long-term creatine supplementation improves muscular performance during resistance training in older...
TRANSCRIPT
ORIGINAL ARTICLE
Long-term creatine supplementation improves muscularperformance during resistance training in older women
Andreo Fernando Aguiar • Renata Selvatici Borges Januario • Raymundo Pires Junior •
Aline Mendes Gerage • Fabio Luiz Cheche Pina • Matheus Amarante do Nascimento •
Carlos Roberto Padovani • Edilson Serpeloni Cyrino
Received: 10 April 2012 / Accepted: 25 September 2012 / Published online: 7 October 2012
� Springer-Verlag Berlin Heidelberg 2012
Abstract This study examined the effects of long-term
creatine supplementation combined with resistance training
(RT) on the one-repetition maximum (1RM) strength,
motor functional performance (e.g., 30-s chair stand, arm
curl, and getting up from lying on the floor tests) and body
composition (e.g., fat-free mass, muscle mass, and % body
fat using DEXA scans) in older women. Eighteen healthy
women (64.9 ± 5.0 years) were randomly assigned in a
double-blind fashion to either a creatine (CR, N = 9) or
placebo (PL, N = 9) group. Both groups underwent a
12-week RT program (3 days week-1), consuming an
equivalent amount of either creatine (5.0 g day-1) or pla-
cebo (maltodextrin). After 12 week, the CR group
experienced a greater (P \ 0.05) increase (D%) in training
volume (?164.2), and 1RM bench press (?5.1), knee
extension (?3.9) and biceps curl (?8.8) performance than
the PL group. Furthermore, CR group gained significantly
more fat-free mass (?3.2) and muscle mass (?2.8) and
were more efficient in performing submaximal-strength
functional tests than the PL group. No changes (P [ 0.05)
in body mass or % body fat were observed from pre- to
post-test in either group. These results indicate that long-
term creatine supplementation combined with RT improves
the ability to perform submaximal-strength functional tasks
and promotes a greater increase in maximal strength, fat-
free mass and muscle mass in older women.
Keywords Aging � Creatine � Resistance training �Ergogenic aid � Muscle strength
Introduction
Age-related sarcopenia leads to declining muscular
strength, power, and endurance and results in an impaired
ability to perform daily activities and may ultimately cause
dependence and disability in older adults (Hunter et al.
2004). Several strategies (e.g., hormone replacement ther-
apy, nutritional intervention, and resistance training) have
been used to attenuate the progressive loss of muscle mass
and function that occurs in concert with biological aging
(for review, see Doherty 2003; Fujita and Volpi 2004).
Among these strategies, resistance training (RT) is the most
suitable intervention aimed decreasing the deleterious
effects of sarcopenia (Hunter et al. 2004). For example,
Yarasheski et al. (1995) reported an increase in mixed
muscle protein synthesis (*50 %) and muscle strength in
older men (65–75 years) after 16 weeks of progressive RT.
Communicated by Michael Lindinger.
A. F. Aguiar (&) � R. S. B. Januario � R. P. Junior
Center of Biological and Health Sciences, North University
of Parana (UNOPAR), Avenue Paris, 675 Jardim Piza,
Londrina, PR 86041-120, Brazil
e-mail: [email protected]
R. S. B. Januario � A. M. Gerage � F. L. C. Pina �M. A. do Nascimento � E. S. Cyrino
Group of Study and Research in Metabolism, Nutrition,
and Exercise, Londrina State University (UEL), Londrina, Brazil
A. M. Gerage
Department of Physical Education, Centre of Sport,
Santa Catarina Federal University, Florianopolis, Brazil
M. A. do Nascimento � E. S. Cyrino
Department of Physical Education, Centre for Physical
Education and Sports, Londrina State University (UEL),
Londrina, PR, Brazil
C. R. Padovani
Department of Biostatistics, Sao Paulo State University
(UNESP), Botucatu, SP, Brazil
123
Eur J Appl Physiol (2013) 113:987–996
DOI 10.1007/s00421-012-2514-6
These authors in a later study also reported increased force
production and mixed protein synthetic rate in the vastus
lateralis muscle of 76- to 92-year-old women and men after
3 months of progressive RT [3 days week-1 at 65–100 %
of one-repetition maximal (1RM)] (Yarasheski et al. 1999).
These findings are consistent with other studies that dem-
onstrated an increase in the muscle strength and fat-free
mass of older adults who underwent progressive RT
(Charette et al. 1991; Campbell et al. 1994). Furthermore,
previous studies have observed 20 to 62 % increases in
muscle fiber hypertrophy among older adults after
9–52 weeks of conventional RT (e.g., 2–3 days week-1)
(Bamman et al. 2003; Trappe et al. 2001; Charette et al.
1991; Newton et al. 2002; Taaffe et al. 1996).
While there is no question that RT is a suitable strategy
for attenuating the progressive loss of muscle mass and
strength associated with the natural aging process,
adjunctive strategies to augment these effects may enhance
the overall efficacy of strength training interventions. In
this context, creatine (Cr) supplementation has been iden-
tified as a potent ergogenic aid to prevent the loss of muscle
mass and strength that occurs with aging. Long-term Cr
supplementation ([12 weeks) combined with RT increases
strength and power, enhances fatigue resistance, and
increases fat-free mass in older men (Chrusch et al. 2001).
Additionally, several studies have found beneficial effects
of short-term Cr supplementation on the performance of
daily activities in older adults (Gotshalk et al. 2002, 2008;
Canete et al. 2006). Canete et al. (2006) reported a 12 %
reduction in time required to complete the sit-stand test in
older women (67 years) following 7 days of Cr supple-
mentation (0.3 g kg-1 day-1). Similarly, Gotshalk et al.
(2002, 2008) found reductions in time required to complete
the sit-stand and tandem gait tests in older men (6–9 %
reduction) and women (5–7 % reduction), following 7 days
of Cr supplementation (0.3 g kg-1 day-1). These studies
and many others (Stout et al. 2007) demonstrate that acute
(*7 days) Cr supplementation has the potential to enhance
muscle function (e.g., daily tasks, 1RM strength, and fati-
gue resistance), increase fat-free mass and, potentially,
improve the performance of daily tasks in older adults.
