Review Article Comparison between specific exercises and ...

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Int J Clin Exp Med 2016;9(9):17028-17039 www.ijcem.com /ISSN:1940-5901/IJCEM0033132 Review Article Comparison between specific exercises and physical therapy for managing patients with ankylosing spondylitis: a meta-analysis of randomized controlled trials Wen-Dien Chang 1 , Yung-An Tsou 2 , Chia-Lun Lee 3 1 Department of Sports Medicine, China Medical University, Taichung, Taiwan (R.O.C); 2 Graduate Institute of Clinical Medical Science, China Medical University, Taichung, Taiwan (R.O.C); 3 Division of Physical and Health Education, Center for General Education, National Sun Yat-sen University, Kaohsiung, Taiwan (R.O.C) Received June 1, 2016; Accepted August 10, 2016; Epub September 15, 2016; Published September 30, 2016 Abstract: Engaging in specific exercises and physical therapy are two strategies for managing ankylosing spondy- litis (AS). In this study, we conducted a systematic review and meta-analysis to compare the differences between the outcomes of these strategies. Data from January 2005 - July 2014 was retrieved from the MEDLINE, PubMed, AMED, Embase, and CINAHL databases. Randomized controlled trials were conducted, and the outcomes of these interventions were compared using a meta-analysis. The outcome assessments were classified into the domains of impairment, activity limitations, and participation restrictions for AS according to the International Classification of Functioning model. Eight articles were included in the analysis, and four specific exercises, namely Pilates, aero- bic and aquatic exercises, and the Global Postural Reeducation method, were compared with physical therapy. The meta-analysis results revealed that some outcomes of chest expansion and pulmonary function favored the specific exercises. The outcomes of the Bath Ankylosing Spondylitis Metrology Index, Bath Ankylosing Spondylitis Disease Activity Index, and Bath Ankylosing Spondylitis Functional Index were favored physical therapy. Both interventions exhibited low to moderate effects on impairment, activity limitations, and participation restriction among the pa- tients with AS. However, different outcomes for specific exercises and physical therapy were found; a combination of both interventions is suggested as a clinical program for patients with AS. Keywords: Ankylosing spondylitis, exercise, meta-analysis Introduction Ankylosing spondylitis (AS), a chronic inflam- matory disease, mainly affects the axial skele- ton, peripheral joints, and tendons [1]. Thus, AS symptoms reduce the physical activity of patients. The main AS symptoms are pain, mus- cle stiffness, decreased function activity, and decreased spinal mobility. These symptoms are often accompanied by sleep disturbances and psychological problems, such as depression [1]. Treatment strategies for AS have several basic principles [2]. Administering immediate analgesics to patients with AS to reduce pain and resolve morning muscle stiffness is criti- cal. Additionally, in patients with early-stage AS it is essential to improve spinal mobility as well as to maintain the appropriate posture and physical condition. When the physical condition of patients with AS improves, treatment strate- gies focus on psychological problems, reducing the likelihood of depression. Furthermore, when short-term treatment goals are achieved, improving spinal mobility and pulmonary func- tion are vital long-term goals for patients with AS [3]. The ideal method of managing AS is using conventional treatments to decrease symptoms and promote long-term quality of life by controlling inflammatory pain and preventing articular deformation [4]. Conventional treatments for AS currently in- clude physical therapy, pharmacological treat- ment, and exercise therapy [3]. Patients with AS

Transcript of Review Article Comparison between specific exercises and ...

Int J Clin Exp Med 2016;9(9):17028-17039www.ijcem.com /ISSN:1940-5901/IJCEM0033132

Review Article Comparison between specific exercises and physical therapy for managing patients with ankylosing spondylitis: a meta-analysis of randomized controlled trials

Wen-Dien Chang1, Yung-An Tsou2, Chia-Lun Lee3

1Department of Sports Medicine, China Medical University, Taichung, Taiwan (R.O.C); 2Graduate Institute of Clinical Medical Science, China Medical University, Taichung, Taiwan (R.O.C); 3Division of Physical and Health Education, Center for General Education, National Sun Yat-sen University, Kaohsiung, Taiwan (R.O.C)

Received June 1, 2016; Accepted August 10, 2016; Epub September 15, 2016; Published September 30, 2016

Abstract: Engaging in specific exercises and physical therapy are two strategies for managing ankylosing spondy-litis (AS). In this study, we conducted a systematic review and meta-analysis to compare the differences between the outcomes of these strategies. Data from January 2005 - July 2014 was retrieved from the MEDLINE, PubMed, AMED, Embase, and CINAHL databases. Randomized controlled trials were conducted, and the outcomes of these interventions were compared using a meta-analysis. The outcome assessments were classified into the domains of impairment, activity limitations, and participation restrictions for AS according to the International Classification of Functioning model. Eight articles were included in the analysis, and four specific exercises, namely Pilates, aero-bic and aquatic exercises, and the Global Postural Reeducation method, were compared with physical therapy. The meta-analysis results revealed that some outcomes of chest expansion and pulmonary function favored the specific exercises. The outcomes of the Bath Ankylosing Spondylitis Metrology Index, Bath Ankylosing Spondylitis Disease Activity Index, and Bath Ankylosing Spondylitis Functional Index were favored physical therapy. Both interventions exhibited low to moderate effects on impairment, activity limitations, and participation restriction among the pa-tients with AS. However, different outcomes for specific exercises and physical therapy were found; a combination of both interventions is suggested as a clinical program for patients with AS.

Keywords: Ankylosing spondylitis, exercise, meta-analysis

Introduction

Ankylosing spondylitis (AS), a chronic inflam- matory disease, mainly affects the axial skele-ton, peripheral joints, and tendons [1]. Thus, AS symptoms reduce the physical activity of patients. The main AS symptoms are pain, mus-cle stiffness, decreased function activity, and decreased spinal mobility. These symptoms are often accompanied by sleep disturbances and psychological problems, such as depression [1]. Treatment strategies for AS have several basic principles [2]. Administering immediate analgesics to patients with AS to reduce pain and resolve morning muscle stiffness is criti-cal. Additionally, in patients with early-stage AS it is essential to improve spinal mobility as well

as to maintain the appropriate posture and physical condition. When the physical condition of patients with AS improves, treatment strate-gies focus on psychological problems, reducing the likelihood of depression. Furthermore, when short-term treatment goals are achieved, improving spinal mobility and pulmonary func-tion are vital long-term goals for patients with AS [3]. The ideal method of managing AS is using conventional treatments to decrease symptoms and promote long-term quality of life by controlling inflammatory pain and preventing articular deformation [4].

Conventional treatments for AS currently in- clude physical therapy, pharmacological treat-ment, and exercise therapy [3]. Patients with AS

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receive pharmacological treatment to relieve pain and discomfort often including non-steroi-dal anti-inflammatory drugs and sulfasalazine, which have analgesic properties [4]. In addition to pain relievers, patients with AS must receive physical and exercise therapies, which could maintain spinal mobility and appropriate pos-ture as well as improve muscular strength and functional activity [5]. Therefore, pain relievers, physical therapy, and exercise therapy are con-ventional treatment strategies for patients with AS. Home-based physical therapy is convenient and can improve self-health having a high degree of patient acceptance [6]. Furthermore, physical therapy for AS includes stretching, strengthening, flexibility, and breathing exercis-es. Under the guidance of physical therapists, hospital-based or home-based physical thera-py could improve trunk stiffness and reduce breathing restrictions [7]. Exercise therapy generally refers to disease-specific exercises, including active exercise training that focusing on improving the physical conditions of patients with AS [8]. Specific exercise is a rehabilitation strategy employed to target specific diseases that are particular to one type of exercise. The exercise is applied using various training meth-ods, focusing on the developments of muscle strength, endurance, flexibility, and cardiopul-

patients [12]. However, the benefits of specific exercises and physical therapy in patients with AS require further exploration. Therefore, this meta-analysis reviewed relevant studies on specific exercises and physical therapy for AS and compared the outcomes of the 2 interventions.

Materials and methods

Study selection

The keywords “ankylosing spondylitis”, “exer-cise”, “physical therapy”, and “rehabilitation” were applied in searches of MEDLINE, PubMed, AMED, Embase, and CINAHL databases to obtain relevant articles. Article inclusion crite-ria in the current study are as follows: random-ized controlled trials, patients with AS as the experimental group, intervention involving spe-cific exercises, control group undergoing physi-cal therapy, and article publication date between January 2005 and July 2014. Studies not published in English, single group study designs, reviews, and case reports were exclud-ed. The searched abstracts were screened and selected by 2 investigators. Finally, the full-text articles were selected and included in the pres-ent study. The Jadad quality score, which is a

Figure 1. Flow chart of the article selection process.

monary function to enhance patient’s quality of life [9]. Specific exercises can be per-formed in different environ-ments for improving AS symp-toms and cardiopulmonary fit-ness [10]. In contrast to physi-cal therapy, specific exercises for patients with AS are more similar to those performed by healthy people entailing low patient susceptibility and psy-chological rejection. Further- more, these exercises may be included in the International Classification of Functioning (ICF) model to increase pa- tient participation [11]. ICF model could categorize func-tion and disability in patients with AS; for designing a suit-able treatment program, the comprehensive descriptions of the ICF could inform clini- cal therapists how AS affects

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Table 1. Characteristics of 8 articles

Author (year) Groups Sample size

Drop out Intervention Quality

scoreDundar (2014) [14] Experimental group 35 0 Aquatic exercise, 1 hr/day, 5 times/week, 4 weeks 5

Control group 34 0 Home-base physical therapy, 1 hr/day, 7 times/week, 4 weeksRoşu (2014) [15] Experimental group 48 0 Pilatesa, 50 min/day, 3 times/week, 48 weeks 3

Control group 48 0 Physical therapy, 50 min/day, 3 times/week, 48 weeksAltan (2012) [16] Experimental group 30 1 Pilates, 1 hr/day, 3 times/week, 12 weeks 5

Control group 25 1 Physical therapyb Günendi (2010) [17] Experimental group 16 0 Aerobic exercise (walking), 1 hr/day, 5 times/weeks, 3 weeks 5

Control group 16 0 Home-base physical therapy, 30 mins/day, 7 times/weeks, 3 weeksKarapolat (2009) [18] Experimental group 15 2 Aquatic exercise (swimming)c, 30 min/day, 3 times/week, 6 weeks 4

Experimental group 15 3 Aerobic exercise (walking)c, 30 min/day, 3 times/week, 6 weeksControl group 15 3 Physical therapy, 30 min/day, 1 time/week, 6 weeks

Durmusx (2009) [19] Experimental group 20 1 GPR, daily, 12 weeks 3Control group 21 2 Physical therapy, daily, 12 weeks

Fernández-de-las-Penas (2006) [20] Experimental group 20 0 GPR, 1 hr/day, 1 time/week, 15 weeks 4Control group 20 0 Physical therapy, 1 hr/day, 1 time/week, 15 weeks

Fernández-de-las-Penas (2005) [21] Experimental group 21 1 GPR, 1 hr/session, 1 session/week, 15 weeks 4Control group 22 2 Physical therapy, 1 hr/session, 1 session/week, 15 weeks

aCombined Heckscher and McKenzie methods with exercise protocol; bThere are no treatment frequency and duration in the article; cCombined physical therapy with exercise proto-col. GPR, Global Postural Reeducation.

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5-point scale, was applied to assess article quality, with higher scores representing higher article quality.

Data extraction and statistical method

Data of the recruited articles were extracted for analysis in three steps. First, data on author, publication year, sample size, interventions, and article quality were collected and reviewed. Second, the intervention types, assessments, and results of specific exercises and physical therapy were extracted, indicating consider-able differences in the outcomes after the interventions. Third, the outcome assessments on the effects of each intervention were classi-fied according to the ICF model as impairment, activity limitations, and participation restric-tions; these terms were based on those from a previous study by Moncur [13]. Furthermore, two investigators collected the extracted data and analyzed the standardized mean differ-ence and 95% confidence intervals by using MedCalc software (Mariakerke, Belgium) for meta-analysis. The publication bias of the recruited articles was investigated to deter-mine its influence on the meta-analysis, as revealed using Rosenthal’s file drawer method, in which a fail-safe number higher than the tol-erance level influences the outcomes. The out-comes of assessment items, representing the effect size, were compared between specific exercises and physical therapy; positive stan-dardized mean differences favored specific exercises, whereas negative values favored physical therapy. Homogeneity was assessed using the Cochran Q test, and P > 0.05 or I2 < 50% was considered significant. According to Cohen’s rule, small (effect size = 0.2-0.5), mod-erate (effect size = 0.5-0.8), and large (effect size > 0.8) effects were expressed for various assessment outcomes.

