Effects of physical therapy for the management of patients

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REVIEWARTICLE
Effects of physical therapy for the management of patients
with ankylosing spondylitis in the biological era
Erika Giannotti & Sabina Trainito & Giovanni Arioli &
Vincenzo Rucco & Stefano Masiero
Received: 2 January 2014 /Revised: 18 March 2014 /Accepted: 20 April 2014 /Published online: 7 May 2014
# Clinical Rheumatology 2014
Abstract Exercise is considered a fundamental tool for the
management of ankylosing spondylitis (AS), in combination
with pharmacological therapy that with the advent of biolog-
ical therapy has improved dramatically the control of signs
and symptoms of this challenging disease. Current evidence
shows that a specific exercise protocol has not been validated
yet. The purpose of this review is to update the most recent
evidence (July 2010–November 2013) about physiotherapy in
AS, analyzing the possible role and synergistic interactions
between exercise and biological drugs. From 117 studies
initially considered, only 15 were included in the review.
The results support a multimodal approach, including educa-
tional sessions, conducted in a group setting, supervised by a
physiotherapist and followed by a maintaining home-based
regimen. Spa exercise and McKenzie, Heckscher, and Pilates
methods seem promising in AS rehabilitation, but their effec-
tiveness should be further investigated in future randomized
controlled trials (RCTs). When performed in accordance with
the American College of Sports Medicine guidelines, cardio-
vascular training has been proven safe and effective and
should be included in AS rehabilitation protocols. Exercise
training plays an important role in the biological era, being
now applicable to stabilized patients, leading ultimately to a
better management of AS by physiatrists and rheumatologists
throughout the world. On the basis of the current evidence,
further research should aim to determine which exercise pro-
tocols should be recommended.
Keywords Ankylosing spondylitis . Exercise therapy .
Physical therapy . Rehabilitation . Tumor necrosis factor
inhibitor therapy
Introduction
Ankylosing spondylitis (AS) is a chronic, inflammatory, and
progressive rheumatic disease characterized by pain, reduced
mobility, and deformity of the spine and associated with
disability and diminished quality of life [1].
According to the Assessment of Spondyloarthritis
International Society-European League Against Rheumatism
(ASAS/EULAR)working groups, the optimal management of
AS requires a combination of nonpharmacological and phar-
macological treatments [2].
Pharmacological treatments have improved dramatically
with the advent of antitumor necrosis factor (TNF) therapy
[3], which has revealed to improve signs and symptoms,
function, and spinal mobility in the short-term [4, 5] and in
the long-term follow-up [6].
Among nonpharmacological therapies, exercise in AS is
considered an important tool to maintain or improve mobility,
functioning, and global health [7–13] and to prevent structural
deformities [14].
Since the introduction of TNF-inhibitor therapy, the effects
of rehabilitation and the characteristics of exercise protocol
performed by patients treated with biological drugs are de-
scribed only in few studies [15].
Combination treatment including rehabilitation and TNF
inhibitor versus TNF inhibitor only seemed to improve more
function, disability, and quality of life in AS patients [15–17].
E. Giannotti : S. Trainito : S. Masiero (*)
Rehabilitation Unit, Department of Neurosciences,
University of Padua, Via Giustiniani 3, 35128 Padua, Italy
e-mail: stef.masiero@unipd.it
G. Arioli
Section of Rehabilitation and Rheumatology, Department of
Neurological Sciences, Carlo Poma Hospital, Via Lago Paiolo 10,
46100 Mantua, Italy
V. Rucco
Unit of Rehabilitation, Spilimbergo and San Vito al Tagliamento
Hospital, Pordenone, Italy
Clin Rheumatol (2014) 33:1217–1230
DOI 10.1007/s10067-014-2647-6
Although benefits of the combination treatment are well
described in the literature [18], the current evidence is not
sufficient to recommend a specific physical therapy program [7].
Moreover, Peters et al. reported an association between AS
and increased risk of cardiovascular disease (CVD) [19], which
would provide an additional indication for AS patients to
develop and maintain cardiovascular fitness. Cardiorespiratory
training is reported to be beneficial not only for CVD prevention
[20] but also for improvement of flexibility in AS patients [21].
Rehabilitation programs in AS should be in accordance
with the American College of Sports Medicine’s (ACSM)
recommendations for developing and maintaining cardiore-
spiratory fitness, muscular strength, and flexibility in AS
patients [22]. Since a dose-response association exists for
exercise, just as it does for drugs, the effect of exercise is
therefore dependent on the patients’ adherence to the pre-
scribed programs, and it is important to identify the most up-
to-date evidence-based physiotherapy in order to educate AS
patients to the correct exercise protocol [23, 24].
Therefore, the aims of this study were the following: (1) to
update the most recent evidence related to physical therapy for
AS and to highlight the short- and long-term effects, (2) to
analyze the existing rehabilitation programs for AS patients,
and (3) to delineate the current evidence in favor of increased
effectiveness of biological therapy in combinationwith exercise.
Methods
We performed a comprehensive search of PubMed, Medline,
Cochrane, CINAHL, Embase, SPORTDiscus, PEDro, and
Google scholar databases using the following search terms:
“spondylitis ankylosing” and “physical therapy,” “physiother-
apy,” “exercise therapy,” and “rehabilitation.” Given the lin-
guistic capabilities of the research team, we considered pub-
lications in English and Italian language. For the purpose of
this review, an updated search was performed (from July 2010
to November 2013). Publications were included if the study
group comprised patients with a diagnosis of AS according to
the classification system described in the New York criteria.
Eligible studies (randomized control studies, nonrandomized
control studies, and observational studies) had to describe
physical therapy intervention in AS. Letters to the editor,
review articles, and physiotherapy trials associated with out-
come measures, complementary, and alternative medicine and
health care utilization were excluded from this review as they
were beyond the scope of this study. Abstracts were read and
screened to ensure that articles met the above criteria, and then
relevant articles were reviewed (Fig. 1). When indicated,
adherence of the study protocols to the ACSM recommenda-
tions [25] was registered. When available, a PEDro score was
retrieved from the PEDro database online to rate the method-
ological quality of the selected studies.
Results
Study selection As shown in the study selection flow diagram
(Fig. 1), of the original database search, identifying 2,201
articles, 390 citations were selected in relation to the publica-
tion period considered, and after reading the title and/or ab-
stract, only 117 studies were considered.
Of the rest, which were obtained as full text, 102 were
excluded because there were letters to the editor or review
articles or physiotherapy research about outcome measures,
complementary and alternative medicine, and health care
utilization or because authors have not indicated frequency
and duration of the rehabilitation program.
As a result of the selection process, 15 studies were includ-
ed in the review (Tables 1, 2, and 3).
Study characteristics Following the selection criteria pro-
posed for the review, 15 clinical studies were retrieved
[26–40], with a total of 1,516 patients with AS. Of the selected
studies, 9/10 were randomized controlled studies [28, 30, 31,
33, 34,36, 37, 39, 40], 3/10 nonrandomized controlled studies
[27, 32, 35], and 3/10 nonrandomized uncontrolled studies
[26, 29, 38].
Based on the physiotherapy options in AS patients, we
proposed to group the studies in the following categories:
exercise therapy, spa therapy and association between phys-
iotherapy and biological drugs, occupational therapy, manual
therapy, and physical therapy. The latter three therapeutic
options listed, although well described in past studies [10,
16, 41, 42], were not retrieved as possible tools for AS
rehabilitation in the time interval considered for this review.
Table 1 described the characteristics of the trials included.
Type of rehabilitation treatment
Exercise therapy Eight studies examining different therapeu-
tic exercise protocols in AS were analyzed [27, 29, 30, 32, 34,
36, 37, 39] (Table 1).
