Rheumatoid arthritis_ cardiovascular disease and physical execicise by akip2012


									Rheumatology 2008;47:239–248                                                                                                                       doi:10.1093/rheumatology/kem260
Advance Access publication 28 November 2007


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

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.

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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                                                                                          facilitates management and improvements of outcome in all four
                                                                                                      of these categories. It helps maintain a healthy life-style, reduce
Rheumatoid arthritis (RA) associates with increased morbidity                                         CVD risk factors including obesity [19], dyslipidaemia [20, 21],
and mortality from cardiovascular disease (CVD) [1], most of                                          hypertension [22], diabetes mellitus [23] and possibly even
which is due to greater prevalence [2] and worse outcome [3] of                                       inflammation [24]; it is also effective for preventing acute coronary
ischaemic heart disease, largely attributed to accelerated athero-                                    syndromes [25–32]. Moreover, exercise helps the management of
sclerosis. The exact processes leading to this phenomenon remain                                      established CVD: both aerobic exercise [33, 34] and resistance
undetermined. Much attention has been paid to the potential role                                      training [35] improve myocardial contractility and quality of life
of high-grade systemic inflammation [4] and its vascular and                                          in patients with chronic heart failure and produce significant
metabolic effects [5]. Sometimes this takes the focus away from                                       functional benefits in people with intermittent claudication [36].
the indisputable fact that classical modifiable CVD risk factors—                                     More importantly, cardiac exercise rehabilitation programmes are
such as hypertension [6, 7], dyslipidaemia [8], insulin resistance/                                   an important part in the management of patients after an acute
metabolic syndrome [9], obesity [10], physical inactivity [11] and                                    coronary syndrome (ACS) [37] and lead to significantly improved
smoking [12]—are highly prevalent but under-investigated and                                          quality of life and reduced mortality rates [38–40]. Interestingly,
suboptimally managed in this group of patients [13]. Even though                                      there is evidence that patients with RA are rarely offered the
these risk factors are not sufficient to explain the entire magnitude                                 opportunity to participate in cardiac rehabilitation programmes
of CVD morbidity and mortality in RA [2], they represent an                                           even after an ACS [3]. This may be, at least in part, because of the
easily identifiable target for intervention, using both pharmaco-                                     specific considerations required when prescribing exercise to such
logical [14–16] and behavioural approaches [17, 18].                                                  patients. These include: (i) whether the individual is physically
   Exercise is one of the most important behavioural interventions                                    able to perform, and psychologically likely to adhere to exercise
that can have a major beneficial impact on the likelihood to                                          regimens designed for cardiovascular improvements; (ii) whether
develop, suffer symptomatically or die from CVD. In the context                                       RA health professionals are sufficiently aware of the evidence
of CVD, people, including those who have RA, could be divided                                         regarding exercise in RA patients and educate their patients
schematically into four categories: those who have neither CVD                                        accordingly; and (iii) whether existing exercise programmes and
nor any significant risk factor burden for it; those who have risk                                    facilities can be adapted to cater for the extra needs that people
factors but no clinical evidence of CVD; those who have clinically                                    with some degree of physical disability may have.
apparent vascular and cardiac disease but have not suffered a life-                                      In the present review, we describe briefly the settings and types
threatening acute cardiovascular event such as a myocardial                                           of exercise used for cardiovascular improvement in the general
infarction (MI); and those who have survived an acute cardio-                                         population. We then present systematic reviews of aerobic exercise
vascular event. There is overwhelming evidence that, in the                                           interventions in RA and of the factors that may influence
general population and several at risk subpopulations, exercise                                       adherence to exercise in this disease. Finally, we give suggestions
provides significant physical and psychosocial benefits, and                                          for exercise interventions suitable for improving the cardiovas-
                                                                                                      cular profile of people with RA and propose areas for future
  University of Wolverhampton, School of Sport, Performing Arts and Leisure,                          research in the field.
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,                          Methods
Trikala, Greece, 4School of Sport and Exercise Sciences and 5School of                                After taking into consideration an evidence-based tool for liter-
Psychology, University of Birmingham, UK.                                                             ature searching specifically for RA [41], six databases [Medline,
   Submitted 6 May 2007; revised version accepted 28 August 2007.                                     Cochrane Library, Cumulative Index to Nursing & Allied Health
  Correspondence to: G. S. Metsios, University of Wolverhampton, Walsall, West                        Literature (CINAHL) research database, Google Scholar,
Midlands. E-mail: gm@wlv.ac.uk                                                                        Excerpta Medica database (EMBASE) and Physiotherapy
ß 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
240                                                          G. S. Metsios et al.

Evidence Database (PEDro)] were searched to identify publica-            increases in daily physical activity are beneficial [59, 60]; for more
tions from 1974 to December 2006 in English regarding RA and             active individuals, higher levels of intensity should be pursued [59].
exercise interventions. The Medical Subject Heading (MeSH)               Depending primarily on the starting levels of physical activity,
terms ‘physical activity’, ‘training’ and ‘exercise’ were employed in    cardiovascular fitness has been reported to increase by 8–51%
combination with ‘rheumatoid arthritis’. Initial searches identified     following an exercise intervention [57, 59, 61–63].
1342 articles (Supplementary Fig. S1, available at Rheumatology             Moderate-intensity exercise of long duration appears to elicit
Online). Full articles were retrieved for assessment if the              the most benefit on CVD risk and mortality [55, 56, 58–60].
information in the abstract fulfilled both of the following criteria:    Current guidelines by the American College of Sports Medicine
(i) studying any aerobic or aerobic combined with resistance             (ACSM) suggest that an individual should engage in exercise at
exercise intervention; and (ii) involving RA patients. Studies           least three times a week, at an intensity of 60–80% of maximum
incorporating only participants with various types of inflamma-          oxygen uptake (VO2max), for at least 20–30 min, in order to
tory arthritis, degenerative arthritis or other inflammatory or          experience significant improvements in cardiorespiratory fitness
connective tissue diseases were excluded. If the title and abstract      and optimum cardiovascular benefits [43]. In terms of caloric
did not provide sufficient information for this process, then the        expenditure, this can be translated to 1000–2000 kcal/week [64].
full-text manuscript was examined. Conference proceedings were           These calories can be expended in either continuous exercise
not included in the review. The quality of the identified                or accumulated from several short bouts of exercise during a day
randomized controlled trials (RCTs) was assessed using standar-          [64–66]. Aerobic exercise is the most appropriate, but this can be
dized procedures as previously described [42]. Due to the limited        supplemented by low-to-moderate intensity resistance training
number of RCTs for certain types of exercise (e.g. dance), cross-        [65, 67]. The exercise regimen should be reconsidered regularly,
sectional and non-randomized longitudinal studies are also               usually every 4–6 weeks, based on the principles of exercise

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presented in the tables. However, the main conclusions and               periodization [68] so that participants continue to improve their
recommendations in this review are based on the results of RCTs.         performance.
   For adherence to exercise in RA, keyword searches of
Medline were carried out using the terms ‘exercise’ and all root
                                                                         Exercise in RA
variations on ‘adherence’ (e.g. ‘nonadherent’) and ‘compliance’
(e.g. ‘complying’) in combination with ‘rheumatoid arthritis’            RA manifestations include pain, stiffness, structural joint damage,
(Supplementary Table S1, available at Rheumatology Online).              bone density loss and muscle weakness [69]. As a result, a large
Half of the identified studies were interventions with a focus on        proportion of patients exhibit decreased range of movement of the
exercise component, and the majority contained only limited              affected joints and general functional limitation in performing
information on the role of adherence/compliance.                         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
Exercise for the prevention and management of                            traditional approach of rheumatology health professionals to
cardiovascular disease                                                   recommend exercise restriction may account for the inactive
                                                                         lifestyle of this population [70, 71]. It is now established that well-
The increasing incidence and prevalence of CVD, together with its
                                                                         designed physical exercise programmes promote prolonged
socioeconomic impact, have raised the need for early and effective
                                                                         improvements [72–74] without inducing harmful effects on disease
prevention strategies (e.g. comprehensive screening and educa-
                                                                         activity and joint damage [71, 75–77].
tion) regarding relevant lifestyle modifications. Exercise has been          Thus far, the main objectives of exercise therapy in RA have
identified as one of the most important behavioural strategies for       been to maintain functional ability and improvement of physical
CVD prevention. Specific guidelines have been developed about            capacity [78]. Exercise programmes with the specific purpose of
the required amount and intensity of daily and weekly physical           improving cardiovascular fitness and reduced CVD mortality
activity [43], and its importance is emphasized by several               have attracted only minimal attention in this population.
campaigns promoting an active lifestyle, including those by the
British Heart Foundation.
   Any physical activity is better than no, or little, physical          Resistance training
activity. The overall physiological adaptations that occur as a          Conventional resistance exercise programmes consisting of
result of exercise [44] provide protection against CVD mortality,        low-impact isometric and range-of-motion exercises have been
even in the presence of well-established CVD risk factors [45, 46].      repeatedly utilized in RA. The application of low-to-moderate
CVD mortality is lower in highly fit than in moderately fit              intensity strength exercise in RA patients increased physical
individuals [47], while physical inactivity is an independent risk       capacity [79, 80] without exacerbating pain or disease activity [81].
factor for the development of CVD [48, 49].                              However, high-intensity resistance exercise programmes represent
   Even though cardiorespiratory fitness may have a familial             a more effective means for increasing muscular strength compared
component [50], it can be increased significantly by exercise            with low-intensity training and range-of-motion exercises, without
training, regardless of age, gender, race and initial fitness levels     any evidence of aggravation of joint symptoms [82]. High-
[51]. The required activity levels can be accrued through formal         intensity exercise has even been reported to decelerate joint
training programmes or leisure-time physical activities [52].            damage in individuals with RA compared with non-exercising RA
Moreover, supervised exercise programmes are more effective              patients [83, 84], although this remains controversial [85, 86].
compared with non-supervised exercise [53, 54], most likely due to       Some patients with extensive structural damage may have to
greater adherence.                                                       refrain from activities that include significant loading of the
   Great controversy still exists about the optimum amount of            damaged joints [87].
exercise for eliciting the greatest cardiovascular benefit. Different       Well-constructed progressive resistance exercise is an effective
exercise intensity [55, 56] and duration [57], as well as various        and safe intervention for stimulating muscle growth in patients
combinations of them [58], may have different impacts on the             with RA and may even reverse rheumatoid cachexia [88]. This
magnitude of cardiorespiratory fitness improvement. Most authors         metabolic abnormality, which affects nearly two-thirds of all
agree that there is a dose–response relation between the amount of       individuals with RA, is characterized by involuntary loss of
exercise, all-cause and cardiovascular mortality [55, 57, 59].           muscle mass and progressive increase of fat mass in the presence
The greatest potential for reduced mortality is in sedentary             of stable or even slightly decreased weight [89]. The exact
individuals (such as many RA patients), in whom even slight              underlying mechanisms are not entirely clear [90]: possible
                                                                        Exercise and rheumatoid arthritis                                                                                     241

contributing factors not only include the overproduction of                                         appears to consistently induce beneficial effects in aerobic
inflammatory cytokines such as TNF-a [89] but also physical                                         capacity, functional ability and muscle strength.
inactivity [91, 92].
   Non-RCTs investigating the effects of resistance training in                                        Aquatic. Different types of water-based exercises such as
RA differ widely in training regimens, methodological approaches                                    aqua-aerobics and deep-water running have been applied in
and outcomes, making any conclusions difficult. The effectiveness                                   people with RA (Table 2). The in-water environment is thought to
of strength training lies on the quality and quantity of its                                        provide the ideal means for exercising in this population, as
application. Indeed, incorrect application of exercise frequency                                    weight-bearing is minimized due to buoyancy [106]. This is
and intensity may not induce improvements in muscular strength;                                     extended by the general belief of patients that this type of exercise
according to the ACSM [93], a successful muscular strength                                          improves their functional ability [107]. Most of the available
training programme for older populations or individuals with                                        evidence suggests that aquatic exercise does improve aerobic
sedentary lifestyles should incorporate at least two sessions per                                   capacity [108–110], muscular strength [85, 111] and psychological
week, involve 8–10 exercises for different muscle groups and allow                                  status [109]. The RCT with the larger number of RA patients
completion of one set of 10–15 repetitions per exercise. RCTs                                       combining both warm water immersion and exercise revealed
complying to these recommendations have revealed significant                                        significant improvements, as assessed by the Arthritis Impact
increases in functional ability [74, 84, 94] and muscular strength                                  Measurement Scales 2. However, this study did not include a
[75], without exacerbating existing joint damage [73, 95] in                                        laboratory-based evaluation of physical activity [109].
patients with RA.
                                                                                                       Dance. The effects of dance exercise have been investigated in

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Aerobic training                                                                                    many non-randomized trials (Table 3), which suggest improve-
                                                                                                    ments in aerobic capacity, walking ability, muscular strength
Patients with RA are less active, and therefore less physically fit,                                [115–117] and psychological parameters, such as anxiety and
compared with healthy individuals of the same age [70, 96]. The                                     depression [115, 118]. The only randomized trial involving dance
most frequently used mode of aerobic exercise training in studies                                   as an intervention in RA patients revealed that despite no
involving RA patients is cycling, followed by aquatic exercise,                                     significant changes in bone mineral density and disease activity,
aerobic dance and walking/running.                                                                  functional capacity and physical activity were significantly
                                                                                                    improved [119].
   Cycling. Cycling is a non-weight-bearing aerobic activity
where participants utilize large muscle groups of the lower                                            Walking and running. Walking has been used as an
extremity. It can be performed both in clinical settings as well as                                 intervention for improving patients’ disease status [108, 121,
outdoors, either individually or in groups [97]. Indoor cycles can                                  122], for the assessment of functional ability via gait analyses
be modified to accommodate the needs of almost every RA                                             [123–125] or walking tests [126], and as a method to predict
patient [98] and can be effective even when the patients are                                        maximal oxygen uptake [127]. Walking or jogging has been
minimally supervised [99]. An overview of the studies using cycling                                 included in training programmes without specifying the exact
is provided in Table 1. Although individual studies vary in exercise                                intensity, duration and frequency, but no RCTs based on walking
frequency and overall duration of the intervention, cycling                                         or running as the main mode of exercise have been conducted

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

                                                                            Cycling programmes

Author [reference]                    n                            EG                                      CG                                 Main outcomes                           Quality
Ekblom et al. [100, 101]          34 RA            DS ¼ 25–40 min                             Rehabilitation programme             Acute increase in aerobic capacity,            2
                                                   Intensity ¼ 50–70% of HRmax                                                     walk test
                                                   Frequency ¼ 5 d/wk, twice daily                                                 No change in pain perception
                                                   PD ¼ 5 wk and 6 months                                                          Long term ¼ increase in aerobic
                                                                                                                                   capacity, muscle strength
Harkcom et al. [102]              17 RA            DS ¼ 15, 25 or                             Routine activities                   Acute increase in aerobic capacity,            2
                                                   35 min                                                                          exercise tolerance
                                                   Intensity ¼ 70% of HRmax                                                        Decrease in disease activity
                                                   Frequency ¼ 3 d/wk
                                                   PD ¼ 12 wk
Karper and Evans [103]            1 RA             DS ¼ 20–30 min                                                                  Improvement of physiological and               Case study
                                                   Intensity ¼ 50–70 Watts                                                         psychological status
                                                   Frequency ¼ 3 d/wk
                                                   PD ¼ 14 wk
Lyngberg et al. [104]             18 RA            DS ¼ 15–45 min                             Routine activities                   Acute decrease in disease activity             No
                                                   Intensity ¼ 50–70% of HRmax                                                     Strength and aerobic status not                randomization
                                                   Frequency ¼ 2 d/wk                                                              reported
                                                   PD ¼ 8 wk
Baslund et al. [105]              18 RA            DS ¼ 15–30 min                             Current physical activities          Increase in aerobic capacity                   2
                                  EG ¼ 8           Intensity ¼ 80% of HRmax                                                        No changes on the immune system
                                  CG ¼ 8           Frequency ¼ 4–5 d/wk                                                            (blood mononuclear cells, prolif-
                                                   PD ¼ 8 wk                                                                       erative response, natural killer cell
Lyngberg et al. [94]              24 RA            DS ¼ 45 min                                Current activities                   Increase in functional capacity and            2
                                  EG ¼ 12          Intensity ¼ 50–70% of HRmax                                                     strength
                                  CG ¼ 12          Frequency ¼ 2 d/wk                                                              No significant differences were
                                                   PD ¼ 3 months                                                                   observed in ESR, number of tender
                                                                                                                                   joints and morning stiffness

  d/wk, day/week; RA, rheumatoid arthritis; EG, intervention for experimental group; CG, intervention for control group; DS, duration of session in minutes; PD, programme duration; HRmax, maximal
heart rate in beats per minute; ESR, erythrocyte sedimentation rate; n, number of participants.
242                                                                                  G. S. Metsios et al.

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

                                                                            Aquatic programmes

Author [reference]                             n                       EG                              CG                                      Results                                  Quality
Danneskiold-Samsoe et al. [112]            8 RA           Water exercise                                                   Increase in maximal quadriceps strength                No randomization
                                                                                                                           Increase in aerobic capacity
Stenstrom et al. [85]                      60 RA          DS ¼ 30–40 min                    Medical treatment              Increase in activity level, grip strength              No randomization
                                                          Frequency ¼ 1 d/wk                                               No changes functional/psychological
                                                          PD ