Received: 3 April 2020 

|
  Revised: 11 July 2020 
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  Accepted: 12 July 2020

DOI: 10.1111/eci.13352

REVIEW

Effects of exercise programmes on pain, disease activity

and function in ankylosing spondylitis: A meta-analysis of
randomized controlled trials

Xinmiao Hu1  | Jialing Chen2  | Wenjuan Tang3  | Wenjian Chen1  | Yan Sang4,5   |

Lina Jia6

1
Department of Nephrology and
Rheumatology, Shanghai Children's
Abstract
Hospital, Shanghai Jiao Tong University, Background: To evaluate the effects of exercise programmes on pain, function and
Shanghai, China disease activity in patients with ankylosing spondylitis (AS).
2
School of Nursing, Nantong University,
Materials and methods: We searched PubMed, Embase, CNKI and Wanfang from
Nantong, China
3 inception to February 2020. Randomized controlled trials comparing exercises with
Department of Nursing, Shanghai Jiao
Tong University, Shanghai Children's nonexercise interventions in AS patients were applied. Studies that assessed the visual
Hospital, Shanghai, China analogue scale (VAS) pain score, the Bath Ankylosing Spondylitis Disease Activity
4
Department of Nursing, Affiliated Hospital Index (BASDAI), the Bath Ankylosing Spondylitis Functional Index (BASFI),
of Nantong University, Nantong, China
5
C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR) were included.
Department of Computer Technology,
Affiliated Hospital of Nantong University, Outcomes of home-based exercise intervention were also reported independently.
Nantong, China Results: Ten studies met the inclusion criteria in all, including 534 patients (278 ex-
6
Department of General Surgery, Shanghai ercise, 256 control). Compared with the nonexercise group, exercise group had statis-
Children's Hospital, Shanghai Jiao Tong
University, Shanghai, China
tically significant improvements in pain (weighted mean difference [WMD]: −1.02
[95% CI: −1.50 to −0.55]) (I2: 31%, P <.0001), BASDAI (WMD: −0.85 [95% CI:
Correspondence −1.09 to −0.61]) (I2: 20%, P <.00001), and BASFI (WMD: −0.66 [95% CI: −0.95
Yan Sang, Department of Nursing,
Department of Computer Technology, to −0.38]) (I2: 0%, P <.00001), but not in CRP and ESR. What's more, home-based
Affiliated Hospital of Nantong University, exercise programmes had positive impacts on BASFI, BASDAI and pain.
No.20 Xisi Road, Nantong, Jiangsu 226001,
Conclusions: For patients with AS, exercise programmes improve pain, function and
China.
Email: [email protected] disease activity. To confirm the results, more well-designed randomized controlled
trials with large number of patients are required.

KEYWORDS
ankylosing spondylitis, exercise, meta-analysis, quality of life

1  |   IN T RO D U C T ION spondylitis (AS). AS is an inflammatory disorder, resulting in

the bony fusion of vertebral joints, which is the cause of chronic
Axial spondyloarthritis (SpA), affecting the axial skeleton, is back pain.1,2 It was reported that the prevalence of AS is 0.1-
the main form of chronic inflammatory disease.1 The term 0.5%, and the female-to-male ratio is approximately 1:2.1,3
axial SpA encompasses both patients with nonradiographic Chronic back pain is a common symptom, but it lacks ef-
and radiographic axial SpA, which is also called as ankylosing fective, satisfactory treatments. 70 to 80% of patients with

© 2020 Stichting European Society for Clinical Investigation Journal Foundation. Published by John Wiley & Sons Ltd

