EFFICACY AND SAFETY OF CONCURRENT TRAINING IN
SYSTEMIC SCLEROSIS
ANA L.S. PINTO,1 NATÁLIA C. OLIVEIRA,1 BRUNO GUALANO,1,2 ROMY B. CHRISTMANN,1
VITOR S. PAINELLI,1,2 GUILHERME G. ARTIOLI,1,2 DANILO M.L. PRADO,1 AND FERNANDA R. LIMA1
1
Laboratory of Assessment and Conditioning in Rheumatology, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil;
and 2Laboratory of Applied Nutrition and Metabolism, School of Physical Education and Sport, University of Sao Paulo, Sao
Paulo, Brazil
ABSTRACT
Pinto, ALS, Oliveira, NC, Gualano, B, Christmann, RB, Painelli, VS,
Artioli, GG, Prado, DML, and Lima, FR. Efficacy and safety of
concurrent training in systemic sclerosis. J Strength Cond Res
25(5): 1423–1428, 2011—The optimal training model for
patients with systemic sclerosis (SSc) is unknown. In this study,
we aimed to investigate the effects of a 12-week combined
resistance and aerobic training program (concurrent training) in
SSc patients. Eleven patients with no evidence of pulmonary
involvement were recruited for the exercise program. Lower and
upper limb dynamic strengths (assessed by 1 repetition maxi-
mum [1RM] of a leg press and bench press, respectively), iso-
metric strength (assessed by back pull and handgrip tests),
balance and mobility (assessed by the timed up-and-go test),
muscle function (assessed by the timed-stands test), Rodnan
score, digital ulcers, Rayland’s phenomenon, and blood
markers of muscle inflammation (creatine kinase and aldolase)
were assessed at baseline and after the 12-week program.
Exercise training significantly enhanced the 1RM leg press
(41%) and 1RM bench press (13%) values and back pull (24%)
and handgrip strength (11%). Muscle function was also
improved (15%), but balance and mobility were not significantly
changed. The time-to-exhaustion was increased (46.5%, p =
0.0004), the heart rate at rest condition was significantly
reduced, and the workload and time of exercise at ventilatory
thresholds and peak of exercise were increased. However,
maximal and submaximal V_ O2 were unaltered (p . 0.05). The
Rodnan score was unchanged, and muscle enzymes remained
within normal levels. No change was observed in digital ulcers
and Raynaud’s phenomenon. This is the first study to
demonstrate that a 12-week concurrent training program is
Address correspondence to Natália C. Oliveira, nataliaovs@gmail.com.
25(5)/1423–1428
Journal of Strength and Conditioning Research
Ó 2011 National Strength and Conditioning Association
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Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
safe and substantially improves muscle strength, function, and
aerobic capacity in SSc patients.
KEY WORDS resistance training, endurance training, sclero-
derma, rheumatic diseases
INTRODUCTION
S
ystemic sclerosis (SSc) or systemic scleroderma is
a rheumatic connective tissue disease of unknown
etiology that causes widespread microvascular
damage, immune system activation, and excessive
collagen deposition in the skin and internal organs (6,25).
There are 2 major subtypes of SSc: limited cutaneous
scleroderma and diffuse cutaneous scleroderma. The former
mainly affects the hands, arms, and face (though pulmonary
hypertension is frequently observed), whereas the latter
presents a rapid progression and affects a large area of the
skin and 1 or more internal organs (frequently the kidneys,
esophagus, heart, and lungs). Clinical manifestations include
Raynaud’s phenomenon (temporary vasoconstriction of the
small vessels of the fingers, toes, tip of the nose, and earlobes),
skin disorders, musculoskeletal dysfunction, gastrointestinal
