Skip Navigation


Rheumatology Advance Access originally published online on November 28, 2007
Rheumatology 2008 47(3):239-248; doi:10.1093/rheumatology/kem260
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Data
Right arrow All Versions of this Article:
47/3/239    most recent
kem260v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (6)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Metsios, G. S.
Right arrow Articles by Kitas, G. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Metsios, G. S.
Right arrow Articles by Kitas, G. D.
Related Collections
Right arrow Rheumatoid Arthritis
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© The Author 2007. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

REVIEWS

Rheumatoid arthritis, cardiovascular disease and physical exercise: a systematic review

G. S. Metsios1–3, A. Stavropoulos-Kalinoglou1–3, J. J. C. S. Veldhuijzen van Zanten2,4, G. J. Treharne2,5, V. F. Panoulas2, K. M. J. Douglas2, Y. Koutedakis1,3 and G. D. Kitas2

1University of Wolverhampton, School of Sport, Performing Arts and Leisure, Walsall, 2Department of Rheumatology, Dudley Group of Hospitals NHS Trust, Russells Hall Hospital, Dudley, West Midlands, UK, 3Research Institute in Physical Performance and Rehabilitation, Centre for Research and Technology Thessaly, Trikala, Greece, 4School of Sport and Exercise Sciences and 5School of Psychology, University of Birmingham, UK.

Correspondence to: G. S. Metsios, University of Wolverhampton, Walsall, West Midlands. E-mail: gm{at}wlv.ac.uk


   Abstract
Top
 Abstract
Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
This systematic review investigates the effectiveness of exercise interventions in improving disease-related characteristics in patients with rheumatoid arthritis (RA). It also provides suggestions for exercise programmes suitable for improving the cardiovascular profile of RA patients and proposes areas for future research in the field. Six databases (Medline, Cochrane Library, CINAHL, Google Scholar, EMBASE and PEDro) were searched to identify publications from 1974 to December 2006 regarding RA and exercise interventions. The quality of the studies included was determined by using the Jadad scale. Initial searches identified 1342 articles from which 40 met the inclusion criteria. No studies were found investigating exercise interventions in relation to cardiovascular disease in RA. There is strong evidence suggesting that exercise from low to high intensity of various modes is effective in improving disease-related characteristics and functional ability in RA patients. Future studies are required to investigate the effects of exercise in improving the cardiovascular status of this patient population.

KEY WORDS: Rheumatoid arthritis, Cardiovascular disease, Dynamic exercise, Aerobic exercise, Physical activity


   Introduction
Top
 Abstract
 Introduction
Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
Rheumatoid arthritis (RA) associates with increased morbidity and mortality from cardiovascular disease (CVD) [1], most of which is due to greater prevalence [2] and worse outcome [3] of ischaemic heart disease, largely attributed to accelerated atherosclerosis. The exact processes leading to this phenomenon remain undetermined. Much attention has been paid to the potential role of high-grade systemic inflammation [4] and its vascular and metabolic effects [5]. Sometimes this takes the focus away from the indisputable fact that classical modifiable CVD risk factors—such as hypertension [6, 7], dyslipidaemia [8], insulin resistance/metabolic syndrome [9], obesity [10], physical inactivity [11] and smoking [12]—are highly prevalent but under-investigated and suboptimally managed in this group of patients [13]. Even though these risk factors are not sufficient to explain the entire magnitude of CVD morbidity and mortality in RA [2], they represent an easily identifiable target for intervention, using both pharmacological [14–16] and behavioural approaches [17, 18].

Exercise is one of the most important behavioural interventions that can have a major beneficial impact on the likelihood to develop, suffer symptomatically or die from CVD. In the context of CVD, people, including those who have RA, could be divided schematically into four categories: those who have neither CVD nor any significant risk factor burden for it; those who have risk factors but no clinical evidence of CVD; those who have clinically apparent vascular and cardiac disease but have not suffered a life-threatening acute cardiovascular event such as a myocardial infarction (MI); and those who have survived an acute cardiovascular event. There is overwhelming evidence that, in the general population and several at risk subpopulations, exercise provides significant physical and psychosocial benefits, and facilitates management and improvements of outcome in all four of these categories. It helps maintain a healthy life-style, reduce CVD risk factors including obesity [19], dyslipidaemia [20, 21], hypertension [22], diabetes mellitus [23] and possibly even inflammation [24]; it is also effective for preventing acute coronary syndromes [25–32]. Moreover, exercise helps the management of established CVD: both aerobic exercise [33, 34] and resistance training [35] improve myocardial contractility and quality of life in patients with chronic heart failure and produce significant functional benefits in people with intermittent claudication [36]. More importantly, cardiac exercise rehabilitation programmes are an important part in the management of patients after an acute coronary syndrome (ACS) [37] and lead to significantly improved quality of life and reduced mortality rates [38–40]. Interestingly, there is evidence that patients with RA are rarely offered the opportunity to participate in cardiac rehabilitation programmes even after an ACS [3]. This may be, at least in part, because of the specific considerations required when prescribing exercise to such patients. These include: (i) whether the individual is physically able to perform, and psychologically likely to adhere to exercise regimens designed for cardiovascular improvements; (ii) whether RA health professionals are sufficiently aware of the evidence regarding exercise in RA patients and educate their patients accordingly; and (iii) whether existing exercise programmes and facilities can be adapted to cater for the extra needs that people with some degree of physical disability may have.

In the present review, we describe briefly the settings and types of exercise used for cardiovascular improvement in the general population. We then present systematic reviews of aerobic exercise interventions in RA and of the factors that may influence adherence to exercise in this disease. Finally, we give suggestions for exercise interventions suitable for improving the cardiovascular profile of people with RA and propose areas for future research in the field.


   Methods
Top
 Abstract
 Introduction
 Methods
Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
After taking into consideration an evidence-based tool for literature searching specifically for RA [41], six databases [Medline, Cochrane Library, Cumulative Index to Nursing & Allied Health Literature (CINAHL) research database, Google Scholar, Excerpta Medica database (EMBASE) and Physiotherapy Evidence Database (PEDro)] were searched to identify publications from 1974 to December 2006 in English regarding RA and exercise interventions. The Medical Subject Heading (MeSH) terms ‘physical activity’, ‘training’ and ‘exercise’ were employed in combination with ‘rheumatoid arthritis’. Initial searches identified 1342 articles (Supplementary Fig. S1, available at Rheumatology Online). Full articles were retrieved for assessment if the information in the abstract fulfilled both of the following criteria: (i) studying any aerobic or aerobic combined with resistance exercise intervention; and (ii) involving RA patients. Studies incorporating only participants with various types of inflammatory arthritis, degenerative arthritis or other inflammatory or connective tissue diseases were excluded. If the title and abstract did not provide sufficient information for this process, then the full-text manuscript was examined. Conference proceedings were not included in the review. The quality of the identified randomized controlled trials (RCTs) was assessed using standardized procedures as previously described [42]. Due to the limited number of RCTs for certain types of exercise (e.g. dance), cross-sectional and non-randomized longitudinal studies are also presented in the tables. However, the main conclusions and recommendations in this review are based on the results of RCTs.

For adherence to exercise in RA, keyword searches of Medline were carried out using the terms ‘exercise’ and all root variations on ‘adherence’ (e.g. ‘nonadherent’) and ‘compliance’ (e.g. ‘complying’) in combination with ‘rheumatoid arthritis’ (Supplementary Table S1, available at Rheumatology Online). Half of the identified studies were interventions with a focus on exercise component, and the majority contained only limited information on the role of adherence/compliance.


   Exercise for the prevention and management of cardiovascular disease
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
The increasing incidence and prevalence of CVD, together with its socioeconomic impact, have raised the need for early and effective prevention strategies (e.g. comprehensive screening and education) regarding relevant lifestyle modifications. Exercise has been identified as one of the most important behavioural strategies for CVD prevention. Specific guidelines have been developed about the required amount and intensity of daily and weekly physical activity [43], and its importance is emphasized by several campaigns promoting an active lifestyle, including those by the British Heart Foundation.