Eur J Clin Invest. 2020;00:e13352.  |

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AS have inflammatory back pain, and it is listed as one of the articles in CNKI and Wanfang, using the following search
three clinical criteria for the diagnosis of AS.2,4,5 Different strategy: “ankylosing spondylitis”［title, abstract, key
therapeutic modalities have been used to reduce pain, im- word］and “exercise”［title, abstract, key word］or “train-
prove muscle strength and maximize long-term health-related ing”［title, abstract, key word］ or “rehabilitation”［title,
QoL. The Assessments of SpondyloArthritis International abstract, key word］ or “physical activity”［title, abstract,
Society and the European League Against Rheumatism key word］. Article type limited to randomized controlled
(ASAS/EULAR) recommends that pharmacologic treatment trials. Moreover, we also examined references of selected ar-
combined with nonpharmacologic treatment is the best way ticles and scanned conference summaries in order to avoid
to treat AS.6–8 One of the nonpharmacologic treatments is omitting valuable articles.
exercise, which includes home-based exercise,9 the Global
Posture Reeducation (GPR) method,10 multimodal exercise
programme,11 Tai Chi12 swimming13 and so on. 2.2  |  Inclusion and exclusion criteria
Several studies have demonstrated that exercise pro-
grammes improve muscle strength, walking performance We used the following inclusion criteria: (a) patients di-
and pulmonary functions and reduce pain effectively.14,15 agnosed by a rheumatologist as having AS and classified
Published meta-analysis involving small number of patients into AS according to the modified New York criteria were
showed that disease activity and function was improved included5, (b) randomized controlled trials, (c) the inter-
through exercise programmes. However, when they assessed vention group performed exercise (specific exercise, a home-
the effectiveness of disease activity by the Bath Ankylosing based exercise supervised by healthcare professionals), (d)
Spondylitis Disease Activity Index (BASDAI), the heteroge- the control group did not perform exercise, (e) the exercise
neity between studies was high (I2:69%, P = .005).16 Home- programme had made explanation exactly, (f) the exercise
based exercise has been regarded as one of the promising programme reported the length of intervention, and (g) the
nonpharmacologic treatments of AS due to its cheapness, outcomes must include either BASFI or BASDAI. Papers
easiness and efficacy.9,10 Previously, a meta-analysis was that did not meet the inclusion criteria were excluded.
conducted by Liang et al on the effectiveness of home-based
exercise interventions in improving health-related quality
of life in patients with AS. However, in their meta-analysis, 2.3  |  Data extraction and quality assessment
they found that home-based exercise could not reduce pain,17
which was the opposite result of other studies.9,18 Thus, these Data were extracted by two independent researchers, and
discrepancies prompted to explore whether exercise therapy discrepancies were resolved by discussions. If necessary, a
provided improvements on pain and disease activity. third author was consulted. The information collected from
Therefore, the aim of this meta-analysis was to assess the ef- each study was as follows: first author, year of publication,
fects of exercise programmes on pain, disease activity and func- country, classification criteria, medical therapy, sample size,
tion. Moreover, we evaluated the effectiveness of home-based modality of exercise, duration of each exercise session, over-
exercise on pain, disease activity and function individually. all duration of the intervention and type of control group. The
quality of each study was assessed independently using the
Jadad scale.21 The scores range from 0 to 5, where the high
2  |  M AT E R IA L S A N D ME T HODS scores indicate high quality.

