Best Practice & Research Clinical Rheumatology 28 (2014) 779e792

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Best Practice & Research Clinical Rheumatology journal homepage: www.elsevierhealth.com/berh

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Nonpharmacologic therapies in spondyloarthritis Andreas M. Reimold a, *, Vinod Chandran b a

Dallas VA Medical Center and University of Texas Southwestern Medical Center, Dallas, TX, USA Division of Rheumatology, Department of Medicine, University of Toronto, and Centre for Prognosis Studies in the Rheumatic Diseases, Toronto Western Hospital, University Health Network, Toronto, ON, Canada

b

a b s t r a c t Keywords: Physiotherapy Rehabilitation Behavioral therapy Smoking Obesity Diet

It is accepted that the optimal management of spondyloarthritis requires a combination of non-pharmacological and pharmacological interventions. Non-pharmacologic therapy in spondyloarthritis has generally focused on the exercise regimens whose purpose is to maintain mobility and strength, relieve symptoms, prevent or decrease spinal deformity, contribute to long-term cardiopulmonary health, and improve overall function and quality of life. Exercise programs such as home exercise, group exercise, inpatient programs, and spa exercise have all been the subject of multiple reports that are reviewed here. Studies reviewed support the use of exercise, spa therapy, manual therapy, and electrotherapeutic modalities. Additional topics that are finding relevance in spondyloarthritis are the behavioral interventions that maximize knowledge, motivation for compliance, and healthy lifestyle choices including smoking cessation, weight management, diet, and probiotics. However, the quality and generalizability of the studies are limited. Published by Elsevier Ltd.

Abbreviations: ACR, American College of Rheumatology; AS, ankylosing spondylitis; BASDAI, Bath Ankylosing Spondylitis Disease Activity Index; BASFI, Bath Ankylosing Spondylitis Functional Index; BASMI, Bath Ankylosing Spondylitis Metrology Index; BDI, Beck Depression Inventory; HEP, home exercise program; HAQ-S, Health Assessment Questionnaire for Spondyloarthropathies; PASI, Psoriasis Area and Severity Index; PGA, patient global assessment; VAS, visual analog scale. * Corresponding author. Rheumatology Section, Dallas VA Medical Center, 4500 S. Lancaster Blvd., Dallas, TX 75216, USA. Tel.: þ1 214 857 2105; fax: þ1 214 462 4650. E-mail addresses: [email protected] (A.M. Reimold), [email protected] (V. Chandran).

http://dx.doi.org/10.1016/j.berh.2014.10.003 1521-6942/Published by Elsevier Ltd.

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Introduction The optimal management of spondyloarthritis (SpA) requires a combination of nonpharmacological and pharmacological treatments. The 2010 update of the Assessment of SpondyloArthritis International Society/European League Against Rheumatism (ASAS/EULAR) recommendations for the management of ankylosing spondylitis (AS) recommends non-pharmacological therapy, the cornerstone being patient education and regular exercise [1]. Non-pharmacologic therapy in SpA has traditionally focused on the exercise regimens whose purpose is to maintain mobility and strength, relieve symptoms, prevent or limit spinal deformity, contribute to long-term cardiopulmonary health, and improve overall function and quality of life. Axial SpA, mainly AS, has been the most-studied condition, while peripheral SpA including psoriatic arthritis (PsA) has been included in fewer reports. Although study techniques have varied widely and no standardized intervention has emerged, exercise programs such as home exercise, group exercise, inpatient programs, spa exercise, mud baths, and manual and electrotherapy have all been the subject of multiple reports that will be reviewed here. In recent years, there has been an added emphasis on maintaining cardiopulmonary function as well as addressing cardiovascular risk factors in SpA patients. In addition, there has been renewed interest in behavioral interventions that maximize disease knowledge and increase motivation for compliance, as well as healthy lifestyle choices including smoking cessation and weight management. Finally, diet and probiotics are becoming the subjects of intensive study as the interaction of the gut, the microbiome, and SpA gains widespread recognition. Home exercise programs Not all physical activity is automatically beneficial to AS patients. In a survey of 397 AS patients diagnosed at least 20 years previously, those with jobs requiring dynamic flexibility consisting of bending, twisting, stretching, and reaching had more functional limitations as measured by Bath Ankylosing Spondylitis Functional Index (BASFI) scores compared to patients without these physical demands [2]. In addition, AS patients who had experienced requirements for dynamic flexibility, extent flexibility, and whole body vibration also had higher Bath Ankylosing Spondylitis Radiology Index for the spine (BASRI-s) scores indicating radiographic spinal damage. A home exercise program (HEP) in the treatment of AS has advantages of low cost, ease of initiation, and a track record of efficacy in trials over the last 25 years. While early studies assessed more limited parameters of finger-to-floor distance and physical function [3], subsequent studies have included assessments of pain, mobility, disease activity, quality of life, and respiratory function [4]. With the recognition of increased cardiovascular risk factors and mortality in patients with SpA, cardiovascular fitness has become an additional area of study [5], although improvement in cardiovascular risk factors has not been claimed. The simplest comparison is of a HEP versus a control without specific intervention. The study by Sweeney et al. consisted of 200 AS patients from a registry, half of whom were assigned an exercise/ intervention video, an exercise progress chart, patient education booklet, and AS exercise reminder stickers for 6 months and half were assigned to a control group without this program [6]. While measures of function (BASFI) and disease activity (Bath Ankylosing Spondylitis Disease Activity Index (BASDAI)) showed no between-group differences, the exercise group showed a significant improvement in self-efficacy, self-reported AS mobility, and in aerobic exercise. In a second study, Lim et al. compared a HEP in 25 AS patients to 25 control patients on a waiting list [7]. The exercises consisted of a daily 20-min program including 16 exercises targeting muscle relaxation, flexibility, strengthening, respiration, and posture. After an 8-week course, there were statistically significant improvements in joint mobility, finger-floor distance, functional capacity, pain scores, and depression scores. A third study, by Durmus et al., included an arm of 19 AS patients performing home exercise, 19 AS patients performing unsupervised global postural re-education (GPR) versus a 13-AS patient standard of care control [8]. The 12-week exercise regimen consisted of 20 exercises, including mobilization, stretching, and respiratory exercise, while the GPR also had warm-up and posture components. The results showed a greater improvement in functional capacity (BASFI), disease activity (BASDAI), fatigue