The uncontrolled clinical study by Gyurcsik et al. demon-
strated pain and spine stiffness reduction and improvement of
several subjective and functional parameters in a group of ten
patients after a complex physical therapy protocol compared
to the baseline [29]. However, only chest expansion (CE)
showed a statistically significant improvement, while other
parameters, such as pain and stiffness, presented only a pos-
itive trend after the exercise program. Tender point count
(TPC) markedly decreased during and after the physiotherapy
program, but statistical analysis was not performed for this
data. The lack of a control group (CG) and of a follow-up
evaluation, the absence of description of patient’s pharmaco-
logical therapy and the small sample examined, might reduce
the validity of the proposed rehabilitation treatment.
1218 Clin Rheumatol (2014) 33:1217–1230
A recent randomized controlled trial (RCT) by Kjeken
et al. [30] found significant evidence in favor of an intensive
3-week inpatient rehabilitation program compared with con-
ventional treatment. The study protocol comprised pool, out-
door and gym activities, individualized for every patient and
adherent to the ACSM guidelines, in order to ensure the
optimal starting level and progression for each patient. After
4 months, the rehabilitation group showed a statistically sig-
nificant improvement in the Bath Ankylosing Spondylitis
Disease Activity Index (BASDAI) score and in the Medical
Outcome Study Short Form-36 (SF-36) variables’ physical
role,mental role, and vitality and bodily pain. After 12months,
even if there were no significant differences between the two
groups, patients who underwent rehabilitation treatment
showed positive effects in primary and secondary outcomes.
The absence of description of the CG treatment and the high
number of dropouts could limit the validity of results and the
application of the proposed physiotherapy treatment.
The study by Aytekin et al. [27] compared patients follow-
ing a home-based exercise program five times a week (exer-
cise group (EXG), n=34) with those exercising less than five
times a week (CG, n=32). Evaluations were performed by the
same clinician at baseline and at 3-month follow-up. A statis-
tically significant improvement was observed in pain evaluated
with VAS tragus–wall distance (TWD), Bath Ankylosing
Spondylitis Functional Index (BASFI), BASDAI, modified
Schober’s test (MST), CE, finger–floor distance (FFD), and
Ankylosing Spondylitis Quality of Life (ASQoL) question-
naire in the EXG at third month. On the contrary, in the CG,
MST, CE, morning stiffness, FFD, and ASQoL, scores were
significantly worse at third month, and the values of VAS,
TWD, BASFI, and BASDAI remained unchanged. Only the
EXG showed significant improvements in forced expiratory
volume in first second (FEV1) and forced vital capacity
(FVC). In the intergroup comparison between the two groups
at third month, no statistically significant difference was re-
trieved in all the parameters examined, except for ASQoL
scores, that were significantly higher in the EXG. The absence
of randomization, the wide variability of the rehabilitation
protocol of CG, and the short follow-up negatively influence
the results of the study.
Altan et al. [34] first studied the effectiveness of Pilates
method in AS in a prospective and single-blind RCT.
Immediately after the 3-month Pilates program (T1), Pilates
group (PI) had a significant improvement in BASFI, Bath
Ankylosing Spondylitis Metrology Index (BASMI),
BASDAI, and CE, while at 6-month follow-up (T2), only
BASFI and BASMI were still significantly improved com-
pared with the baseline. There were no changes for ASQoL at
T1 and T2. In the CG (receiving standard treatment), no
Results from 
electronic databases 
search strategy (n= 
2201)
Article included after 
screening title and/or 
abstract (n= 117)
Excluded (n= 1815)
Trails included, in 
relation to publication 
period considered
(n= 390)
Nonrandomized 
uncontrolled 
studies
n=3
Nonrandomized 
control studies
n= 3
Randomized 
control 
studies 
n=9
Studies considered, after 
reading full article, in 
the review (n= 15)
Excluded (n= 277)
Excluded (n= 102)
Fig. 1 Study selection flow
diagram
Clin Rheumatol (2014) 33:1217–1230 1219
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ra
m
at
th
e
en
d
of
st
ud
y.
A
lth
ou
gh
th
er
e
w
er
e
si
gn
if
ic
an
t
im
pr
ov
em
en
ts
in
C
E
in
bo
th
gr
ou
ps
as
co
m
pa
re
d
to
ba
se
lin
e
th
is
pa
ra
m
et
er
1220 Clin Rheumatol (2014) 33:1217–1230
T
ab
le
1
(c
on
tin
ue
d)
St
ud
y
ID
N
o.
of
pa
tie
nt
s
St
ud
y
de
si
gn
P
ar
tic
ip
an
ts
’
ch
ar
ac
te
ri
st
ic
s
Ph
ys
io
th
er
ap
y
pr
ot
oc
ol
A
dd
iti
on
al
th
er
ap
y
F
ol
lo
w
-u
p
O
ut
co
m
e
m
ea
su
re
R
es
ul
ts
in
cr
ea
se
d
si
gn
if
ic
an
tly
on
ly
in
gr
ou
p
I;
st
at
is
tic
al
ly
si
gn
if
ic
an
t
im
pr
ov
em
en
to
f
V
C
af
te
r
tr
ea
tm
en
ti
n
th
e
SG
in
th
e
in
te
rg
ro
up
co
m
pa
ri
so
n.
Si
lv
a
et
al
.
(2
01
0)
38
(2
2
=
G
P
R
gr
ou
p;
16
=
C
G
)
C
on
tr
ol
le
d
cl
in
ic
al
st
ud
y
-
26
M
,9
F
-
A
ge
:
G
R
P
gr
ou
p:
35
.3
±
12
.2
C
G
:4
4.
27
±
10
.5
5
-
D
is
ea
se
du
ra
tio
n
(y
rs
)
G
R
P
gr
ou
p:
10
.1
±
5.
67
C
G
:7
.0
7
±
4.
81
G
PR
(p
os
iti
on
s
th
at
st
re
tc
he
d
th
e
sh
or
te
ne
d
m
us
cl
e
ch
ai
ns
),
on
ce
a
w
ee
k
×
1
h
×
16
w
ee
ks
N
ot
in
di
ca
te
d
N
on
e
Pa
in
in
te
ns
ity
w
ith
V
A
S
sc
al
e,
m
or
ni
ng
st
if
fn
es
s
(m
in
ut
e)
,c
er
vi
ca
l
sp
in
e
m
ob
ili
ty
(c
hi
n-
to
-s
te
rn
um
,
oc
ci
pu
t-
to
-w
al
l
di
st
an
ce
s,
an
d
ce
rv
ic
al
ro
ta
tio
n)
,l
um
ba
r
sp
in
e
m
ob
ili
ty
(f
in
ge
r-
to
-f
lo
or
di
st
an
ce
an
d
M
S
I)
C
E
,H
A
Q
-S
,
SF
-3
6,
B
A
SD
A
I
St
at
is
tic
al
ly
si
gn
if
ic
an
t
im
pr
ov
em
en
ti
n
al
lt
he
pa
ra
m
et
er
s
in
bo
th
gr
ou
ps
fr
om
ba
se
lin
e.
G
re
at
er
im
pr
ov
em
en
t
fo
r
th
e
G
P
R
gr
ou
p
fo
r
m
or
ni
ng
st
if
fn
es
s
an
d
ce
rv
ic
al
an
d
lu
m
ba
r
sp
in
e
m
ob
ili
ty
pa
ra
m
et
er
s
R
od
ri
gu
ez
-
L
oz
an
o
et
al
.(
20
13
)
75
6
(3
81
=
ed
uc
at
io
n
in
te
rv
en
tio
n;
37
5
=
C
G
)
Pr
os
pe
ct
iv
e
m
ul
tic
en
te
r
co
nt
ro
lle
d
st
ud
y
-
72
%
M
-
m
ea
n
ag
e
45
yr
s
2-
h
in
fo
rm
at
iv
e
se
ss
io
n
ab
ou
t
A
S,
no
n-
su
pe
rv
is
ed
ex
er
ci
se
pr
og
ra
m
at
ho
m
e
N
ot
av
ai
la
bl
e
A
tt
he
en
d
of
th
e
tr
ea
tm
en
t
Pr
im
ar
y:
B
A
S
D
A
I,
B
A
S
FI
Se
co
nd
ar
y:
VA
S
fo
r
to
ta
lp
ai
n,
no
ct
ur
na
l,
A
SQ
oL
,s
el
f-
ev
al
ua
tio
n
or
di
na
l
sc
al
e,
di
ar
y
ca
rd
of
da
ily
ex
er
ci
se
A
t6
m
o,
st
at
is
tic
al
ly
si
gn
if
ic
an
ts
up
er
io
r
re
su
lts
in
B
A
SD
A
I,
B
A
SF
I,
V
A
S
fo
r
to
ta
l
pa
in
,p
at
ie
nt
’s
gl
ob
al
as
se
ss
m
en
t,
an
d
A
SQ
oL
w
er
e
fo
un
d
in
th
e
ed
uc
at
io
n
gr
ou
p.
Pt
s
in
th
e
ed
uc
at
io
n
gr
ou
p
in
cr
ea
se
d
kn
ow
le
dg
e
ab
ou
tt
he
di
se
as
e
an
d
its
tr
ea
tm
en
ts
si
gn
if
ic
an
tly
an
d
pr
ac
tic
ed
m
or
e
re
gu
la
r
ex
er
ci
se
th
an
co
nt
ro
ls
in
a
si
gn
if
ic
an
tm
an
ne
r
N
ie
de
m
an
n
et
al
.
(2
01
3)
10
6
(5
3
=
tr
ai
ni
ng
gr
ou
p;
53
=
C
G
)
R
C
T
-
68
M
,1
8
F
-
A
ge
:
S
tu
dy
gr
ou
p:
50
.1
±
11
.9
C
G
:4
7.
6
±
12
.4
-
D
is
ea
se
du
ra
tio
n
(y
rs
)
S
G
:9
(0
.5
–4
5)
C
G
:8
(0
.5
–3
9)
E
xc
lu
si
on
cr
ite
ri
on
:
he
ar
td
is
ea
se
(N
Y
H
A
II
I
an
d
IV
)
S
up
er
vi
se
d
N
W
tr
ai
ni
ng
30
m
in
tw
ic
e/
w
ee
k
on
×
12
w
ee
ks
in
di
vi
du
al
ly
m
on
ito
re
d
m
od
er
at
e
he
ar
tr
at
e
(H
R
)
in
te
ns
ity
le
ve
ls
+
>
1/
w
k
ad
di
tio
na
lu
ns
up
er
vi
se
d,
he
ar
tr
at
e-
m
on
ito
re
d
ca
rd
io
va
sc
ul
ar
tr
ai
ni
ng
M
ed
ic
al
tr
ea
tm
en
t.
A
ll
pt
s
al
so
pe
rf
or
m
ed
th
e
st
an
da
rd
fl
ex
ib
ili
ty
ex
er
ci
se
pr
og
ra
m
N
on
e
C
ar
di
ov
as
cu
la
r
fi
tn
es
s,
as
se
ss
ed
w
ith
a
su
bm
ax
im
al
bi
cy
cl
e
te
st
fo
llo
w
in
g
th
e
PW
C
75
%
pr
ot
oc
ol
,t
ot
al
B
A
S
D
A
I
sc
or
e
an
d
th
e
su
bs
ca
le
s
fo
r
sp
in
al
pa
in
,p
er
ip
he
ra
lp
ai
n
an
d
fa
tig
ue
,B
A
SF
I,
B
A
S
M
I,
B
A
S
G
I;
ty
pe
,
am
ou
nt
an
d
in
te
ns
ity
of
ph
ys
ic
al
ac
tiv
ity
(P
A
)
ev
al
ua
tio
n:
St
at
is
tic
al
ly
si
gn
if
ic
an
t
im
pr
ov
em
en
ti
n
ca
rd
io
va
sc
ul
ar
fi
tn
es
s
an
d
pe
ri
ph
er
al
pa
in
B
A
SD
A
I
su
bs
ca
le
in
th
e
SG
co
m
pa
re
d
to
th
e
C
G
.
Clin Rheumatol (2014) 33:1217–1230 1221
significant variation in the parameters was retrieved at T1 and
T2. Comparison of the groups (PI and CG) showed signifi-
cantly superior results for BASDAI at T1 in the PI, for BASFI
and BASMI at T2, suggesting a long-term beneficial effect of
Pilates. The absence of the description of standard treatment
of CG and the short-term follow-up are the limitations of the
study.
The study by Rosu et al. [37] evaluated the effect of a
multimodal exercise program combining Pilates, McKenzie,
and Heckscher techniques on pulmonary function and func-
tion and disease activities in patients with AS. Ninety-six
patients were randomized to a group performing the multi-
modal program and to a CG assigned to the classical kinetic
program. At 48-week follow-up, both groups reported a sig-
nificant improvement from the baseline for all AS-related
parameters. However, significant improvement was found in
pain, MST, FFD, BASFI, BASDAI, and BASMI in the mul-
timodal program group at the end of study. Although there
were significant improvements in CE in both groups as com-
pared to baseline, this parameter increased significantly only
in group I. Vital capacity (VC) did not change significantly
from the baseline in both groups, but in the intergroup com-
parison, significant differences were found in favor of the
multimodal group. All the evaluations were conducted only
at the end of treatment, and no follow-up was available.
Silva et al. [32] analyzed the effects of Global Postural
Reeducation (GPR) in patients with AS compared with a CG
performing conventional segmental self-stretching and breath-
ing exercises twice a week for 40 min for 16 weeks. Both
groups were supervised by an experienced physical therapist
and received educational guidelines. In the intergroup com-
parison, better results were retrieved in the GPR group with
regard to morning stiffness, spinal mobility (except FFD), CE,
and quality of life. Disease activity, functional capacity, and
emotional aspects of SF-36 profile improved, and pain inten-
sity decreased in both the GPR groups (for pain in the cervical
and lumbar regions) and in the CG (pain in cervical, lumbar,
and dorsal regions), with no statistically significant difference
between the groups. The inability to control patients’ con-
sumption of medications, the absence of follow-up and the
small sample limit the evidence of effectiveness of the pro-
posed treatment in AS patients, especially over time.
The prospective multicenter RCT by Rodriguez-Lozano
et al. [39] evaluated the impact of an education–intervention
program in 756 AS patients, randomized to the study group,
performing a 6-month educational session and a
nonsupervised home-based exercise program and to a CG,
receiving standard care. At 6 months, statistically significant
superior results in BASDAI, BASFI, and VAS for total pain,
patient’s global assessment, and ASQoL were found in the
education group. Although the proposed programwas feasible
and helped to increase knowledge and exercise practice, the
magnitude of these benefits in terms of disease activity andT
ab
le
1
(c
on
tin
ue
d)
St
ud
y
ID
N
o.
