Abstract
Objectives:
This prospective long-term study examines the effects of a Pilates training intervention on spinal mobility, disease activity, and functional capacity in patients with ankylosing spondylitis (AS).
Design:
The study design was quasi experimental and single blind.
Subjects:
11 subjects were recruited among patients undergoing followup of AS diagnosed according to modified New York criteria at the rheumatology clinic.
Interventions:
Over a 12-month period, 11 patients completed a training program consisting of two sessions per week of selected Pilates exercises. There was no control group.
Outcome measures:
The primary outcome variable was functional capacity measured using the Bath Ankylosing Spondylitis Functional Index (BASFI) questionnaire. Exploratory outcome measures were Bath Ankylosing Spondylitis Disease Activity Index (BASDAI), Bath Ankylosing Spondylitis Metrology Index (BASMI), and chest expansion and fingertip-to-floor (FTF) test. Baseline and follow-up examinations were performed immediately before the intervention and during the course of treatment at 4, 8, and 12 months.
Results:
After the exercise intervention, improvements were observed in BASFI (77.51%), BASDAI (64.39%) and BASMI (58.95%) scores, FTF distance (71.92%), and chest expansion (88.74%).
Conclusions:
These findings suggest that Pilates training could be useful in AS patients and provide direction for larger controlled trials designed to determine the therapeutic benefits of Pilates in the management of these patients.
Introduction
Ankylosing spondylitis (AS) is a chronic, systemic rheumatic disease that causes inflammation and ankylosis of the axial skeleton. AS is a type of axial spondyloarthritis (SpA), for which recent progress has been faster than for peripheral SpA. 1 The prevalence of AS is from 0.1% to 1.4%. 2,3 A characteristic feature of AS is inflammation of ligament or tendon insertions on bones (entheses). Disease progression often leads to spinal pain, stiffness, deformity, functional impairment, disability, and poor quality of life. 4,5
Average weekly physical activity is significantly reduced in patients with AS. 6 Physical exercise is considered a nonpharmacologic treatment by the Assessment of SpondyloArthritis International Society (ASAS) and European League against Rheumatism (EULAR). 7 The basic goal of AS therapy is to reduce pain and morning stiffness, prevent skeletal deformity, and to maintain good posture, physical condition, and psychosocial health. 8
Recent advances in understanding basic disease mechanisms have led to new treatment strategies, including antitumor necrosis factor-α (anti-TNF) therapy. Agents that inhibit TNF have proven to have beneficial impacts on disease activity, pain, and function and are also thought to have a structural effect. 9 When combined, biologic therapy and physical activity 10 –12 have synergistic effects and may benefit spinal flexibility and muscle strength thus preventing deformities, reducing pain, and improving quality of life. In a recent meta-analysis 12 of eight trials involving different training programs (home-based exercises, swimming, Pilates training, or supervised exercises), one of the most striking conclusions was the importance of including core exercises in all modalities to improve disease activity and body function in AS.
Pilates is a well-known discipline of physical exercise based on mind–body relaxation and focusing on controlled movements, posture, and breathing. 13 Because of its perceived benefits, Pilates has recently gained popularity in rehabilitation programs.
As a rehabilitation strategy, Pilates has been shown effective in achieving desired outcomes, particularly in terms of reducing pain and disability in musculoskeletal disorders, among others. 14,15 In a recent systematic review, 15 eight studies showed that Pilates was effective at reducing pain and disability in patients with lower back pain. A further two studies were designed to assess the effects of a Pilates training intervention in patients with AS. 11,16 In one of these studies, the authors, Altan et al., 11 reported significant improvements in Bath Ankylosing Spondylitis Functional Index (BASFI), Bath Ankylosing Spondylitis Metrology Index (BASMI), Bath Ankylosing Spondylitis Disease Activity Index (BASDAI), and chest expansion in weeks 12 and 24 compared with a control group of patients. In the other study by Roşu et al., 16 significant improvements were recorded in pain, lumbar spine motility, BASFI, BASDAI, and BASMI in response to a combined treatment intervention (Pilates, McKenzie and Heckscher) of 12-week duration. Pilates training therefore seems beneficial in AS patients.