However, it is unclear whether the ergogenic effects of
long-term Cr supplementation combined with RT also
occur specifically in older women.
Based on the positive findings of previous studies
involving acute (*7 days) Cr supplementation, we
hypothesized that long-term Cr supplementation combined
with RT would promote additional beneficial effects on
body composition (e.g., increased fat-free mass and muscle
mass) and muscle strength (e.g., increased 1RM and
functional strength) beyond what is observed with training
alone. Despite an abundance of studies, only one study on
long-term Cr supplementation (8 weeks) in older adults has
included women as subjects (Bermon et al. 1998), and the
authors failed to found any additional beneficial effect of
Cr supplementation on body composition and several
measurement of muscle performance. Failure to detect a
statistically significant effect of Cr supplementation on
performance in older adults may partially be attributed to
insufficient reliability of testing protocols (Bermon et al.
1998). Gotshalk et al. (2008) argue that several (five or
more) familiarization sessions are critical to establish a
control for day-to-day variability and the reliability of
maximal effort performances in order to detect a small
(5–10 %) effect of Cr supplementation in older women.
The present investigation is the first who applied a long
resistance training period (12 weeks) following several
(six) familiarization sessions before the randomization.
This approach can avoid any learning bias and hence
ensures a high reliability of maximal effort performances to
detect statistically significant effects of Cr supplementation
in older women. Furthermore, this is the first study that
attempted to examine the effects of long-term Cr supple-
mentation combined with RT on muscle strength and body
composition in exclusively older women.
Methods
Experimental approach
A randomized, double-blind and placebo-controlled design
with repeated measures was employed to create two groups
(Placebo, N = 9; Creatine N = 9) (Fig. 1). Initially, all
subjects completed six familiarization sessions to receive
instruction on proper techniques and to practice the one-
repetition maximal (1RM) and functional testing protocols
(30-s chair stand, arm curl, and getting up from lying on the
floor tests). Subsequently, all participants underwent a
12-weeks RT program (3 days week-1) to obtain similar
physical fitness levels with regard to muscle performance.
The training regimen aimed to work all the major muscle
groups (e.g., pectoralis, latissimus dorsi, biceps, triceps,
quadriceps, gastrocnemius, and abdominals). After this
initial 12-weeks phase, the subjects were matched
according to age, body mass, and 1RM performance and
then randomly assigned in a double-blind fashion to a
Creatine (CR) or Placebo (PL) group, and they continued
an additional 12 weeks of continuous RT (3 days week-1)
while consuming their appropriate supplements (Fig. 1).
The RT program was designed in accordance with the
ACSM Position Stand guidelines on exercise and physical
activity for older adults (Chodzko-Zajko et al. 2009). To
examine the effects of Cr supplementation on muscle
strength and body composition, both the CR and PL groups
completed a battery of 1RM tests, upper- and lower body
988 Eur J Appl Physiol (2013) 113:987–996
123
functional tests, and body composition measurements on
two separate occasions (pre- and post-training program);
the upper- and lower body 1RM tests were performed
alternately to minimize the effects of fatigue. All tests were
performed on the same place, between 2 and 5 pm. We
used a two-group design because of potential problems
with a within-subjects (cross-over) experimental approach
in Cr supplementation studies that examine physical per-
formance. Furthermore, cross-over design studies can be
influenced by the differences in dietary Cr intake and
intersubject variability in Cr accumulation and depletion.
We ensured that the experimental approach used in the
present study would provide an effective way to investigate
the effects of Cr supplementation during long-term RT on
the muscle strength and body composition of older women.
Subjects
Health, nonathletic, women older than 60 years were
invited to attend a meeting aimed at explaining the purpose
and details of the study protocol. To be qualify as partic-
ipants, the women were required to (1) not be vegetarian,
(2) be aged between 60 and 80 years, (3) have not ingested
any ergogenic supplement for the previous 6 months before
the start of study, (4) have not ingested any medication that
could affect muscle growth or the ability to train intensely
during the study, (5) not be involved in the practice of
systematized physical activity (i.e., 2–3 days week-1) for
the previous 6 months before the start of study, (6) have a
detailed description of their lifestyle and daily food intake,
and (7) have medical approval for the practice of physical
exercise. Eighteen women (64.9 ± 5.0 years) who met
these criteria volunteered to participate in the study. After
baseline assessments, the subjects were matched for 1RM
performance in three weight lifting exercises (see strength
assessments) and were then randomly assigned in a double-
blind fashion to either a CR (N = 9) or PL (N = 9) group.
The physical characteristics of the CR and PL groups at
baseline are presented in Table 1. All subjects were
informed of the purpose, procedures and possible risks of
the investigation before they gave written informed consent
to participate in the study. All procedures involved in this
investigation were approved by the Human Research Eth-
ics Committee of the University (project no: 4743; protocol
no: 21750/2006) and were in accordance with the 1964
Declaration of Helsinki.
Resistance training program
The 12 weeks RT program focused on all of the major
muscle groups (e.g., pectoralis, latissimus dorsi, biceps,
triceps, quadriceps, gastrocnemius, and abdominals) and
was designed specifically to increase strength and muscle
size. The RT consisted of eight whole-body exercises pri-
marily using exercise machines (Bad Boy Gym equipment,
Sao Paulo, Brazil), and the exercises were performed in the
following order: (1) vertical bench press, (2) lat pulldown,
(3) biceps curl, (4) triceps pushdown, (5) knee extension,
(6) leg curl, (7) seated calf raise, and (8) abdominal crunch.
Both the CR and PL groups trained under the same training
protocol (3 days week-1; 2 sets of 10–15 repetitions with
60- and 120-s rests between the sets and exercises,
respectively) during the 12-weeks RT program; the only
exceptions were the exercises for the calf (15–20 repeti-
tions) and abdominal muscle groups (20–30 repetitions
with no additional overload) muscle groups. Each training
session began with stretching exercises for whole body.