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(Multidimensional Assessment of Fatigue Scale), depression (Beck Depression Inventory scores), and (QOL) Quality of Life (Short Form 36) in the pooled exercise groups. Group physical therapy compared to an HEP Several studies have addressed whether supervised group exercise provides superior results compared to an unsupervised HEP. The first of these was a randomized study of 144 AS patients who underwent a daily 30-min HEP compared with the same HEP plus a 3-h weekly group physical therapy session consisting of exercises, sport, and hydrotherapy. While both groups achieved a benefit, there was a statistically significant further gain for the physical therapy patients in thoracolumbar flexion and extension, improved maximum load in ergometry, and patient global assessment [9]. A second study was a prospective, double-blind study comparing 51 AS patients receiving an exercise program under the supervision of a physical therapist (50-min session, three times weekly, for 6 weeks) with an HEP carried out individually [10]. The same exercise program was taught to both groups and included stretching, mobilization, and strengthening of the back and extremities, aerobic exercise on a stationary bicycle, and postural and respiratory exercises. The group exercise patients, but not the HEP patients, had a statistically significant improvement on measures of physical flexibility, Astrand test of physical conditioning, Beck Depression Scale, BASFI, but not pain scores. A third study compared 12 weeks of supervised twice-weekly group physical therapy plus an HEP to the unsupervised HEP alone [11]. At 3 months after the intervention, the supervised group demonstrated improved BASFI and SF-36 scores. A fourth study compared three different conditions: group exercise 3 days a week for 3 years, 1 month annually of supervised individual exercise along with unsupervised home exercise for the remainder of 3 years, and an HEP alone for 3 years [12]. This was the longest of the studies and no significant differences were found between groups. The most recent study was a non-randomized, 6week study of 41 patients receiving either a group exercise program three times a week, compared to an HEP [13]. Both groups achieved statistically significant improvement in BASDAI, Bath Ankylosing Spondylitis Metrology Index (BASMI), and several subscores of the Nottingham Health Profile, but there were no significant differences between the two groups. Instructions in proper posture and exercises to improve posture have been variably included in previous exercise programs. Elyan and Khan summarized the goal of minimizing spinal deformity by: (1) keeping the spine straight while walking or sitting, (2) avoiding prolonged stooping or bending, and (3) sleeping on the back using a firm mattress and the thinnest possible pillow [14]. The method of GPR has been described where the goal is to perform exercises that stretch and strengthen shortened muscle chains, such as eccentric work of the erector spine muscle, the posterior muscle chain in the pelvic region, and the anterior chain of the scapular girdle [15]. In a randomized 4-month trial of 45 AS patients, one group received weekly exercises based on the GPR method, while the other had a weekly session of 20 conventional exercises used in previous clinical trials [15]. The results showed that the GPR group achieved a greater improvement than the control group in all clinical measures of the BASMI except tragus-to-wall distance, and in the BASFI index. The same group followed up 1 year later on those patients who had continued their assigned exercise program at least three times per month and found that, compared to pre-intervention status, the GPR group had significant differences in all mobility measures of the BASMI, except for cervical rotation, and in the BASFI, in favor of the GPR group [16]. In a more recent trial of at least 4 months, 22 patients received GPR and were compared to 16 control patients undergoing conventional segmental self-stretching and breathing exercises [17]. All tested parameters had improved at the end of the trial in both groups, while select ones differed between the two groups. Patients in the GPR group had statistically significantly greater improvement in morning stiffness, spine mobility parameters, chest expansion, and the physical aspect component of the SF-36. One study has specifically focused on the effects of a rehabilitation program in AS patients whose disease has already stabilized on a tumor necrosis factor (TNF) inhibitor [18]. Sixty-two patients were randomized to rehabilitation plus an educational-behavioral program, to the educational-behavioral program alone, or to a control group. The educational-behavioral training consisted of two behavioral sessions and 10 exercise training sessions over 20 weeks, while the rehabilitation group added 12 twice-weekly exercise sessions (respiratory, stretching, mobilization, proprioceptive, and endurance).