The purpose of this study was to examine the effects of a 1-year Pilates training program on functional capacity in AS patients. As secondary outcome measures, the authors also examined the benefits of this long-term Pilates intervention on disease activity, spinal mobility, chest expansion, and fingertip-to-floor (FTF) test distance.
Materials and Methods
Subjects
Subjects were recruited among patients undergoing follow-up of AS diagnosed according to modified New York criteria at the rheumatology clinic. Exclusion criteria were any systemic disorder contraindicating exercising, active peripheral arthritis, total spinal ankylosis, or C-reactive protein more than 10 times the normal value. Patients were also excluded if their treatment regimen had been modified in the 2 months before study outset. Inclusion criteria were treatment with a nonsteroidal anti-inflammatory drug (NSAID) and the rheumatologist ensured that this treatment was stable in each patient during the follow-up period.
Patients were instructed to continue with their usual treatment regimen and not to use supplementary drugs or modify the usual dosages throughout the study period. For more accurate pain assessment, they were also requested to refrain from taking pain killers on the morning of a follow-up examination. Participants were informed about the nature and purpose of the study before giving their written consent to participate. The study protocol was approved by the Research Ethics Committee of the Camilo José Cela University. Although only a preliminary study, this clinical trial was prospectively registered in the Australian and New Zealand Clinical Trials Registry (ACTRN12618001169235).
Treatment protocol
Participants completed a program of Pilates exercise sessions given by a certified physiotherapist with 10 years of clinical experience at this center. The program consisted of 1-h sessions held 2 times a week for 12 months. Exercise sessions varied month by month. In the first month, sessions started with six repetitions of each exercise and 40 sec of rest between sets. In the following months, the number of repetitions was increased until 10 repetitions of each exercise with only 15 sec of rest between sets of exercises (Table 1). An attendance register was kept. The exercise program followed the basic principles of the Pilates method with special emphasis placed on movements of low to intermediate level of difficulty to adapt them to the physical capacity of the patients. The protocol comprised several modules, which were similar to those described by Altan et al. 11 : basic principles, breathing exercises, posture exercises, search for neutral position, sitting exercises, antalgic exercises, stretching exercises, and proprioceptivity exercises. Resistance bands, foam rollers, hoops, and 26 cm Pilates balls were used as supportive equipment. There was no control or comparison group.
Pilates Training Prescription Month by Month
Outcome measures
Assessments were performed just before (baseline), and in the 4th, 8th, and 12th months of the intervention during routine clinical practice by the same clinician who was blind to the nature of the rehabilitation program assigned to the patient. Participants were requested not to give information to the examiner about their training intervention. In this study, the same measurements as Altan et al. 11 were made although the authors added the FTF test. During the follow-up period, patients were asked about their life habits. Sixty percent of the patients continued with swimming pool exercises they had been carrying out for 2–5 years before the study.
Primary outcome measure
Functional capacity
To assess functional capacity, the authors used the version of the BASFI questionnaire adapted to Spanish-speaking patients, which has been shown to be valid and reliable. 17,18 This self-assessment instrument consists of eight specific questions regarding function in AS and two questions reflecting the patient's ability to cope with everyday life. Each question is answered on a horizontal 10 cm line (easy-to-impossible), the mean of which gives the BASFI score (0–10). 19
Exploratory outcome measures
Disease activity
This was determined using the Spanish version of the BASDAI questionnaire comprising a set of six questions. 17,18 The questionnaire contains six 10 cm horizontal visual analogue scales to measure severity of fatigue, spinal and peripheral joint pain, tenderness, and morning stiffness during the past week only. The final average score from 0 to 10 was obtained by dividing the total sum by 5.
Spinal mobility
The authors used the BASMI developed to assess spinal mobility in AS patients. 20,21 This index was obtained by measuring cervical rotation (degrees), tragus-to-wall distance (cm), lumbar side flexion (cm), modified Schober's test (cm), intermalleolar distance (cm), and scoring limitations for each criterion between 0 and 10. The final average score from 0 to 10 was obtained by dividing the total sum by 5.