Any physical activity is better than no, or little, physical activity. The overall physiological adaptations that occur as a result of exercise [44] provide protection against CVD mortality, even in the presence of well-established CVD risk factors [45, 46]. CVD mortality is lower in highly fit than in moderately fit individuals [47], while physical inactivity is an independent risk factor for the development of CVD [48, 49].

Even though cardiorespiratory fitness may have a familial component [50], it can be increased significantly by exercise training, regardless of age, gender, race and initial fitness levels [51]. The required activity levels can be accrued through formal training programmes or leisure-time physical activities [52]. Moreover, supervised exercise programmes are more effective compared with non-supervised exercise [53, 54], most likely due to greater adherence.

Great controversy still exists about the optimum amount of exercise for eliciting the greatest cardiovascular benefit. Different exercise intensity [55, 56] and duration [57], as well as various combinations of them [58], may have different impacts on the magnitude of cardiorespiratory fitness improvement. Most authors agree that there is a dose–response relation between the amount of exercise, all-cause and cardiovascular mortality [55, 57, 59]. The greatest potential for reduced mortality is in sedentary individuals (such as many RA patients), in whom even slight increases in daily physical activity are beneficial [59, 60]; for more active individuals, higher levels of intensity should be pursued [59]. Depending primarily on the starting levels of physical activity, cardiovascular fitness has been reported to increase by 8–51% following an exercise intervention [57, 59, 61–63].

Moderate-intensity exercise of long duration appears to elicit the most benefit on CVD risk and mortality [55, 56, 58–60]. Current guidelines by the American College of Sports Medicine (ACSM) suggest that an individual should engage in exercise at least three times a week, at an intensity of 60–80% of maximum oxygen uptake (VO2max), for at least 20–30 min, in order to experience significant improvements in cardiorespiratory fitness and optimum cardiovascular benefits [43]. In terms of caloric expenditure, this can be translated to 1000–2000 kcal/week [64]. These calories can be expended in either continuous exercise or accumulated from several short bouts of exercise during a day [64–66]. Aerobic exercise is the most appropriate, but this can be supplemented by low-to-moderate intensity resistance training [65, 67]. The exercise regimen should be reconsidered regularly, usually every 4–6 weeks, based on the principles of exercise periodization [68] so that participants continue to improve their performance.


   Exercise in RA
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
RA manifestations include pain, stiffness, structural joint damage, bone density loss and muscle weakness [69]. As a result, a large proportion of patients exhibit decreased range of movement of the affected joints and general functional limitation in performing daily physical tasks: this may significantly compromise their fitness levels compared with people of the same age and sex [70]. RA patients’ fear for disease aggravation and an indefensible traditional approach of rheumatology health professionals to recommend exercise restriction may account for the inactive lifestyle of this population [70, 71]. It is now established that well-designed physical exercise programmes promote prolonged improvements [72–74] without inducing harmful effects on disease activity and joint damage [71, 75–77].

Thus far, the main objectives of exercise therapy in RA have been to maintain functional ability and improvement of physical capacity [78]. Exercise programmes with the specific purpose of improving cardiovascular fitness and reduced CVD mortality have attracted only minimal attention in this population.

Resistance training
Conventional resistance exercise programmes consisting of low-impact isometric and range-of-motion exercises have been repeatedly utilized in RA. The application of low-to-moderate intensity strength exercise in RA patients increased physical capacity [79, 80] without exacerbating pain or disease activity [81]. However, high-intensity resistance exercise programmes represent a more effective means for increasing muscular strength compared with low-intensity training and range-of-motion exercises, without any evidence of aggravation of joint symptoms [82]. High-intensity exercise has even been reported to decelerate joint damage in individuals with RA compared with non-exercising RA patients [83, 84], although this remains controversial [85, 86]. Some patients with extensive structural damage may have to refrain from activities that include significant loading of the damaged joints [87].

Well-constructed progressive resistance exercise is an effective and safe intervention for stimulating muscle growth in patients with RA and may even reverse rheumatoid cachexia [88]. This metabolic abnormality, which affects nearly two-thirds of all individuals with RA, is characterized by involuntary loss of muscle mass and progressive increase of fat mass in the presence of stable or even slightly decreased weight [89]. The exact underlying mechanisms are not entirely clear [90]: possible contributing factors not only include the overproduction of inflammatory cytokines such as TNF-{alpha} [89] but also physical inactivity [91, 92].

Non-RCTs investigating the effects of resistance training in RA differ widely in training regimens, methodological approaches and outcomes, making any conclusions difficult. The effectiveness of strength training lies on the quality and quantity of its application. Indeed, incorrect application of exercise frequency and intensity may not induce improvements in muscular strength; according to the ACSM [93], a successful muscular strength training programme for older populations or individuals with sedentary lifestyles should incorporate at least two sessions per week, involve 8–10 exercises for different muscle groups and allow completion of one set of 10–15 repetitions per exercise. RCTs complying to these recommendations have revealed significant increases in functional ability [74, 84, 94] and muscular strength [75], without exacerbating existing joint damage [73, 95] in patients with RA.

Aerobic training
Patients with RA are less active, and therefore less physically fit, compared with healthy individuals of the same age [70, 96]. The most frequently used mode of aerobic exercise training in studies involving RA patients is cycling, followed by aquatic exercise, aerobic dance and walking/running.

Cycling
Cycling is a non-weight-bearing aerobic activity where participants utilize large muscle groups of the lower extremity. It can be performed both in clinical settings as well as outdoors, either individually or in groups [97]. Indoor cycles can be modified to accommodate the needs of almost every RA patient [98] and can be effective even when the patients are minimally supervised [99]. An overview of the studies using cycling is provided in Table 1. Although individual studies vary in exercise frequency and overall duration of the intervention, cycling appears to consistently induce beneficial effects in aerobic capacity, functional ability and muscle strength.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Interventional training regimens in patients with rheumatoid arthritis—cycling programmes

 
Aquatic
Different types of water-based exercises such as aqua-aerobics and deep-water running have been applied in people with RA (Table 2). The in-water environment is thought to provide the ideal means for exercising in this population, as weight-bearing is minimized due to buoyancy [106]. This is extended by the general belief of patients that this type of exercise improves their functional ability [107]. Most of the available evidence suggests that aquatic exercise does improve aerobic capacity [108–110], muscular strength [85, 111] and psychological status [109]. The RCT with the larger number of RA patients combining both warm water immersion and exercise revealed significant improvements, as assessed by the Arthritis Impact Measurement Scales 2. However, this study did not include a laboratory-based evaluation of physical activity [109].


View this table:
[in this window]
[in a new window]

  		TABLE 2. Interventional training regimens in patients with rheumatoid arthritis—aquatic programmes

 
Dance
The effects of dance exercise have been investigated in many non-randomized trials (Table 3), which suggest improvements in aerobic capacity, walking ability, muscular strength [115–117] and psychological parameters, such as anxiety and depression [115, 118]. The only randomized trial involving dance as an intervention in RA patients revealed that despite no significant changes in bone mineral density and disease activity, functional capacity and physical activity were significantly improved [119].


View this table:
[in this window]
[in a new window]

  		TABLE 3. Interventional training regimens in patients with rheumatoid arthritis—dancing programmes

 
Walking and running
Walking has been used as an intervention for improving patients’ disease status [108, 121, 122], for the assessment of functional ability via gait analyses [123–125] or walking tests [126], and as a method to predict maximal oxygen uptake [127]. Walking or jogging has been included in training programmes without specifying the exact intensity, duration and frequency, but no RCTs based on walking or running as the main mode of exercise have been conducted in RA. Interestingly, a case study has described a female with RA who completed a whole marathon run following a training programme [128].

Combination of aerobic and strength training
The combination of intensive aerobic and strength training has been the most widely used exercise regimen in recent research in RA and produces an effective physical stimulus to achieve desirable physiological adaptations (Table 4). An RCT by van den Ende and colleagues [129] has highlighted that combining intense aerobic and resistance training can lead to significant enhancement in both cardiorespiratory capacity and muscular strength. Other RCTs support the beneficial effects of this type of exercise in patients with recent-onset [95], active [129] or inactive RA [130]. As a result of these findings, the American College of Rheumatology updated the treatment guidelines to introduce dynamic exercise as an effective means for the management of RA [131].