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At follow-up at 2 and 6 months, patients in the rehabilitation program were able to further improve spine mobility and reduce pain, stiffness, and disability on top of their existing response to TNFinhibitor treatment. A large nationwide study in Spain assessed the impact of a structured education and HEP in daily practice patients with AS [19]. A total of 756 patients with AS (72% males, mean age 45 years) participated in a 6-month prospective multicenter controlled study, 381 of whom were randomized to an education intervention (a 2-h informative session about the disease and the implementation of a non-supervised physical activity program at home) and 375 to standard care (controls). At 6 months, there was a significant difference in the education group in BASDAI and BASFI as well as in visual analog scale (VAS) for total pain, patient's global assessment, and in AS Quality of Life (ASQoL) compared to those in standard care. Patients in the education group increased their knowledge about the disease and its treatments and practiced more regular exercise than controls [19]. A study attempted to develop a clinical prediction rule to identify AS patients who are likely to benefit from group-based exercise therapy [20]. Thirty-five consecutive patients with AS underwent a standardized examination and then received eight physical therapy sessions during a 2-month period, which included an exercise program based on the GPR method. Patients were classified as having experienced a successful outcome at 1 month after discharge based on a 20% reduction on BASFI and a self-perceived global rating of change. Sixteen patients (46%) experienced a successful outcome. Regression analysis identified three predictors e physical role (from the MOS 36-Item Short Form Health Survey) >37, bodily pain (from the MOS 36-Item Short Form Health Survey) >27, and BASDAI >31. The most accurate predictor of success was if the patient exhibited two of the three variables, and the positive likelihood ratio was 11.2 (95% confidence interval, 1.7e76.0) and the posttest probability of success increased to 91%. Thus, patients with less disease severity will likely have better outcomes with group-based exercise. The clinical prediction rule requires further validation. Overall, these studies of group exercise show improvements in multiple of the parameters that were measured compared to baseline, with the majority showing a statistically significant benefit of group exercise as compared to an HEP. As little as one weekly group physical therapy session provided a benefit [9]. Adding a rehabilitation program to patients already controlled by TNF-inhibitor therapy added further benefit. However, the studies were small, many of short duration, and effective blinding, where attempted, was difficult with this physical intervention. Water therapy, balneotherapy, Spa exercise, mud baths Therapies involving bathing in water or experiencing the massage effects of flowing water are collectively referred to as water therapy or hydrotherapy. Balneotherapy indicates that these activities are carried out in mineral waters, often at a spa. Spa therapy often involves a program with multiple daily activities that may include group exercise, postural correction, hydrotherapy, balneotherapy, thermal baths, sauna treatments, and sports. A recent randomized trial compared 69 patients assigned to 20 sessions of aquatic therapy over 4 weeks with patients assigned to home-based exercises demonstrated once by a physical therapist [21]. The results showed that six scales of the SF-36 focused on pain and quality of life were statistically superior in the aquatic group compared to the home exercise group when studied at 4 and 12 weeks posttreatment. Previously, a small randomized, controlled study found that 6 weeks of outpatient hydrotherapy with home exercises was associated with significantly better short-term improvement in neck mobility and VAS for pain and stiffness compared with 6 weeks of exercise alone, but no significant differences remained 6 months later [22]. A small study of balneotherapy compared 28 patients receiving daily 30-min sessions for 3 weeks along with a daily 30-min HEP for 6 months with 26 patients on an HEP alone for all 6 months [23]. At the end of the first 3 weeks, the balneotherapy group had better disease activity and quality of life measures (BASDAI, Nottingham Health Profile, pain, tiredness, and sleep score, physical activity, patient's and physician's global evaluation) than the HEP alone. At 6 months of follow-up, only the patient's global evaluation and modified Schober's test were better in the balneotherapy group but there were no significant between-group differences in physical function, pain, stiffness, or spinal mobility.