FTF distance
For this test, which is not included in the BASMI, the patient was asked to bend forward and try to touch the floor with the fingertips. The distance between the patient's right long finger and the floor was measured using a standard measuring tape.
Chest expansion
This variable is also not included in the BASMI. After maximum inhalation following a forced exhalation, the increase produced in chest circumference was measured at the level of the fourth intercostal space.
Statistical analysis
All statistical tests were performed using SPSS 22.0 software (SPSS Science, Chicago, IL). The Shapiro–Wilk test confirmed a normal distribution of the quantitative outcome measures (p > 0.05). A one-way analysis of variance (ANOVA) for repeated measures was used to compare intragroup scores for each variable during the study. In all tests, effect size (η 2 ) and statistical power (SP) were calculated. The general linear model procedure generates an effect size, known as partial η 2 , categorized as small (<0.01), medium (0.01–0.06), and large (>0.14). All data are provided as their means, standard deviations, and 95% confidence intervals (CIs) when data are provided as percentages. Percentage improvements were calculated using the equation ([post − pre]/pre × 100). Analysis was performed at the 95% confidence level. Significance was set at p < 0.05.
Results
Study population
Of 32 AS patients invited to participate in this study, 26 gave their consent, among whom 8 were excluded because of complete spinal ankylosis. Of the remaining 18 individuals allocated to the Pilates treatment intervention, 7 withdrew from the program over the course of the year. The reasons for this were as follows: 1 pregnancy (after 4 months), 3 work incompatibility (2 after two and a half months and at 4 months), 2 lack of motivation (both after a month and a half), and 1 discomfort after training (after 2 months). None of the other six participants who left the study manifested discomfort after the training.
The remaining 11 participants (6 men, 5 women) were ages 28–55 (mean: 40.27 ± 9.66 years). Disease duration was 2–25 (mean: 10.90 years). Besides their usual NSAID regimen, around half the participants (54.4%) were under treatment with a biologic agent. The baseline characteristics of the study participants and normal distribution of quantitative outcomes are shown in Table 2. These participants completed 92.3% of the Pilates training sessions. Among the participants who continued with the intervention and those who did not continue, there were no differences (p > 0.05) in the baseline values of BASFI (5.18 vs. 5.07), BASDAI (6.94 vs. 6.54), BASMI (5.61 vs. 5.48), FTF (16.68 vs. 20), and chest expansion (4.08 vs. 3.42).
Baseline Characteristics of the Study Participants
Shapiro–Wilk test.
Minimum reference score to consider the disease as mild.
This score is considered to indicate active disease.
BASDI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; BASMI, Bath Ankylosing Spondylitis Metrology Index; CI, confidence interval; SD, standard deviation.
Primary outcome measure
As shown in Table 3, BASFI scores showed significant improvement in response to the Pilates training intervention. Through repeated-measures ANOVA, a significant time effect emerged [F(3, 30) = 45.22; p < 0.001; η 2 = 0.819; SP = 1.000). Improvements in BASFI (Table 4) were 1.09 (21.94%) at 4 months, 2.46 (46.36%) at 8 months, and 4.03 (77.51%) after a year. At 4 months, 7 of the 11 participants improved more than 25%, 2 improved 4%, 1 showed no improvement, and the remaining subject returned a worsened BASFI score. At 8 months, 6 participants improved more than 50%, 3 more than 25%, 1 improved 9%, and the remaining subject showed no improvement. After 1 year, all participants had improved from a minimum of 55.6% to a maximum of 95.8%. The improvement average every 4 months was 35.6% (95% CI: 28.0–43.3).
Results and Analysis of Covariance of Baseline and Post-Treatment (4-, 8-, and 12 Months) Variables
p-Value, within-subjects effects.