of
pa
tie
nt
s
St
ud
y
de
si
gn
P
ar
tic
ip
an
ts
’
ch
ar
ac
te
ri
st
ic
s
Ph
ys
io
th
er
ap
y
pr
ot
oc
ol
A
dd
iti
on
al
th
er
ap
y
F
ol
lo
w
-u
p
O
ut
co
m
e
m
ea
su
re
R
es
ul
ts
O
IM
Q
,a
cc
el
er
om
et
er
;
H
A
D
S-
D
(G
er
m
an
ve
rs
io
n
of
H
os
pi
ta
l
A
nx
ie
ty
an
d
D
ep
re
ss
io
n
Sc
al
e)
;
E
U
R
O
-Q
uo
l;
E
S
R
an
d
C
re
ac
tiv
e
pr
ot
ei
n
C
PR
,c
ho
le
st
er
ol
an
d
tr
ig
ly
ce
ri
de
s
R
C
T
ra
nd
om
iz
ed
co
nt
ro
lle
d
tr
ia
l,
yr
s
ye
ar
s,
m
o
m
on
th
s,
T
P
C
te
nd
er
po
in
ts
co
un
t,
VA
S
vi
su
al
an
al
og
sc
al
e,
B
A
SF
I
B
at
h
A
nk
yl
os
in
g
S
po
nd
yl
iti
s
F
un
ct
io
na
lI
nd
ex
,B
A
SD
A
I
B
at
h
A
nk
yl
os
in
g
S
po
nd
yl
iti
s
D
is
ea
se
A
ct
iv
ity
In
de
x,
M
SI
m
od
if
ie
d
Sc
ho
be
r’
s
in
de
x,
C
E
ch
es
te
xp
an
si
on
,L
L
F
lu
m
ba
rl
at
er
al
fl
ex
io
n,
O
W
D
oc
ci
pu
t-
to
-w
al
ld
is
ta
nc
e,
F
F
D
lu
m
ba
rf
or
w
ar
d
fl
ex
io
n,
B
A
S-
G
B
at
h
A
nk
yl
os
in
g
S
po
nd
yl
iti
s
G
lo
ba
lS
co
re
,B
A
SM
I
B
at
h
A
nk
yl
os
ing
S
po
nd
yl
iti
s
M
et
ro
lo
gy
In
de
x,
SF
-3
6
M
ed
ic
al
O
ut
co
m
e
St
ud
y
Sh
or
tF
or
m
-3
6,
F
E
V
1
fo
rc
ed
ex
pi
ra
to
ry
vo
lu
m
e
in
fi
rs
ts
ec
on
d,
F
V
C
fo
rc
ed
vi
ta
lc
ap
ac
ity
,A
SQ
oL
A
nk
yl
os
in
g
Sp
on
dy
lit
is
Q
ua
lit
y
of
L
if
e,
H
A
Q
-S
H
ea
lth
A
ss
es
sm
en
t
Q
ue
st
io
nn
ai
re
–S
po
nd
yl
oa
rt
hr
op
at
hi
es
,
G
P
R
G
lo
ba
l
P
os
tu
ra
l
R
ee
du
ca
tio
n,
P
E
F
pe
ak
ex
pi
ra
to
ry
fl
ow
,
V
C
vi
ta
l
ca
pa
ci
ty
,
M
A
F
M
ul
tid
im
en
si
on
al
A
ss
es
sm
en
t
of
Fa
tig
ue
,B
D
I
B
ec
k
D
ep
re
ss
io
n
In
ve
nt
or
y,
TL
C
to
ta
l
lu
ng
ca
pa
ci
ty
,R
V
re
si
du
al
vo
lu
m
e,
6M
W
D
6-
m
in
w
al
k
di
st
an
ce
,R
G
re
ha
bi
lit
at
io
n
gr
ou
p,
C
G
co
nt
ro
lg
ro
up
,E
X
G
ex
er
ci
se
gr
ou
p,
SG
st
ud
y
gr
ou
p
1222 Clin Rheumatol (2014) 33:1217–1230
T
ab
le
2
Sp
a
th
er
ap
y
St
ud
y
ID
N
o.
of
pa
tie
nt
s
St
ud
y
de
si
gn
Pa
rt
ic
ip
an
ts
’
ch
ar
ac
te
ri
st
ic
s
P
hy
si
ot
he
ra
py
pr
ot
oc
ol
A
dd
iti
on
al
th
er
ap
y
Fo
llo
w
-u
p
O
ut
co
m
e
m
ea
su
re
R
es
ul
ts
A
yd
em
ir
et
al
.(
20
10
)
28
C
lin
ic
al
st
ud
y
(u
nr
an
do
m
iz
e,
no
co
nt
ro
l
gr
ou
p)
-
27
M
,1
F;
-
M
ea
n
ag
e
(y
rs
):
24
.3
9
±
2.
97
(r
an
ge
:
20
–3
3)
.
-
M
ea
n
du
ra
tio
n
of
di
se
as
e
(y
rs
):
4.
71
±
1.
86
(r
an
ge
:
2–
9)
.
S
pa
tr
ea
tm
en
t(
37
°C
th
er
ap
eu
tic
po
ol
)
fo
r
3
w
ee
ks
(3
0
m
in
/d
,
5
da
ys
/w
ee
k)
,
in
cl
ud
in
g
un
de
rw
at
er
ex
er
ci
se
s;
20
m
in
ve
nt
ila
tio
n
an
d
20
m
in
po
st
ur
e
ex
er
ci
se
af
te
r
th
er
ap
eu
tic
po
ol
S
ul
fa
sa
la
zi
ne
2,
00
0
m
g/
da
y
an
d
in
do
m
et
ha
ci
n
75
m
g/
da
y
fo
r
at
le
as
t6
m
o
1
m
o
G
lo
ba
li
nd
ex
,B
A
SD
A
I,
B
A
SF
I,
B
A
S
M
I,
SF
-3
6,
C
E
,
pu
lm
on
ar
y
fu
nc
tio
n
te
st
in
g
(F
V
C
,
F
E
V
1,
F
E
V
1/
F
V
C
,
P
E
F,
V
C
)
Si
gn
if
ic
an
td
ec
re
as
e
of
B
A
SM
I
sc
or
e;
no
rm
al
iz
ed
pu
lm
on
ar
y
fu
nc
tio
n
in
3/
6
pa
tie
nt
s
w
ith
re
st
ri
ct
iv
e
pu
lm
on
ar
y
di
so
rd
er
fo
llo
w
in
g
ba
ln
eo
th
er
ap
y;
(n
ot
st
at
is
tic
al
ly
si
gn
if
ic
an
t)
C
ip
ri
an
et
al
.(
20
13
)
30
(1
5
=
SG
;
15
=
C
G
)
R
an
do
m
iz
ed
,
co
nt
ro
lle
d
an
d
si
ng
le
-
bl
in
d
tr
ia
l
-
28
M
,2
F.
-
A
ge
(y
rs
)
SG
:4
7.
8
±
10
.0
C
G
:4
5.
6
±
11
.8
-
D
is
ea
se
du
ra
tio
n
(y
rs
)
SG
:1
3.
9
±
8.
6
C
G
:1
3.
2
±
8.