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Spa therapy has been evaluated in a randomized controlled study for 40 weeks, assigning 40 patients each to two European resorts for a 3-week spa program plus 37 weeks of supervised group exercise, and a third group of 40 patients to 40 weeks of supervised group exercise alone [24]. The spa plus exercise groups showed significant improvement in pain and Health Assessment Questionnaire for Spondyloarthropathies (HAQ-S) scores through 4 weeks, but no significant between-group differences remained by week 40. Use of spa therapy cost 3023 or 3240 euros, compared with 1754 euros for the group exercise controls [25]. Bathing in the waters of the Dead Sea, at times with the addition of mud-bath treatments, has been studied in three prospective trials of PsA and one of AS, as reviewed in 2012 [26]. In PsA, the largest study had 166 patients, all of whom underwent Dead Sea water balneotherapy and phototherapy [27]. In addition, 146 of the patients also received treatment with additional mudpacks and sulfur baths. Both groups had significant improvement in clinical parameters, with additional significant reduction in spinal pain and improved lumbar spine range of motion only in the mudpack/sulfur bath group. AS was studied in a randomized prospective 2-week trial with a blinded researcher, treating 14 patients using a freshwater pool in the Dead Sea and comparing them to 14 patients treated with mudpacks and a sulfur pool [28]. There were significant improvements in both groups in BASDAI, the VAS for pain, and the VAS for spinal movement. Quality of life improved due to pain reduction in the mudpacks/sulfur pool group only. Uncontrolled small trials from other parts of the world have also reported benefits for peloid therapy (therapeutic mud application) and bathing in radon-containing water [29]. Manual therapy Manual therapy is a physical treatment that includes kneading and manipulation of muscles, joint mobilization, and joint manipulation used to treat musculoskeletal pain and disability [30]. The first known trial to examine manual therapy for AS was reported in 2009 [31]. This prospective, randomized controlled study randomized 32 men, aged between 23 and 60 years, with AS to active or no treatment for 8 weeks. The patients in the treatment group were given individualized self- and manual mobilization for 1 h twice a week for 8 weeks. The physiotherapeutic intervention consisted initially of warming up the soft tissue of the back muscles (with vibrations via a vibrator) and gentle mobility exercises. This was followed by both active angular and passive mobility exercises in the physiological directions of the joints in the spinal column and in the chest wall in three directions of motion (flexion/extension, lateral flexion, and rotation) and in different starting positions (lying face down, sideways, on the back, and in a sitting position). Passive mobility exercises consisted of general, angular movements and specific, translatory movements. Stretching of tight muscles was done using the contractingerelaxing method. Soft tissue treatment (manual massage) of the neck was performed followed by relaxation exercises in a standing position and resting for some minutes lying on the treatment bench. Patients in the treatment group showed significant improvement in chest expansion, posture, spinal mobility, and the BASMI. There were no differences between the two groups with regard to vital capacity, BASDAI, Bath Ankylosing Spondylitis Global scale (BAS-G), or BASFI. At 4 months follow-up of the treatment group, cervical spine posture, lumbar flexion, and range of motion as well as BASMI remained improved. Electrotherapy Electrotherapy has a well-established role within physiotherapy practice [32]. The modalities may be classified into thermal, electrical, electromagnetic, and sonic. However, few studies have formally investigated the use of electrotherapy in SpA. A pilot study investigated the effect of a new modality for whole-body hyperthermia, named infrared (IR) sauna, in rheumatoid arthritis (RA) and AS [33]. Seventeen AS and 17 RA patients were studied. Pain and stiffness decreased clinically, and improvements were statistically significant during an IR session. Fatigue also decreased. However, no statistically significant improvement in pain, stiffness, and fatigue could be demonstrated at the end of 4week treatment period. No relevant changes in disease activity scores were found. Interestingly, whole-body cryotherapy has also been investigated. In a prospective study, 12 patients with AS and 48 with RA underwent treatment with whole-body cryotherapy twice a day [34]. In patients with AS, statistically significant reduction in BASDAI was demonstrated. Reduction in pain over 2 months was demonstrated in these patients. The authors opined that the relief of pain could allow an intensification