2.1  |  Data sources and searches

2.4  |  Outcome measures
The review protocol was registered in PROSPERO with the
registration number CRD42019145975. The review followed The outcomes were pain, disease activity, function, C-reactive
the preferred reporting items for systematic review and meta- protein (CRP) and erythrocyte sedimentation rate (ESR). The
analysis (PRISMA) checklist.19 Reporting of the study con- disease activity was assessed by the BASDAI, which in-
forms to broad EQUATOR guidelines.20 cludes six questions concerned with the five main symptoms:
Two researchers independently searched PubMed, fatigue, spinal pain, joint pain or swelling, areas of localized
Embase, CNKI and Wanfang for articles in Chinese or tenderness, severity and duration of morning stiffness. The
English until 4 February 2020. The search terms were as lower the score, the less active the disease. The functional
follows: Ankylosing spondylitis and Randomized Controlled status was evaluated by the BASFI, which consists of ten
Trial and Exercise OR Training OR Physical Activity OR questions: two questions that assess the ability of the patient
Rehabilitation. We searched for original Chinese language to cope with daily life and eight questions that assess daily
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activities. The high scores indicate more severe impairment. criteria and were included in the meta-analysis (Figure  1).
The visual analogue scale (VAS) pain score evaluated the Table 1 showed the basic qualities of the included studies.
pain of the patients, with higher scores indicating more pain. There were 534 patients in this meta-analysis (278 in the ex-
ercise group and 256 in the control group). The quality scores
of 10 trials were between 1 and 4. Among these trials, 7 trials
2.5  |  Data analysis had a score of 3 or 4.
The modalities of exercise can be Tai Chi, home-based ex-
Each study evaluated the effectiveness of the intervention- ercise, Swiss ball exercises, supervised exercises and Pilates.
control group by calculating a weighted mean difference The control group were education, usual care or usual treat-
(WMD) and 95% confidence interval (95% CI) for different ment. The duration of the exercise programmes ranged from
variable (VAS, BASFI, BASDAI, ESR and CRP). The re- 8 to 24 weeks (Table 1).
sults of each trial were pooled through a meta-analysis using Sulphasalazine (SLZ) were used in 5 of the 10 studies,
an inverse variance method with a fixed effects model. I2 val- methotrexate (MTX) were used in 3 of the 10 studies, nonste-
ues were used to evaluate the total variation due to heteroge- roidal anti-inflammatory drugs (NSAIDs) were used in 7 of
neity rather than chance, which ranged from 0% to 100%. The the 10 studies, and anti-tumour necrosis factor-α (anti-TNF-α)
high values indicated high heterogeneity. We also assessed agents were used in 4 of the 10 studies. There was 1 study12
the effectiveness of home-based exercise programmes on continuing their current prescription medication in the past
pain, function and disease activity separately. 4 weeks, but that study did not clarify clearly (Table 1).
We used Revman (version 5.3) to perform statisti-
cal analysis and P  <  .05 was considered statistically
significant. 3.2  |  Effects of the exercise programmes

3.2.1  | BASFI
3  |   R E S U LTS
Eight trials9,10,14,15,22,24–26 including 421 AS patients inves-
3.1  |  Study selection and characteristics tigated on BASFI were initiated. Compared with the control
group, the exercise programmes provided a positive impact
A total of 3681 studies were identified by the literature on BASFI (WMD: −0.66 [95% CI: −0.95 to −0.38]) (I2: 0%,
search, of which 10 studies9,10,12,14,15,22–26 met the inclusion P <.00001) (Figure 2).

F I G U R E 1   Flow chart
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T A B L E 1   Characteristics of included studies

Intervention group Control group

Jadad Classification Sample Length, Sample

Study Country Score criteria Medical therapy size Exercise type weeks size Comparator
Durmus et al, Turkey 1 New York criteria NSAIDs, MTX, SLZ 25 Supervised home 12 18 Usual treatment
20099 exercise
Durmus et al, Turkey 2 New York criteria NSAIDs, MTX, SLZ 19 Supervised home 12 13 Usual treatment
200910 exercise
Durmus et al, Turkey 2 New York criteria NSAIDs, MTX, SLZ 19 Supervised home 12 13 Usual treatment
200910 exercise
Altan et al, Turkey 3 New York criteria NSAIDs, SLZ, anti-TNF-α 29 Pilates 12 24 Usual treatment
201222
Souza et al, Brazil 3 New York criteria NSAIDs, MTX, SLZ, 30 Swiss ball exercises 16 30 Usual care
201714 anti-TNF-α
Lee et al, South Korea 3 New York criteria Lack of exact explanationa 13 Tai Chi 8 17 Usual care
200812
Chen et al, China 3 New York criteria NSAIDs 43 Tai Chi 8 43 Usual treatment
201524
Masiero et al, Italy 4 New York criteria anti-TNF-α 21 Supervised home 12 22 Education
201425 exercise + Education
Widberg et al, Sweden 4 New York criteria NSAIDs, DMARD 16 Home exercise 8 16 Usual care
200926
Li et al, 201223 China 2 New York criteria NSAIDs, SLZ 43 Supervised 24 40 Usual treatment
Masiero et al, Italy 3 New York criteria anti-TNF-α 20 Supervised home 12 20 Education
201115 exercise + Education
Abbreviations: anti-TNF-α, anti-tumour necrosis factor-α; DMARD, disease modifying anti-rheumatic drug; MTX, methotrexate; NSAIDs, nonsteroidal anti-inflammatory drugs; SLZ, sulphasalazine.
a
Continue their current prescription medication in the past 4 weeks.
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F I G U R E 2   The effect of exercise programme on BASFI