BASDAI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; BASMI, Bath Ankylosing Spondylitis Metrology Index; CI, confidence interval; FTF, fingertip-to-floor distance; SD, standard deviation.
Clinical Improvements Produced During the Study
BASDAI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; BASMI, Bath Ankylosing Spondylitis Metrology Index; BL, baseline; CI, confidence interval; FTF, fingertip-to-floor distance; SD, standard deviation.
Exploratory outcome measures
Disease activity, spinal mobility
BASDAI and BASMI scores also significantly improved over the intervention time. In the supporting repeated-measures ANOVA, a significant time effect was produced for both indices: BASDAI F(3, 30) = 24.19, p < 0.001, η 2 = 0.708, SP = 0.993; BASMI F(3, 30) = 387.25, p < 0.001, η 2 = 0.975, SP = 1.000. Median BASDAI improvements (Table 4) were 1.54 (21.77%) at 4 months, 3.60 (46.71%) at 8 months, and 4.6 (64.39%) after a year. At 4 months, 8 of the 11 participants improved more than 20%. At 8 months, 8 improved more than 50%, 2 more than 20%, and only 1 worsened, while after 1 year, all participants had improved from 34.15% to 85.71%. The improvement average every 4 months was 27.89% (95% CI: 18.17–37.60). Median BASMI improvements (Table 4) were 1.25 (22.44%) at 4 months, 2.65 (47.60%) at 8 months, and 3.29 (58.95%) after a year. At 4 months, 8 participants improved more than 20%, and 3 improved more than 17%. All participants improved more than 40% at 8 months and more than 50% after 1 year. The improvement average every 4 months was 25.28% (95% CI: 23.92–46.65).
FTF distance and chest expansion
Significant improvements were also observed in FTF distance and chest expansion along with significant time effects: FTF F(3, 30) = 14.66, p < 0.001, η 2 = 0.595, SP = 0.991; chest expansion F(3, 30) = 20.10, p < 0.001, η 2 = 0.668, SP = 0.991. Improvements noted in FTF (Table 4) were 5.50 (18.06%) at 4 months, 6.25 (34.2%) at 8 months, and 12.30 (71.92%) after a year. The improvement average every 4 months was 24.44% (95% CI: 18.29–30.59). Chest expansion increases (Table 4) were 1.60 (51.91%) at 4 months, 2.73 (79.12%) at 8 months, and 2.96 (88.74%) after a year. The improvement average every 4 months was 27.02% (95% CI: 37.66–16.39).
Discussion
The main outcome variable in this pilot study was designed to assess the benefits of a long-term Pilates training intervention on the functional capacity of AS patients. Other outcomes assessed were disease activity and spinal mobility. These findings indicate considerable improvements in all outcome measures in response to the intervention, confirming that exercises based on the Pilates method could be a useful component of treatment for AS patients.
According to the BASDAI score, the disease of all participants was active (defined as a score >3). 7 EULAR and American College of Rheumatology recommendations 22 highlight the potential effects of exercise in reducing disease activity and functional disability in AS. Functional capacity gradually diminishes in AS patients. 23 Several studies have shown that physiotherapeutic exercise improves spinal mobility and functional impairment in AS patients. 24,25 Thus, greater benefits of exercise programs than no intervention in improving functional capacity have been reported. 12 A multimodal program 26 of aerobic, stretching, and breathing exercises was found to improve spinal mobility, work capacity, and chest expansion than a similar program without physiotherapy. In a study comparing a 4-month exercise program with home therapy, 27 a significantly shorter FTF distance was recorded in the former group, yet pain, occiput-to-wall distance, and morning stiffness duration failed to vary between the groups. Analay et al. 28 noted significant improvements in BASFI scores in their exercise group under the supervision of a physiotherapist. Fernández-de-Las-Peñas et al. 29 proposed that while not all exercises are beneficial for AS, overall, posture reeducation may help with several AS measures, especially BASFI, BASDAI, and BASMI. The role of exercise in managing patients with AS has been poorly defined and recommended physical exercise modalities need to be specified. 12 In the present pilot study designed to assess the feasibility of a Pilates training intervention, the authors provide details about the exercises involved, number of repetitions, and rest intervals between repetition sets.
