Muscle hypertrophy resistance training13

Joseph
Janet

with

large-scale
Afichael

weight
(1 Carlso,i.

loss and
Janes

E Donnelly,
E 14 hatley, and

Teresa
Richard

Sharp,

Joseph G Israel

Houmnard.

0 Hill,

ABSTRACT
restriction controversial. This muscle hypertrophy females received

The combined
on changes in body

effects
fat and

of exercise
fat-free mass

and

energy
are

groups groups. Thus. hypertrophy undergoing

used this

for exercise study could severe

is offset

by losses to determine by weight

from

other whether

muscle muscle

(FFM)

study was conducted to determine whether is possible during weight loss. Fourteen obese liquid diet for 90 d. Seven subjects

was conducted be produced energy restriction.

training

in subjects

a 3360-kJ/d

received a weight training (WT) regimen and seven subjects remained sedentary (C). Biopsy samples were obtained from the vastus lateralis muscle at baseline and after 90 d of treatment. The average weight loss over the 90-d period was 16 kg with 24% of the weight loss from FFM and 76% from fat. The amount fast twitch significantly and composition fibers was ofthe unchanged in WT weight loss did not differ between

Downloaded from www.ajcn.org by on September 27, 2006

Methods
Twenty-one energy training obese females participated in a 90-d trial of severe

restriction (C) (WT). Approval

or severe energy restriction plus weight from the Committee for the Protection and any informed contesting or parwere excluded any condition performance were assigned Seven subjects or for reasons in

WT and C groups.
increased

The cross-sectional
subjects.

area

of slow twitch
in C subjects that muscle loss.

and
but weight

by treatment

ofHuman sent from

Subjects ofVanderbilt University the subjects were obtained before had a medical disease or ifthey their health testing.

It appears

training can produce vere energy restriction Nutr 1993:58:561-5.

hypertrophy in skeletal and large-scale weight

during se.lmmz J (liii

ticipation. All subjects ifthey had metabolic that would jeopardize the subsequent to study did not groups complete

exam and exhibited The subjects

or hamper

physiological

KEY
ercise.

WORDS
severe energy

Muscle
restriction,

hypertrophy,
weight

weight
training

reduction.

ex-

at baseline by random selection. the study for personal reasons Characteristics group differed weight and

Table

of noncompliance. I . The WT in measures

of the subjects are shown in significantly from the C group body composition because of

of body

Introduction
Endurance shows equivocal exercise results combined for retention with Studies energy found severe energy mass restriction (FFM) over sefor ( 1 , 2)

the seven subjects who did not complete the study. The groups did not differ significantly on the major variables of interest, which were muscle fiber size and knee-extension strength.
Die/art Ireatmnent

of fat-free

severe energy restriction alone. vere energy restriction to severe with subjects endurance that used exercise severe have energy (3).

that have compared restriction in conjunction less decrease with in FFM exercise

All subjects Management formula

received Resources.

for 90 d a liquid-formula Boston) that contained 97 g carbohydrate,

diet (Health 3360 kJ/d. The 10 g fat, and

restriction

included

80 g protein.

or found no difference which the use ofendurance showed restriction Weight tensively prising shown that greater decreases

Furthermore, exercise with

there are severe energy with that has

studies in restriction energy been exI From the Human Performance Laboratory. University of Nebraska at Kearney: the Energy Balance Laboratory. and the Department of Medicine. Diabetes Research and Training Center, Vanderbilt University. Nashville: and the Human Performance Laboratory. East Carolina University. Greenville. NC. 2 Supported by Health Management Resources. Boston: The Kim

in FFM

compared

severe not

alone (4, 5). training is a mode studied because in subjects in conjunction maintenance that 5040 consume kJ/d

of exercise

with weight loss. This is suror increases in FFM have been a normal (7). Donnelly diet (6) and et al (3) in subjects previously with than suggest severe it could in muscle Society

consume

Dayani

Human

Performance

Center

and

the

General

Clinical

Research

used severe energy weight training and when that also severe the effects that Vutr energy with

restriction-2 found no restriction training

184 kJ/d-combined greater retention of FFM was used are not alone. This may with as evident However, ofFFM

of weight moderate any

as compared suggest
(ii,?

energy

restriction.

increase

or maintenance Printed in USA.