3.2.2  | BASDAI 3.4  |  Effects on biological parameters

Ten trials9,10,12,14,15,22–26 including 534 AS patients reported on CRP and ESR were assessed in only 3 trials.14,23,24 Exercise
BASDAI were initiated. The fixed-effect model assessment did not have any positive effect on CPR (WMD: 0.43 [95%
showed that there was no significant heterogeneity between CI: −1.39 to −2.24]) (I2: 38%, P  =  .64) and ESR (WMD:
the exercise group and the control group in BASDAI (P = .25, −0.46 [95% CI: −3.17 to 2.26]) (I2: 38%, P = .74) (Figures 5
I2  =  20%). A statistically difference was observed  (WMD: and 6).
−0.85 [95% CI: −1.09 to −0.61]) (P < .00001), which showed
that compared with the control group, exercise interventions
reduced the BASDAI scores (Figure 3). 3.5  |  Effect of the home-based
exercise programmes

3.3  | Pain Out of the ten studies, five studies9,10,15,25,26 assessed the ef-
fectiveness of home-based exercise programmes. One trial25
Only five trials10,15,23–25 including 399 patients reported reported two different home-based exercises: a conventional
on pain were evaluated. Two studies10,25 used the VAS exercise regimen and exercises based on the GPR method.
to assess pain in different parts of the body. Exercise Moreover, two trials,10,25 which were reported on VAS, as-
has a positive effect on pain. The total WMD was −1.02 sessed pain in different parts of the body. Patients in four
(95%CI, −1.50 to −0.55) for pain, and the I2 value was studies9,10,15,25 were telephoned weekly by the researchers
31% (P  <  .0001), which was favourable for the exercise or experienced physiotherapists to enhance compliance
programmes. (Figure 4). with the home-based exercise programme. One study26

F I G U R E 3   The effect of exercise programme on BSADI

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F I G U R E 4   The effect of exercise programme on pains

F I G U R E 5   The effect of exercise programme on CRP

F I G U R E 6   The effect of exercise programme on ESR

had regular physiotherapeutic visits to compliance with the 4  |  DISCUSSION

self-exercise.
Table 2 shows home-based exercise indicated positive im- This meta-analysis showed that exercise programmes had
pacts on BASFI (WMD: −0.69 [95% CI: −1.11 to −0.27]) greater benefits than no invention group in improving pain,
(I2: 28%, P =.001), BASDAI (WMD: −0.75 [95% CI: −1.11 physical function and disease activity, especially in some
to −0.40]) (I2: 12%, P <.0001) and pain (WMD: −1.38 [95% studies that involve AS patients receiving home-based exer-
CI: −2.42 to −0.33]) (I2: 0%, P =.01). Given the effects of cise. But exercise programmes did not have positive effects
exercise duration, the home-based exercise with different on CPR and ESR.
exercise duration was also analysed. There were significant In AS, the modified New York criteria have been used
improvements for BASDAI and BASFI scores in different ex- widely for the classified purpose, but are not applicable in early
ercise duration. Except for 24 weeks, there were significant stages of disease when the characteristic radiographic sacroi-
improvements in the VAS pain. liitis are not visible.27 Magnetic resonance imaging (MRI) has
been used to detect inflammation in the spine and sacroiliac
joints, which has helped in the early identification of axial SpA
3.6  |  Funnel plot of publication bias in the ‘non-radiographic stage’ of the disease.2 This resulted
in the concept of axial SpA including both patients with and
The asymmetric results of funnel plot analysis indicate that there without radiographic damage. New classification criteria for
may be publication bias in the included research. (Figure 7). the broader group of axial SpA have been proposed by ASAS.
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T A B L E 2   Meta-analyses. Results showing BASFI score, BASDAI score and pain between home-based exercise and control groups