8
10
se
ss
io
ns
of
sp
a
th
er
ap
y
an
d
re
ha
bi
lit
at
io
n
ov
er
a
2
w
ee
ks
pe
ri
od
.E
ac
h
se
ss
io
n
w
as
m
ad
e
up
of
2
pa
rt
s:
(a
)
m
ud
pa
ck
fo
llo
w
ed
by
th
er
m
al
ba
th
,(
b)
gr
ou
p
re
ha
bi
lit
at
io
n
se
ss
io
n
pe
rf
or
m
ed
fo
r
an
ho
ur
in
a
po
ol
of
th
er
m
al
w
at
er
(s
pi
ne
m
ob
ili
za
tio
n
m
us
cu
la
r
sp
in
e
st
re
ng
th
en
in
g
an
d
re
sp
ir
at
or
y
ki
ne
si
th
er
ap
y
T
N
F
in
hi
bi
to
rs
(e
ta
ne
rc
ep
t
or
in
fl
ix
im
ab
)
fo
r
at
le
as
t3
m
o
be
fo
re
th
e
tr
ia
lb
eg
an
an
d
co
nt
in
ue
d
th
ro
ug
ho
ut
th
e
st
ud
y
pe
ri
od
A
tt
he
en
d
of
tr
ea
tm
en
t;
3
m
o
an
d
6
m
o
P
ri
m
ar
y:
B
A
S
F
I;
Se
co
nd
ar
y:
B
A
SD
A
I,
B
A
SM
I,
V
A
S
fo
r
ba
ck
pa
in
,
H
A
Q
L
on
g-
te
rm
cl
in
ic
al
st
at
is
tic
al
ly
si
gn
if
ic
an
t
im
pr
ov
em
en
ti
n
m
os
to
f
th
e
ev
al
ua
tio
n
in
di
ce
s
w
er
e
im
pr
ov
ed
in
th
e
S
G
yr
s
ye
ar
s,
m
o
m
on
th
s,
VA
S
vi
su
al
an
al
og
sc
al
e,
B
A
SF
IB
at
h
A
nk
yl
os
in
g
S
po
nd
yl
iti
s
Fu
nc
tio
na
lI
nd
ex
,B
A
SD
A
IB
at
h
A
nk
yl
os
in
g
S
po
nd
yl
iti
s
D
is
ea
se
A
ct
iv
ity
In
de
x,
C
E
ch
es
te
xp
an
si
on
,B
at
h
A
nk
yl
os
in
g
B
A
SM
I
Sp
on
dy
lit
is
M
et
ro
lo
gy
In
de
x,
SF
-3
6
M
ed
ic
al
O
ut
co
m
e
St
ud
y
Sh
or
tF
or
m
-3
6,
F
E
V
1
fo
rc
ed
ex
pi
ra
to
ry
vo
lu
m
e
in
fi
rs
ts
ec
on
d,
F
V
C
fo
rc
ed
vi
ta
lc
ap
ac
ity
,H
A
Q
H
ea
lth
A
ss
es
sm
en
tQ
ue
st
io
nn
ai
re
,
P
E
F
pe
ak
ex
pi
ra
to
ry
fl
ow
,V
C
vi
ta
lc
ap
ac
ity
,C
G
co
nt
ro
lg
ro
up
,S
G
st
ud
y
gr
ou
p,
T
N
F
tu
m
or
ne
cr
os
is
fa
ct
or
Clin Rheumatol (2014) 33:1217–1230 1223
T
ab
le
3
Ph
ys
io
th
er
ap
y
an
d
bi
ol
og
ic
al
dr
ug
s
St
ud
y
ID
N
o.
of
pa
tie
nt
s
S
tu
dy
de
si
gn
Pa
rt
ic
ip
an
ts
’
ch
ar
ac
te
ri
st
ic
s
Ph
ys
io
th
er
ap
y
pr
ot
oc
ol
A
dd
iti
on
al
th
er
ap
y
Fo
llo
w
-u
p
O
ut
co
m
e
m
ea
su
re
R
es
ul
ts
Ph
ys
io
th
er
ap
y
an
d
bi
ol
og
ic
al
dr
ug
s
Y
ig
it
et
al
.
(2
01
3)
40
(2
0
=
E
G
;
20
=
C
G
)
C
on
tr
ol
le
d
cl
in
ic
al
st
ud
y
(u
nr
an
do
m
iz
e)
-
32
M
,8
F.
-
A
ge
(y
rs
)
E
G
:4
0.
30
±
8.
05
C
G
:3
6.
45
±
7.
19
;
-
D
ur
at
io
n
si
nc
e
di
ag
no
si
s
(y
rs
)
E
G
:9
.5
5
±
5.
19
C
G
:7
.9
5
±
4.
59
H
om
e
in
di
vi
du
al
ly
ex
er
ci
se
pr
og
ra
m
(m
us
cl
e
re
la
xa
tio
n,
sp
in
al
fl
ex
ib
ili
ty
ex
er
ci
se
s,
ra
ng
e
of
m
ot
io
n
ex
er
ci
se
s
of
co
xo
fe
m
or
al
jo
in
ts
,
st
re
tc
hi
ng
ex
er
ci
se
s
m
us
cu
la
r
st
re
ng
th
en
in
g,
st
ra
ig
ht
po
st
ur
e
an
d
re
sp
ir
at
or
y
ex
er
ci
se
s),
5
tim
es
/w
ee
k
at
le
as
t
30
m
in
/s
es
si
on
fo
r
10
w
ee
ks
T
N
F
in
hi
bi
to
rs
(a
da
lim
um
ab
,
or
et
an
er
ce
pt
or
in
fl
ix
im
ab
)
fo
r
at
le
as
t6
m
o
be
fo
re
th
e
tr
ia
l
be
ga
n
an
d
co
nt
in
ue
d
th
ro
ug
ho
ut
th
e
st
ud
y
pe
ri
od
A
tt
he
en
d
of
tr
ea
tm
en
t
(T
1)
B
B
A
SD
A
I,
B
A
SF
I,
B
A
SM
I,
M
A
F,
B
D
I,
SF
-3
6
B
A
SD
A
I,
B
A
SF
I,
B
A
SM
I,
B
D
I,
M
A
F,
an
d
SF
-3
6
sc
or
es
,s
ho
w
ed
st
at
is
tic
al
ly
si
gn
if
ic
an
t
im
pr
ov
em
en
ts
at
T
1
in
E
G
(p
<
0.
05
)
w
hi
le
va
lu
e
re
m
ai
ne
d
un
ch
an
ge
d
in
C
G
M
as
ie
ro
et
al
.
(2
01
1)
69
(2
2
=
R
G
,
24
=
E
G
,
23
=
C
G
)
R
an
do
m
iz
ed
,c
on
tr
ol
le
d
an
d
si
ng
le
-b
lin
d
tr
ia
l
-
55
M
,1
4
F.
-
A
ge
(m
ed
ia
n)
:
R
G
:4
7.
5
yr
s
E
G
:4
4.
0
yr
s
C
G
:4
7.
5
yr
s
-
T
im
e
si
nc
e
di
ag
no
si
s
(m
ed
ia
n)
:
R
G
:9
.5
yr
s
E
G
:6
.5
yr
s
C
G
:9
.0
yr
s
R
es
pi
ra
to
ry
ex
er
ci
se
s
(2
se
ri
es
of
10
re
pe
tit
io
ns
ea
ch
;
10
m
in
);
ex
er
ci
se
s
to
m
ob
ili
ze
th
e
ve
rt
eb
ra
e
(2
se
ri
es
of
10
re
pe
tit
io
ns
ea
ch
;1
5
m
in
);
ba
la
nc
in
g
an
d
pr
op
ri
oc
ep
tiv
e
ex
er
ci
se
s
(2
se
ri
es
of
10
re
pe
tit
io
ns
ea
ch
;
10
m
in
);
po
st
ur
al
ex
er
ci
se
s
an
d
sp
in
al
an
d
lim
b
m
us
cl
e
st
re
tc
hi
ng
an
d
st
re
ng
th
en
in
g
(2
re
pe
tit
io
ns
of
an
av
er
ag
e
of
ab
ou
t
30
/4
0
s
ea
ch
fo
r
st
re
tc
hi
ng
;
15
m
in
);
en
du
ra
nc
e
tr
ai
ni
ng
(1
0
m
in
)
12
tim
es
w
ee
kl
y
se
ss
io
ns
la
st
in
g
60
m
in
T
N
F
in
hi
bi
to
rs
(a
da
lim
um
ab
,
or
et
an
er
ce
pt
or
in
fl
ix
im
ab
)
fo
r
at
le
as
t9
m
o
be
fo
re
th
e
tr
ia
l
be
ga
n
an
d
co
nt
in
ue
d
th
ro
ug
ho
ut
th
e
st
ud
y
pe
ri
od
4
m
o
C
er
vi
ca
la
nd
lu
m
ba
r
pa
in
in
te
ns
ity
w
ith
V
A
S,
C
E
,B
A
SM
I,
B
A
SD
A
I,
B
A
SF
I,
ce
rv
ic
al
an
d
th
or
ac
ic
-
lu
m
bo
sa
cr
al
m
ov
em
en
ts
.
A
tT
1
an
d
at
6
m
o
in
th
e
R
G
,a
ll
pa
ra
m
et
er
s
st
at
is
tic
al
ly
im
pr
ov
ed
co
m
pa
re
d
to
C
G
,w
hi
le
C
E
,B
A
SM
I,
an
d
so
m
e
of
sp
in
e
m
ov
em
en
ts
st
at
is
tic
al
ly
im
pr
ov
ed
co
m
pa
re
d
to
E
G
M
as
ie
ro
et
al
.
(2
01
3)
69
(2
2
=
R
G
,
24
=
E
G
,
23
=
C
G
)
R
an
do
m
iz
ed
,c
on
tr
ol
le
d
an
d
si
ng
le
-b
lin
d
tr
ia
l
-
A
ge
(m
ea
n,
SD
):
R
G
:4
9.
11
yr
s
(1
1.
8)
E
G
:4
3.
85
yr
s
(8
.1
)
C
G
:4
6.
15
yr
s
(1
0.
3)
-
T
im
e
si
nc
e
di
ag
no
si
s
(m
ea
n,
SD
):
R
G
:9
.1
1
yr
s
(6
.9
)
E
G
:7
.4
1
yr
s
(4
.7
)
C
G
:9
.1
5
yr
s
(4
.2
3)
Se
e
M
as
ie
ro
et
al
.2
01
1
Se
e
M
as
ie
ro
et
al
.2
01
1
12
m
o
Se
e
M
as
ie
ro
et
al
.2
01
1
St
at
is
tic
al
ly
si
gn
if
ic
an
t
ga
in
s
(p
<
0.
05
)
in
R
G
fr
om
ba
se
lin
e
fo
r
al
l
ou
tc
om
es
.S
ig
ni
fi
ca
nt
di
ff
er
en
ce
s
in
C
E
,
B
A
SD
A
I,
ce
rv
ic
al
ro
ta
tio
n,
to
ra
co
lu
m
ba
r
ro
ta
tio
n,
an
d
to
ta
l
ce
rv
ic
al
m
ov
em
en
ts
in
R
G
co
m
pa
re
d
to
E
G
an
d
C
G
1224 Clin Rheumatol (2014) 33:1217–1230
T
ab
le
3
(c
on
tin
ue
d)
St
ud
y
ID
N
o.
of
pa
tie
nt
s
S
tu
dy
de
si
gn
Pa
rt
ic
ip
an
ts
’
ch
ar
ac
te
ri
st
ic
s
Ph
ys
io
th
er
ap
y
pr
ot
oc
ol
A
dd
iti
on
al
th
er
ap
y
Fo
llo
w
-u
p
O
ut
co
m
e
m
ea
su
re
R
es
ul
ts
So
et
al
.(
20
12
)
46
(2
3
=
SG
;
23
=
C
G
)
R
an
do
m
iz
ed
op
en
-l
ab
el
ca
se
-c
on
tr
ol
si
ng
le
-c
en
te
r
st
ud
y
-
44
M
,2
F
-
A
ge
,(
yr
s)
SG
:3
8.
0
±
9.
1;
C
G
:3
4.
6
±
5.
9.
-
To
ta
ls
ym
pt
om
du
ra
tio
n
(y
rs
):
SG
:1
2.
9
±
7.
3;
C
G
:1
2.
2
±
6.
4
-
B
A
SD
A
I
sc
or
es
in
th
e
pr
ev
io
us
3
m
o
w
er
e
10
un
its
.
Fl
ex
ib
ili
ty
ex
er
ci
se
s
of
sp
in
e;
st
re
tc
hi
ng
of
sp
in
e
m
us
cl
e,
ha
m
st
ri
ng
m
us
cl
es
,
an
d
sh
ou
ld
er
m
us
cl
es
;
ch
es
te
xp
an
si
on
ex
er
ci
se
s;
co
nt
ro
l
ab
do
m
in
al
an
d
di
ap
hr
ag
m
br
ea
th
in
g
ex
er
ci
se
s;
(2
0
ex
er
ci
se
s
fo
r
30
m
in
on
ce
a
da
y
)
In
ce
nt
iv
e
sp
ir
om
et
er
;(
30
m
in
on
ce
a
da
y)
fo
r
16
w
ee
ks
.
T
N
F
in
hi
bi
to
rs
(a
da
lim
um
ab
,
or
et
an
er
ce
pt
or
in
fl
ix
im
ab
)
fo
r
at
le
as
t6
m
o
be
fo
re
th
e
tr
ia
l
be
ga
n
an
d
co
nt
in
ue
d
th
ro
ug
ho
ut
th
e
st
ud
y
pe
ri
od
A
tt
he
en
d
of
tr
ea
tm
en
t
B
A
SF
I,
B
A
SD
A
I,
F
V
C
,F
E
V
1,
F
E
V
1/
FV
C
,V
C
,
T
L
C
,R
V
,6
M
W
D
T
he
S
G
im
pr
ov
ed
si
gn
if
ic
an
tly
F
V
C
,
T
L
C
,V
C
,a
nd
FE
V
1/
FV
C
G
yu
rc
si
k
et
al
.
(2
01
3)
10
A
S
pa
tie
nt
s
w
ith
bi
ol
og
ic
al
th
er
ap
y
Pr
os
pe
ct
iv
e,
no
nr
an
do
m
iz
ed
se
lf
-c
on
tr
ol
le
d
tr
ia
l
-
6
M
,4
F
-
ag
e
52
.4
±
13
.6
yr
s
C
on
ve
nt
io
na
le
xe
rc
is
e,
gl
ob
al
po
st
ur
e
re
ed
uc
at
io
n,
br
ea
th
in
g
ex
er
ci
se
s,
m
an
ua
lm
ob
ili
za
tio
n
of
th
e
ch
es
t,
st
re
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Clin Rheumatol (2014) 33:1217–1230 1225
physical function was poor. All the evaluations were conduct-
ed only at the end of treatment, and no follow-up was
available.
The RCT by Niedermann et al. [36] investigated the effect
of cardiovascular training on physical fitness and BASDAI in
106 AS patients, randomized in a study group, experimenting
Nordic walking training and in a CG, participating in discus-
sions on coping strategies. Both groups were also treated with
the conventional flexibility exercise program. Results were
controlled for treatment with TNF inhibitors, gender, age,
body mass index, baseline fitness, physical activity levels,
and BASDAI. After the 3-month trial period, cardiovascular
fitness, assessed with a submaximal bicycle test following the
physical work capacity (PWC 75 %) protocol, was signifi-
cantly higher in the study group compared to the CG. There
was no difference between the two groups in the BASDAI
total score at 3-month follow-up. For the subscores, a signif-
icantly lower level of peripheral pain was found in the training
group. This is the first RCT to test the effect of cardiovascular
training in addition to standard flexibility exercise in AS
patients. In addition, the proposed training program reached
sufficient adherence from the patients enrolled. However, a
statistically significant decrease in the resting heart rate in the
training group could not be detected in the short training
period. No follow-up was available for this study, with con-
sequent limitation to the interpretation of the preventive role
of the described protocol on cardiovascular disease.
None of these studies was adherent to the ACSM recom-
mendations, while the PEDro score was available only for the
studies by Kjeken et al. (6/10) [30] and Rodriguez-Lozano
et al. (6/10) [39].
Spa therapy Two studies about application of spa therapy to
AS patients were included in the review [26, 28] (Table 2).
The study by Aydemir et al. analyzed the effects of
balneotherapy on disease activity, functional status, metrology
index, pulmonary function, and quality of life in 28 patients
with AS. Although 1 month after balneotherapy, a large
amount of clinical parameters improved (BASDAI, global
index, BASMI, and some SF-36 parameters), none was sta-
tistically significant, except for the decrease in BASMI total
score. Pulmonary function test resulted normalized following
balneotherapy in three out of six (50 %) patients with restric-
tive pulmonary disorder; however, as well as for the other
parameters, this result did not reach the level of significance.
The study is limited by the absence of follow-up and of a CG
[26].
Ciprian et al. [28] studied the effects of combined spa
therapy and rehabilitation (study group), in comparison with
pharmacological therapy only (CG) in patients with AS treat-
ed with TNF inhibitors. The patients of the study group had a
persistent and significant improvement in the BASFI at the
end of treatment, at 3 and 6-month follow-up in comparison
with baseline. Also, the secondary outcome measures
(BASMI, VAS for back pain, BASDAI, and HAQ) showed
a positive evolution at follow-up in the study group.
Conversely, in the CG, all the outcome measures were stable
with respect to baseline values. No adverse effect or disease
relapse was found associated with thermal treatment. The
absence of double-blinding, the small number of patients,
and the absence of comparison of the proposed spa therapy
with a standard rehabilitation treatment are the limitations of
the study.
None of these studies was adherent to the ACSM recom-
mendations, while the PEDro score was available only for the
study by Kjeken et al. (4/10) [28].
Effects of physiotherapy combined with biological drugs Five
studies about physiotherapy in patients with stabilized AS on
treatment with biological drugs were included in the review
[31, 33, 35, 38, 40] (Table 3).
The RCT by Yigit et al. analyzed the effect of a 10-week
home-based exercise program combined with education in
patients treated with TNF-α inhibitors. Since at the end of
treatment, only half of enrolled patients were performing
correctly the home rehabilitation protocol, the authors com-
pared a group of 20 patients who followed the program five
times per week at least 30 min per session, as prescribed
(EXG), with a CG who did not practice regularly. At the end
of the proposed treatment, BASDAI, BASFI, BASMI, Beck
Depression Inventory (BDI), Multidimensional Assessment
of Fatigue (MAF) scale, and SF-36 scores showed statistically
significant improvement in EXG, while they were unchanged
in the CG. The intergroup comparison highlighted a signifi-
cant difference in BASDAI, BASFI, BASMI, BDI, MAF
scores, and SF-36 (except social functioning subscale) be-
tween groups in favor of EXG. In this study, patients’ educa-
tion was not effective in increasing compliance and adherence
of AS patients to regular home-based exercise. There are
several limitations in this study such as the small sample, the
short follow-up, and the lack of randomization [35].
In the study by Masiero et al. [31], 62 AS patients treated
with TNF-inhibitor therapy were randomly allocated either to
a rehabilitation program, including educational–behavioral
training associated with exercise (rehabilitation group (RG)),
or to educational–behavioral therapy only (educational group
(EG)), or to a CG, receiving no intervention. The educational–
behavioral program was administered during3-h sessions,
including 8–12 patients per session, every 2 weeks. The
exercise program was performed in groups of 4–6 subjects,
supervised by an experienced physiotherapist. Patients were
instructed to perform the exercises at home at least three to
four times per week, with a continual feedback with the
physiotherapist at the following session. At the end of the
rehabilitation treatment, patients were provided with a DVD
containing the complete exercise and educational program,
1226 Clin Rheumatol (2014) 33:1217–1230
and compliance with home exercise was verified through
telephone feedback. In the RG, several parameters (CE, fa-
tigue and morning stiffness of the BASDAI score, and spine
mobility in the thoracic and lumbosacral regions) improved
significantly at the end of treatment and at 6-month follow-up
compared with EXG and CG. In the RG, VAS for pain at the
end of treatment and 6-month follow-up was significantly
reduced in the cervical and lumbar regions compared to the
CG, but not to the EXG. BASFI showed significant improve-
ment in both the RG and EG compared to the CG both at the
end of treatment and 6-month follow-up.
The results of this RCT are strengthened by a 12-month
follow-up study [40] of the same educational and rehabilita-
tion protocol on a new sample of patients with stabilized AS
on TNF-inhibitor treatment. In the RG, a statistically signifi-
cant improvement was gained for all the outcomes from the
baseline. In the intergroup comparison, improvement in CE,
BASDAI, cervical rotation, toracolumbar rotation, and total
cervical movements was statistically superior in the RG com-
pared to the CG and the EXG. According to the authors, the
composite education–intervention program yielded positive
effects on pain, mobility, and physical function, not only in
the short-term but also in the long-term follow-up. The pro-
gram proposed is adherent to the ACSM guidelines, and
compliance to the exercise program at 12 months was high
(91 %), probably thanks to the regular phone feedback [40].
So et al. compared the effects of a combination treatment,
including incentive spirometer exercise (ISE) and convention-
al exercises (CE) to CE alone in AS patients stabilized by
TNF-inhibitor therapy. Patients were stratified for the effects
of TNF-inhibitor therapy, considering patients with low dis-
ease activity. The exercise setting was home-based, but pa-
tients were widely instructed by a physiotherapist before
starting the program, and compliance was verified through
an exercise diary. After completing the 16-week exercise
program, both groups improved significantly in CE, FFD,
and BASFI scores. However, only the study group improved
significantly in FVC, TLC, VC, and FEV1/FVC. A mild
superiority was detected also in functional ability and pulmo-
nary function in the study group. Although this is the first trial
about combined exercise treatment and ISE, the short-term
follow-up and the small sample limit the validity of these
results [33].
Gyurcsik et al. studied retrospectively the clinical data from
75 patients with (n=55) or without (n=20) biological therapy
and found significant difference in disease activity and pain
intensity in favor of the group treated with biological drugs. In
the second part of the study, ten volunteers from the biological
group were recruited for a prospective, nonrandomized
physiotherapeutic trial, including conventional exercise,
GPR, breathing exercises, manual mobilization of the chest,
stretching of the shortened muscles, and joint prevention
strategies. The exercise program was conducted individually
during the first 4 weeks and in small groups during the
following 8 weeks, in sessions of 1.5 h performed twice a
week for 12 weeks. Patient assessment of disease activity and
pain intensity, BASFI, BASDAI, FFD, CE, and modified
Schober’s index (MSI) significantly improved after the phys-
ical therapy program. The respiratory functional parameters
showed a nonsignificant tendency toward improvement. All
the evaluations were conducted only at the end of treatment,
and no follow-up was available [38].
None of the studies analyzed was adherent to the ACSM
recommendations, while the PEDro score was 7/10 in the
study by Masiero et al. [31] and 6/10 in the study by So
et al. [33].
Discussion
From the analysis of the literature, it seems well established
that non-pharmacological therapy, including education, exer-
cise, and physiotherapy, is an essential tool in the global
strategy for AS, recommended for all phases of the disease
[2, 43]. According to the review by Dagfinrud et al. [7], in
patients with AS, home-based or supervised exercise is supe-
rior compared to no exercise, group exercise is better than
home exercise, and the addition of spa-based exercises to
weekly group exercises is more effective than weekly group
exercises alone.
In the present review, 15 studies about physiotherapy op-
tions in AS were analyzed, 8 of which were specifically
dedicated to physical exercise [27, 29, 30, 32, 34, 36, 37,
39], while the other 7 [26, 28, 31, 33, 35, 38, 40], although not
focused expressively on this topic but on other options (spa-
exercise, association with biological drugs, and educational
therapy), also included exercise therapy. This feature may
limit the interpretation of the effectiveness of the additional
treatment, especially when the CG is represented by subjects
untreated [28, 31], since the results observed may be due
partly to the additional option (spa, education, association
with biological drugs, and respiratory training) but also to
therapeutic exercise included in the protocol. The modality
of exercise was outpatient supervised in 6/15 studies [26, 28,
32, 34, 36, 38], home-based in 4/15 studies [27, 33, 35, 39],
and inpatient in 1/15 studies [30]. In the studies by Masiero
et al. and Rosu et al., the modality was mixed, with an
outpatient-assisted learning module followed by prosecution
of the training program in a home-based setting [31, 37, 40].
One study [38] did not specify the setting in which exercise
was featured. From the results of the studies, the role of
educational–behavioral support and supervision seems pivotal
[39], not only to improve the performing technique but also to
increase motivation and adherence to exercise treatment,
which is the basis for home exercise therapy. On the other
hand, when compared to a composite exercise-educational
Clin Rheumatol (2014) 33:1217–1230 1227
program, the effect of an educational-only approach appears
mild and inconclusive [39, 40]. Home exercise protocol has
been proven effective only when performed at least for 30 min
per day, 5 days per week [27, 35, 44]. As a result, a home-
based program can be impaired by scarce compliance and
should be used as valid prosecution of an inpatient or a
supervised outpatient program, as proposed by Masiero et al.
[31, 40] and Rosu et al. [37], rather than a first line option.
The primary aim of exercise treatment is to avoid
stiffening in a flexed position and to maintain or improve
functional capacity and quality of life (QoL). The long-
term goal is the maintenance of a good posture [12]. In
the trials analyzed, the rehabilitation protocol was associ-
ated with a statistically significant improvement in func-
tional capacity (expressed by BASFI) and spinal mobility
(expressed by BASMI) in 10/15 studies. A statistically
significant improvement in quality of life expressed by
SF-36, HAQ, and ASQoL was found in 6/15 studies,
and BASDAI, the disease activity index, also registered
a statistically significant decrease in 9/15 studies. Exercise
has positive effects on psychological distress and fatigue,
thus improving quality of life, which should therefore
always be included between the outcomes of rehabilitation
treatment [44–46]. These observations are confirmed by a
recent survey by Brophyet al. [23], reporting functional
improvement in highly physically active and motivated
patients with AS despite the level of disease activity.
The RCT by Altan et al. [34] is the first study about Pilates
training in AS, reporting a statistically significant improve-
ment in the study group for BASDAI at the end of treatment
and for BASFI and BASMI at 3-month follow-up, suggesting
long-term effect of Pilates training. Rosu et al. proposed a
multimodal approach, including Pilates, Heckscher, and
McKenzie training, that could be interestingly investigated
in future studies [37].
Two studies about spa therapy were analyzed. Aydemir
et al. [26] retrieved only a positive trend toward improvement
in several response parameters in the treated group, with a
statistically significant improvement only for BASMI [28].
The persistent improvement retrieved on BASFI in patients
treated with spa therapy and TNF inhibitors in the study by
Ciprian et al. [28] is in line with the results of a previous RCT
in AS patients receiving standard drug treatment [47].
With the research criteria adopted, only the study by So
et al. was found in the literature in support of respiratory
rehabilitation [33]. The study by Ozdem et al. [48], excluded
from the present review for the study design (nonexperimen-
tal, case-control study), demonstrates that exercise intolerance
in AS patients is mainly due to decreased pulmonary function
rather than to musculoskeletal impairment, underlining the
pivotal role of cardiorespiratory training in these patients.
The interpretation of results was limited by a marked
heterogeneity between the studies included in the review.
The comparison between them was restricted by differences
in the study design, follow-up, sample size, and outcome
measures. Only 5/15 studies were rated in the PEDro database,
with a mean rating score of 5.8/10. As a result, this review is
lacking a proper rating system of the quality of studies.
Follow-up was variable between none (evaluation only at
the end of treatment, no follow-up) [26, 29, 32, 33, 35–37,
39], 3 [27, 34], 4 [31], 6 [28], and 12 months [40]. Some
studies were consistently limited by a small sample [28, 29,
32, 33, 38], a high rate of withdrawals [30], and an absent or
short follow-up. Furthermore, some studies did not specify the
medical therapy, and the rehabilitation protocol, along with
the treatment administered to the CG, was poorly described in
most of the studies. Again, adherence of the rehabilitation
protocols to the ACSM recommendations was not mentioned
in most of the studies, and the comparison of a proposed
protocol with a standard treatment was performed only in
7/15 studies, while the rest of the trials were uncontrolled or
expressed results in comparison to an untreated group [26, 28,
29, 31, 38, 40], or to patients with poor compliance [27, 35].
The inclusion of a CG receiving standard treatment should be
the first choice for future studies, in order to rate the effec-
tiveness of a new protocol compared to the conventional one.
A study protocol in rehabilitation should therefore include
a thorough, fully understandable description of the exercise
program, to make it reproducible throughout the world. In this
perspective, a valid option could be represented by the com-
posite educational and exercise program proposed byMasiero
et al. [31, 40]. The present study is characterized by a clear and
full description of the medical and rehabilitation treatment; in
particular, the protocol included two educational meetings and
12 rehabilitation exercise sessions which patients then contin-
ued in the home setting. In addition, the protocol was con-
ceived in accordance with the ACSM guidelines.
The success obtained with TNF inhibitors does not pre-
clude the need for physical therapy or exercise [5, 49, 50],
which plays a central role in AS patients’management also in
the era of biological drugs [17, 43]. Since this association
seemed to be more effective than a simple rehabilitation
program, a synergistic role between biological drugs and
rehabilitation might in fact be hypothesized, although the
mechanisms of functioning of the combination treatment are
not clear yet. An advantage of physiotherapy in AS patients
treated with TNF inhibitors is the more accurate standardiza-
tion of drug doses and evaluation of patients through disease
scales before starting a rehabilitation protocol. This increased
tendency to an objective dose-response rating may implement
a more standardized evaluation of clinical and rehabilitation
parameters in AS patients.
All the studies presented about association of rehabilitation
and biological drugs included a full description of the medical
treatment and adopted as a selection criteria stable clinical
picture, e.g., with a change in the BASDAI of no more than
1228 Clin Rheumatol (2014) 33:1217–1230
±1/10 units in the previous 3 months [31, 40] or a value of
BASDAI <4/10 units[33]. In the study by Ciprian et al. [28],
both the study and the CG showed an improvement of base-
line BASFI after receiving anti-TNF treatment administered
before the study period, suggesting a stabilizing role of bio-
logical drugs that could favor the synergistic role of rehabili-
tation in promoting recovery of functional abilities of these
patients.
The conclusions of our review are limited by the large
variability and lack of high level evidence of the literature
available. In many cases, association of a rehabilitation
option with other treatments in the absence of a CG
receiving standard treatment limited the evidence of effec-
tiveness of the exercise program itself. Therefore, strict
and homogeneous inclusion and exclusion criteria should
be adopted before referring patients to any treatment pro-
tocol. Furthermore, we did not include a statistic analysis
to support the evidence of our review. On the other hand,
at our knowledge, our review is the first in the literature
to analyze the superior effectiveness of exercise in addi-
tion to biological drugs in AS treatment compared to
biological treatment alone, addressing the role of possible
factors implicated in this synergy. In addition, an updated
research about the latest news in AS rehabilitation (spa
exercise, Pilates training combined with McKenzie and
Heckscher methods, Nordic walking) is provided.
Conclusion
Along with pharmacological therapy, exercise in AS has
shown effectiveness in terms of functional, mobility, qual-
ity of life, and interestingly, disease activity indices, espe-
cially when supervised. Supervision leads not only to
improvement of performing technique but also to
increased motivation, which ultimately has a positive
effect on mood and quality of life, controlling fatigue
and disease activity. Home-based exercise should be there-
fore adopted as a second-line choice after an outpatient
supervised regimen, possibly including educational–
behavioral sessions. New perspectives in AS rehabilitation,
which deserve future RCT and protocol-based research, are
represented by spa exercise and Pilates training and also
combined with other methods (McKenzie and Heckscher)
in a multimodal approach. Nordic walking may represent a
feasible cardiovascular training strategy, based on the
current and established ASCM recommendations, improv-
ing cardiovascular fitness and peripheral pain in patients
with AS. Rehabilitation in AS patients stabilized with
TNF inhibitors is a field of growing interest for physiat-
rists and rheumatologists, which will take advantage from
a proper standardization of pharmacological and exercise
therapy.
Conflict of interest None
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