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of physiotherapy. Transcutaneous electrical nerve stimulation (TENS) can reduce pain in many musculoskeletal disorders. No recent reports have emerged on the use of this modality in AS, although previous trials suggest that TENS may provide relief of pain and stiffness [35]. Inpatient rehabilitation An inpatient rehabilitation program gives the opportunity for intensive therapy sessions multiple times a day, use of multiple modalities, as well as education and reinforcement of techniques. A small, randomized controlled study included 15 AS patients assigned to an inpatient rehabilitation arm consisting of five weekly group exercise sessions and three weekly hydrotherapy sessions for 3 weeks and compared them to 14 patients assigned to performing 6 weeks of home exercises alone [22]. All patients were then encouraged to continue home exercises long term. The inpatient regimen provided only short-term improvement in pain and stiffness compared to the home exercise patients, with no between-group differences remaining at 6 months. A second randomized trial consisted of 39 AS patients undergoing 3 weeks of inpatient physical therapy but added passive hip joint stretching in 27 of them [36]. The results showed improvement in hip range of motion, except flexion, in those undergoing hip joint stretching, with reassessment of seven patients 6 months later suggesting that benefits were sustained in those who continued the exercises on their own. There are also negative studies of inpatient rehabilitation programs. A 3-week twice-daily HEP was compared with 3 weeks (15 sessions) of inpatient rehabilitation for 60 AS patients [37]. The inpatient program included physical therapy, occupational therapy, and therapeutic exercise, while the home program was of postural, respiratory, and stretching exercises, walking endurance, and mobilization. Assessment was of BASDAI every 3 months and BASFI at 15 months, and showed no significant between-group differences. Similar negative findings were part of EULAR 2003 presentation that was not published as a full study [38]. Multimodal Programs with Aerobic and Pulmonary Exercises, and Incentive Spirometry. The investigation of measures that include cardiopulmonary fitness is attractive in the setting of AS, an inflammatory disease with elevated cardiovascular morbidity and mortality as well as mechanical restriction of the chest bellows function due to bone deposition and fusion. A small, randomized controlled study of a multimodal exercise program was performed in a convenience sample of 30 AS patients [39]. The 3-month study compared a supervised exercise program with 50 min of aerobic exercise, stretching, and pulmonary exercises three times weekly to medical treatment alone. The exercise group showed significantly better chest expansion, chin to chest distance, modified Schober's test, occiput to wall distance, and spinal mobility. In addition, the cardiopulmonary parameters of physical work capacity and vital capacity improved in the exercise group but declined in the controls. A more recent multimodal HEP consisted of breathing, postural, and stretching exercises (based on the Pilates, Heckscher, and McKenzie methods) [40]. The results showed significantly improved disease activity, physical function, spinal mobility, and vital capacity compared to an exercise program that combined step aerobics and stretching. Karapolat et al. have performed a randomized, controlled study in 45 AS patients to investigate the effects of adding aerobic exercise (swimming or walking three times per week for 6 weeks) to an HEP of stretching and mobility [41]. While all groups showed improvement in FEV1, FVC, and VC, the two groups adding aerobic exercise to the HEP showed an improvement in the 6-min walk test and in maximal oxygen uptake. A recent report of a randomized study in 106 AS patients found that adding cardiovascular training in the form of supervised Nordic walking 30 min/day, 2 days/week for 6 weeks resulted in greater cardiovascular fitness on a bicycle test but did not alter risk factors such as cholesterol or triglycerides, disease activity, quality of life, or spinal mobility [5]. Finally, adding incentive spirometry for 30 min daily for 16 weeks to an HEP did not result in improved measures of disease activity, pulmonary function tests, or 6-min walk testing [42]. Summary of exercise studies and recommendations Efforts have been under way for over two decades to study exercise regimens in AS, with overall benefits now widely accepted although details vary from study to study. However, even experts in

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the field, such as members of the ASAS (Assessment of Ankylosing Spondylitis) group, have been slow to recognize higher-level evidence in the field, such as from Cochrane reviews and randomized, controlled trials [43]. Patients are aware of the benefits of exercise but many admit to low adherence to a regimen in the long run. In responding to questionnaires about exercise, 61 patients with AS of mean 14.7 years duration reported walking (three times/week) or stretching (three times/week) in 35.0% and 32.8% of cases, respectively [44]. Despite noting the benefits for their level of physical fitness and their cardiovascular system, patients also felt that a barrier to exercise was its tiring effect. The strengths of the several existing reports include: 1. inclusion of well-defined AS patients, usually by modified New York criteria, 2. randomization to two or more treatment arms, with a control group usually receiving some type of exercise intervention as well, and 3. the addition of cardiopulmonary exercises, evaluation, and risk factor reduction to several trials. On the other hand, limitations also exist in the available studies. Most reports have low patient numbers, often fewer than 50 in each arm. Randomized and controlled trials have been performed, but double-blind studies have not been possible given the complex exercise interventions. Although the patients are well characterized, most studies include more than 70% men, making the applicability to women less well studied [45]. In addition, exclusion criteria varied markedly between trials, so that use of certain medications, peripheral joint involvement, severe comorbidity, and long-standing disease might restrict studies to relatively younger, healthier, and less-affected patients. Most studies were of a short-duration intervention of 6e12 weeks, whereas axial SpA may well need a lifelong approach to mobility and exercise treatments. The exercise and training programs were not standardized between trials so that it remains unclear which program is the most effective. Furthermore, outcome measures were also non-standardized, although use of BASDAI, BASFI, and BASMI indexes is now often at least one aspect of the measurements. The exact physiologic impact of complex interventions is often not well defined a priori, potentially making testing for a specific outcome imprecise. With this type of heterogeneity between studies, systematic reviews rating the strength of evidence have been possible, while meta-analyses have not. Outcomes from the available studies lead to these conclusions: 1. Exercise programs improve physical function, disease activity, and chest expansion. The evidence for improvement in pain, stiffness, spinal mobility, and cardiorespiratory function is low level and requires further study. Even programs as simple as home exercises learned from an instructional video can give these benefits. 2. Supervised group exercise programs have better short-term outcomes than unsupervised home exercises. 3. Water exercises, balneotherapy, spa stays, and 3-week inpatient programs with exercises all show short-term benefits that diminish or disappear over 6e15 months. 4. Short-term programs of 6e12 weeks that include aerobic exercises improve measures of cardiorespiratory function. Cardiovascular risk factors such as cholesterol and triglycerides have not shown a response, although longer studies may be needed. A summary of practical interventions and recommendations for exercise programs include the following: 1. Discuss the importance of an exercise and conditioning program with every axial SpA patient. 2. Develop practical options of where the patient should get training: a. patient handouts describing specific exercises, b. referral to online videos of experts such as physical therapists demonstrating exercises, c. referral to patient advocacy and educational websites such as that of the Spondylitis Association of America (SAA), d. referral to a physical therapist for teaching of a program, and e. referral to a physical therapy department for group exercises. 3. Develop a comprehensive referral set of instructions for exercises rather than relying on other medical professionals to come up with them.

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4. Follow-up in the office on patient's standardized testing of BASDAI, BASFI, and BASMI. Perform Pulmonary Function Tests (PFTs), possibly measures of cardiac function and conditioning. Determine cardiovascular risk factors at regular intervals. Behavioral management Environmental factors may lead to stress that can play a role in disease flares for AS patients. In a recent study of 272 patients followed prospectively, each logged on to a website every 3 months to report stressful or traumatic life events, infections, or vaccinations [46]. Outcome variables included the BASDAI, BASFI, and pain and patient global assessment. The results showed statistically significant elevation in all these measures for life events, elevation in BASDAI only after vaccinations, and no influence from infections. A separate study evaluated 243 AS patients for disease activity and risks for depression and anxiety and compared them to 118 matched healthy controls [47]. AS patients with high risk for depression and anxiety had higher scores in BASDAI, BASFI, worse pain, patient global assessment, physician global assessment, HAQ-S, and ASQoL (AS Quality of Life). Overall, the psychological status demonstrated close interaction with disease activity and quality of life in AS patients. Behavioral management has been considered for AS patients regardless of immediate life stressors. The goal of self-management of disease aims to maximize quality of life by having the patient recognize the disease's manifestations, respond with appropriate health behaviors including lifestyle changes, and take charge of day-to-day disease management rather than relying on a physician. A group from the Ankylosing Spondylitis International Federation performed a literature review of behavioral and environmental adaptations, ranked and modified them, and reported a core set of behavioral recommendations that span the events of daily life as well as lifestyle modification [48]. The multiple domains included not only daily and physical tasks such as walking, the sitting position, exercising, sports and recreation, fall prevention, work-related issues, and driving a car, but also diet and lifestyle, sexuality and pregnancy, and membership in an AS-specific patient organization. Previous literature had considered very specific behavioral interventions. In a controlled trial to improve self-control strategies, 22 AS patients were given a cognitiveebehavioral treatment program for pain control, while 17 patients on a waiting list served as controls [49]. The program consisted of training in progressive muscle relaxation, cognitive restructuring, attention-related techniques, and pleasant activity scheduling. After 6 months, there was a benefit of the program on pain intensity, anxiety, depression, psychophysiological complaints, and sleep disturbances but not on symptoms during pain attacks. Benefits were maintained at 12 months for pain intensity, anxiety, and psychophysiological complaints [50]. In a more recent study, 167 patients with RA or PsA underwent randomized intervention to compare the effects of a modular behavioral or a standard information-focused education program [51]. The results at 6 months showed that the behavioral group had statistically better pain, fatigue, functional ability, and self-efficacy scores and greater use of health behaviors. At 12 months, they continued to have better pain, self-efficacy, and psychological status scores and greater use of some health behaviors. Therefore, the conclusion was that attending the behavioral education program is effective for at least 1 year to reduce pain, improve psychological status, and self-manage their condition. Overall, interventions have used cognitive, behavioral, and educational approaches to allow increased self-management in patients with chronic disease. While physical therapists already focus on posture, specific exercises, and pain-relief modalities, the widest-ranging programs utilize different teaching methods to cover the disease description in detail, manage fatigue, stress and relaxation, diet, complementary therapies, insurance issues, and open discussion. [52] Smoking cessation Substantial recent evidence has emphasized that cigarette smoking is especially damaging to patients with axial SpA [53,54]. Specifically, smokers have earlier disease onset, increased systemic inflammation, and worse clinical measures and outcomes, including functional ability, physical mobility, and health-related quality of life [55,56]. Smoking is associated with a dose-dependent worsening of new bone formation and structural damage progression in the spine, making it as