View this table:
[in this window]
[in a new window]

  		TABLE 4. Interventional training regimens involving the combination of dynamic aerobic and strength exercises in patients with rheumatoid arthritis

 

   Adherence to exercise in RA
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 
Consistent engagement in an exercise regimen is essential to reach improvements in fitness and physical well-being as well as psychological benefits in people with RA. We therefore carried out a systematic investigation of the evidence as to whether RA patients adhere to exercise regimens and what factors may influence this. In general, adherence/compliance has either been mentioned in relation to lack of long-term continuation of exercise after an intervention [139] or has been investigated in exercise regimes not specifically targeted at RA patients [99, 140–148]. This has made it difficult to reach any definitive conclusion [139, 149–158]. The Ottawa Panel's meta-analysis [154] reviewing previous RCTs of exercise regimens for RA patients demonstrated that adherence/compliance was included as an outcome only in two studies [148, 159]; the first was excluded from the meta-analysis for being a head-to-head study rather than a fully controlled study (it assessed dynamic muscle training vs progressive muscle relaxation) [148]; the second was excluded for having adherence as the sole outcome with little specific detail of the content of the (hand only) exercise intervention [159]. Other studies can also be criticized for inadequate-sized samples, short follow-up, inappropriate control conditions and poor conformity with the interventions [151]. Long-term adherence may be particularly important as a 12-week RCT comparing dynamic exercise with isometric and range-of-motion exercises among RA patients found that benefits for aerobic capacity and strength were lost another 12 weeks after the intervention [129]. O’Grady et al. [153] also stated that long-term adherence would be required for sustained cardiovascular benefits in RA patients, but none of the studies they reviewed had addressed this.

General patient education has been reported to be effective in increasing the time spent exercising [141, 142]; however, this is not a consistent finding [146]. It seems that increased adherence to exercise associates with lower baseline functional disability and disease activity [160] as well as the baseline levels of physical activity and fatigue [99]. Social factors, such as support of friends, significantly contribute to increased adherence to exercise regimens [145]. This suggests that appropriate regimens should be chosen for patients with more severe disease; dance sessions, for example, have high attendance [120], which is potentially due to the relatively low demands of this mode of exercise together with its social component. Indeed, tailoring exercise regimens has been suggested to improve adherence [144, 153].

In summary, adherence to exercise has not been adequately studied in RA. High-quality evidence is rare, and appears to suggest that well-controlled disease, better functional ability and strong social structure may facilitate adherence to exercise by patients with RA. Rigorous investigations are required to test whether tailoring exercise regimens around these considerations improves long-term adherence and goes on to improve cardiovascular outcomes for these patients.


   RA, cardiovascular disease and exercise
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
Supplementary data
 Acknowledgements
 References
 
Suggestions for future practice and research
We propose the systematic introduction of exercise training as part of the routine multidisciplinary care of patients with RA, with the specific aim of reducing cardiovascular risk and preventing or managing CVD. This will require further research, adaptation of existing knowledge and resources where available, as well as development of new services.

Education on the cardiovascular aspects of rheumatoid disease and the role of exercise in preventing CVD and managing RA itself is a major area for future research and clinical practice development; this needs to be targeted both to patients and to healthcare professionals, aiming to achieve not just improved knowledge but mainly sustained lifestyle changes. This may require a combination of approaches, including behavioural approaches, involving several healthcare professionals [161]. It can link in with the further research required into ways of optimising long-term adherence to an active lifestyle and exercise regimes in this population.

The short- and longer-term effects of different exercise regimens on important metabolic factors and on vascular function need to be specifically investigated in the RA population. These have never been researched in any populations characterized by ‘high grade’ systemic inflammation, where their regulation may be under overwhelming pressure from inflammatory networks [4] rendering them less susceptible to beneficial change through exercise. Ultimately, long-term RCTs are needed to show whether structured exercise programmes can be adhered to in the long term, provide sustained cardiovascular benefits and reduce CVD mortality in RA.

In the meantime, a pragmatic approach can be taken, building upon existing infrastructure, knowledge and expertise. Rheumatology clinical nurse specialists [162], liaising with their cardiology counterparts and local cardiac rehabilitation services, can incorporate the important role of exercise in their RA patient education programmes. Equipment and expertise available in cardiac rehabilitation centres and community fitness clubs can be adopted to provide exercise opportunities and classes for people with variable (and changing) degrees of physical disability, such as those with RA. Exercise can then be ‘prescribed’ on the basis of a person's exact needs.

In Fig. 1, we propose a general schema of the factors that need to be considered in any patient with RA, and their possible operationalization, with regard to the main objectives of their personalized exercise regimen. This includes two main categories of factors: (i) cardiovascular status and objectives; and (ii) overall and specific physical ability to exercise, related to RA status. We suggest as general principles that: (i) exercise is part of the general management of the RA patient and can be facilitated by other interventions (e.g. pharmacological, educational, behavioural); (ii) its main targets are first the attainment and maintenance of optimal (for the individual patient) function of the musculoskeletal system, which can then facilitate exercises focused on cardiorespiratory fitness; and (iii) exercise is tailored to the individual (although it can be delivered in a group environment), taking into account their baseline fitness and physical ability as well as their personal preferences and objectives, so that ideally a concordance of objectives can be achieved between the patients and the therapist [162].


Figure 1
View larger version (10K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		FIG. 1. Major considerations in designing individualized exercise training in patients with rheumatoid arthritis.

 
Cardiovascular status
We suggest a schematic division into those in whom exercise is aimed at reducing/managing CVD risk and those in whom it is incorporated in the management of existing CVD (before or after an acute coronary syndrome). Exercise for the latter has already been discussed in previous sections (but will need to be adopted according to the individual patient's physical constraints, as discussed subsequently). For the former, the ACSM has developed a risk stratification algorithm, in order to optimize the safety of participation in exercise programmes. This is based on consideration of the following specific risk factors: total cholesterol >6.5 mmol/l; smoking; family history of CVD; sedentary lifestyle; diabetes mellitus (blood glucose >6.7 mmol/l); systolic blood pressure >140 mmHg and overweight or obesity with BMI >25 kg/m2: individuals with less than three of these components are considered at low risk for developing CVD-related complications while exercising, whereas those with three or more of these components are at higher risk [43]. The thresholds for some of these risk factors may need to be altered for the RA population: for example, total cholesterol may be spuriously low during periods of active RA [8] and BMI thresholds for overweight reduced to 23 kg/m2, as recently described [10]. Based on this, exercise of appropriate mode, intensity, duration and frequency can be designed to provide adequate workload for cardiovascular benefits [68]. There is a wide range of options, but current ACSM guidance for optimum cardiovascular benefits and enhanced cardiorespiratory capacity includes regular participation (>3 times weekly) at sufficient intensities (60–80% of VO2max) and time (at least 20–30 min) [43]. Thus, determining the current level of fitness (usually by a graded exercise test, during which the workload is increased at regular intervals until self-reported exhaustion) prior to starting an exercise intervention, will help to establish the appropriate workload for each individual and to refine their personalized exercise programme.

Physical ability to exercise
We have schematically divided patients into those with good overall physical ability (mostly those with little current inflammation and little accumulated permanent joint damage); and those with limited physical ability (usually patients with a lot of joint inflammation, a lot of structural joint damage or both). This can help refine the overall multidisciplinary approach, incorporating specific exercise regimens, to their treatment. In the former, pharmacological therapy would be aimed at maintaining good disease control; some range of motion exercises and resistance training could be utilized to maintain a good level of musculoskeletal system mobility and function; and the main focus should be aerobic training aiming at optimizing cardiovascular fitness, to the degree determined by their current levels of fitness and allowed by their cardiovascular risk stratification. Patients in the group with limited physical ability to exercise due to the impact of RA have been subdivided into three subgroups: In those with a lot of current inflammation, but little structural damage, we propose aggressive pharmacological therapy to quickly reduce active inflammation and prevent muscle loss, due to rheumatoid cachexia, as the mainstay of therapy here; the focus of exercise should be to maintain a good level of musculoskeletal system mobility and function with aerobic training for cardiovascular fitness instituted as soon as possible. In those with a lot of inflammation and a lot of structural damage, pharmacological therapy is equally important to the group above; the focus of exercise should be initially maintenance and then improvement of musculoskeletal system mobility and function, followed by aerobic exercise within the patient's physical and cardiovascular limitations. Finally, in those with little inflammation but a lot of structural damage, pharmacological therapy would be aimed at maintaining control of inflammation; range of motion exercises and resistance training could be utilized to optimize musculoskeletal system mobility and function, followed by addition of aerobic exercise within the patient's limitations, to improve their cardiorespiratory fitness as much as possible. Patients with extensive structural damage should initially utilize the non-damaged joints; load on damaged joints should happen progressively, with the intensity of exercise progressing from range of motion exercises to low-load exercise. Sufficient pain relief will need to be ensured throughout any exercise training programme.

Conclusions
Surprisingly little has been investigated and published on the role of exercise as a means to control risk and manage CVD in individuals with RA. Focused research is required to identify the optimal regimens, timing and environment for exercise, as well as educational and behavioural interventions that will facilitate long-term adherence to an active lifestyle and/or structured exercise. In the meantime, a pragmatic approach is proposed, incorporating combined range of motion, strength and aerobic training, provided in a patient-specific context as part of the multidisciplinary care of the individual with RA.

Formula


   Supplementary data
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
Acknowledgements
 References
 
Supplementary data are available at Rheumatology Online.


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
References
 
Funding: G.S.M. was supported by grants received from the Greek State Scholarships Foundation (IKY). This study was funded by the Dudley Group of Hospitals R&D directorate cardiovascular programme grant and a Wolverhampton University equipment grant.

The Department of Rheumatology, Dudley Group of Hospitals, has an infrastructure support grant from the Arthritis Research Campaign (number: 17682).

Disclosure statement: The authors have declared no conflicts of interest.


   References
Top
 Abstract
 Introduction
 Methods
 Exercise for the prevention...
 Exercise in RA
 Adherence to exercise in...
 RA, cardiovascular disease and...
 Supplementary data
 Acknowledgements
 References
 