complications, pulmonary complications, scleroderma renal
crisis, and dryness of the eyes and mouth (6,9,10,25).
Prognosis is determined by the degree of internal organ
involvement; prognosis is poor if cardiac, pulmonary, or renal
manifestations present early in the disease progression.
Although no disease-modifying therapy has been proven
effective for SSc treatment, complications of SSc are
treatable, and interventions for organ-specific manifestations
have improved substantially (9,10).
It has been established that physical inactivity and some
drugs used to treat rheumatic disorders (e.g., corticoids) may
have severe negative effects on the cardiovascular and muscle
systems, leading to deterioration of the physical condition
(6,12,21,23). In parallel, accumulated evidence suggests that
exercise training is able to partially counteract these side
effects in several rheumatic diseases (1,4,11,19). Despite this
evidence, SSc patients have often been encouraged to avoid
physical activity and exercise because of the anecdotal belief
that exercise would aggravate muscle inflammation
VOLUME 25 | NUMBER 5 | MAY 2011 | 1423
 Concurrent Training in Systemic Sclerosis
or microvascular disorders. In fact, there have been very few
studies regarding the safety and efficacy of exercise
interventions in SSc. Accordingly, we have only recently
shown that aerobic training can be safely tolerated by these
patients and can be effective in improving aerobic capacity
(14). However, there has been no study investigating the role
of resistance training in SSc. Theoretically, combined
strengthening and aerobic exercises (concurrent training),
rather than aerobic training alone, constitutes a reasonable
training model that is capable of equally attenuating aerobic
deconditioning and muscle weakness and disability in SSc
patients.
Thus, because of lack of exercise recommendations for SSc
patients, the aim of this study was to evaluate the safety and
efficacy of concurrent training on aerobic capacity and muscle
strength and function in this disease.
METHODS
Experimental Approach to the Problem
Because SSc is a rare disease, we were unable to perform
a randomized controlled study. Thus, we adopted a quasiex-
perimental design (pre–post). Women with SSc were tested
before a 12-week combined resistance and aerobic training
program and again at the end of this period. Given that this
model of training can increase both strength and aerobic
capacity, we speculated that it could benefit SSc patients, who
often present low aerobic conditioning and muscle weakness.
To assess muscle strength, 1 repetition maximum (1RM)
leg press, 1RM bench press, low back isometric strength, and
isometric handgrip were measured. To assess muscle function,
timed up-and-go and timed-stands tests were performed,
whereas aerobic conditioning was evaluated by the V_ O2max
test. Creatine kinase (CK) and aldolase were measured as
markers of muscle damage.
Subjects
The medical histories of all outpatients from the Systemic
Sclerosis Clinic of the Rheumatology Division of the
University of Sao Paulo, School of Medicine were analyzed.
Women who were diagnosed with SSc (according to the
American Rheumatism Association criteria [20]) and were
physically inactive for at least 6 months (defined by the lack
of regular physical activity 1 or more times per week) were
eligible. Exclusion criteria included: evidence of moderate or
severe pulmonary involvement, echocardiographic evidence
of cardiac impairment, pulmonary artery systolic pressure
equal to or above 40 mm Hg, history of myositis, history of
tobacco use, renal insufficiency, hypertension, and anemia.