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important a factor as the baseline radiographic damage and elevation of acute-phase reactants in predicting X-ray progression [57,58]. With the chest bellows function already potentially compromised in SpA, further pulmonary damage from smoking represents an additional insult to respiratory health in these patients. The many effects of smoking on some health outcomes have been difficult to study in all their complexity, as stress reduction from smoking, improved weight control, but decreased compliance with medications and exercise regimens in smokers may have complicated impacts on overall health. An area of controversy exists in PsA, where one study found an inverse association of smoking with the development of PsA [59]. However, the Nurses' Health Study II demonstrated that smoking was associated with an increased risk of PsA (with or without the presence of skin psoriasis), and cumulative measures of smoking were associated with a higher risk of PsA in this population [60]. A recent publication further found that although current smokers with PsA have a lower swollen joint count than never smokers, they have multiple unfavorable statistically significant parameters: higher patient global and fatigue scores, worse HAQ score, shorter treatment adherence, and poorer response to TNF inhibitors [61]. Overall, smoking cessation, by whatever method that achieves the desired result, is strongly recommended for all SpA patients. Management of obesity Obesity is an increasing socioeconomic problem in both the developed and developing world [62]. Obesity plays a significant role in the risk for developing SpA, especially PsA, and influences disease management. Obesity may influence response to pharmacological and non-pharmacological therapy. Management of obesity is important in the context of long-term disease management since cardiovascular disease is an important comorbidity that patients with SpA have [63]. Obesity is a risk factor for PsA in patients with psoriasis [64e66]. Thus, reducing body weight in psoriasis patients who often suffer from the metabolic syndrome and obesity may help prevent PsA as well as improve overall health. It has also been demonstrated that overweight and obese patients with PsA are less likely to achieve sustained minimal disease activity compared to those of normal weight [67,68]. In axial SpA, overweight patients have a greater burden of symptoms, worse perceptions regarding the benefits of exercise, and enhanced awareness of their barriers to exercising [69]. Overweight axial SpA patients also have a lower rate of success in obtaining response when treated with anti-TNF drugs [70,71]. Therefore, weight loss in overweight and obese patients with SpA may have significant benefits. However, there are not many studies that have investigated the benefits of weight loss in SpA. Recently, results were reported from a 12-month, randomized single-blind clinical trial to determine whether long-term exercise and dietary weight loss are more efficacious, either separately or in combination, than standard care alone in improving physical function, pain, fatigue, depression, and systemic inflammation in obese adults with PsA [72]. Fifty-five obese adult PsA patients with a body mass index (BMI) 30 were randomized into usual lifestyle (controls), diet only, exercise only, and diet plus exercise groups together with the continued use of standard treatment. At 12 months, the mean reduction in body weight was 15.0% in the intervention groups and was 2% in the control group (p ¼ 0.001). In the diet plus exercise group, there was significant improvement in American College of Rheumatology (ACR20), Psoriasis Area and Severity Index (PASI), DAS28-CRP, Beck Depression Inventory (BDI), fatigue, patient global assessment (PGA) and HAQ together with significant reductions in the serum levels of IL-6, TNF-alpha, hsCRP, and IL-17 compared to controls. In the exercise group, there was significant improvement in ACR20, PASI, PGA, HAQ, BDI, and fatigue. The diet-only group showed significant reductions in systemic inflammatory markers and significant improvement in ACR20 and PASI75 response at 12 months. Thus, lifestyle modification in conjunction with pharmacotherapeutic intervention can enhance clinical outcomes in patients with PsA. Diet and probiotics With the known association of gut inflammation and the presence of SpA, there has been an interest in modifying the diet or intestinal microbiome to alter this effect. Case reports exist for AS improvement from drastic changes such as fasting or change to a vegan diet, but no rigorous studies have been

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presented [73]. A Swedish trial of 165 AS patients found no correlation between diet and disease activity as measured by BASDAI and BASFI. However, the presence of gastrointestinal (GI) pain was significantly associated with eating more vegetables and less milk or soured milk products [74]. The GI symptoms were independent of non-steroidal anti-inflammatory drug (NSAID) usage. Dietary supplements have also been of interest in addressing intestinal and systemic inflammation. One group compared 3 weeks of dietary supplementation with high-dose versus low-dose omega-3 fatty acids in patients with AS [75]. The nine patients who completed the high-dose group showed a significant decrease in BASDAI, compared to the nine low-dose patients, with no differences in drug consumption or functional capacity. The authors called for a larger study. In a separate study, there was a positive correlation between levels of arachidonic acid in plasma phospholipids and disease activity assessed by BASDAI in patients with AS [76]. A Western diet did not appear to influence this correlation, but seemed to affect blood lipids involved in the atherogenic process. Rashid and Ebringer have published on the possibility of Klebsiella pneumoniae as a trigger for AS and Crohn's disease based on the molecular mimicry to self-antigens [77]. They have proposed the use of low-starch diet to try to eradicate Klebsiella microbes from the bowel as a treatment for these rheumatic conditions. Other groups did not find a clinical impact of such a strategy [78]. There is intense interest in altering the gut microbiome using probiotics. Probiotics are defined by the World Health Organization as “live microorganisms which when administered in adequate amounts confer a health benefit on the host.” [79] Probiotics are given with the intention of altering the relative percentages of existing intestinal flora, or introducing new microorganisms with beneficial properties such as favorably altering innate and adaptive immune responses. Of the many hundreds of species known to exist in the gut, only a few have been used as probiotics to date: mainly certain lactic acid bacteria, bifidobacteria, bacilli, and yeasts. Animal models have shown that Lactobacillus casei can downregulate Th1 effector functions and joint damage in mouse collagen-induced arthritis, while HLAB27 transgenic rats had less relapse of colitis when given Lactobacillus rhamnosus GG [80e82]. A few initial studies of probiotics in SpA patients have appeared. A pilot study of 18 patients investigated the effects of giving Lactobacillus acidophilus and Lactobacillus salivarius daily for 4 weeks in patients with quiescent ulcerative colitis but active SpA [83]. Significant improvements were seen in BASDAI and a pain VAS, with no flare of bowel disease. In a separate report, 147 patients with SpA were enrolled in an Internet-based randomized, controlled trial of using a probiotic with four strains of bacteria for 4 weeks (Lactobacillus paracasei, L. salivarius, Bifidobacterium infantis, Bifidobacterium bifidum), versus a placebo [84]. With 65% of subjects completing the trial, an intention-to-treat analysis showed that probiotics did not improve patient well-being or bowel symptoms. A further randomized, controlled, double-blind trial of 63 active SpA patients was performed using three probiotics (Streptococcus salivarius, Bifidobacterium lactis, and L. acidophilus) daily for 12 weeks, or placebo [85]. The trial demonstrated no benefit in any of the standardized measures used, including BASFI, BASDAI, or ASAS core domains. Clearly there are many choices of probiotic organisms, treatment regimens, and studies of longterm effects that are still needed. Comprehensive studies of the microbiome in SpA patients are starting to reveal differences from healthy subjects and may become the starting point for targeted adjustment of the bowel flora in patients. It will be of great interest to study the extent of systemic effects from such treatments. Summary This review has synthesized the current knowledge on non-pharmacological therapy in SpA, especially AS. Broadly, despite the limited amount of quality data, it is well accepted that exercisebased interventions have a favorable impact on AS. There is also support for the use of spa therapy, manual therapy, and electrotherapeutic modalities. There is evidence that smoking cessation and weight management will also have a positive impact. However, it is recognized that studies investigating non-pharmacological interventions have been few, small, heterogeneous, and have targeted specific subgroups. Thus, the quality and generalizability are limited. Non-pharmacological interventions have a significant role to play in the management of SpA and the gaps in research in this area need to be addressed.

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Practice points  Exercise programs improve physical function, disease activity, and chest expansion in patients with axial SpA.  Supervised group exercise programs have better short-term outcomes than unsupervised home exercises.  Smoking cessation and management of obesity should be emphasized to improve long-term disease outcomes.

Research agenda  There is a need for standardized research protocols of different modes, frequency, intensity, duration, and adherence of nonpharmacologic treatments that are more inclusive of SpA patients besides male AS, are long term, and are comparable enough that a future metaanalysis becomes possible.  With the growing recognition of cardiovascular risks in SpA, there is a need for studies of long-term cardiovascular risk factor modification by pharmacologic and non-pharmacologic means.

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Nonpharmacologic therapies in spondyloarthritis.

It is accepted that the optimal management of spondyloarthritis requires a combination of non-pharmacological and pharmacological interventions. Non-p...
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