  1. Kitas GD, Erb N. Tackling ischaemic heart disease in rheumatoid arthritis. Rheumatology (2003) 42:607–13.[Free Full Text]
  2. del Rincon ID, Williams K, Stern MP, Freeman GL, Escalante A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum (2001) 44:2737–45.[CrossRef][Web of Science][Medline]
  3. Douglas KM, Pace AV, Treharne G J, et al. Excess recurrent cardiac events in rheumatoid arthritis patients with acute coronary syndrome. Ann Rheum Dis (2005) 65:348–53.[CrossRef][Web of Science][Medline]
  4. Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how ‘high-grade’ systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation (2003) 108:2957–63.[Abstract/Free Full Text]
  5. Stevens RJ, Douglas KM, Saratzis AN, Kitas GD. Inflammation and atherosclerosis in rheumatoid arthritis. Expert Rev. Mol Med (2005) 7:1–24.[Medline]
  6. Erb N, Pace AV, Douglas KM, Banks MJ, Kitas GD. Risk assessment for coronary heart disease in rheumatoid arthritis and osteoarthritis. Scand J Rheumatol (2004) 33:293–9.[CrossRef][Web of Science][Medline]
  7. McEntegart A, Capell HA, Creran D, Rumley A, Woodward M, Lowe GD. Cardiovascular risk factors, including thrombotic variables, in a population with rheumatoid arthritis. Rheumatology (2001) 40:640–4.[Abstract/Free Full Text]
  8. Situnayake RD, Kitas G. Dyslipidemia and rheumatoid arthritis. Ann Rheum Dis (1997) 56:341–2.[Free Full Text]
  9. Dessein PH, Tobias M, Veller MG. Metabolic syndrome and subclinical atherosclerosis in rheumatoid arthritis. J Rheumatol (2006) 33:2425–32.[Web of Science][Medline]
  10. Stavropoulos-Kalinoglou A, Metsios GS, Koutedakis Y, et al. Redefining overweight and obesity in rheumatoid arthritis patients. Ann Rheum Dis (2007) in press.
  11. Carnethon MR, Gulati M, Greenland P. Prevalence and cardiovascular disease correlates of low cardiorespiratory fitness in adolescents and adults. JAMA (2005) 294:2981–8.[Abstract/Free Full Text]
  12. Gerli R, Sherer Y, Vaudo G, et al. Early atherosclerosis in rheumatoid arthritis:effects of smoking on thickness of the carotid artery intima media. Ann NY Acad Sci (2005) 1051:281–90.[CrossRef][Web of Science][Medline]
  13. Banks M, Kitas G. Patients’ physical disability may influence doctors’ perceptions of suitability for risk assessment of CHD. Br Med J (1999) 319:1266–7.[Free Full Text]
  14. McInnes IB, McCarey DW, Sattar N. Do statins offer therapeutic potential in inflammatory arthritis? Ann Rheum Dis (2004) 63:1535–7.[Free Full Text]
  15. Endres M. Statins: potential new indications in inflammatory conditions. Atheroscler Suppl (2006) 7:31–5.[Web of Science][Medline]
  16. Gonzalez-Gay MA, Garcia-Unzueta MT, De Matias JM, et al. Influence of anti-TNF-alpha infliximab therapy on adhesion molecules associated with atherogenesis in patients with rheumatoid arthritis. Clin Exp Rheumatol (2006) 24:373–9.[Web of Science][Medline]
  17. Myers J. Cardiology patient pages. Exercise and cardiovascular health. Circulation (2003) 107:e2–5.[Free Full Text]
  18. Carroll S, Dudfield M. What is the relationship between exercise and metabolic abnormalities? A review of the metabolic syndrome. Sports Med (2004) 34:371–418.[CrossRef][Web of Science][Medline]
  19. Bensimhon DR, Kraus WE, Donahue MP. Obesity and physical activity: a review. Am Heart J (2006) 151:598–603.[CrossRef][Web of Science][Medline]
  20. Svendsen OL, Hassager C, Christiansen C. Effect of an energy-restrictive diet, with or without exercise, on lean tissue mass, resting metabolic rate, cardiovascular risk factors, and bone in overweight postmenopausal women. Am J Med (1993) 95:131–40.[CrossRef][Web of Science][Medline]
  21. Stefanick ML, Mackey S, Sheehan M, Ellsworth N, Haskell WL, Wood PD. Effects of diet and exercise in men and postmenopausal women with low levels of HDL cholesterol and high levels of LDL cholesterol. N Engl J Med (1998) 339:12–20.[Abstract/Free Full Text]
  22. Kelemen MH, Effron MB, Valenti SA, Stewart KJ. Exercise training combined with antihypertensive drug therapy. Effects on lipids, blood pressure, and left ventricular mass. JAMA (1990) 263:2766–71.[Abstract/Free Full Text]
  23. Wallberg-Henriksson H, Rincon J, Zierath JR. Exercise in the management of non-insulin-dependent diabetes mellitus. Sports Med (1998) 25:25–35.[CrossRef][Web of Science][Medline]
  24. Kasapis C, Thompson PD. The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol (2005) 45:1563–9.[Abstract/Free Full Text]
  25. Noda H, Iso H, Toyoshima H, et al. Walking and sports participation and mortality from coronary heart disease and stroke. J Am Coll Cardiol (2005) 46:1761–7.[Abstract/Free Full Text]
  26. Shaw DI, Hall WL, Williams CM. Metabolic syndrome: what is it and what are the implications? Proc Nutr Soc (2005) 64:349–57.[CrossRef][Web of Science][Medline]
  27. Murtagh EM, Boreham CA, Nevill A, Hare LG, Murphy MH. The effects of 60 minutes of brisk walking per week, accumulated in two different patterns, on cardiovascular risk. Prev Med (2005) 41:92–7.[CrossRef][Web of Science][Medline]
  28. Balagopal P, George D, Patton N, et al. Lifestyle-only intervention attenuates the inflammatory state associated with obesity: a randomized controlled study in adolescents. J Pediatr (2005) 146:342–8.[CrossRef][Web of Science][Medline]
  29. Sesso HD, Paffenbarger RS Jr, Lee IM. Physical activity and coronary heart disease in men: The Harvard Alumni Health Study. Circulation (2000) 102:975–80.[Abstract/Free Full Text]
  30. Blair SN, Kohl HW, Barlow CE. Physical activity, physical fitness, and all-cause mortality in women: do women need to be active? J Am Coll Nutr (1993) 12:368–71.[Abstract]
  31. Ornish D, Brown SE, Scherwitz LW, et al. Can lifestyle changes reverse coronary heart disease? The Lifestyle Heart Trial. Lancet (1990) 336:129–33.[CrossRef][Web of Science][Medline]
  32. Ornish D, Scherwitz LW, Billings JH, et al. Intensive lifestyle changes for reversal of coronary heart disease. JAMA (1998) 280:2001–7.[Abstract/Free Full Text]
  33. Haykowsky M, Vonder Muhll I, Ezekowitz J, Armstrong P. Supervised exercise training improves aerobic capacity and muscle strength in older women with heart failure. Can J Cardiol (2005) 21:1277–80.[Web of Science][Medline]
  34. Klocek M, Kubinyi A, Bacior B, Kawecka-Jaszcz K. Effect of physical training on quality of life and oxygen consumption in patients with congestive heart failure. Int J Cardiol (2005) 103:323–9.[CrossRef][Web of Science][Medline]
  35. Levinger I, Bronks R, Cody DV, Linton I, Davie A. The effect of resistance training on left ventricular function and structure of patients with chronic heart failure. Int J Cardiol (2005) 105:159–63.[CrossRef][Web of Science][Medline]
  36. Leng GC, Fowler B, Ernst E. Exercise for intermittent claudication. In: Cochrane Database Syst Rev (2000) CD000990.
  37. Clark AM, Hartling L, Vandermeer B, McAlister FA. Meta-analysis: secondary prevention programs for patients with coronary artery disease. Ann Intern Med (2005) 143:659–72.[Abstract/Free Full Text]
  38. Rees K, Taylor RS, Singh S, Coats AJ, Ebrahim S. Exercise based rehabilitation for heart failure. In: Cochrane Database Syst Rev (2004) CD003331.
  39. Mears S. The importance of exercise training in patients with chronic heart failure. Nurs Stand (2006) 20:41–7.[Medline]
  40. Ko JK, McKelvie RS. The role of exercise training for patients with heart failure. Eura Medicophys (2005) 41:35–47.[Medline]
  41. McGowan J. Evidence-based Rheumatology, Literature Searching. Tugwell P, ed. (2005) London, UK: BMJ Publishing Group. 3–18.
  42. Jadad AR, Moore A, Carroll D, et al. Assessing the quality of reports of randomised clinical trials: is blinding necessary? Controlled Cl Trials (1996) 17:1–12.[CrossRef]
  43. ACSM. ACSM's Guidelines for Exercise Testing and Prescription. (2005) Seventh edn. USA: Lippincott Williams & Wilkins.
  44. Bassuk SS, Manson JE. Physical activity and the prevention of cardiovascular disease. Curr Atheroscler Rep (2003) 5:299–307.[CrossRef][Medline]
  45. Farrell SW, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fitness levels and other predictors on cardiovascular disease mortality in men. Med Sci Sports Exerc (1998) 30:899–905.
  46. Blair SN, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA (1996) 276:205–10.[Abstract/Free Full Text]
  47. Eaton CB. Relation of physical activity and cardiovascular fitness to coronary heart disease, Part II: Cardiovascular fitness and the safety and efficacy of physical activity prescription. J Am Board Fam Pract (1992) 5:157–65.[Medline]