Pathologic lung impairment was also an exclusion criterion,
determined when forced vital capacity, measured by
spirometry, and diffusion lung capacity of carbon monoxide,
measured in a single breath, were ,75% of the predicted value
for age and gender. Patients who presented symptoms such as
coughing, dyspnea, thoracic pain, malabsorption, dysmotility,
and resting arrhythmia in a preliminary clinical examination
were also excluded from the study.
the TM
1424 Journal of Strength and Conditioning Research
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Eleven patients (age: 44 6 13 years; weight: 61 6 12 kg; and
height: 1.59 6 0.06 m) qualified to participate in the study.
Eight patients had no evidence of pulmonary involvement,
and 3 had pulmonary artery systolic pressure equal to or
slightly higher than 35 mm Hg (35, 37, and 42 mm Hg). All
patients were taking diltiazem. Four patients also used metho-
trexate. The other drugs used were prednisone (n = 1),
azathioprine (n = 1), and cyclophosphamide (n = 1).
The SSc group included 3 patients with limited cutaneous
SSc and 8 patients with diffuse cutaneous SSc. The mean
disease duration was 7.36 6 1.8 years, and the mean modified
Rodnan score (24), a skin thickness score assessment tool,
was 26.33 6 13.55.
After a complete explanation about the study’s purpose and
the procedures involved with participation, all subjects gave their
written informed consent to participate in this trial. The
procedures were approved by the Ethical Committee of General
Hospital (University of Sao Paulo, School of Medicine).
Procedures
Cardiopulmonary Exercise Test. The exercise test was per-
formed after 2 hours of fasting and 24 hours of caffeine
abstinence. All subjects participated in a cardiopulmonary
exercise test performed on a treadmill (Inbramed Millenium,
RS, Brazil). Subjects underwent the test according to the
conventional Bruce protocol (5) before and after the 12-week
exercise program. This protocol has fixed increments in
speed and inclination at 3-minute intervals and was selected
because it has been widely used in other studies, including
those investigating populations with low physical fitness.
Oxygen uptake (V_ O2), carbon dioxide production (V_ CO2), and
ventilation (V_ E) were determined by means of gas exchange
on a breath-by-breath basis using a computerized system
(Aerosport-teem100, Ann Arbor, MI, USA) with Micromed
ErgoPC Elite 3.2 (Brası́lia, Brazil) software. V_ O2peak was
defined as the maximum attained V_ O2 at the end of the
exercise period in which the subject could no longer maintain
treadmill speed because of symptoms (dyspnea or fatigue)
that precluded continuation of the test.
The ventilatory anaerobic threshold (VAT) was determined
to occur at the break point between the increase of V_ CO2
output and V_ O2 (V-slope) or where the ventilatory equivalent
for oxygen (V_ E /V_ O2 ratio) was at the lowest value before
a systematic increase. The respiratory compensation point
(RCP) was determined to occur where the ventilatory
equivalent for carbon dioxide (V_ E /V_ CO2 ratio) was at the
lowest value before a systematic increase. Heart rates were
monitored continuously by electrocardiogram. Arterial blood
pressure was monitored noninvasively during rest and at
peak exercise.
Blood Markers of Inflammation and Muscle Damage. To evaluate
the blood concentration of CK and aldolase, blood samples
were collected in the morning, after 12 hours of rest and 8
hours of fasting. Creatine kinase and aldolase were analyzed
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Journal of Strength and Conditioning Research | www.nsca-jscr.org

by a HITACHI UV-2000 spectrophotometer, using Boeh-
ringer Mannheim reagents. The CV for CK and aldolase were
2.2 and 2.0%, respectively.
Strength and Functional Muscle Assessments. Patients underwent
3 familiarization sessions, separated by at least 72 hours, for all
strength and functional tests. Before the 1RM test, 3 warm-up
sets of 5 repetitions at loads of 40–60% of the perceived
exertion were performed, with a 1-minute rest period
between sets. Thereafter, patients had up to 5 attempts to
reach 1RM, with 5-minute rest periods between attempts.
Patients were instructed to perform each attempt with
maximum effort. The highest exercise load that allowed the
patient to perform the full range of motion in an attempt was
considered to be the 1RM load. The 1RM tests were
conducted for 2 exercises: bench press and leg press.
Moreover, strength was determined isometrically for hand-
grip, with the dominant arm, and low back strength (13).
Finally, we assessed balance, mobility, and muscle function
(timed up-and-go, and timed-stands tests) according to
previous descriptions (2,17).
Exercise Training Program. The exercise program consisted of
12 weeks of supervised training. Exercise sessions occurred
twice a week. Training sessions consisted of a 5-minute
treadmill warm-up followed by 30 minutes of resistance
training, 20 minutes of treadmill aerobic training, and 5
minutes of stretching exercises. All sessions were monitored
by at least 1 fitness professional and 1 physician. The exercise
program was performed in an intrahospital gymnasium
(Laboratory of Assessment and Conditioning in Rheumatol-
ogy, School of Medicine, University of Sao Paulo).
Resistance training included 5 exercises for the main muscle
groups: bench press, leg press, lat pull down, leg extension,
and seated row. Patients were required to perform 4 sets of
8–12RM, except during the first week, when they performed
only 2 sets of approximately 15–20RM for each exercise (as
an adaptation to resistance training). Progression to greater
resistance levels was imple-
mented when the subject could
perform 12 or more repetitions
on the last training set for 2 TABLE 1. Effects of a 12-week concurrent training program on dynamic strength
(1RM in leg press and in bench press), isometric strength (handgrip and back pull),
consecutive workouts. Aerobic
muscle function (timed-stands tests), and balance and mobility (timed-up-and-go) in
training intensity was set at the SSc patients (n = 11).*†
corresponding heart rate of
approximately 70% of V_ O2peak.
correlation coefficient (ICC), SEM, and minimal difference
(MD), according to Weir (26). All tests were highly reliable
(1RM bench press: ICC = 0.998, SEM = 0.9, MD = 2.6,
coefficient of variation (CV) = 0.2%; 1RM leg press: ICC =
0.998, SEM = 1.3, MD = 3.7, CV = 0.2%; handgrip: ICC =
0.996, SEM = 0.6; MD = 1.7, CV = 0.4%; low back strength:
ICC = 0.999, SEM = 0.3; MD = 0.8, CV = 5%; timed-stands:
ICC = 0.983, SEM = 0.3, MD = 0.9, CV = 0.4%; and timed up-
and-go: ICC = 0.990, SEM = 0.1, MD = 0.2, CV = 0.5%). The
CV for CK and aldolase were 2.2 and 2.0%, respectively.
Additionally, we calculated the effect sizes (ES) for the
dependent variables (3). The analyses were conducted using
SPSS 14.0 software (SPSS Inc, Chicago, IL, USA).
RESULTS
As a result of the training program, significant increases in the
1RM for bench press and leg press were observed. Improve-
ments in isometric strength and muscle function were also
observed, although the gain in the timed up-and-go test did
not reach statistical significance. Table 1 summarizes the data
regarding strength and functional muscle assessments.
There were no changes in V_ O2peak (pre: 21.6 6 1.2, post:
22.1 6 1.6 ml
kg21
min21; p = 0.7; ES = 0.2). However, the
heart rate at rest was significantly reduced after the exercise
training program (pre: 101.7 6 3.5, post: 92.8 6 5.1 b
min21;
p = 0.02; ES = 0.8). In addition, exercise training improved
the workload and time of exercise at VAT, RCP, and peak of
exercise (Table 2).
Throughout the training period, there were no reports of
pain, muscle injury, cramps, muscle soreness, bruise, excessive
exhaustion, or any apparent exercise-related adverse epi-
sodes. No apparent change in serum markers of muscle
damage (CK pre: 5.2 6 2.3, post: 5.4 6 2.3 UI
L21; aldolase
pre: 113 6 87, post: 122 6 90 UI
L21; p . 0.1 and ES , 0.2)
was observed as a consequence of exercise training, and
regular physical examinations revealed no abnormalities.
Furthermore, the Rodnan score was also unchanged, and no
PRE POST D (%) Sig. (p) ES