Qualified personnel supervised individually each partici-
pant during every workout. Each subject received a training
logbook, in which the researchers recorded the weekly
Fig. 1 Experimental design
Eur J Appl Physiol (2013) 113:987–996 989
123
training load (weight) used for each exercise. The training
load was adjusted weekly, based on the number of repeti-
tions performed at the end of the second set of each
exercise. Specifically, 1 kg-load was added every one
(lower extremity) or two (upper extremity) repetitions that
exceeded the 15 repetitions of second set of each exercise.
The training volume (weight 9 sets 9 repetitions) was
progressive throughout the training program, and each
participant was able to complete 15 repetitions on the
second set of each exercise. At the end of each session,
approximately 5 min were used for stretching the exercised
muscles on the RT session. The total time of one training
session for each participant was approximately 60 min and
remained the same throughout the 12-weeks training pro-
gram. Sessions were performed between 6 and 11 am. The
1RM and functional fitness tests and the body composition
assessments occurred during the weeks before and after the
RT program.
Maximal dynamic strength
The bench press, knee extension and biceps curl strength
were assessed using a 1RM standard testing procedure
before and after the 12-weeks RT program. A recognized
1RM testing protocol and exercise execution guidelines
were followed, as previously documented (Baechle and
Earle 2008). Briefly, attempts of 1RM with progressively
increasing load were performed with each attempt sepa-
rated by 3- to 5-min rest intervals. Each test exercise was
separated with a 5-min rest break. 1RM was defined as the
greatest load lifted through a full range of motion before
two failed attempts at a given load. Before begin test, the
participants were kept at rest while received guidance from
the instructors, and verbal encouragement was provided
during all 1RM attempts. The reproducibility of the
strength measurements was determined on 8 subjects,
2 weeks apart. The intraclass correlation coefficient
(R) and coefficient of variation (CV) for the 1RM tests
were bench press: R = 0.99, CV = 2.5 %; biceps curl:
R = 0.98, CV = 2.8 %; and knee extension: R = 0.96,
CV = 3.2 %.
Upper- and lower body functional tests
To assess the upper- and lower extremity functional per-
formance, the 30-s chair stand and arm curl tests (Rikli and
Jones 1999a, b) and a test of getting up from lying on the
floor (Kuriansky and Gurland 1976) were performed before
and after the 12-weeks RT program. Briefly, to test the
ability to rise from a chair without using the arms (30-s
chair stand test), a straight-backed chair without arms
(40 cm high) was used. The test began with the participant
seated in the middle of the chair, back straight and feet flat
on the floor, with the arms folded across the chest. The
subjects were instructed to rise to a full standing position
and then return to a fully seated position to complete as
many full stands as possible within the 30-s time limit. The
arm curl test was performed to assess the upper body
strength. The test began with the participant seated on a
chair, back straight and feet flat on the floor, with the
dominant side of the body close to the side edge of the
chair. A 5 lb dumbbell was held at the side in the dominant
hand (handshake grip), with the arm down beside the chair,
perpendicular to the floor. At the signal ‘‘go,’’ the subject
turned the palm up while curling the arm through a full
range of motion and then returned to the fully extended
position. The subjects were encouraged to execute as many
curls as possible within the 30-s time limit. Both the 30-s
chair stand and arm curl tests were performed after a
demonstration by the examiner, and a practice trial of three
repetitions for each participant checked for proper tech-
nique. The test to get up from lying on the floor was per-
formed to assess the ability to rise from the floor using the
arms. The test began with the participant lying on a mat in
the dorsal decubitus position, with the arms extended
beside the body and the legs extended. At the signal ‘‘go,’’
the subjects were encouraged to rise from the floor as
quickly as possible to a full standing position on a line
marked 40 cm in front of the mat. Three trials were con-
ducted, and the fastest time was recorded. Before begin
each test, the participants were kept at rest while received
guidance from the instructors. A digital stopwatch con-
trolled by a technician was used for timing.
Creatine supplementation
After baseline testing, the CR group began consuming
creatine monohydrate (Phosphagen, EAS, Inc., Golden,
CO, USA) in capsules (5.0 g day-1; once per day), while
Table 1 Baseline characteristics
Creatine (N = 9) Placebo (N = 9)
Age (years) 64 ± 4 65 ± 6
Body mass (kg) 60 ± 9 57 ± 7
Height (cm) 156 ± 5 156 ± 6
Fat-free mass (kg) 35 ± 2 35 ± 4
Fat mass (kg) 25 ± 7 22 ± 6
Body fat (%) 41 ± 6 39 ± 7
1RM bench press (kg) 29 ± 5 29 ± 5
1RM biceps curl (kg) 17 ± 2 17 ± 2
1RM knee extension (kg) 26 ± 2 26 ± 5
Values are mean ± SD
There were no differences between the groups
1RM one repetition maximum
990 Eur J Appl Physiol (2013) 113:987–996
123
the PL group ingested an identical-looking and equivalent
amount of the placebo, maltodextrin (NeoNutri, MG,
Brazil), during the 12-weeks RT program. To ensure the
double-blind design, an individual who was not involved in
the study was responsible for placing the supplements into
bags and labeling the capsules with the subjects’ names
according to the randomization list. The Cr dose was
chosen based on previously reported intakes by older adults
(Brose et al. 2003; Eijnde et al. 2003). All subjects con-
sumed their supplement capsules dissolved in a carbohy-
drate (CHO) drink immediately after the training session,
as has been previously demonstrated to increase muscle
creatine accumulation (Green et al. 1996a, b) and achieve
optimal muscle adaptation (Cribb and Hayes 2006;
Esmarck et al. 2001).
Nutrient intake
Under the supervision of nutritionists, the subjects com-
pleted 3-day dietary intake records (including 1 weekend
day) before and after the 12-weeks RT program; standard
portions were used to assess the amount of food and drink
consumed. The total energy intake and macronutrient
amounts were calculated using software for nutritional
assessment (Avanutri, version 3.1.4, Rio de Janeiro-RJ,
Brazil). Participants were instructed to maintain their
habitual daily diet but to avoid caffeinated products (e.g.,
coffee, chocolate, mate, guarana, Coca-Cola, and energy
drinks) because caffeine appears to eliminate the effect of
Cr (Vandenberghe et al. 1996). Water intake was ad libi-
tum. The participants were also instructed to report in the
dietary records any adverse events from the supplements
on their health status. No adverse events were reported by
the participants.
Body composition
Total fat-free mass, fat mass and the percentage body fat
were determined using dual-energy X-ray absorptiometry
(DEXA) with a Lunar Prodigy (model GE PRODIGY—
LNR 41.990, GE Medical Systems, Madison, WI, USA).
The same licensed operator performed whole-body scans
on the same apparatus. The quality control calibration and
scanning procedures were performed according to the
manufacturer’s instructions. Participants were scanned at
the same time of day (i.e., in the morning) in a fasted state.
The appendicular lean tissue mass (ALTM) was deter-
mined by summing the lean tissue from the upper- and
lower body extremity. The ALTM values were converted
to muscle mass (MM) using the equation proposed by Kim
et al. (2004), where MM (kg) = 1.19 9 ALTM - 1.65.
For longitudinal studies in which relatively small changes
in body composition need to be detected, whole-body
scanning with this instrument has been demonstrated to be
accurate and reliable (coefficient of variation 0.8–2.8 %)
(Prior et al. 1997). The reproducibility of the DEXA was
determined on 7 subjects, 2 weeks apart. The intraclass
R for fat-free mass and fat tissue mass was 0.98, and the
CVs were 0.86 % for fat-free mass and 1.5 % for fat mass.
Statistical analyses
Statistical analyses were performed using SPSS statistical
analysis software (SPSS version 13.0; Chicago, IL, USA).
To ensure data reliability, the statistical procedures were
performed after the preliminary study of the variables
related to the normality and equality of variance between
groups, with a statistical power of 80 % for the compari-
sons assessed. The percent change (D%) in the maximal
strength and training volume between groups was analyzed
using a two-tailed unpaired t test (Zar 1999). A two (group:
creatine and placebo) 9 two (time: pre- and post-test)
repeated measures ANOVA (Johnson and Wichern 2002)
was used to evaluate the data across time and between
groups. When significant differences were confirmed with
ANOVA, multiple comparisons testing was performed
using Bonferroni post hoc analysis to identify these dif-
ferences. The level of significance was set at P B 0.05.
Data are expressed as the mean ± SD.
Results
Participant characteristics
All participants (CR, N = 9; PL, N = 9) who began the
12-weeks RT program completed the study. The baseline
characteristics of the subjects are presented in Table 1.
Both the CR and the PL groups had similar (P [ 0.05)
baseline physical characteristics. In addition, no significant
(P [ 0.05) differences in the daily dietary intakes were
Table 2 Dietary analyses
Creatine (N = 9) Placebo (N = 9)
Carbohydrate (%)
Pre 67.1 ± 7.8 66.5 ± 5.3
Post 66.7 ± 7.6 65.1 ± 6.2
Protein (%)
Pre 19.5 ± 5.4 20.4 ± 5.1
Post 19.6 ± 5.1 21.1 ± 4.7
Fat (%)
Pre 13.4 ± 4.1 13.1 ± 1.7
Post 13.7 ± 4.4 13.7 ± 2.6
There were no differences between the groups
Eur J Appl Physiol (2013) 113:987–996 991
123
observed between the groups before and after the 12-weeks
intervention period (Table 2).
Maximal dynamic strength
The 1RM for each group is presented in Fig. 2. Significant
group-by-time interactions indicated that the delta change
in 1RM strength for the bench press (D%, CR: 14.3 ± 6.7
vs. PL: 9.2 ± 4.4, P \ 0.05), knee extension (D%, CR:
8.6 ± 2.7 vs. PL: 4.7 ± 1.8, P \ 0.05), and biceps curl
(D%, CR: 22.3 ± 7.1 vs. PL: 13.5 ± 3.9, P \ 0.05) were
significantly greater in CR group compared to PL group.
Training volume
A significant group 9 time interaction was observed for
training volume (Fig. 3). The percent change (D%) in the
training volume during the intervention period was more
than twofold greater (P \ 0.01) in the CR group
(294.1 ± 85.8 %) than the PL group (129.9 ± 52.4 %).
The number of sets and repetitions was similar between the
CR and PL groups, so the only difference between the
groups was the training load (weight lifted). The results
indicate that the CR group was able to lift more weight
than the PL group within the same training regimen.
Upper- and lower body functional performance
The functional performance for each group is illustrated in
Fig. 4. Both the CR and PL groups demonstrated a sig-
nificant (P \ 0.01) improvement in the 30-s chair stand
and arm curl (increased number of repetitions) tests and a
greater ability to get up from lying on the floor (decreased
time) from pre- to post-test. Significant group-by-time
interaction indicated that the CR group was 18.7, 10.2, and
10.7 % more efficient (P \ 0.01) in the 30-s chair stand,
arm curl, and getting up from lying on the floor tests at
post-test than PL group.
Body composition
The body mass and body composition are presented in
Table 3. Significant group-by-time interactions indicated
that the CR group gained significantly more fat-free mass
(D%, CR: 3.2 % vs. PL: 0.0 %; P \ 0.01) and muscle mass
(D%, CR: 3.7 % vs. PL: 0.9 %; P \ 0.01) than the PL
group. The body mass, fat mass, and percentage body fat
values were unchanged for the CR and PL groups from pre-
to post-test.
Discussion
To our knowledge, this study the first that has exclusively
examined the effects of long-term Cr supplementation
combined with RT on muscle strength and body compo-
sition in older women. Based on a previous finding
that indicated an ergogenic effect of short-term Cr
Fig. 2 Delta change in one repetition maximum (1RM) bench press
(upper panel), knee extension (middle panel), and biceps curl (lowerpanel) after 12 weeks of resistance training in the creatine and
placebo groups. D% = (pre-post/pre) 9 100. aP \ 0.05 compared to
placebo group
Fig. 3 Percent change (D%) in the training volume after 12 weeks of
resistance training in the creatine and placebo groups. D% = (pre-
post/pre) 9 100. aP \ 0.01 compared to the placebo group
992 Eur J Appl Physiol (2013) 113:987–996
123
supplementation in older women (Gotshalk et al. 2008), we
hypothesized that long-term Cr supplementation in con-
junction with RT would promote beneficial effects in older
women, beyond what is observed with training alone. The
major findings of this study were that (1) Cr supplemen-
tation increased the training volume and 1RM bench press,
biceps curl, and knee extension performance; (2) Cr sup-
plementation increased the efficiency to perform submax-
imal-strength functional tests (30-s chair stand, arm curl,
and getting up from lying on the floor tests); and (3) Cr
supplementation in conjunction with RT promoted a
greater increase in fat-free mass and muscle mass com-
pared to RT alone.
The results of the current study indicate that the CR
group was able to train with a greater volume than the PL
group during the 12-weeks RT program. This increase in
the ability to train is perhaps not surprising considering
previously published data on Cr-supplemented younger
(Volek et al. 1999) and older (Chrusch et al. 2001) subjects.
Any creatine dose (e.g., 0.3–5.0 g kg-1 day-1) that is
sufficient to increase the muscle Cr levels (Chrusch et al.
2001; Volek et al. 1999; Vandenberghe et al. 1997) appears
to have the potential to improve the muscles’ ability to
train with high workloads. The additional training volume
observed in CR group resulted in greater 1RM bench press,
biceps curl, or knee extension performance after 12 weeks
of RT. Our results are similar to previous work involving
long- and short-term Cr supplementation in older adults
(Chrusch et al. 2001; Gotshalk et al. 2002, 2008). Chrusch
et al. (2001) reported greater increases in the leg press
1RM (creatine vs. placebo group, respectively) (?50.1 vs.
?31.3 kg) and knee extension 1RM (?14.9 vs. ?10.7 kg)
in older men following 12 weeks of RT. In addition,
Gotshalk et al. (2002) demonstrated significant improve-
ments in the bench press (4.1 ± 1.4 kg) and leg press
Fig. 4 Numbers of repetitions performed during the 30-s chair stand
(upper panel) and arm curl (middle panel) tests and the time required
to complete a test of getting up from lying on the floor (lower panel)in creatine and placebo groups at pre- and post-test. Values are the
mean ± SD. aP \ 0.01 compared to the corresponding pretest value,
and bP \ 0.05 compared to the creatine post-test value
Table 3 Body composition
Creatine (N = 9) Placebo (N = 9)
Body mass (kg)
Pre 60.5 ± 9.4 57.1 ± 7.3
Post 61.2 ± 9.6 57.4 ± 7.5
D% 1.2 0.5
Fat mass (kg)
Pre 25.4 ± 7.4 22.4 ± 5.8
Post 25.0 ± 7.4 22.6 ± 6.4
D% -1.6 1.2
Body fat (%)
Pre 41.3 ± 5.6 38.8 ± 6.6
Post 40.1 ± 5.7 38.9 ± 7.4
D% -2.8 0.4
Fat-free mass (kg)
Pre 35.1 ± 2.3 34.7 ± 4.0
Post 36.2 ± 2.5a 34.7 ± 3.8
D% 3.2 0.0
Muscle mass (kg)
Pre 15.5 ± 1.5 15.4 ± 2.6
Post 16.1 ± 1.4a 15.5 ± 2.5
D% 3.7 0.9
Values are mean ± SD
Delta change (D%) = (pre-post/pre) 9 100a P \ 0.01 compared to the corresponding initial value
Eur J Appl Physiol (2013) 113:987–996 993
123
(16.1 ± 4.4 kg) 1RM strength in older men after 7 days of
Cr supplementation (0.3 g kg-1 day-1). In a more recent
study, the authors also reported a greater increase in 1RM
bench press and leg press in Cr-supplemented older women
compared to placebo (Gotshalk et al. 2008). The current
study extends the findings of those previous work (Chrusch
et al. 2001; Gotshalk et al. 2002, 2008) by showing that
long-term Cr supplementation has the potential to increase
maximal strength in older women, which may in turn lead
to increased functional capacity and decreased risk of
injury.
Although improvements in the ability to perform max-
imal strength tests are of obvious interest for young pop-
ulations, Canete et al. (2006) argue that these tests would
be of little practical relevance for older people. The authors
also report that submaximal-strength tests for repeated
contractions (e.g., the sit-stand test or 30-s chair stand test)
may be more appropriate for assessing the effects of Cr
supplementation on the ability to perform daily life tasks in
older populations. In the current study, Cr supplementation
improved the performance of upper- and lower body
functional activities in older women. A direct statistical
comparison supports this interpretation; when compared to
the PL post-test, the CR post-test group was 18.7, 10.2, and
10.7 % more efficient in the 30-s chair stand, arm curl, and
getting up from lying on the floor tests, respectively. Our
data support previous findings of functional-studies that
have reported an improved ability to perform submaximal-
strength tasks (e.g., the sit-stand test) in Cr-supplemented
older women (Canete et al. 2006; Gotshalk et al. 2008).