  48. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med (2002) 346:793–801.[Abstract/Free Full Text]
  49. Gibbons LW, Mitchell TL, Wei M, Blair SN, Cooper KH. Maximal exercise test as a predictor of risk for mortality from coronary heart disease in asymptomatic men. Am J Cardiol (2000) 86:53–8.[Web of Science][Medline]
  50. Bouchard C, An P, Rice T, et al. Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE Family Study. J Appl Physiol (1999) 87:1003–8.[Abstract/Free Full Text]
  51. Skinner JS, Jaskolski A, Jaskolska A, et al. Age, sex, race, initial fitness, and response to training: the HERITAGE Family Study. J Appl Physiol (2001) 90:1770–6.[Abstract/Free Full Text]
  52. Fletcher GF, Balady G, Blair SN, et al. Statement on exercise: benefits and recommendations for physical activity programs for all Americans. A statement for health professionals by the Committee on Exercise and Cardiac Rehabilitation of the Council on Clinical Cardiology, American Heart Association. Circulation (1996) 94:857–62.[Free Full Text]
  53. Bendermacher BL, Willigendael EM, Teijink JA, Prins MH. Supervised exercise therapy versus non-supervised exercise therapy for intermittent claudication. In: Cochrane Database Syst Rev (2006) CD005263.
  54. Deforche B, De Bourdeaudhuij I. Differences in psychosocial determinants of physical activity in older adults participating in organised versus non-organised activities. J Sports Med Phys Fitness (2000) 40:362–72.[Web of Science][Medline]
  55. Oguma Y, Shinoda-Tagawa T. Physical activity decreases cardiovascular disease risk in women: review and meta-analysis. Am J Prev Med (2004) 26:407–18.[CrossRef][Web of Science][Medline]
  56. Slentz CA, Aiken LB, Houmard JA, et al. Inactivity, exercise, and visceral fat. STRRIDE: a randomized, controlled study of exercise intensity and amount. J Appl Physiol (2005) 99:1613–8.[Abstract/Free Full Text]
  57. Kraus WE, Houmard JA, Duscha BD, et al. Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med (2002) 347:1483–92.[Abstract/Free Full Text]
  58. Jakicic JM, Marcus BH, Gallagher KI, Napolitano M, Lang W. Effect of exercise duration and intensity on weight loss in overweight, sedentary women: a randomized trial. JAMA (2003) 290:1323–30.[Abstract/Free Full Text]
  59. Duscha BD, Slentz CA, Johnson JL, et al. Effects of exercise training amount and intensity on peak oxygen consumption in middle-age men and women at risk for cardiovascular disease. Chest (2005) 128:2788–93.[CrossRef][Web of Science][Medline]
  60. Fletcher GF. The antiatherosclerotic effect of exercise and development of an exercise prescription. Cardiol Clin (1996) 14:85–95.[Medline]
  61. Gossard D, Haskell WL, Taylor CB, et al. Effects of low- and high-intensity home-based exercise training on functional capacity in healthy middle-aged men. Am J Cardiol (1986) 57:446–9.[CrossRef][Web of Science][Medline]
  62. Crouse SF, O’Brien BC, Grandjean PW, et al. Training intensity, blood lipids, and apolipoproteins in men with high cholesterol. J Appl Physiol (1997) 82:270–7.[Abstract/Free Full Text]
  63. O’Donovan G, Owen A, Bird SR, et al. Changes in cardiorespiratory fitness and coronary heart disease risk factors following 24 wk of moderate- or high-intensity exercise of equal energy cost. J Appl Physiol (2005) 98:1619–25.[Abstract/Free Full Text]
  64. Pescatello LS. Exercise and hypertension: recent advances in exercise prescription. Curr Hypertens Rep (2005) 7:281–6.[CrossRef][Web of Science][Medline]
  65. Pescatello LS, Guidry MA, Blanchard BE, et al. Exercise intensity alters postexercise hypotension. J Hypertens (2004) 22:1881–8.[CrossRef][Web of Science][Medline]
  66. Mestek ML, Garner JC, Plaisance EP, Taylor JK, Alhassan S, Grandjean PW. Blood lipid responses after continuous and accumulated aerobic exercise. Int J Sport Nutr Exerc Metab (2006) 16:245–54.[Web of Science][Medline]
  67. Pollock ML, Franklin BA, Balady GJ, et al. AHA Science Advisory. Resistance exercise in individuals with and without cardiovascular disease: benefits, rationale, safety, and prescription: an advisory from the Committee on Exercise, Rehabilitation, and Prevention, Council on Clinical Cardiology, American Heart Association; Position paper endorsed by the American College of Sports Medicine. Circulation (2000) 101:828–33.[Free Full Text]
  68. Koutedakis Y, Metsios GS, Stavropoulos-Kalinoglou A. Periodisation of exercise training in Sport. In: The physiology of training—Whyte G, ed. (2006) Philadelphia: Churchill Livingstone, Elsevier. 1–21.
  69. Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet (2001) 358:903–11.[CrossRef][Web of Science][Medline]
  70. Ekdahl C, Broman G. Muscle strength, endurance, and aerobic capacity in rheumatoid arthritis: a comparative study with healthy subjects. Ann Rheum Dis (1992) 51:35–40.[Abstract/Free Full Text]
  71. Scott DL, Wolman RL. Rest or exercise in inflammatory arthritis? Br J Hosp Med (1992) 48:445–447.[Web of Science][Medline]
  72. Lineker SC, Bell MJ, Wilkins AL, Badley EM. Improvements following short term home based physical therapy are maintained at one year in people with moderate to severe rheumatoid arthritis. J Rheumatol (2001) 28:165–8.[Abstract/Free Full Text]
  73. de Jong Z, Munneke M, Zwinderman AH, et al. Is a long-term high-intensity exercise program effective and safe in patients with rheumatoid arthritis? Results of a randomized controlled trial. Arthritis Rheum (2003) 48:2415–24.[CrossRef][Web of Science][Medline]
  74. Hakkinen A, Sokka T, Kotaniemi A, et al. Dynamic strength training in patients with early rheumatoid arthritis increases muscle strength but not bone mineral density. J Rheumatol (1999) 26:1257–63.[Web of Science][Medline]
  75. Hakkinen A, Sokka T, Kautiainen H, Kotaniemi A, Hannonen P. Sustained maintenance of exercise induced muscle strength gains and normal bone mineral density in patients with early rheumatoid arthritis: a 5 year follow up. Ann Rheum Dis (2004) 63:910–6.[Abstract/Free Full Text]
  76. Hakkinen A. Effectiveness and safety of strength training in rheumatoid arthritis. Curr Opin Rheumatol (2004) 16:132–7.[CrossRef][Web of Science][Medline]
  77. Lyngberg KK, Ramsing BU, Nawrocki A, Harreby M, Danneskiold-Samsoe B. Safe and effective isokinetic knee extension training in rheumatoid arthritis. Arthritis Rheum (1994) 37:623–8.[Web of Science][Medline]
  78. van Den Ende CH, Vliet Vlieland TP, Munneke M, Hazes JM. Dynamic exercise therapy for rheumatoid arthritis. In: Cochrane Database Syst Rev (2000) CD000322.
  79. Ekdahl C, Andersson SI, Moritz U, Svensson B. Dynamic versus static training in patients with rheumatoid arthritis. Scand J Rheumatol (1990) 19:17–26.[Web of Science][Medline]
  80. Ekdahl C, Ekman R, Petersson I, Svensson B. Dynamic training and circulating neuropeptides in patients with rheumatoid arthritis: a comparative study with healthy subjects. Int J Clin Pharmacol Res (1994) 14:65–74.[Web of Science][Medline]
  81. Bearne LM, Scott DL, Hurley MV. Exercise can reverse quadriceps sensorimotor dysfunction that is associated with rheumatoid arthritis without exacerbating disease activity. Rheumatology (2002) 41:157–66.[Abstract/Free Full Text]
  82. Bostrom C, Harms-Ringdahl K, Karreskog H, Nordemar R. Effects of static and dynamic shoulder rotator exercises in women with rheumatoid arthritis: a randomised comparison of impairment, disability, handicap, and health. Scand J Rheumatol (1998) 27:281–90.[CrossRef][Web of Science][Medline]
  83. Nordemar R, Ekblom B, Zachrisson L, Lundqvist K. Physical training in rheumatoid arthritis: a controlled long-term study. I. Scand J Rheumatol (1981) 10:17–23.
  84. de Jong Z, Munneke M, Zwinderman AH, et al. Long term high intensity exercise and damage of small joints in rheumatoid arthritis. Ann Rheum Dis (2004) 63:1399–405.[Abstract/Free Full Text]
  85. Stenstrom CH, Lindell B, Swanberg E, Swanberg P, Harms-Ringdahl K, Nordemar R. Intensive dynamic training in water for rheumatoid arthritis functional class II–a long-term study of effects. Scand J Rheumatol (1991) 20:358–65.[Web of Science][Medline]
  86. Hansen TM, Hansen G, Langgaard AM, Rasmussen JO. Longterm physical training in rheumatoid arthritis. A randomized trial with different training programs and blinded observers. Scand J Rheumatol (1993) 22:107–12.[Web of Science][Medline]