Statistical Analyses Leg press (kg) 67 6 23 95 6 27 41 0.0006 1.6

Bench press (kg) 37 6 17 42 6 17 13 0.08 0.5
All data are expressed as mean 6
Handgrip (kg) 20 6 9 22 6 11 11 0.02 0.2
SD. Paired t-tests were used to Low back strength (kg) 59 6 27 73 6 24 24 0.001 1.4
analyze all dependent variables. Timed-up-and-go (s) 6.9 6 0.7 6.3 6 0.7 29 0.12 0.6
The significance level adopted Timed-stands (n) 15 6 2 17 6 3 15 0.04 1.3
to reject the null hypothesis was
*SSc = systemic sclerosis;1RM = 1 repetititon maximum; ES = effect size.
set at p # 0.05. To determine the †Values are means 6 SD.
reliability of the tests performed,
we calculated the intraclass

VOLUME 25 | NUMBER 5 | MAY 2011 | 1425

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 Concurrent Training in Systemic Sclerosis

TABLE 2. Effects of a 12-week concurrent training program on workload and time of exercise at VAT, RCP, and the peak of
exercise in SSc patients (n = 11).*†‡

AT RCP Peak

Pre Post Pre Post Pre Post

Speed (mph) 2.1 6 0.1 3.0 6 0.1§ 3.1 6 0.1 4.0 6 0.1§ 3.3 6 0.2 4.3 6 0.1§
Slope (%) 11.0 6 0.3 13.2 6 0.3§ 13.3 6 0.3 15.4 6 0.3§ 13.8 6 0.4 16.2 6 0.2§
Time of exercise (min) 3.4 6 0.3 5.9 6 0.6§ 6.2 6 0.3 9.2 6 0.6§ 7.5 6 0.4 10.7 6 0.5§
*VAT = ventilatory anaerobic threshold; AT = anaerobic threshold; RCP = respiratory compensation point; Peak = peak exercise;
SSc = systemic sclerosis; ES = effect size.
†Values are means 6 SD.
‡The ESs for speed at AT, RCP, and peak were 2, 1.7, and 2.9, respectively. The ES for slope at AT, RCP, and peak were 2, 1.7, 3.5,
respectively. The ES for time of exercise at AT, RCP, and peak were 1.4, 1.7, and 2.1, respectively.
§p # 0.05 vs. preintervention.

difference was observed in digital ulcers and Raynaud’s
phenomenon.
DISCUSSION
It is well known that physical inactivity combined with the
chronic use of drugs (e.g., corticoids) often leads to
deconditioning and muscle weakness in rheumatic patients
(23). Although a growing body of literature has shown that
exercise training is capable of improving strength and aerobic
capacity in several diseases (reviewed in [16]), regrettably few
studies have examined this valuable tool in rheumatic
diseases. Therefore, we aimed to investigate the efficacy
and safety of a combined aerobic and resistance training
program in SSc patients. As a result, we showed that this
exercise program might be useful in improving muscle
strength, function, and aerobic conditioning.
It is well established that aerobic capacity is a strong and
independent factor negatively associated with all-cause
mortality (22). Recently, a prospective cohort study demon-
strated that muscular strength is also inversely and in-
dependently associated with death from all causes and cancer
in men, even after adjusting for cardiorespiratory fitness and
other potential confounders (18). In light of these findings, it
is necessary to investigate the efficacy and safety of training
programs, including aerobic and strengthening exercises, in
broader populations. In this context, we previously showed
that aerobic training is well tolerated and significantly
improves exercise tolerance, aerobic capacity, and oxygen
saturation in SSc patients, supporting the notion that
achieving improved exercise capacity is a feasible goal in
SSc management. In the present study, we examined, for the
first time, a combined resistance and aerobic training
(concurrent training) program in the management of SSc
symptoms.
As expected, concurrent training promoted substantial
increases in muscle function and strength. Moreover, aerobic
the TM
improvements such as resting bradycardia, which is an
important indicator of aerobic training efficiency, were
observed (8). We also observed an increase in both workload
and time of exercise at VAT, RCP, and peak of exercise,
ultimately suggesting an improvement in aerobic metabo-
lism. Importantly, this adaptation may be particularly
beneficial for SSc patients, because we previously reported
a lower time between VAT and RCP in these patients
compared with healthy subjects, revealing impairment
of aerobic metabolism during exercise (15). Further studies
should explore the central (i.e., cardiorespiratory) and
peripheral (i.e., muscle phenotype and genotype) mecha-
nisms responsible for exercise-induced aerobic condition
improvement in SSc.
It is important to note that the aerobic benefits experienced
by the patients in this study were modest compared with
those observed when aerobic exercise alone was applied (14)
(i.e., an increase in V_ O2peak of 2.3% [p . 0.05] vs. 12.6% [p =
0.006], respectively). There are 2 apparent explanations for
this. First, it is noteworthy that the current aerobic training
volume was substantially lower than that in our previous
study (30 vs. 20 minutes, respectively), which might have
been insufficient to elicit greater aerobic adaptations. Second,
it is possible that the concurrent training adopted in this
study might have precluded greater aerobic benefits.
Corroborating this hypothesis, there is evidence that
concurrent training performed by healthy untrained individ-
uals may not interfere with strength development but may
hinder development of maximal aerobic capacity (7). Thus,
the lack of improvement in V_ O2peak in the present study
may be a result of low aerobic training volume, concurrent
effect of resistance training, or by a combination of these
factors.
Regarding the safety of the intervention, the Rodnan score
was unaltered, and digital ulcers and Raynaud’s phenomenon
remained stable. Furthermore, the lack of any apparent