Results

Study characteristics

In the present study, through keyword search-ing, 57 related articles were obtained, compris-ing 31 review articles, three case reports, 20 experimental articles, and eight randomized controlled trials that conformed to the inclu-sion criteria (Figure 1 and Table 1) [14-21]. Furthermore, four specific exercises, namely Pilates, aerobic and aquatic exercises, and the

Global Postural Reeducation (GPR) method, were used in the experimental group (Table 2). Physical therapy was applied in the control group in all included articles, which comprised hospital-based and home-based physical ther-apy, involving flexibility, stretching, muscular strengthening, and respiratory training for patients with AS under physiotherapist guid-ance (Table 3). The Jadad quality scores of the included articles ranged 3-5, indicating high study quality.

Outcome assessments

The outcome assessments of the eight articles were recorded and measured using the follow-ing three categories.

Physical activity outcomes: Chest expansion was used to measure the increased chest cir-cumference at the level of the fourth intercos-tals during maximum inspiration, representing the respiratory movement limitations [16, 18, 19]. The finger-to-floor distance, modified Schober, and lumbar side flexion tests were used to measure the degree of lumbar spine flexibility [14, 15, 20, 21]. Moreover, the tragus-to-wall distance and cervical rotation tests were applied to measure the degree of cervical spine flexibility [14, 15, 20, 21]. The intermal-leolar distance test was employed to measure the degree of genu varum or valgum [20, 21]. The Bath Ankylosing Spondylitis Metrology Index (BASMI), a 10-point scale, was used to measure the severity of trunk stiffness in the patients with AS; this index was combined with the results of cervical rotation, tragus-to-wall distance, lumbar side flexion, modified Scho- ber, and intermalleolar distance tests. Scores of 0 and 10 represent no limitation and most severe limitation, respectively [14-16, 20, 21].

Cardiopulmonary and endurance outcomes: The exercise test included a cardiopulmonary test conducted using the Bruce protocol for patients with AS and employing Masterscreen CPX (Viasys Health Care, Jaeger, Wurzburg, Germany) to record the cardiopulmonary parameters, namely forced expiratory volume in 1 second (FEV1), vital capacity (VC), forced VC (FVC), FEV1-FVC, and pVO2 [18, 19]. The 6-min walking test (6 MWT) was used to assess the functional performance and endurance of patients while walking. The maximum distance

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Table 2. Summary of the assessments and results of experimental groups

Author (year) Specific exercises Assessments Results

Dundar (2014) [14] Aquatic exercise VAS, chest expansion, BASFI, BASMI, BASDAI, SF-36, modified Schober test VAS, BASFI, BASMI, and BASDAI decreased; SF-36 improved after intervention*VAS, BASMI, BASDAI decreased and SF-36 improved after 12 wks follow-up*

Roşu (2014) [15] Pilates VAS, modified Schober test, finger-to-floor distance, BASMI, BASFI, BASDAI, chest expansion

VAS, BASMI, BASFI, and BASDAI decreased; modified Schober test, finger-to-floor distance, and chest expansion improved after intervention*

Altan (2012) [16] Pilates BASFI, BASMI, BASDAI, ASQoL, Chest expansion BASFI, BASMI, and BASDAI decreased; chest expansion increased after intervention*BASFI, and BASMI decreased at 24 wks follow-up*

Günendi (2010) [17] Aerobic exercise BASDAI, BASFI BASDAI and BASFI decreased after intervention*

Karapolat (2009) [18] Aquatic exerciseAerobic exercise

BASMI, BASFI, BDI, Chest expansion, NHP, BASDAI, 6 MWT, exercise test Swimming: 6 MWT, NHP decreased; chest expansion increased; exercise test improved after intervention*Walking: 6 MWT, NHP decreased; exercise test improved after intervention*

Durmusx (2009) [19] GPR VAS, BASFI, BASDAI, chest expansion, 6 MWT, exercise test VAS, BASFI, and BASDAI decreased; chest expansion, 6 MWT, and exercise test improved after intervention*

Fernández-de-las-Penas (2006) [20]

GPR BASFI, BASMI, BASDAI, tragus-to-wall distance, modified Schober test, cervi-cal rotation, lumbar side flexion, intermalleolar distance