These studies found 5–12 % reductions in the time
required to complete the sit-stand test among older women
following 7 days of Cr supplementation at a dose of
0.3 g kg-1 day-1; however, they did not confirm whether
long-term Cr supplementation also promotes beneficial
effects in older women. We believe that long-term CR
loading is more important than short-term Cr for main-
taining functional capacity in daily life tasks. Our results
demonstrate for the first time that long-term Cr intake
(5.0 g day-1) may be beneficial for increasing the func-
tional capacity in submaximal-strength activities (30-s
chair stand, arm curl, and getting up from lying on the floor
tests) among older women. These results are clinically
relevant because the increase in the functional ability to
perform daily life tasks is inversely related to mortality
(Beltran et al. 2001; Von Strauss et al. 2003). Furthermore,
the functional tests applied in the current study correlate
reasonably well with major indicators of lower body- (e.g.,
knee flexor strength, stair-climbing ability, walking speed,
and risk of falling) and upper body (e.g., household chores,
carrying groceries, lifting a suitcase, and picking up
grandchildren) strength (Bohannon 1995; Csuka and
McCarty 1985; Rikli and Jones 1999a). Therefore, the high
test–retest reliability of the tests used in the present study
provides strong evidence that long-term Cr supplementa-
tion could be a suitable strategy for improving the perfor-
mance of older women in submaximal-strength tasks
during an RT program.
Additionally, Cr supplementation in conjunction with
RT promoted a greater increase in fat-free mass (D%, CR:
3.2 vs. PL: no change) and muscle mass (D%, CR: 3.7 vs.
PL: 0.9) than RT alone. The increase in fat-free mass fol-
lowing Cr supplementation has been demonstrated in some
(Vandenberghe et al. 1997; Willoughby and Rosene 2001;
Gotshalk et al. 2002, 2008; Brose et al. 2003) but not all
(Eijnde et al. 2003; Bermon et al. 1998) previous studies.
The advantages of the present study compared to previous
studies in this area include the exclusive analysis of older
women. To date, most studies involving older adults have
examined the effects of Cr supplementation in older men
only or in a mixed group of men and women, which could
mask the lack of an ergogenic effect in older women. In
this regard, gender may influence the Cr effects. Mihic
et al. (2000) found a gender-specific ergogenic effect for Cr
supplementation in young subjects; the authors reported an
increase in total body mass for men but not for women
(men: ?1.6 vs. women: ?0.45 kg) and observed a strong
trend toward a smaller increase in fat-free mass for women
(men: ?1.3 vs. women: ?0.44 kg) in response to 5-days Cr
supplementation. In addition, Ferguson and Syrotuik
(2006) have not found any additional effect of Cr supple-
mentation on strength and lean body mass in experienced
resistance trained women after a 10-weeks RT program. It
is possible that women may have a greater muscle total Cr
(TCr) concentration before loading (Forsberg et al. 1991;
Harris et al. 1992), which could attenuate the loading
potential of the female participants (Harris et al. 1992).
Indeed, the increase in fat-free mass has been inversely
related to muscle TCr and phosphocreatine (PCr) contents
before loading (Mihic et al. 2000). Thus, the increase in
fat-free mass and muscle mass found in our study is most
likely explained by the fact that older subjects had lower
muscle TCr (Tarnopolsky Tarnopolsky and MacLennan
2000) and PCr concentrations (Rawson et al. 2002) before
loading, leading to a better ergogenic response of Cr
supplementation.
Surprisingly, the increase in fat-free mass and muscle
mass did not reflect significant changes in body mass in the
CR group compared to the PL group (D%, CR: 1.2 vs. PL:
0.5). In this regard, contradictory results have been
observed on the effects of Cr supplementation on the body
mass of older subjects. While some authors have reported a
significant increase in body mass associated with increased
muscle strength in older men ([60 years) after acute Cr
supplementation (Jakobi et al. 2001; Gotshalk et al. 2002),
others have reported an increase in muscle strength without
994 Eur J Appl Physiol (2013) 113:987–996
123
any significant changes in body mass in older men and
women following a 52-days RT program combined with Cr
supplementation (Bermon et al. 1998). Give that short-term
Cr supplementation promotes increase in body mass in
older adults (Gotshalk et al. 2002, 2008), it is not clear why
the body mass remained unchanged in our subjects after
long-term Cr supplementation. There are two possibilities
that might explain this paradox. First, the women present a
greater muscle total Cr (TCr) concentration before loading
(Forsberg et al. 1991; Harris et al. 1992); this could
attenuate the loading potential of the women participants
(Harris et al. 1992) and, consequently, compromises the
gain in body mass. This hypothesis is supported by studies
that showed a lower increase (e.g., 0.6 vs. 1.9 %) in body
mass in women compared to men after acute Cr supple-
mentation (Mihic et al. 2000). In fact, a 3.2 % increase in
fat-free mass in current study was not enough to provoke
an increment in the total body weight. It is important to
note that in Cr-supplemented older subjects, any increases
in body mass are generally of small magnitude (e.g., *2 %
total body mass) (Canete et al. 2006; Gotshalk et al. 2002,
Rawson et al. 2000) and despite an increase (7 %) in the
total muscle PCr content occurring after Cr supplementa-
tion, no reciprocal change is observed in the body mass
(Rawson et al. 2002). Thus, the lack of a significant
increase in body mass does not necessarily indicate that our
subjects did not experience an increase in the intramuscular
PCr or Cr contents.
Second, the lack of an additional effect of Cr loading in
the body mass could be related to the age-related decline in
the TCr and PCr concentrations (Mesa et al. 2002; Smith
et al. 1998), presumably associated with a decrease in the
type II muscle fiber content during the aging process.
Several studies have confirmed that type II fibers have a
greater ability to uptake and store Cr than type I fibers (for a
review, see Casey and Greenhaff 2000). Although a limi-
tation of our study was that we did not collect muscle
biopsies for TCr and PCr measures, our results indicate that
the potential of Cr supplementation to increase the fat-free
mass and lower- and upper body functional performance in
older women is not necessarily associated with changes in
body mass. Indeed, Cr supplementation resulted in an
increase in the number of repetitions for the 30-s chair stand
(27 % increase) and arm curl (22 % increase) tests and a
19 % reduction in the time required to get up from lying on
the floor. Similar to a previous long-term study (12 weeks)
with young subjects (Volek et al. 1999), our data indicate
that the ergogenic effects of Cr supplementation in older
women extend up to 12 weeks of RT and perhaps longer.