Heterogeneity
Number of Sample
Character studies size WMD 95% CI Chi2 df P I2
Home-based exercise
Overall
BASFI 6 222 −0.69 (−1.11, −0.27) 6.98 5 .001 28
BASDAI 6 222 −0.75 (−1.11, −0.40) 5.67 5 <.0001 12
Pain 6 230 −1.38 (−2.42, −0.33) 3.62 5 .010 0
Exercise Duration
8 weeks
BASFI 2 118 −0.73 (−1.17, −0.29) 0.67 1 .001 0
BASDAI 3 148 −1.03 (−1.43, −0.63) 4.34 2 <.00001 50
Pain 1 86 −1.62 (−2.39, −0.85) Not applicable <.0001 Not applicable
8＜n ≤ 16 weeks
BASFI 7 303 −0.61 (−0.99, −0.24) 6.23 6 .001 4
BASDAI 7 303 −0.67 (−1.00, −0.34) 6.09 6 <.0001 1
Pain 6 230 −1.38 (−2.42, −0.33) 3.62 5 .010 0
≤24 weeks
BASDAI 1 83 −1.10 (−1.78, −0.42) Not applicable .002 Not applicable
Pain 1 83 −0.30 (−1.03, 0.43) Not applicable .42 Not applicable
Abbreviations: BASDAI, The Bath Ankylosing Spondylitis Disease Activity Index; BASFI, The Bath Ankylosing Spondylitis Functional Index; CI, confidential
interval; WMD, weighted mean difference.