BASFI, BASMI, and BASDAI decreased; tragus-to-wall distance, modified Schober test, cervical rotation, lumbar side flexion, intermalleolar distance improved after intervention and 1 year follow-up*

Fernández-de-las-Penas (2005) [21]

GPR BASFI, BASMI, BASDAI, tragus-to-wall distance, modified Schober test, cervi-cal rotation, lumbar side flexion, intermalleolar distance

BASFI, and BASMI decreased; tragus-to-wall distance, modified Schober test, cervical rotation, lumbar side flexion, intermalleolar distance improved after intervention

*P < 0.05, before vs. after intervention or follow-up. VAS, visual analog scale; BASMI, Bath Ankylosing Spondylitis Metrology Index; BASDAI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; 6 MWT, 6-minute walking test; ASQoL, ankylosing spondylitis quality of life; NHP, Nottingham Health Profile.

Table 3. Summary of the assessments and results of control groupsAuthor (year) Physical therapy Assessments ResultsDundar (2014) [14] Muscle relaxation, flexibility, stretching, respi-

ratory, and muscular strengthening VAS, chest expansion, BASFI, BASMI, BASDAI, SF-36, modified Schober test

VAS, BASFI, BASMI, and BASDAI decreased; SF-36 improved after physical therapy*VAS, BASMI, BASDAI decreased and SF-36 improved after 12 wks follow-up*

Roşu (2014) [15] Muscular stretching, and strengthening VAS, modified Schober test, finger-to-floor dis-tance, BASMI, BASFI, BASDAI, chest expansion

VAS, BASMI, BASFI, and BASDAI decreased; modified Schober test, finger-to-floor distance, and chest expansion improved after physical therapy*

Altan (2012) [16] Physical activity training BASFI, BASMI, BASDAI, ASQoL, Chest expansion BASMI decreased; chest expansion increased after physical therapy.BASMI decreased at 24 wks follow-up.

Günendi (2010) [17] Muscular stretching, and strengthening BASDAI, BASFI BASDAI and BASFI increased after physical therapy

Karapolat (2009) [18] Flexibility, stretching, and respiratory trainings BASMI, BASFI, BDI, chest expansion, NHP, BASDAI, 6 MWT, exercise test

Exercise test improved after physical therapy*

Durmusx (2009) [19] Flexibility, stretching, and respiratory trainings VAS, BASFI, BASDAI, chest expansion, 6 MWT, exercise test

VAS, BASFI and BASDAI decreased; chest expansion, 6 MWT and exercise test improved after physical therapy*

Fernández-de-las-Penas (2006) [20]

Flexibility, stretching, muscular strengthening, and respiratory trainings

BASFI, BASMI, BASDAI, tragus-to-wall distance, modified Schober test, cervical rotation, lumbar side flexion, intermalleolar distance

Tragus-to-wall distance, lumbar side flexion after physical therapy and 1 year follow-up*

Fernández-de-las-Penas (2005) [21]

Flexibility, stretching, muscular strengthening, and respiratory trainings

BASFI, BASMI, BASDAI, tragus-to-wall distance, modified Schober test, cervical rotation, lumbar side flexion, intermalleolar distance

Tragus-to-wall distance, lumbar side flexion after physical therapy*

*P < 0.05, before vs. after physical therapy or follow-up. VAS, visual analog scale; BASMI, Bath Ankylosing Spondylitis Metrology Index; BASDAI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; 6 MWT, 6-minute walking test; ASQoL, ankylosing spondylitis quality of life; NHP, Nottingham Health Profile.

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within the 6-min period was recorded in meters [18, 19].

Self-reported outcomes: On the 10-point VAS pain assessment scale, 0 represents no pain and 10 represents severe pain, revealing patient pain status regarding discomfort in inflamed or stiff joints [14, 15, 18]. The Bath Ankylosing Spondylitis Disease Activity Index (BASDAI) assesses six factors, namely fatigue, spinal pain, joint pain and swelling, localized tenderness, stiffness duration, and severity, for reporting the severity of AS. It is a 10-point scale, with 1 and 10 representing no symptoms and the most severe symptoms, respectively [14-21]. The SF-36 questionnaire was used to assess the physical and mental health status of patients with AS; the questionnaire involves

eight concepts: physical functioning, role limita-tion caused by physical problems, body pain, general health, vitality, social functioning, role limitation caused by emotional problems, and mental health [14]. The Nottingham Health Profile (NHP) was used for assessing the sub-jective health status of the patients with AS [18]. The questionnaire is divided into two parts, and the first part has 38 items on pain, physical mobility, emotional reactions, energy, social isolation, and sleep problems, whereas the second part has seven items on the effects of AS on daily life. Ankylosing Spondylitis Qua- lity of Life Scale (ASQOL) is a tool for assessing the quality of life of patients with AS; scores for 18 items are summed, with higher scores indi-cating high patient quality of life [16]. The Bath Ankylosing Spondylitis Functional Index (BASFI),

Figure 2. The forest plot of meta-analysis of the articles comparing the specific exercises with physical therapy on the changes in VAS, BSAMI, chest expansion and modified Schober test.

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a 10-point scale, comprises 10 items, focusing on the changes in the function of patients with AS; a higher score indicates that a patient has greater difficulty in performing activities of daily living [14-21].

Data analysis

The results of the recruited articles revealed that 199 patients with AS in the experimental group performed specific exercises. Seven patients withdrew from the exercise session, and 192 completed the exercise. Moreover, 184 patients in the control group received physical therapy. Six patients withdrew from therapy, and thus, 178 completed therapy. The results of the present study revealed that 3-48 weeks of aquatic exercises, Pilates, aerobic exercises, and GPR significantly improved the impairment, activity limitations, and participa-tion restrictions of the outcome assessments. The publication bias did not influence the meta-analysis results because the fail-safe number

of 132 exceeded the tolerance level of 50. Furthermore, the results of the tests for assess-ing impairment (i.e., BASMI, BASDAI, chest expansion, and modified Schober test), activity limitations (i.e., 6 MWT), and participation re- strictions (i.e., BASFI) before and after the inter-vention were reported in eight articles. Four articles provided follow-up outcomes (12 weeks-1 year) [14, 16, 20, 21]; additionally, Fernández-de-las-Penas et al. recruited the same patients with AS in two studies [20, 21].

In Figures 2, 3, significant heterogeneity was observed in the BASMI, chest expansion, mo- dified Schober test, BASDAI, and 6 MWT. Significant homogeneity was observed in the VAS and BASFI in the subgroup analysis. Among the patients with AS who performed specific exercises, we observed significant total effects in chest expansion, modified Schober test, and 6 MWT, which were superior to those observed in the patients who received physical therapy. By contrast, physical therapy revealed signifi-

Figure 3. The forest plot of meta-analysis of the articles comparing the specific exercises with physical therapy on the changes in BASDAI, 6 MWT and BASFI.

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cant total effects in the VAS, BASMI, BASDAI, and BASFI, which were superior to those observed in specific exercises. The meta-analy-sis results revealed that some outcomes in impairment (chest expansion and modified Schober test) and activity limitations (6 MWT) favored specific exercises (Figure 4), which had small to moderate effects (total effects of standardized mean difference = 0.39-0.76). Physical therapy had a small effect on patients with AS (total effects of standardized mean dif-ference = -0.39 - -0.48) regarding impairment (BASMI and BASDAI), and participation restric-tion (BASFI).

Discussion

In recent years, disability care, including that for AS, has focused on health improvement rather than curing the condition. The ICF model has facilitated the assessments of intervention efficacy for patients with AS [22]. The findings of the present meta-analysis confirm that phys-ical therapy effectively improves the impair-ment, and participation restrictions of patients with AS. We compared the outcomes of Pilates, the GPR method, and aerobic and aquatic exer-cises with those of physical therapy. The spe-cific exercises were focused on increasing trunk flexibility and mobility to achieve training goals, which caused the differences among the chest expansion, modified Schober test, and 6 MWT. Therefore, the effects in the impairment and activity limitations of ICF favored specific exercises.

Pilates, developed by J. H. Pilates, emphasize core muscle strength and stretching training for

healthy people [23]. Some studies have report-ed that Pilates are widely employed in manag-ing patients with musculoskeletal diseases positive effects [15, 16]. The main training pro-gram for Pilates included postural and breath-ing education, assuming a neutral body posi-tion, and stretching and proprioceptive exercis-es [23]. Pilates training had a low to moderate intensity, and the training was amended accord-ing to the convenience of the patients with AS. The specific exercise for the AS patients focused on improving functional capacity, phys-ical activity, spinal mobility, and quality of life [15, 16]. The GPR method, developed in accor-dance with the clinical experience of Souchard [24], is another specific exercise for patients with AS. The use of specific strengthening and flexibility exercises for particularly shortened muscle groups improves the flexibility of patients with AS [21]. The GPR training program mainly includes certain stretching, dynamic axial, static postural, and respiratory exercises for specific muscle chains [19]; this training program for patients with AS focuses on improv-ing the functional capacity, mobility, and activi-ty. Previous studies have shown that the GPR method has short- and long-term effects in improving the pulmonary function in patients with AS [20, 21]. The GPR method and Pilates are supervised interventions and include spe-cific strengthening and flexibility exercises for patients with AS. Furthermore, the GPR method focuses on the short muscle chains of patients with AS, and includes analytic stretching [20]. According to the results of Fernández-de-las-Penas et al. [20, 21], the GPR method could improve impairment, activity limitations, and participation restrictions in patients with AS.

Figure 4. The forest plot of meta-analysis of outcomes in ICF components.

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Furthermore, Durmusx et al. [19] proved that the GPR method has a positive effect on pul-monary function. These reports have suggest-ed that the GPR method is superior to physical therapy in treating AS patients. Hence, the GPR method and Pilates were applied for the spe-cific stretch of the trunk in AS patients, and had significant effects on improvements in chest expansion and modified Schober test.

Aquatic exercise refers to active exercise in thermal water and differs from passive spa therapy [25]. Dundar et al. [14] proposed func-tional movements, such as jumping, jogging, and stretching exercise, for performance in swimming pools (32°C-33°C) by patients with AS. Karapolat et al. [18] selected a specific type of swimming training, similar to aerobic exercise, for training patients with AS. The patients performed freestyle swimming for 30 min in a thermal pool (32°C) and warm-up ex- ercises for 10-15 min before and after swim-ming training. The swimming intensity was in accordance with the mean heart rate recorded during the exercise. The specific exercise aimed to improve trunk flexibility, chest expansion, and cardiopulmonary function in patients with AS. Moreover, compared with aerobic exercise performed on land, aquatic exercise could reduce joint loading and has benefits for arthri-tis, particularly in AS patients [26]. Dundar et al. [14] considered swimming to be an uncon-ventional aquatic exercise program. Aquatic exercises required supervision because no standard guidelines regarding exercise dura-tion or frequency for patients with AS has previ-ously been provided [14]. Engaging in specific supervised aquatic exercises may be more beneficial for AS patents compared with swim-ming alone; this requires further exploration. Furthermore, the present meta-analysis results revealed that aquatic exercise in a thermal pool led to significant improvements in chest expan-sion and the BASMI. The specific exercise pro-gram focusing on trunk flexibility in a thermal environment, providing tissue circulation, ben-efitted the patients with AS.

Karapolat et al. [18] considered walking as an aerobic exercise, in which the intensity of exer-cise reaches 60%-70% of the maximal heart rate (beats/min) yielding 13-15 points for the perceived exertion rating. A Polar Beat watch was used for heart rate monitoring during exer-

cise. Günendi et al. [17] used an exercise pro-cedure that included a 30-min walk on a tread-mill until the exercise intensity reached 60%-80% of the maximal heart rate (beats/min). Roşu et al. [15] employed a combination of Pilates and aerobic exercises performed using the Heckscher and McKenzie methods, focus-ing on correcting posture and improving core muscle strength and cardiopulmonary fitness. The specific exercises aim to improve function-al capacity, aerobic capacity, and cardiopulmo-nary function. The present meta-analysis reported similar outcomes to those of prior study, evidencing significant effects regarding improvements in the BASMI, BASDAI and 6 MWT [27]. The improvements in cardiopulmo-nary function, allowing the more oxygen to be transported and used by muscles, enhanced functional activity of the patients with AS. Moreover, pulmonary involvement was com-monly observed in early-stage AS patients, and prompt aerobic exercise improved the cardio-pulmonary function and prevented the func-tional restriction [28]. For patients with AS, an aerobic exercise training program requires fur-ther consideration, because the insufficient exercise duration observed in this study could not induce the adaptation and activation of an antioxidant activity [29]. However, overtraining in aerobic exercise could cause injuries [30]. Günendi et al. [17] suggested conducting a future study for assessing oxidant and antioxi-dant statuses and devising a suitable aerobic exercise program for patients with AS.

The present meta-analysis revealed that physi-cal therapy had a small effect, and was there-fore superior to the specific exercises regarding improvements in impairment, and participation restrictions in patients with AS. This result was possibly yielded because of the evaluation and formulation of physical therapy in accordance with the treatment course of patients with AS. However, specific exercises revealed small to moderate effects on the outcomes of chest expansion, 6 MWT, and modified Schober test, resulting in improvements in cardiopulmonary function. The inclusion of specific exercises in the treatment program of physical therapy may improve the cardiopulmonary function and aer-obic capacity for patients with early-stage AS. Roşu et al. [15] used the Heckscher and McKenzie methods in the Pilates program in the experimental group and added the land

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step exercise in the control group. Various assessments of impairment, activity limita-tions, and participation restrictions revealed significant improvements in both groups after the intervention. The outcomes of the experi-mental group were far superior to those of the control group. Therefore, physical therapy in combination with aerobic exercise is recom-mended. Regular exercises could increase anti-oxidant enzyme activity and enhance resis-tance to oxidative stress [29]. Some studies have considered that oxidative stress causes physiological changes in the pathogenesis of AS [29, 31]; Günendi et al. [17] considered this factor to underlie the benefits of aerobic exer-cise in patients with AS. A 12-week follow-up study by Dundar et al. [14] revealed that aquat-ic exercises can significantly improve results of the VAS, BASMI, BASDAI, and SF-36 for AS patients. Altan et al. [16] reported that Pilates could significantly improve the results of the BASFI and BASMI at 24-week follow-up. Furthermore, Fernández-de-las-Penas et al. [20] revealed that GPR could the results of the BASFI, BASMI and BASDAI, and improve the tragus-to-wall distance, modified Schober test, cervical rotation, lumbar side flexion, and inter-malleolar distance in patients with AS at a 1-year follow-up

Günendi et al. [17] reported that muscular stretching and strengthen training used in home-based physical therapy increased the results of the BASDAI and BASFI. The results of the aforementioned studies indicated that the symptoms of patients with AS worsen after the intervention, thus suggesting that the home-based physical therapy program might be unsuitable for these patients. By contrast, a supervised physical therapy program has been shown to be more effective for patients with AS as suggested by Lubrano et al. [32] and Dagfinrud et al. [33]. The present study sug-gested that supervised specific exercise or physical therapy programs are more clinically suitable according to the requirements of patients with AS. This meta-analysis study compared the benefits of four specific exercis-es with those of physical therapy in patients with AS. A small to moderate effect was shown regarding the impairment and activity limita-tions of ICF components for the specific exer-cises, whereas a small effect was observed concerning impairment and participation res-

triction for physical therapy. The study findings could provide information for clinical therapists regarding comparisons of the outcomes for various treatments. However, the study had some limitations. First, physical therapy for AS is a specific therapy, and a generalized conclu-sion could not be drawn from the diverse treat-ments. Second, because studies on specific exercises for AS were scarce, meta-analysis of the outcomes was difficult and prone to bias, particularly because of the inadequate out-comes of the exercise test. Cardiopulmonary function is a critical factor for patients with AS; however few studies have assessed this factor. Although 6 MWT is a simple tool for cardiopul-monary function assessment, a detailed assessment of the pulmonary function could assist in designing effective exercise prescrip-tions for patients with AS.

The present meta-analysis reveals that Pilates, the GPR method, and aerobic and aquatic ex- ercises could improve the impairment and activity limitations of patients with AS. The assessed outcomes revealed the benefits and small effects of physical therapy on AS. The findings regarding chest expansion and pulmo-nary function favor specific exercises, evidenc-ing small to moderate effects in patients with AS. However different outcomes of for specific exercises and physical therapy were found respectively, a combination of both interven-tions is suggested as an effective clinical pro-gram for patients with AS.

Disclosure of conflict of interest

None.

Address correspondence to: Dr. Yung-An Tsou, De- partment of Otorhinolaryngology, China Medical Un- iversity and Hospital, Graduate Institute of Clinical Medical Science, China Medical University, No. 91, Hsueh-Shih Road, Taichung 40402, Taiwan (R.O.C). E-mail: [email protected]

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