1426 Journal of Strength and Conditioning Research

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exercise-related adverse episode, such as muscle injury or
pain, suggests that the exercise volume was appropriate with
respect to safety. Altogether, these data indicate that
concurrent training seems to be safe for SSc patients, and it
does not worsen the activity of the disease.
The major limitation of the present study was the absence
of a nontrained control group. Because of the very low
prevalence of this disease (50–300 per million) (6) combined
with the rigid inclusion criteria adopted, we were unable to
select a sufficiently large number of patients for a randomized
controlled trial. However, these rigid inclusion criteria
allowed for the selection of a homogeneous sample, which
is a key factor when such a heterogeneous disease is
investigated. Moreover, we also adopted rigid criteria of
familiarization to avoid learning effects in strength and
functional tests. As a result, the stability and reliability data of
these dependent variables allowed us to assume that the
changes observed are related to the exercise program rather
than to random variance or systematic bias (e.g., learning
effects) in testing. In addition, our patients had no pulmonary
involvement, so caution should be exercised in extrapolating
these findings to patients with pulmonary impairment.
In summary, we demonstrated that concurrent training
improves muscle strength and function and aerobic capacity,
supporting the notion that this model of exercise constitutes
a promising therapeutic tool in SSc. However, the optimal
training volume and workload capable of eliciting the greatest
benefits for the disease remain to be determined.
PRACTICAL APPLICATIONS
Exercise training has not been recommended for SSc patients
because physicians believed that it could aggravate the
inflammatory process and microvascular disorders. In fact,
there has been no evidence indicating that concurrent
training is safe and effective for this disease. However, the
findings from this study confirm that concurrent training is a
reasonable training model, capable of counteracting both the
muscle weakening and aerobic deconditioning that are often
experienced by SSc patients. Therefore, we recommend that
aerobic and functional muscle strengthening exercise be
considered in the management of SSc patients.
The exercise program, comprising resistance training (4 sets
at 8–12RM of 5 exercises for the major muscle groups) and
moderate-intensity aerobic training (20 minutes at 70% of
V_ O2peak), can effectively improve muscle strength and
function, but the benefits for aerobic capacity seem to be
modest. It is likely that greater gains in aerobic capacity
may be achieved with a longer (.30 minutes), with a more
intensive (.70% of V_ O2peak) aerobic training program or
with a combination of both.
ACKNOWLEDGMENTS
Bruno Gualano and Guilherme Giannini Artioli were sup-
ported by the Conselho Nacional de Pesquisa e Tecnologia.
The results of the present study do not constitute an
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endorsement of the product by the authors or the National
Strength and Conditioning Association. There are no
conflicts of interest.
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the TM

1428 Journal of Strength and Conditioning Research

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.