Defined cutoffs for minimum clinically important improvements are 1.1 for BASDAI and 0.6 for BASFI. 30 Minimum clinically important differences are 17.5% for BASFI and 22.5% for BASDAI. 31 At the end of this exercise intervention, the authors detected reductions of 4.03 (77.51%) and 4.6 (64.39%) in BASFI and BASDAI scores, respectively, and no worsening in any of the remaining outcome measures examined. Although these improvements were produced in response to a fairly intense Pilates exercise intervention lasting a whole year, outcomes were similar in those who dropped out before the end of the intervention, suggesting that a less intense program would be more suitable in these patients.
Pilates is a well-known modality of physical exercise based on mind–body relaxation that focuses on controlled movement, posture, and breathing. 13 The improvement noted in BASFI could be attributed to the specific focus of Pilates on spine mobility and transversus abdominis muscle exercises. 32 In effect, sequential dynamic stretching has proven to be a safe and functional way to improve flexibility. 11 This increased flexibility will have enabled the patients to perform better in movements such as unassisted sock-wearing. 33
In the study by Altan et al., 11 improvement in the Pilates group was noted immediately after the program, but at 24 weeks, BASDAI scores were not significantly different from pretreatment values. These authors suggested that patients should undertake this exercise program regularly and continuously. Better results could therefore be the consequence of this program having been long term. To objectively examine impacts on restricted spinal mobility, the authors also compared changes produced in BASMI scores with reported values. These results indicate a 3.29-point improvement (58.95%), which is in agreement with the findings of two other studies. 11,16 They also observed improvements in FTF distance in the FTF test, as a factor related to trunk flexibility. 34,35
Ankylosis of the rib cage is a feature of advanced AS, which may limit chest expansion and vital capacity. 1,4 In effect, chest wall restriction is a challenging problem in AS treatment. 36 The variable chest expansion is not included in the BASMI but showed improvement in AS patients (88.74%). This was not unexpected because Pilates focuses on correct and conscious breathing and aiding breathing movements is an integral part of this method. 13,15 The authors would nevertheless suggest measurement of vital capacity by spirometry as performed by Roşu et al. 16
Besides its small population size, a main limitation of this study was that Pilates was not the only therapeutic strategy as, for obvious reasons, the authors could not interrupt the patients' ongoing medication or other activities such as swimming. Another major limitation was the high dropout rate of around 39%. The reasons offered for abandoning the program were as follows: lack of motivation (11%), discomfort (5.5%), and reasons not related to the study (22%). This high dropout rate will also mean that this study participants were only the most motivated subjects, which will also bias its results. In retrospect, the authors believe the high frequency, intensity, and time burden of the intervention tested (two sessions a week for a year) were excessive, explaining the high dropout rate. In future work, they will adjust the frequency and duration of this program so that it can be generalized to the real-world setting. Perhaps 6 months of one session per week would be more realistic. It would also be interesting to continue monitoring patients for a further 2 months after completing the training intervention to examine the stability of any improvements noted. Further larger studies are needed and these should include a control group of patients refraining from Pilates training who are well matched for patient factors and medication.
In conclusion, the improvements in physical and functional capacity noted in the AS patients completing this pilot study confirm that Pilates training is a therapeutic option that warrants further investigation.
Footnotes
Authors' Contributions
E.S.R.L. has full access to all data in the study and takes responsibility for the integrity and accuracy of the data analysis. Study concept and design: E.S.R.L., V.E.G.-G., J.G.-P., P.G.-F., and M.R.-L. Acquisition, analysis, and interpretation of data: V.E.G.-G., P.G.-F., and M.R.-L. Drafting the article: E.S.R.L. and J.G.-P. Critical revision of the article for important intellectual content: V.E.G.-G., P.G.-F., and M.R.-L. Study supervision and management: E.S.R.L. and J.G.-P.
Author Disclosure Statement
No competing financial interests exist.