  87. Munneke M, de Jong Z, Zwinderman AH, et al. Effect of a high-intensity weight-bearing exercise program on radiologic damage progression of the large joints in subgroups of patients with rheumatoid arthritis. Arthritis Rheum (2005) 53:410–7.[CrossRef][Web of Science][Medline]
  88. Marcora SM, Lemmey AB, Maddison PJ. Can progressive resistance training reverse cachexia in patients with rheumatoid arthritis? Results of a pilot study. J Rheumatol (2005) 32:1031–9.[Abstract/Free Full Text]
  89. Roubenoff R, Roubenoff RA, Cannon JG, et al. Rheumatoid cachexia: cytokine-driven hypermetabolism accompanying reduced body cell mass in chronic inflammation. J Clin Invest (1994) 93:2379–86.[Web of Science][Medline]
  90. Walsmith J, Roubenoff R. Cachexia in rheumatoid arthritis. Int J Cardiol (2002) 85:89–99.[CrossRef][Web of Science][Medline]
  91. Rall LC, Roubenoff R. Rheumatoid cachexia: metabolic abnormalities, mechanisms and interventions. Rheumatology (2004) 43:1219–23.[Abstract/Free Full Text]
  92. Metsios GS, Stavropoulos-Kalinoglou A, Koutedakis Y, Kitas GD. Rheumatoid Cachexia: causes, significance and possible interventions. Hospital Chronicles (2006) 1:20–6.
  93. ACSM. American College of Sports Medicine Position Stand. The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Med Sci Sports Exerc (1998) 30:975–91.
  94. Lyngberg KK, Harreby M, Bentzen H, Frost B, Danneskiold-Samsoe B. Elderly rheumatoid arthritis patients on steroid treatment tolerate physical training without an increase in disease activity. Arch Phys Med Rehabil (1994) 75:1189–95.[CrossRef][Web of Science][Medline]
  95. Hakkinen A, Hakkinen K, Hannonen P. Effects of strength training on neuromuscular function and disease activity in patients with recent-onset inflammatory arthritis. Scand J Rheumatol (1994) 23:237–42.[Web of Science][Medline]
  96. Beals CA, Lampman RM, Banwell BF, Braunstein EM, Albers JW, Castor CW. Measurement of exercise tolerance in patients with rheumatoid arthritis and osteoarthritis. J Rheumatol (1985) 12:458–61.[Web of Science][Medline]
  97. Westby MD. A health professional's guide to exercise prescription for people with arthritis: a review of aerobic fitness activities. Arthritis Rheum (2001) 45:501–11.[CrossRef][Web of Science][Medline]
  98. Namey TC. Exercise and arthritis. Adaptive bicycling. Rheum Dis Clin North Am (1990) 16:871–86.[Web of Science][Medline]
  99. Daltroy LH, Robb-Nicholson C, Iversen MD, Wright EA, Liang MH. Effectiveness of minimally supervised home aerobic training in patients with systemic rheumatic disease. Br J Rheumatol (1995) 34:1064–9.[Abstract/Free Full Text]
  100. Ekblom B, Lovgren O, Alderin M, Fridstrom M, Satterstrom G. Effect of short-term physical training on patients with rheumatoid arthritis I. Scand J Rheumatol (1975) 4:80–6.[Web of Science][Medline]
  101. Ekblom B, Lovgren O, Alderin M, Fridstrom M, Satterstrom G. Effect of short-term physical training on patients with rheumatoid arthritis. a six-month follow-up study. Scand J Rheumatol (1975) 4:87–91.[Web of Science][Medline]
  102. Harkcom TM, Lampman RM, Banwell BF, Castor CW. Therapeutic value of graded aerobic exercise training in rheumatoid arthritis. Arthritis Rheum (1985) 28:32–9.[Web of Science][Medline]
  103. Karper WB, Evans BW. Cycling program effects on one rheumatoid arthritic. Am J Phys Med (1986) 65:167–72.[Web of Science][Medline]
  104. Lyngberg K, Danneskiold-Samsoe B, Halskov O. The effect of physical training on patients with rheumatoid arthritis: changes in disease activity, muscle strength and aerobic capacity. A clinically controlled minimized cross-over study. Clin Exp Rheumatol (1988) 6:253–60.[Web of Science][Medline]
  105. Baslund B, Lyngberg K, Andersen V, et al. Effect of 8 wk of bicycle training on the immune system of patients with rheumatoid arthritis. J Appl Physiol (1993) 75:1691–5.[Abstract/Free Full Text]
  106. Melton-Rogers S, Hunter G, Walter J, Harrison P. Cardiorespiratory responses of patients with rheumatoid arthritis during bicycle riding and running in water. Phys Ther (1996) 76:1058–65.[Abstract/Free Full Text]
  107. Bilberg A, Ahlmen M, Mannerkorpi K. Moderately intensive exercise in a temperate pool for patients with rheumatoid arthritis: a randomized controlled study. Rheumatology (2005) 44:502–8.[Abstract/Free Full Text]
  108. Minor MA, Hewett JE, Webel RR, Anderson SK, Kay DR. Efficacy of physical conditioning exercise in patients with rheumatoid arthritis and osteoarthritis. Arthritis Rheum (1989) 32:1396–405.[Web of Science][Medline]
  109. Hall J, Skevington SM, Maddison PJ, Chapman K. A randomized and controlled trial of hydrotherapy in rheumatoid arthritis. Arthritis Care Res (1996) 9:206–15.[Medline]
  110. Suomi R, Collier D. Effects of arthritis exercise programs on functional fitness and perceived activities of daily living measures in older adults with arthritis. Arch Phys Med Rehabil (2003) 84:1589–94.[CrossRef][Web of Science][Medline]
  111. Sanford-Smith S, Mackay-Lyons M, Nunes-Clement S. Therapeutic benefit of aquaerobics for individuals with Rheumatoid Arthritis. Physiother Canada (1998) 50:40–6.
  112. Danneskiold-Samsoe B, Lyngberg K, Risum T, Telling M. The effect of water exercise therapy given to patients with rheumatoid arthritis. Scand J Rehabil Med (1987) 19:31–5.[Web of Science][Medline]
  113. Minor MA, Hewett JE. Physical fitness and work capacity in women with rheumatoid arthritis. Arthritis Care Res (1995) 8:146–54.[Web of Science][Medline]
  114. Rintala P, Kettunen H, McCubbin JA. Effects of water exercise program for individuals with rheumatoid arthritis. Sports Med Training Rehabil (1996) 7:31–8.
  115. Noreau L, Martineau H, Roy L, Belzile M. Effects of a modified dance-based exercise on cardiorespiratory fitness, psychological state and health status of persons with rheumatoid arthritis. Am J Phys Med Rehabil (1995) 74:19–27.[Web of Science][Medline]
  116. Noreau L, Moffet H, Drolet M, Parent E. Dance-based exercise program in rheumatoid arthritis. Feasibility in individuals with American College of Rheumatology functional class III disease. Am J Phys Med Rehabil (1997) 76:109–13.[CrossRef][Web of Science][Medline]
  117. Neuberger GB, Press AN, Lindsley HB, et al. Effects of exercise on fatigue, aerobic fitness, and disease activity measures in persons with rheumatoid arthritis. Res Nurs Health (1997) 20:195–204.[CrossRef][Web of Science][Medline]
  118. Perlman SG, Connell KJ, Clark A, et al. Dance-based aerobic exercise for rheumatoid arthritis. Arthritis Care Res (1990) 3:29–35.[Medline]
  119. Westby MD, Wade JP, Rangno KK, Berkowitz J. A randomized controlled trial to evaluate the effectiveness of an exercise program in women with rheumatoid arthritis taking low dose prednisone. J Rheumatol (2000) 27:1674–80.[Web of Science][Medline]
  120. Moffet H, Noreau L, Parent E, Drolet M. Feasibility of an eight-week dance-based exercise program and its effects on locomotor ability of persons with functional class III rheumatoid arthritis. Arthritis Care Res (2000) 13:100–11.[CrossRef][Web of Science][Medline]
  121. Melikoglu MA, Karatay S, Senel K, Akcay F. Association between dynamic exercise therapy and IGF-1 and IGFBP-3 concentrations in the patients with rheumatoid arthritis. Rheumatol Int (2006) 26:309–13.[CrossRef][Web of Science][Medline]
  122. Allen SH, Minor MA, Hillman LS, Kay DR. Effect of exercise on the bone mineral density and bone remodelling indices in women with rheumatoid arthritis: 2 case studies. J Rheumatol (1993) 20:1247–9.[Web of Science][Medline]
  123. Keenan MA, Peabody TD, Gronley JK, Perry J. Valgus deformities of the feet and characteristics of gait in patients who have rheumatoid arthritis. J Bone Joint Surg Am (1991) 73:237–47.[Abstract/Free Full Text]
  124. Platto MJ, O’Connell PG, Hicks JE, Gerber LH. The relationship of pain and deformity of the rheumatoid foot to gait and an index of functional ambulation. J Rheumatol (1991) 18:38–43.[Web of Science][Medline]
  125. Fransen M, Edmonds J. Off-the-shelf orthopedic footwear for people with rheumatoid arthritis. Arthritis Care Res (1997) 10:250–6.[Web of Science][Medline]
  126. Hakkinen A, Pakarinen A, Hannonen P, et al. Effects of prolonged combined strength and endurance training on physical fitness, body composition and serum hormones in women with rheumatoid arthritis and in healthy controls. Clin Exp Rheumatol (2005) 23:505–12.[Web of Science][Medline]
