cortisol, or SHBG during either the 4-wk control periodor the course of the 21-wk strength-training period.

The individual concentrations of serum free testos-terone correlated with the individual averaged totalCSA of the QF muscle before the training (r 5 0.69, P ,0.05) and after the 21-wk training period (r 5 0.65, P ,0.05). The individual concentrations of serum free tes-tosterone correlated with the individual muscle fiberareas of type II before the training (r 5 0.86, P , 0.001)and after the 21-wk training period (r 5 0.79, P ,0.01). The individual mean concentrations (averagedover the 21-wk period) of serum testosterone correlatedwith the changes in the CSA of QF muscle over the21-wk training (r 5 0.64, P , 0.05). The individualmean concentrations (averaged over the 21-wk period)of serum free testosterone correlated slightly (r 5 0.48,not significant) with the individual changes in maxi-mal force recorded during the latest period of the 21-wktraining.

Serum hormone concentrations of total and free tes-tosterone, and GH, remained unaltered during thecontrol days (pre and post samples within 1 h) at week0 (before training) and at week 21 (after 21 wk ofstrength training) (Table 4). The mean concentrationsof serum total and free testosterone did not changeduring the heavy-resistance loading protocol either at

pretraining or at posttraining (Figs. 7 and 8). Themean concentration of GH did not increase signifi-cantly at pretraining, whereas a significant acute in-crease took place at posttraining (P , 0.05) and re-mained significant (P , 0.05) up to 15 min (P , 0.05)and up to 30 min (P , 0.05) postloading (Fig. 9). Therelative acute changes in GH at pretraining correlatedwith the relative changes recorded in maximal forceduring the latest training period of the 21-wk training(r 5 0.68, P , 0.05).

DISCUSSION

The present progressive strength training performedonly twice a week but for 21 wk led to large gains inmaximal and explosive isometric as well as concentricforce production characteristics of the leg extensors inolder women. The strength gains were accompanied bysignificant increases in the voluntary neural activationof the trained agonist muscles accompanied by signif-icant enlargements in muscle fiber areas of types I, IIa,and IIb as well as in the total CSA of the trainedextensor muscles. Interestingly, the data furthershowed that the increases in the CSA of the total QFtook place throughout the Lf, but the magnitudes of theCSA increases along the Lf differed specifically be-tween the four individual muscles of the QF. No sig-nificant training-induced changes occurred in the basalconcentrations of serum anabolic and catabolic hor-mones, but the mean level of individual serum testos-terone correlated significantly with the gains recordedin the CSA of the trained muscles, and a systematicacute exercise-induced increase of GH was observedonly after the 21-wk strength-training period.

The 21-wk progressive strength training, althoughperformed only twice a week, led to large gains inmaximal strength recorded in both isometric and con-centric bilateral actions of the leg extensors in ourolder women. It is of some importance to point out thatthe present increases in maximal strength were aslarge as 29–37%, although the subjects trained onlytwo times a week. These strength gains in our olderwomen were thus well in line with previous observa-tions that maximal muscle strength in previously un-trained healthy subjects can be increased “easily” dur-ing progressive strength training independently of age,gender, and type of actions, whether isometric or dy-namic (7, 12, 13, 15–18, 22, 26, 28, 30, 31). Thus, animportant conclusion from the practical standpoint isthe fact that the frequency of strength training in

Fig. 6. Mean 6 SD changes of the CSAs of the individual muscles ofthe VL, VM, VI, and RF and the total QF muscle group at the lengthof the site (the lower third portion of the thigh) of the muscle biopsyof (the VL muscle) in older women after the 21-wk strength-trainingperiod (*P , 0.05; **P , 0.01).

Table 2. Fiber areas of the vastus lateralis musclebefore and after a 21-wk strength-trainingperiod in older women

Pre Post

Type I, mm2 4,1316980 4,8786778*Type IIa, mm2 3,0516902 3,8996946†Type IIb, mm2 2,1836820 3,0146839†

Values are means 6 SD; n 5 10 subjects. Significant differencepre- to posttraining (*P , 0.05; †P , 0.001).

Table 1. Fiber distribution of the vastus lateralismuscle before and after a 21-wk strength-trainingperiod in older women

Pre Post

Type I, % 45617 40614Type IIa, % 32611 38611Type IIb, % 23615 22614

Values are means 6 SD; n 5 10 subjects. Pre, before strengthtraining; Post, after strength training.




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previously untrained older female (or male) subjectscan be as low as twice a week, when the loadingintensity of training is sufficient and increased pro-gressively (i.e., periodized) throughout the training pe-riod. Both muscle strength and the ability of the legextensor muscles to develop force rapidly are impor-tant performance characteristics in older people, con-tributing to several functional performance tasks ofdaily life such as climbing stairs, walking actions suchas crossing the road, or even prevention of falls and/ortrips (3, 12, 17, 39, 42, 44). In the present study, weapproached the aspect of explosive strength only sothat heavy-resistance training was combined with ex-ercises of explosive nature. Nevertheless, the presentobservation that explosive force production capacity ofthe neuromuscular system did remain trainable evenin older women should also be of practical value, forexample, in primary and secondary prevention offrailty and in physical rehabilitation programs for ag-ing people of both genders (16, 17).

The strength training led to large increases in themaximal voluntary activation of the agonist musclesrecorded during both isometric and concentric leg ex-tension actions. The magnitudes and the time coursesof the EMG increases (Fig. 2) were rather similar tothose changes recorded for the isometric voluntarystrength (Fig. 1) of the same muscle group. This findingindicates that the contributing role of the nervoussystem for strength development during the presentheavy-resistance training may have been of great im-portance. The largest increases in the iEMGs werenoted during the first 7 wk of training, supporting theconcept that, in previously untrained subjects, not onlyin younger adults but also in older persons, large initial

increases in maximal strength observed during theinitial weeks of strength training can be attributedlargely to the increased motor unit activation of thetrained agonist muscles (16–18, 22, 32, 38). Strengthtraining-induced increases in the magnitude of EMGcould result from the increased number of active motorunits and/or increase in their firing frequency (38).Increases in net excitation of the motoneurons mayresult from increased excitatory input, reduced inhib-itory input, or both (38). The present EMG data addi-tionally showed that the increases in the maximaliEMGs took place in our older women to some degreealso during the later course of the 21-wk trainingperiod. This may be explained by the facts that thetraining loads of the exercises were progressively in-creased in a periodized manner and that the subjectsactivated their muscles highly also during the explo-sive actions throughout the training period. Althoughthe actual nature of the adaptations in the nervoussystem is difficult to determine, not only can progres-sive strength training lead to increased activation ofthe agonists but also training-induced learning effectsin terms of reduced coactivation of the antagonists mayplay a contributive role. The latter phenomenon canalso enhance the net strength production of the ago-nists in younger adults (6) and, maybe even moreimportantly, especially in older subjects during multi-joint actions (16).

No statistically significant transformation of type IImuscle fiber subtypes or changes in the percentage oftype I fibers were observed pre- to posttraining in ourolder women. Type II subtype transformation, goingfrom type IIb to IIab to IIa, has been previously ob-served in younger (1, 27, 40, 41) and older men (18) but

Table 3. Serum total and free testosterone, GH, DHEAS, IGF-I, cortisol, and SHBG basal concentrationsin older women during the 4-wk control period (week 24 to week 0) and the courseof the 21-wk strength-training period (weeks 0, 7, 14, and 21)

Weeks

24 0 7 14 21

Testosterone, nmol/l 1.861.2 1.960.9 1.660.6 1.160.5 1.560.7Free testosterone, pmol/l 4.962.0 4.861.9 4.262.2 3.460.7 4.362.6GH, mg/l 0.960.7 2.462.5 1.663.3 2.363.6 2.263.7DHEAS, mmol/l 2.461.1 2.361.3 2.461.0 2.161.2 2.361.0IGF-I, nmol/l 18.468.8 17.768.9 18.869.9 17.366.3 17.465.8Cortisol, mmol/l 0.5760.20 0.4960.17 0.3660.10 0.4760.13 0.4760.10SHBG, nmol/l 51.4619.9 56.6620.8 59.4621.3 58.5620.8 56.8617.9

Values are means 6 SD; n 5 10 subjects. GH, growth hormone; DHEAS, dehydroepiandrosterone sulfate; IGF-I, insulin-like growth factorI; SHBG, sex hormone-binding globulin.

Table 4. Serum total and free testosterone and GH concentrations in older women during the 2 control dayswith no exercise (pre and post samples within 1 h) at weeks 0 (before training)and 21 (after 21 wk of strength training)

Testosterone, nmol/l Free Testosterone, pmol/l GH, mg/l

Pre Post Pre Post Pre Post

At week 0 1.160.5 1.260.4 3.662.3 3.362.3 0.961.5 1.962.4At week 21 1.360.7 2.363.2 3.963.9 3.763.6 0.560.4 0.560.4

Values are means 6 SD; n 5 10 subjects.




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not significantly in older women (17). The presentsubject group also showed a similar trend for thisduring the training period, although some cautionmust be exercised with the data because of the lownumbers of subjects and muscle fibers included in theanalysis. However, skeletal muscles of older people ofboth genders seem to retain the capacity to undergotraining-induced hypertrophy provided that the vol-ume, intensity, and the duration of the training periodare sufficient (7, 12, 13, 17, 18, 37). The present resis-tance training performed only twice a week did lead tosignificant increases in muscle fiber areas of types I,IIa, and IIb of the VL, in line with some previousfindings in older women (7, 17, 37), although no train-ing-induced hypertrophy has also been reported (28).In line with previous studies using older men as sub-jects (13), the increases in the sizes of individual mus-cle fibers of both types I and II were in the presentstudy larger than the enlargements observed in thetotal CSA of the QF. However, some caution must beexercised when interpreting the present muscle fiberarea data with a relative low number of fibers analyzedin the present biopsy sample obtained from the VLmuscle.

Recently, Tracy et al. (43) examined the phenomenonof selective hypertrophy of the QF in older womenduring strength training. Their data showed thatstrength training-induced muscle hypertrophy wasgreatest in the region of the largest CSA (at midthigh)

and that the increases in the CSA became progres-sively smaller toward the proximal and distal regionsof the QF. The authors concluded that the single-slicemethod may overestimate the true muscle CSAchanges in other regions of the QF and may be prone toerror. However, the individual muscles of the QF areknown to differ, with regard to not only the averageCSA of each muscle but also largely the CSAs along thebelly of these muscles. Interestingly, the present datashowed that the increases in the CSA of the total QFtook place throughout the Lf, whereas the magnitudesof the CSA increases along the Lf did differ specificallybetween the individual muscles of the QF. Thus theCSA of the VL increased during the 21-wk trainingsignificantly at 7–12/15 Lf but not at 3–6/15 Lf (Fig. 5),whereas the corresponding increases of the VM weresignificant at 3–8/15 Lf but not at 9–12/15 Lf (Fig. 5).The increases in both cases were thus greater in theregions of the largest CSAs, at proximal portions forthe VL and at distal portions for the VM. However, thiswas not the case for the increases recorded in the VI orRF muscles. Although the large training-induced in-creases observed in the maximal global iEMG of the VLand VM muscles did not differ significantly from eachother, the differences in the degree of hypertrophybetween the two muscles could be explained by specificdifferences in muscle activation (and tension) and/ordifferences in contractile proteins synthesis along thebelly of the individual muscles (34). It should also bepointed out that we did use a typical training programwith two common exercises for the thigh musculatureand that the choice of the exercises might contribute tothe degree of the selective hypertrophy of the musclestrained. Because the present increase in strength wasmuch greater than the overall degree of muscle hyper-trophy, it is also possible that, in addition to increasedvoluntary muscle activation, architectural changes,e.g., changes in pennation angle of the muscle fibers,may have taken place during strength training (23),contributing to strength development. The presentdata obtained in older women further showed that theincreases of the CSAs of the muscles measured at thelength of the muscle biopsy site were significant for theVL and VM and for the whole QF (Fig. 6). Thus thepresent biopsy site for the VL, as commonly used, todetermine the degree of hypertrophy of individualmuscle fibers, may actually be a reasonable one. How-

Fig. 7. Mean 6 SD values for serum testosterone concentrationsbefore (pre), immediately after the heavy-resistance loading sessions(post), and after a recovery for 15 min (post 15) and 30 min (post 30)both before (pretraining) and after the 21-wk strength training(posttraining) in older women.

Fig. 8. Mean 6 SD values for serum free testosterone concentrationsat pre, post, post 15, and post 30 time points both pretraining andposttraining in older women.

Fig. 9. Mean 6 SD values for serum growth hormone (GH) concen-trations pre, post, post 15, and post 30 both pretraining and post-training in older women (*P , 0.05).




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ever, the same site may not be that valid for the VI orRF. To conclude, the present MRI data showed that theenlargements of the muscle CSA seem to differ largelybetween the individual muscles of the QF muscle groupwhen measured at the same Lf, suggesting the advan-tages of the multiple-slice method to indicate the accu-rate growth of the muscle tissue taking place duringthe strength training.

No systematic changes were observed during thecourse of the 21-wk strength-training period in theconcentrations of serum testosterone, free testoster-one, DHEAS, GH, IGF-I, or cortisol, nor in the testos-terone-SHBG ratios. In general, these observations arerather similar to those found earlier in both middle-aged and older subjects of both genders, when theyhave utilized typical heavy-resistance training pro-grams over a period of a few months (20, 22, 26, 35).The overall loading of the present training programmay have thus been within the physiological rangenormal, because maximal strength increased greatlythroughout the 21-wk training period with no system-atic changes in the concentrations of anabolic andcatabolic hormones. In general, the data indicate thatalthough a basal level of the anabolic hormone testos-terone is lowered in older women, they seem to be ableto gain in strength to about the same extent as middle-aged or young adult women or men (22) when utilizingthe present type of low-volume total-body strength-training protocol over the 5- to 6-mo period. However,it has been shown that, in those older women who havedemonstrated very low basal testosterone levels, theindividual gains in maximal strength during thestrength-training period may be minor compared withthose with higher testosterone concentrations (22). Thepresent data further showed that also the individualgains in the CSA of the trained muscles were minor inthose older women who demonstrated lower basal tes-tosterone concentrations compared with those withhigher testosterone concentrations (r 5 0.64, P , 0.05).The findings strengthen the suggestion that basal con-centrations of blood testosterone may be of great im-portance; even so, a low level of testosterone may be alimiting factor in older women, for both strength de-velopment and overall training-induced muscle hy-pertrophy, when typical total body heavy-resistancetraining programs are utilized. In this study, only theserum levels of testosterone were measured. It is pos-sible that, even though the blood testosterone levelswould remain unaltered, strength training can inducechanges, e.g., at the receptor level. Dehydroepiandros-terone and its conjugated form DHEAS are androgenssecreted from adrenal cortex (2). As in the case oftestosterone, no systematic training-induced changeswere observed in the circulating levels of this androgenin our older women during the present 21-wk strength-training period. No systematic changes occurred in GHfor resting concentrations with the present training,either. However, the lack of changes in immunoreac-tive GH may not present the complete picture of theadaptational responses of GH variants to resistancetraining (26). The lack of changes in serum IGF-I with

the training may suggest that IGF-I in the circulationmay not be a good marker of the implicit activity of theGH-IGF-I system. Actually, strength training in olderpeople has been shown to lead to a substantial increasein the presence of IGF-I in skeletal muscle tissue (11).

In addition to the basal levels of the hormones,serum total and free testosterone as well as GH con-centrations were measured in the present study duringthe single heavy-resistance exercise session both be-fore and after the 21-wk strength-training period. Se-rum testosterone concentration is known to increaseduring a typical heavy-resistance session in youngmen, whereas the response in women may be minor(10, 21, 24, 45). The acute exercise-induced testoster-one response is usually lower in older than in youngermen (8, 21, 25). In the present study, no acute re-sponses were observed at pretraining in serum totaland free testosterone in our older women. This is inline with previous observations (21, 22). The same wastrue also after the 21-wk training period. It is alsounclear whether the lack of serum testosterone re-sponse in our older women in both loading conditions isa limiting factor in strength development or musclehypertrophy as seems to be the case for the low basalserum testosterone level (22).

It has been shown previously that the acute responseof GH to heavy-resistance loading is decreased due toaging both in men and especially in older women at theage of ;70 yr (21, 22). The present results showed thatthe loading at pretraining did result in some acuteincrease in GH, but it was not statistically significantbecause of large interindividual variation in the re-sponse (Fig. 9). However, it was physiologically inter-esting to observe that the individual acute changesnoted in GH at pretraining correlated with the individ-ual changes in maximal force during the latest trainingperiod of the 21-wk training. Second, after the 21-wktraining period the increase in serum GH concentra-tions in our older women at the age of 64 yr not onlywas significant immediately at postloading but alsoremained significant up to 30 min postloading. Becauseof the pulsatile nature of GH secretion, the interpre-tation of single measures must be done cautiously.However, the observation can be considered as an in-dication of the training-induced adaptation of theendocrine system showing that the acute GH hormoneresponse may become more systematic after strengthtraining even in older women. The magnitude and timeduration of the response may be important physiolog-ical indicators of training-induced anabolic adapta-tions.

In summary, the present progressive strength train-ing performed twice a week for 21 wk led to large gainsin maximal and explosive force production character-istics of the leg extensors in older women. The strengthgains were accompanied by significant increases in thevoluntary neural activation of the trained agonist mus-cles accompanied by significant enlargements in mus-cle fiber areas of types I, IIa, and IIb as well as in thetotal CSA of the trained extensor muscles. Interest-ingly, the increases in the CSA of the total QF took




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place throughout the Lf, but the magnitudes of theCSA increases along the Lf differed between the fourindividual muscles of the QF. The increases weregreater in the regions of the largest CSAs, at proximalportions for the VL and at distal portions for the VM,whereas this was not the case for the increases re-corded in the VI or RF muscles. No systematic changesoccurred in the basal concentrations of serum anabolicand catabolic hormones examined during the trainingperiod, but a low level of testosterone, especially inolder women, may be a limiting factor in overall train-ing-induced muscle hypertrophy. A systematic acuteexercise-induced increase of GH not only took place inolder women only after the 21-wk strength-trainingperiod immediately postloading but also it remainedsignificant further up to 15 and 30 min postloading. Itis possible that the magnitude of the acute GH hor-mone response as well as the time duration of theresponse are both important physiological indicators ofanabolic adaptations taking place during systematicprolonged strength training even in older women.

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