In summary, long-term Cr supplementation combined
with a supervised RT program improved the ability to
perform submaximal-strength functional tasks (e.g., rising
from a chair, bending the arm, and getting up from the floor)
and promoted a greater increase in maximal strength, fat-
free mass and muscle mass in older women than RT alone.
Acknowledgments We address a special thanks to Andrea Diniz for
their great help in the encapsulation of creatine. We are also grateful
to all the participants for their engagement in this study and the
Coordination of Improvement of Higher Education Personnel
(CAPES/Brazil) for the doctoral scholarships conferred to M.A.N.
and A.M.G., and the National Council of Technological and Scientific
Development (CNPq/Brazil) for the grant conceded to E.S.C. Part of
this work was supported by the Araucaria Foundation for the Support
of Scientific and Technological Development of Parana - FAADCT/
Brazil (Protocol number 15466).
Conflict of interest No conflicts of interest, financial or otherwise,
are declared by the author(s).
References
Baechle TR, Earle RW (2008) Resistance training and spotting
techniques. In: Earle R, Baechle T (eds) Essentials of strength
and conditioning: national strength and conditioning association,
3rd edn. Human Kinetics, Champaign, pp 326–376
Bamman MM, Hill VJ, Adams GR, Haddad F, Wetzstein CJ, Gower
BA, Ahmed A, Hunter GR (2003) Gender differences in
resistance-training-induced myofiber hypertrophy among older
adults. J Gerontol A Biol Sci Med Sci 58(2):108–116
Beltran B, Cuadrado C, Martin ML, Carbajal A, Moreiras O (2001)
Activities of daily living in the Spanish elderly. Association with
mortality. J Nutr Health Aging 5(4):259–260
Bermon S, Venembre P, Sachet C, Valour S, Dolisi C (1998) Effects
of creatine monohydrate ingestion in sedentary and weight-
trained older adults. Acta Physiol Scand 164(2):147–155
Bohannon RW (1995) Sit-to-stand test for measuring performance of
lower extremity muscles. Percept Mot Skills 80(1):163–166
Brose A, Parise G, Tarnopolsky MA (2003) Creatine supplementation
enhances isometric strength and body composition improve-
ments following strength exercise training in older adults.
J Gerontol A Biol Sci Med Sci 58(1):11–19
Campbell WW, Crim MC, Young VR, Evans WJ (1994) Increased
energy requirements and changes in body composition with
resistance training in older adults. Am J Clin Nutr 60(2):167–175
Canete S, San Juan AF, Perez M, Gomez-Gallego F, Lopez-Mojares
LM, Earnest CP, Fleck SJ, Lucia A (2006) Does creatine
supplementation improve functional capacity in elderly women?
J Strength Cond Res 20(1):22–28
Casey A, Greenhaff PL (2000) Does dietary creatine supplementation
play a role in skeletal muscle metabolism and performance? Am
J Clin Nutr 72(2):607S–617S
Charette SL, McEvoy L, Pyka G, Snow-Harter C, Guido D, Wiswell
RA, Marcus R (1991) Muscle hypertrophy response to resistance
training in older women. J Appl Physiol 70(5):1912–1916
Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT,
Nigg CR, Salem GJ, Skinner JS (2009) American College of
Sports Medicine position stand. Exercise and physical activity
for older adults. Med Sci Sports Exerc 41(7):1510–1530
Chrusch MJ, Chilibeck PD, Chad KE, Davison KS, Burke DG (2001)
Creatine supplementation combined with resistance training in
older men. Med Sci Sports Exerc 33(12):2111–2117
Cribb PJ, Hayes A (2006) Effects of supplement timing and resistance
exercise on skeletal muscle hypertrophy. Med Sci Sports Exerc
38(11):1918–1925
Eur J Appl Physiol (2013) 113:987–996 995
123
Csuka M, McCarty DJ (1985) Simple method for measurement of
lower extremity muscle strength. Am J Med 78(1):77–81
Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl
Physiol 95(4):1717–1727
Eijnde BO, Van Leemputte M, Goris M, Labarque V, Taes Y,
Verbessem P, Vanhees L, Ramaekers M, Vanden Eynde B, Van
Schuylenbergh R, Dom R, Richter EA, Hespel P (2003) Effects
of creatine supplementation and exercise training on fitness in
men 55–75 yr old. J Appl Physiol 95(2):818–828
Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M
(2001) Timing of postexercise protein intake is important for
muscle hypertrophy with resistance training in elderly humans.
J Physiol 535(1):301–311
Ferguson TB, Syrotuik DG (2006) Effects of creatine monohydrate
supplementation on body composition and strength indices in
experienced resistance trained women. J Strength Cond Res
20(4):939–946
Forsberg AM, Nilsson E, Werneman J, Bergstrom J, Hultman E
(1991) Muscle composition in relation to age and sex. Clin Sci
81(2):249–256
Fujita S, Volpi E (2004) Nutrition and sarcopenia of ageing. Nutr Res
Rev 17(1):69–76
Gotshalk LA, Volek JS, Staron RS, Denegar CR, Hagerman FC,
Kraemer WJ (2002) Creatine supplementation improves muscular
performance in older men. Med Sci Sports Exerc 34(3):537–543
Gotshalk LA, Kraemer WJ, Mendonca MA, Vingren JL, Kenny AM,
Spiering BA, Hatfield DL, Fragala MS, Volek JS (2008) Creatine
supplementation improves muscular performance in older
women. Eur J Appl Physiol 102(2):223–231
Green AL, Hultman E, Macdonald IA, Sewell DA, Greenhaff PL
(1996a) Carbohydrate ingestion augments skeletal muscle cre-
atine accumulation during creatine supplementation in humans.