Center. Vanderbilt University, Nashville: and Research Services Council, University of Nebraska at Kearney. 3 Reprints not available. Address correspondence to IE Donnelly, Human Performance Laboratory, University of Nebraska at Kearney, Kearney, NE 68849. Received September 17, 1992. Accepted for publication April 15. 1993. for Clinical Nutrition
561

.4!?! .1

1993:58:561-5.

(c 1993 American

562 TABLE Baseline I characteristics

DONNELLY

ET

AL was were from measured Corp. body conducted density with St Louis). for a Med-Science Seven each subject. trial 505D Percent by using the Nitralyzer fat was the results averaged cal-

breathing of the subjects4 Weight training

(,i=7)

(Med-Science weighing culated equation

to 10 trials

of hydrostatic revised of the and

for each et al (8).

Control
(ii=7)

of Lohman

Subsequently,

Age (y) Weight (kg) Percent fat Fat-free mass (kg) Slow-twitch fibers (pm2)
Fast-twitch fibers (j.tm2)

36.3 105.7 48.5

54.3

8.9 15.7 2.7

44.4 89.7 44.9

49.4

9.8t 1 l.7t 3.91 7.31 1072 81 1 15.1

body-fat values that did not differ by > 1% were were used to represent the body fat of the subject.
Muscle biopsy.

lateralis

muscle

A muscle ofthe right

biopsy was obtained leg for each subject.

from the vastus A Bergstrom 5by

7.7 712 1024

4294
4160

4324
3713

mm canula was used with the aid of suction as described Evans et al (9). Samples were mounted in an OCT-Tragacanth Gum matrix (Sigma Chemical Co. St Louis) frozen isopentane and stored at -70 #{176}C liquid in nitrogen. were stained with the a-glycerophosphate technique cross-sectional 25 fast try to twitch determine area (Ff) was calculated fibers cross-sectional Sausalito, CA). strength, BP, that l-RM LAT, KE, tests and were KF. To measure exercises: from area 25 slow computerized (A UTOSKETCH twitch (1 1-1 3) with

Knee
4

extension

(kg)

58.3

22.3

43.4

#{149}: SD. t Significantly

in cooled Sections (10) and (ST) and

2.0;

different

from

control.

<

0.05.

digitome-

the recommended daily allowance of vitamins The diet was ingested at five scheduled times Subjects libitum tioned signed
Exercise

and during

minerals. the day.

AUTODESK,

Strength
pleted mine

testing.

comOne

were allowed to consume nonenergetic throughout the study. Adherence to the ifweight a weekly
program

beverages ad diet was queseach diet. subject

for the the greatest

following amount

RM was determined
time (14). A strength of the l-RM values as either the amount per kg FFM. The (Body Masters, for all training

by administering
ofweight

a series
could

of trials
be lifted

to deter-

Downloaded from www.ajcn.org by on September 27, 2006

loss was declaration

<

1 .4 kg/wk. Additionally. of adherence to the

a single

index (SI) was calculated by using the sum (BP+ LAT+ KE+ KF), and was expressed (in kg) lifted or the amount (in kg) lifted same stationary LA) was used weight-training for both l-RM equipment testing and

Subjects were given

who were randomly eight weight-training

assigned to the exercise exercises. The amount

condition of weight

Rayne, sessions.

each subject lifted was based on the results from the initial onerepetition maximum (1 RM) tests administered at baseline. Weight training was assigned at 70% of l-RM values for weeks 1-4 and the subjects performed three sets of exercises in the descending order training progressed of 8-6-6 repetitions. to 80% of l-RM During weeks 5-12, weight values and the subjects perorder of 8-6-6-4 for each training (LAT), knee arm pullover, training in 30-40 Wednesday, assistant. that each sessions, subjects The sesmm and resubject that exadhered

Statistical
Means tests were or to show

analisis
and used SDs were used to describe from variables. baseline to further Students groups the to show differences in changes were terms. calculated in variables between illustrate

differences

to 90 d. In some

formed four sets of exercises repetitions. The weight-lifting session were the bench press extension (KE), knee flexion biceps sions. and Friday training was curl, Each and triceps weight-training were direct

in the descending exercises used

instances, percentages data in more practical

(BP), lateral pull-down (KF), military press, throughout was completed program on Monday, of a research for verifying of the exercise and that the the session

Results
The amount and composition ofweight loss during treatment are shown in Figure

extension

1. Both

groups

preceded sessions under

by a 5-7-mm performed supervision

of stretching.

Weight-

body weight during treatment 4.7 kg for WT). Weight loss weight the total was nor 16.2% and 16.8% change relative

lost significant amounts of (1 7. 1 5.3 kg for C and 15.1

of baseline respectively. differed between body Neither C WT, weight

as a percentage

for C and in body

search assistant was responsible completed a minimum of 90% ercises were completed schedule. measures measures of treatment. were correctly,

and WT. between

Likewise, groups.

the composition Body-fat percentage of total weight loss

ofweight loss did not differ declined 6. 1 2.2% in The loss and of FFM 25% in in C subjects

WT

subjects

and
24%

5. 1 2. 1% in C subjects.

to the daily
Dependent Dependent the initiation

represented

WT subjects.
obtained All measures Center University. weighing body fat. testing at baseline were and taken 90 d from either Clinical volume was a Detecto reat Strength declined significantly significantly in WT subjects (Fig 13.3% less weight after treatment jects before. at residual Body weight by using were able to lift the change FFM, was 23.9% 0.05). 17.6% more (NS) subjects were in strength When in C subjects, but increased 2). C subjects were able to lift than before, whereas WT subweight was was after 5.4% were reported treatment in C subjects significant as a result than and expressed as kg lifted

the Dayani Human Performance Research Center of Vanderbilt Body was corded used composition. to determine to the nearest Hydrostatic percent

or the General

in strength for WT

per kilogram the increase group cases (P < weight-training differences

the decline in change

(P < 0.05).

The betweenin both of the

0. 1 kg before

Platform Scale (Webb City, MD), and underwater weight was recorded to the nearest 25 g with a Chatillion Autopsy Scale (Kew Gardens, NY). Residual lung volume was determined simultaneously nitrogen-dilution with hydrostatic technique. weighing Nitrogen by using a closed-circuit concentration during re-

No injuries program.

Because the muscle volved in KE, changes arately (Fig 2). Total

used for biopsy (vastus lateralis) was inin the 1 RM for KE were evaluated sepweight lifted during bilateral l-RM KE

MUSCLE
Body C Weight WI (kg) FFM (kg)

HYPERTROPHY
Fat (7.)

WITH
50

WEIGHT
1

LOSS
2.0 1.6

563

WT

WI 40 30 U, a 0)
C

#{176}II

T.#

1.2 0.6k

20 10
U

4) 0)
C

0 -C
0

0.4. 0.0 .e 0) -0.4

-0.8 (1)

0 0 C
0
In

.C -10

#{182} _____
C Strength
WI

0.

-1.2 -1.6 -2.0

WI

E
0 0
>%

WI

C St/kg FFM

cn
undergoing and lifted weight per

Index

Knee Extension

FIG 2. Changes
severe training fat-free within groups. maximum)

in strength
energy (WT: mass group,
ti

restriction kg (FFM). values. P

<

index (SI) from baseline to 90 d for subjects (C: n = 7) or severe energy restriction
7), expressed Changes
.

as weight in knee

lifted extension

and are

weight l-RM

(repetition

SD.

4Significantly
different

different
from

from

FIG 1. Body-weight and body-composition changes from baseline to 90 d for subjects undergoing severe energy restriction (C: n = 7) or severe energy restriction and weight training (WT: n = 7). . SD. 4Significantly different from baseline. P < 0.05.

Downloaded from www.ajcn.org by on September 27, 2006

baseline

0.05.

Significantly

baseline

between

<

0.05.

and and showed a nonsignificant 1 1 .0 groups

kg,

27.7%

increase

in muscle Some

fiber

cross-sectional have

area found

for ST pref-

FT fibers.

respectively.

investigators

decline P
<

during 0.05).

the

treatment

period

in

C subjects
(20. 1 between Results

(5.3 8.5 kg, or 9. 1%) and

or 36.8%; were also significant area

increased in WT subjects The changes in 1 RM

erential hypertrophy 20): however, others hypertrophy young men reported for FT et al(22) and 27.6% in response increases fibers.

in FT fibers compared with ST fibers (19, have not. Ewing et al (2 1 ) found greater than men one in FT over fibers fibers (17.1% training. compared no effect vs 10.2%) Frontera training with of 22 in to 10 wk ofisokinetic in ST At least of 33.5% shows

in ST fibers studied 12 elderly

(P

< 0.05).

for cross-sectional

of muscle

fibers

are

shown

in

12 wk ofstrength

Figure

3. Neither

ST or FT fiber area changed

significantly

with

treatment in C subjects: however, both ST and FT cross-sectional fiber area increased significantly (P < 0.05) in WT subjects (1 162 1265 zm2 for ST and 1 344 1 335 tm2 for FT). The difference in ST cross-sectional fiber subjects was not statistically difference nificant (P in FT cross-sectional < 0.05). area of 774 significant fiber zm2 between (P = 0. 10): area C and however, WT the sig-

report

of I 03 1 zm2 was

(I,

C 0

Discussion
These fiber training position agrees kJ/d) weight amount when males concurrent results with indicate during declines that weight training of severe weight can energy and FFM. elicit musclerestriction Weight

C)

hypertrophy

periods of body

a
a)

had no overall of the weight with earlier combined training of weight compared (3).

effect on total weight loss or the comloss between C and WT. This finding energy restriction or in conjunction neither affected of the weight alone in obese (2184 with the loss fea) 0
U-

findings in that severe with weight training and loss with endurance nor the energy exercise composition restriction

Others have demonstrated muscle ing weight training in conjunction

hypertrophy with normal 5040 fiber showed kJ/d kg (7). The body-weight

in subjects usenergy intakes energy current intake study area 21.7% FIG 3. Changes
to 90 d for severe nificantly different energy from subjects restriction from baseline different

( 1 5- 1 8), or in subjects
and had a moderate that in humans. simultaneously
kg

who weight

received loss of 3.89 in muscle

in muscle
undergoing and between

fiber cross-sectional
severe weight within groups. energy group. training (WT:

area from
restriction
,i =

baseline
(C:

(B)

z = 7) or

demonstrates can occur of 1 5. 1

increases with The

cross-sectional a significant

7). .

SD. 4SigSignificantly

large-scale group

reductions

baseline

P
0.05.

<

0.05.

WT

<

564

DONNELLY of strength on muscle (23). ofsubject Much training fiber of this or strength training area may ofprior plus for either be due physical endurance ST or FT to the vast training,

ET

AL The ofST restriction However, results and indicate FT muscle with that fibers weight during of these declines training periods findings of body can weight elicit and await of en-

wk fibers array

unknown. hypertrophy energy FFM.

training

cross-sectional discrepancy history protocols, Additionally, response

of severe

concurrent the clinical

characteristics,

significance

and experimental training meaningful comparisons. are wide training The variations in animals mechanisms in the (24) for

which do not always provide it is recognized that there of muscle fibers to strength hypertrophy weight loss hypertrofasting acid in rats. transport, of to

the results of long-term trials using ergy restriction and weight-training

various combinations regimens. Lange, Sam Ewing, for their assistance

El
Zafer with

and in humans (13). increases in muscle-fiber with studied muscle to enhance concomitant work-induced during amino

We thank Cindy Vigil, Lira Martinez, Dan Karabulut, Ding Lin, and Martha Butterfield laboratory testing and medical management.

during severe energy are unclear. Goldberg phy of the soleus activity protein muscles activity and Muscular decrease working muscular during muscles. the

restriction et al (25) plantaris appeared

References
JO. Sparling PB, Shields TW, Heller PA. Effects ofexercise and food restriction on body composition and metabolic rate in obese women. Am I Clin Nutr 1987;46:622-30. 2. Pavlou KN, Steffee WP, Lerman RH, Burrows BA. Effects of dieting and exercise on lean body mass, oxygen uptake, and strength. Med
1. Hill Sci Sports Exerc l985;17:466-71.

catabolism. to catabolic may override

and decrease the sensitivity hormones. These adaptations the signals for muscular wasting thus selectively sparing working ofworking muscles may explain vastus lateralis muscle, which total

nutrient deprivation, This selective sparing seen in the

3. Donnelly
composition Nutr 4. Krotkiewski

JE, Pronk
and

NP, Jacobsen
diet and metabolic L, Bjorntorp

DI, Pronk
physical rate training

SI, Jakicic
regimens females. effect and IM,

hypertrophy

was FFM

of a very-low-calorie resting 1991:54:56-61. M, Toss

IM. Effects on body

Am ofa I Clin

exercised in the weight-training group even though declined. The exercise program also resulted in a significant overall strength (SI), as measured by the total amount lifted agree sistent trained, period from or the total with with previous the weight results report by obese energy also consistent a normal training in the lifted from Ballor per kilogram Donnelly and Katch FFM. (26) strength findings is known

in obese

Downloaded from www.ajcn.org by on September 27, 2006

increase in of weight These that results are conweightduring a for 1 RM regarding a

P. Holm

G. The

very-

low-calorie diet with sex hormones. plasma

concentrations 5. Hammer RL, Barrier

and without
proteins, women. CA. Roundy

chronic
uptake, ES, Int I Obes

exercise
insulin

on thyroid

and

oxygen

C peptide Fisher AG.

et al (3) and

in obese

198 1:5:287-93.

Bradford

moderately of moderate KE were receive weight (NS)

females increased restriction. The with what diet or moderate (6, 7). Subjects amount

subjects that and undergo small reduction

<

energy restriction from C showed lifted, whereas

Calorie-restricted low-fat diet and exercise in obese women. Am I Clin Nutr 1989:49:77-85. 6. Fleck SI, Kraemer WI. Resistance training: physiological responses and adaptations. Phys Sports Med 1988:16:108-24. 7. Ballor DL, Katch VL. Becque MD. Marks CR. Resistance weight
training during calorie restriction enhances lean body weight

of weight

the subjects values (P weight

23. 27).

from WT showed an increase of 0.05). Other investigators have of 1 3-50% in response to weight

37% from baseline shown increases in training ( 1 5, 17,

maintenance. Am I Clin Nutr l988;47:l9-25. 8. Lohman TG, Slaughter MH, Boileau RA. Bunt I, Lussier L. Bone mineral measurements and their relation to body density in children,
youth and adults. Hum sample Biol size. 1984:56:667-79.

lifted

9. Evans
biopsy
.)

Wi.

Phinney

SD. Young

YR.
Med

Overall strength despite no change found area decreases in obese in

declined in muscle 1-RM after for

in group C during weight reduction cross-sectional area. Ballor et al (7) BP with moderate decreases no change energy in strength in muscle-bone restriction. without The de-

maximizes

Suction Sci Sports

applied to a muscle Exerc 1982:14:10 1-

females responsible

mechanisms

dines in muscle cross-sectional area or muscle and bone area during severe and moderate energy restriction are uncertain. Nutritional deprivation has been shown to increase intracellular muscular increased biochemical malnourished tion, include hydrogenase, and calcium muscular concentrations fatigue and which (28), which are associated slower relaxation (29). with Other fed or funcde(30) may

10. Wattenberg LW. Leong IL. Effects ofcoenzyme Qio and menadione on succinate dehydrogenase activity as measured by tetrazolium salt reduction. I Histochem Cytochem I 960:8:296-303. I 1 . Tesch PA. Thorsson A, Essen-Gustavson B. Enzyme activities of Fr and ST muscle fibers in heavy-resistance trained athletes. I AppI
Physiol 1989:67:83-7.

12. Coyle

abnormalities humans, a decline acyl CoA

found with hypoenergetically may adversely affect muscle and these succinate glycogen factors

EF. Feiring DC, Rotkis TC. et al. Specificity of power improvements through slow and fast isokinetic training. I Appl Physiol 198 1:5 1: 1437-42. 13. Simoneau IA, Bouchard C. Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am I Physiol 1989;257:
E567-72.

in phosphofructokinase, dehydrogenase (28), water (3 1). Although speculative during

14. Wilmore
iological

IH, Costill
basis of the

DL. Training
conditioning

for sport
process.

and activity:
3rd ed.

the physIA:

Dubuque,

a rise in intracellular

be plausible
the diet-only not measured It has also

explanations
group, in the been they suggested present

for the decrease

are only study. that

in strength
because

found
they

in
were

nutritional

deprivation the fibers

there is selective atrophy present results showing would declines The restriction not support this

of FT fibers (28, no change in both hypothesis for explaining

32): however, ST and FT muscle were with studied. severe remains

strength energy largely

1988. 15. Sale DG, Jacobs I, MacDougall ID, Garner S. Comparison of two regimens of concurrent strength and endurance training. Med Sci Sports Exerc 1990:22:348-56. 16. MacDougall ID. EIderGCB, Sale DG, Moroz JR. Sutton JR. Effects of strength training and immobilization on human muscle fibers. Eur I AppI Physiol 1980:43:25-34. 17. Fontera WR, Meredith CN, OReilly KP, Evans WI. Strength training and determinants of V,,_ in older men. I AppI Physiol 1990:68:

WC Brown,

in the groups of obese females that use ofweight training in conjunction is relatively new and the clinical

utility

329-33. 18. Gollnick PD, Armstrong RB, Saltin WL, Shepard RE. Effect of training

B, Saubert

CW,
activity

Sembrowich
and fiber

on enzyme

MUSCLE
composition of human skeletal muscle.

HYPERTROPHY
1973:34:107-

WITH
26. Ballor
by

WEIGHT
DL. Katch

LOSS
VL. Strength
restriction.

565
gains in obese
Eur I

I AppI Physiol

females
Appl

are unaffected
1989;59:

moderate

dietary

Physiol

19. Tesch PA, Karlsson I. Muscle fiber types and size in trained and untrained muscles of elite athletes. I Appl Physiol 1985;59: 1716-20. 20. Alway SE, Grumby WH, Gonyea WI, Stray-Gundersen I. Contrasts in muscle and myofibers of elite male and female bodybuilders. I Appl Physiol 1989:67:24-3 1. 21. Ewing JL, Wolfe DR, Rogers MA, Amundson ML, Stull GA. Effects of velocity of isokinetic training on strength, power, and quadriceps muscle fibre characteristics. Eur I AppI Physiol 1990:61:159-62. 22. Frontera WR, Meredith CN, OReilly KP, Knuttgen HG, Evans WI. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. I Appl Physiol 1988;64:1038-44. 23. Sale DG, MacDougall ID, Jacobs I, Garner S. Interaction between concurrent strength and endurance training. I AppI Physiol 1990:68: 260-70. 24. Mikesky AE, Giddings CI. Matthews W, Gonyea WI. Changes in muscle fiber size and composition in response to heavy-resistance exercise. Med Sci Sports Exerc 1991;23: 1042-9. 25. Goldberg AL, Etlinger ID, Goldspink DF, lablecki C. Mechanism of work-induced hypertrophy of skeletal muscle. Med Sci Sports I 975:7:248-61.

35 1-4.

27. Cureton K, Collins MA, Hill DW, McElhannon FM. Muscle hypertrophy in men and women. Med Sci Sports Exerc 1988:20:33844. 28. Russell DM, Walker PM, Leiter LA, et al. Metabolic and structural changes in skeletal muscle during hypocaloric dieting. Am I Clin
Nutr 1984:39:503-13.

29.

Russell DM, Leiter LA, Whitwell I, Marliss EB, Jeejeebhoy KN. Skeletal muscle function during hypocaloric diets and fasting: a comparison with standard nutritional assessment parameters. Am

I Clin Nutr
30. Jacobs glycogen Physiol 3 1 . Russell

1983;37:133-8.
P. Tesch in P. Muscle human strength skeletal and muscle fatigue fibers. after Eur selective I AppI

I. Kaiser depletion

1981:46:47-53.

DM, Prendergast P1, Darby PL, Garfinkel PE, Whitwell I, Ieejeebhoy KN. A comparison between muscle function and body composition in anorexia nervosa: the effect of refeeding. Am I Clin
Nutr 1983:38:229-37.

32. Lopes I. Russell DM. Whitwell I, Jeejeebhoy. Skeletal tion in malnutrition. Am I Clin Nutr 1982:36:602-10.

muscle

func-

Downloaded from www.ajcn.org by on September 27, 2006