  127. Macsween A, Johnson NJ, Armstrong G, Bonn J. A validation of the 10-meter incremental shuttle walk test as a measure of aerobic power in cardiac and rheumatoid arthritis patients. Arch Phys Med Rehabil (2001) 82:807–10.[CrossRef][Web of Science][Medline]
  128. Bluestone R. A marathon runner with high fever, arthralgia. Hosp Pract (Off Ed) (1983) 18:114–9.[Medline]
  129. van den Ende CH, Hazes JM, le Cessie S, et al. Comparison of high and low intensity training in well controlled rheumatoid arthritis. Results of a randomised clinical trial. Ann Rheum Dis (1996) 55:798–805.[Abstract/Free Full Text]
  130. van den Ende CH, Breedveld FC, le Cessie S, Dijkmans BA, de Mug AW, Hazes JM. Effect of intensive exercise on patients with active rheumatoid arthritis: a randomised clinical trial. Ann Rheum Dis (2000) 59:615–21.[Abstract/Free Full Text]
  131. ACR. Guidelines for the management of rheumatoid arthritis: 2002 Update. Arthritis Rheum (2002) 46:328–46.[CrossRef][Web of Science][Medline]
  132. Nordemar R, Berg U, Ekblom B, Edstrom L. Changes in muscle fibre size and physical performance in patients with rheumatoid arthritis after 7 months physical training. Scand J Rheumatol (1976) 5:233–8.[Web of Science][Medline]
  133. Stenstrom CH. Home exercise in rheumatoid arthritis functional class II: goal setting versus pain attention. J Rheumatol (1994) 21:627–34.[Web of Science][Medline]
  134. Komatireddy GR, Leitch RW, Cella K, Browning G, Minor M. Efficacy of low load resistive muscle training in patients with rheumatoid arthritis functional class II and III. J Rheumatol (1997) 24:1531–9.[Web of Science][Medline]
  135. Hakkinen A, Sokka T, Kotaniemi A, Hannonen P. A randomized two-year study of the effects of dynamic strength training on muscle strength, disease activity, functional capacity, and bone mineral density in early rheumatoid arthritis. Arthritis Rheum (2001) 44:515–22.[CrossRef][Web of Science][Medline]
  136. Hakkinen A, Sokka T, Lietsalmi AM, Kautiainen H, Hannonen P. Effects of dynamic strength training on physical function, Valpar 9 work sample test, and working capacity in patients with recent-onset rheumatoid arthritis. Arthritis Rheum (2003) 49:71–7.[CrossRef][Web of Science][Medline]
  137. Hakkinen A, Hannonen P, Nyman K, Lyyski T, Hakkinen K. Effects of concurrent strength and endurance training in women with early or longstanding rheumatoid arthritis: comparison with healthy subjects. Arthritis Rheum (2003) 49:789–97.[CrossRef][Web of Science][Medline]
  138. de Jong Z, Munneke M, Lems WF, et al. Slowing of bone loss in patients with rheumatoid arthritis by long-term high-intensity exercise: results of a randomized, controlled trial. Arthritis Rheum (2004) 50:1066–76.[CrossRef][Web of Science][Medline]
  139. Kettunen JA, Kujala UM. Exercise therapy for people with rheumatoid arthritis and osteoarthritis. Scand J Med Sci Sports (2004) 14:138–42.[CrossRef][Web of Science][Medline]
  140. April KT, Feldman DE, Platt RW, Duffy CM. Comparison between children with juvenile idiopathic arthritis and their parents concerning perceived treatment adherence. Arthritis Rheum (2006) 55:558–63.[CrossRef][Web of Science][Medline]
  141. Brus HL, Taal E, van de Laar MA, Rasker JJ, Wiegman O. Patient education and disease activity: a study among rheumatoid arthritis patients. Arthritis Care Res (1997) 10:320–4.[CrossRef][Web of Science][Medline]
  142. Brus HL, van de Laar MA, Taal E, Rasker JJ, Wiegman O. Effects of patient education on compliance with basic treatment regimens and health in recent onset active rheumatoid arthritis. Ann Rheum Dis (1998) 57:146–51.[Abstract/Free Full Text]
  143. Carpenter JO, Davis LJ. Medical recommendations–followed or ignored? Factors influencing compliance in arthritis. Arch Phys Med Rehabil (1976) 57:241–6.[Web of Science][Medline]
  144. Mahowald ML, Steveken ME, Young M, Ytterberg SR. The Minnesota Arthritis Training Program: emphasis on self-management, not compliance. Patient Educ Couns (1988) 11:235–41.[CrossRef][Web of Science][Medline]
  145. Minor MA, Brown JD. Exercise maintenance of persons with arthritis after participation in a class experience. Health Educ Q (1993) 20:83–95.[Web of Science][Medline]
  146. Neuberger GB, Smith KV, Black SO, Hassanein R. Promoting self-care in clients with arthritis. Arthritis Care Res (1993) 6:141–8.[Medline]
  147. Rapoff MA, Lindsley CB, Christophersen ER. Parent perceptions of problems experienced by their children in complying with treatments for juvenile rheumatoid arthritis. Arch Phys Med Rehabil (1985) 66:427–9.[Web of Science][Medline]
  148. Stenstrom CH, Arge B, Sundbom A. Home exercise and compliance in inflammatory rheumatic diseases–a prospective clinical trial. J Rheumatol (1997) 24:470–6.[Web of Science][Medline]
  149. Bradley LA. Adherence with treatment regimens among adult rheumatoid arthritis patients: current status and future directions. Arthritis Care Res (1989) 2:S33–9.[Medline]
  150. Brus H, van de Laar M, Taal E, Rasker J, Wiegman O. Compliance in rheumatoid arthritis and the role of formal patient education. Semin Arthritis Rheum (1997) 26:702–10.[CrossRef][Web of Science][Medline]
  151. Crofford LJ, Appleton BE. Complementary and alternative therapies for fibromyalgia. Curr Rheumatol Rep (2001) 3:147–56.[CrossRef][Medline]
  152. Hawley DJ. Psycho-educational interventions in the treatment of arthritis. Baillieres Clin Rheumatol (1995) 9:803–23.[CrossRef][Web of Science][Medline]
  153. O’Grady M, Fletcher J, Ortiz S. Therapeutic and physical fitness exercise prescription for older adults with joint disease: an evidence-based approach. Rheum Dis Clin North Am (2000) 26:617–46.[CrossRef][Web of Science][Medline]
  154. Ottawa Panel. Ottawa Panel evidence-based clinical practice guidelines for therapeutic exercises in the management of rheumatoid arthritis in adults. Phys Ther (2004) 84:934–72.[Abstract/Free Full Text]
  155. Rapoff MA. Assessing and enhancing adherence to medical regimens for juvenile rheumatoid arthritis. Pediatr Ann (2002) 31:373–9.[Web of Science][Medline]
  156. Schrieber L, Colley M. Patient education. Best Pract. Res Clin Rheumatol (2004) 18:465–76.[CrossRef]
  157. Swezey RL, Swezey AM. The physician and the arthritis patient: informed partners in therapy. Postgrad Med (1983) Spec No: 57–63.
  158. Zinna EM, Yarasheski KE. Exercise treatment to counteract protein wasting of chronic diseases. Curr Opin Clin Nutr Metab Care (2003) 6:87–93.[CrossRef][Web of Science][Medline]
  159. Waggoner CD, LeLieuvre RB. A method to increase compliance to exercise regimens in rheumatoid arthritis patients. J Behav Med (1981) 4:191–201.[CrossRef][Medline]
  160. Munneke M, de Jong Z, Zwinderman AH, et al. Adherence and satisfaction of rheumatoid arthritis patients with a long-term intensive dynamic exercise program (RAPIT program). Arthritis Rheum (2003) 49:665–72.[CrossRef][Web of Science][Medline]
  161. Hale ED, Treharne GJ, Kitas GD. The Common-sense model of self-regulation of health and illness: how can we use it to understand and respond to our patients’ needs? Rheumatology (2007) 46:944–51.[Abstract/Free Full Text]
  162. John H, Hale ED, Treharne GJ, Kitas GD. Patient education on cardiovascular aspects of rheumatoid disease: An unmet need. Rheumatology (2007) 46:1513–16.[Free Full Text]
Submitted 6 May 2007; revised version accepted 28 August 2007.
Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Br. J. Sports. Med.Home page
U M Kujala
Evidence on the effects of exercise therapy in the treatment of chronic disease
Br. J. Sports Med., August 1, 2009; 43(8): 550 - 555.
[Abstract] [Full Text] [PDF]

Home page
 Rheumatology (Oxford)Home page
V. F. Panoulas, G. S. Metsios, A. V. Pace, H. John, G. J. Treharne, M. J. Banks, and G. D. Kitas
Hypertension in rheumatoid arthritis
Rheumatology, September 1, 2008; 47(9): 1286 - 1298.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Data
Right arrow All Versions of this Article:
47/3/239    most recent
kem260v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (6)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Metsios, G. S.
Right arrow Articles by Kitas, G. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Metsios, G. S.
Right arrow Articles by Kitas, G. D.
Related Collections
Right arrow Rheumatoid Arthritis
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?