Am J Physiol 271(5):821–826
Green AL, Simpson EJ, Littlewood JJ, Macdonald IA, Greenhaff PL
(1996b) Carbohydrate ingestion augments creatine retention
during creatine feeding in humans. Acta Physiol Scand 158(2):
195–202
Harris RC, Soderlund K, Hultman E (1992) Elevation of creatine in
resting and exercised muscle of normal subjects by creatine
supplementation. Clin Sci 83(3):367–374
Hunter GR, McCarthy JP, Bamman MM (2004) Effects of resistance
training on older adults. Sports Med 34(5):329–348
Jakobi JM, Rice CL, Curtin SV, Marsh GD (2001) Neuromuscular
properties and fatigue in older men following acute creatine
supplementation. Eur J Appl Physiol 84(4):321–328
Johnson RA, Wichern DW (2002) Applied multivariate analysis, 5th
edn. Prentice-Hall, Upper Saddle River
Kim J, Heshka S, Gallagher D, Kotler DP, Mayer L, Albu J, Shen W,
Freda PU, Heymsfield SB (2004) Intermuscular adipose tissue-
free skeletal muscle mass: estimation by dual-energy X-ray
absorptiometry in adults. J Appl Physiol 97(2):655–660
Kuriansky JB, Gurland B (1976) Performance tests of activities of
daily living. Int J Aging Hum Dev 7:343–352
Mesa JL, Ruiz JR, Gonzalez-Gross MM, Gutierrez Sainz A, Castillo
Garzon MJ (2002) Oral creatine supplementation and skeletal
muscle metabolism in physical exercise. Sports Med 32(14):
903–944
Mihic S, MacDonald JR, McKenzie S, Tarnopolsky MA (2000) Acute
creatine loading increases fat-free mass, but not affect blood
pressure, plasma creatinine, or CK activity in men and women.
Med Sci Sport Exerc 32(2):291–296
Newton RU, Hakkinen K, Hakkinen A, McCormick M, Volek J,
Kraemer WJ (2002) Mixed-methods resistance training increases
power and strength of young and older men. Med Sci Sports
Exerc 34(8):1367–1375
Prior BM, Cureton KJ, Modlesky CM, Evans EM, Sloniger MA,
Saunders M, Lewis RD (1997) In vivo validation of whole body
composition estimates from dual-energy X-ray absorptiometry.
J Appl Physiol 83:623–630
Rawson ES, Clarkson PM (2000) Acute creatine supplementation in
older men. Int J Sports Med 21(1):71–75
Rawson ES, Clarkson PM, Price TB, Miles MP (2002) Differential
response of muscle phosphocreatine to creatine supplementation
in young and old subjects. Acta Physiol Scand 174(1):57–65
Rikli R, Jones J (1999a) Development and validation of a function
fitness test for community-residing older adults. J Aging Phys
Activ 7(2):129–161
Rikli R, Jones J (1999b) Functional fitness normative scores for
community-residing older adults, ages 60-94J. Aging Phys Activ
7(2):162–181
Smith SA, Montain SJ, Matott RP, Zientara GP, Jolesz FA, Fielding
RA (1998) Creatine supplementation and age influence muscle
metabolism during exercise. J Appl Physiol 85(4):1349–1356
Stout JR, Sue Graves B, Cramer JT, Goldstein ER, Costa PB, Smith
AE, Walter AA (2007) Effects of creatine supplementation on
the onset of neuromuscular fatigue threshold and muscle strength
in elderly men and women (64–86 years). J Nutr Health Aging
11(6):459–464
Taaffe DR, Pruitt L, Pyka G, Guido D, Marcus R (1996) Comparative
effects of high- and low-intensity resistance training on thigh
muscle strength, fiber area, and tissue composition in elderly
women. Clin Physiol 16(4):381–392
Tarnopolsky MA, MacLennan DP (2000) Creatine monohydrate
supplementation enhances high-intensity exercise performance
in males and females. Int J Sport Nutr Exerc Metab 10(4):
452–463
Trappe S, Godard M, Gallagher P, Carroll C, Rowden G, Porter D
(2001) Resistance training improves single muscle fiber con-
tractile function in older women. Am J Physiol Cell Physiol
281(2):C398–C406
Vandenberghe K, Gillis N, Van Leemputte M, Van Hecke P,
Vanstapel F, Hespel P (1996) Caffeine counteracts the ergogenic
action of muscle creatine loading. J Appl Physiol 80(2):452–457
Vandenberghe K, Goris M, Van Hecke P, Van Leemputte M,
Vangerven L, Hespel P (1997) Long-term creatine intake is
beneficial to muscle performance during resistance training.
J Appl Physiol 83(6):2055–2063
Volek JS, Duncan ND, Mazzetti SA, Staron RS, Patukian M, Gomez
AL, Pearson DR, Fink WJ, Kraemer WJ (1999) Performance and
muscle fiber adaptations to creatine supplementation and heavy
resistance training. Med Sci Sport Exerc 31(8):1147–1156
Von Strauss E, Aguero-Torres H, Kareholt I, Winblad B, Fratiglioni L
(2003) Women are more disabled in basic activities of daily
living than men only in very advanced ages: a study on
disability, morbidity, and mortality from the Kungsholmen
Project. J Clin Epidemiol 56(7):669–677
Willoughby DS, Rosene J (2001) Effects of oral creatine and
resistance training on myosin heavy chain expression. Med Sci
Sports Exerc 33(10):1674–1681
Yarasheski KE, Zachwieja JJ, Campbell JA, Bier DM (1995) Effect
of growth hormone and resistance exercise on muscle growth
and strength in older men. Am J Physiol 268(2):E268–E276
Yarasheski KE, Pak-Loduca J, Hasten DL, Obert KA, Brown MB,
Sinacore DR (1999) Resistance exercise training increases mixed
muscle protein synthesis rate in frail women and men C 76 yr
old. Am J Physiol 277(1):E118–E125
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper
Saddle River
996 Eur J Appl Physiol (2013) 113:987–996
123