One meta-analysis was conducted to assess the strength of

exercise versus physical activity, which only included 3 stud-
ies in quantitative synthesis, found that exercise had greater
power than physical activity in BASFI and BASDAI.29 The
other meta-analysis involving 331 patients indicated that ex-
ercise could improve disease activity and physical function.16
But this meta-analysis included a study, whose group control
had a rehabilitation. These results were similar to our study.
Besides, our meta-analysis involved 534 patients with AS,
and all control groups of included studies had no exercise
intervention.
NSAIDs are highly efficacious in reducing stiffness and
back pain in AS patients and are recommended as first-
F I G U R E 7   Funnel plot line treatment for patients in AS.30 They should be used
in accordance with the patient's symptoms. If the patient
is in remission, dose reduction or discontinuation should
However, classification criteria are for case identification of have a try.1 The safety of long-term NSAIDs therapy has
clinical research, which are quite different from the diagnostic been a concern for a long time. Haroon et al31 conducted
criteria. Classification criteria are applicable to patients who are a retrospective study and discovered that NSAIDs treat-
already diagnosed by the current signs and symptoms of the ment was linked to reduced cardiovascular risk and a de-
disease and the patient characteristics. Because we lack of gold crease in inflammation in AS patients. However, Bakland
standards in axial SpA, classification criteria, some clinical in- et al32 studied patients in Norway and found that infrequent
dices and some laboratory indices are needed to combine for NSAIDs therapy was even linked to increased mortality in
accurate diagnosis of axial SpA.27,28 patients with long-term AS. Conventional disease mod-
As far as we know, 2 meta-analyses assessing the effective- ifying anti-rheumatic drugs (DMARDs), such as SLZ,
ness of exercise in patients with AS have been published.16,29 MTX or leflunomide, are not effective in the therapy of
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axial manifestations of spondyloarthritis. But Lie and his differed between trials. Despite these limitations, we found
co-workers33 found that a combination of a DMARD with exercise programmes were efficient in improving function
a tumour necrosis factor (TNF) blocker had an advantage. and disease activity.
When NSAID treatment is inadequate or contraindicated in Our results show that exercise programmes improve
AS patients, TNF inhibitors liking infliximab, etanercept, function, pain and disease activity, and should be consid-
adalimumab, golimumab and certolizumab are a mainstay ered as an important complement in the management of
of therapy.1,2 A short disease duration, a high baseline level patients with AS. Our study also indicates that home-based
of inflammatory markers, a young age and a low baseline exercises are efficacious and should be recommended to
level of functional disability the predictors of a good re- AS patients. Further studies are needed to investigate the
sponse to TNF inhibitors, patients at any disease stage may effects of specific exercise (Pilates, Tai Chi, Swiss ball ex-
benefit.2 What's more, treatments targeting the interleu- ercises, etc) on pain, quality of life, function and disease
kin-23-interleukin-17 pathway have appeared to be prom- activity.
ising in AS patients,1,2,34 but its role in treating AS patients Treatment of AS requires multidisciplinary management
remains to be confirmed. coordinated by the rheumatologist, and it must be rooted in a
As a distressing symptom in AS patients, pain impairs shared decision between the rheumatologist and the patient.
their QoL and influences working capacity.35–37 Up to Management should aim at the best possible health-related
now, lots of nonpharmacologic measures have been taken quality of life in AS patients.
to reduce pain in patients with AS, like aquatic exercise,38
exergames,39 relaxation programme40 and so on. Exercise ACKNOWLEDGEMENTS
programmes have an influence on the management of AS. The authors would like to thank Science and technology
Home-based exercise,41 group exercise42 and supervised Project of Nantong City (Grant No. MSZ19191); The pro-
training43 have been proved to alleviate pain, which support ject of 333 Natural Science Foundation of Jiangsu (Grant
our results, with a WMD for pain of −1.02 (95% CI, −1.50 No. BRA2019206); and Innovation Training Program for
to −0.55) without heterogeneity. Two of five trials that were Nantong University (Grant No. 2019116 and 2019129).
included to assess the power of exercise on pain showed
a positive influence. In the study by Chen,24 indicating a CONFLICT OF INTEREST
slight improvement, the exercise programme was rooted in The authors have no conflicts of interest to declare.
30 minutes of Tai Chi, and all patients were allowed to take
routine treatment. AUTHOR CONTRIBUTIONS
There were lots of various modalities of exercise pro- XMH and YS designed the study. XMH and WJT carried
grammes. Our study investigated the effects of home-based out experiments. JLC, YS and LNJ analysed the data. WJT,
exercise versus nonexercise inventions, which indicated that JLC, and WJC made the figures. XMH, YS drafted and re-
home-based had positive influences on pain, disease activity vised the paper; all authors approved the final version of the
and body function. The meta-analysis,17 published in 2015, manuscript.
put forward the conclusion that home-based exercise interven-
tions improved body function and disease activity, but had no ORCID
positive effects on pain. It included 4 different instruments to Yan Sang  https://orcid.org/0000-0003-0856-2318
assess pain, such as VAS pain score, the Nottingham Health
Profile (NHP), Self-Efficacy Scale (SES) and the Medical R E F E R E NC E S
Outcomes Short-Form-36 questionnaire (SF-36). But our 1. Sieper J, Poddubnyy D. Axial spondyloarthritis. Lancet.
study used VAS pain score only to assess the strength of exer- 2017;390:73-84.
cise on pain. Several studies evaluating pain in different parts 2. Taurog JD, Chhabra A, Colbert RA. Ankylosing spondylitis and
axial spondyloarthritis. N Engl J Med. 2016;374:2563-2574.
of the body were included in quantitative synthesis.10,25
3. Wang R, Ward MM. Epidemiology of axial spondyloarthritis: an
There were some limitations of this meta-analysis that
update. Curr Opin Rheumatol. 2018;30:137-143.
should be acknowledged. First, all included studies were 4. van den Berg R, de Hooge M, Rudwaleit M, et al. ASAS modifica-
published only in English and Chinese, which might have tion of the Berlin algorithm for diagnosing axial spondyloarthritis:
resulted in a potential language bias. Second, only 10 trials results from the SPondyloArthritis Caught Early (SPACE)-cohort
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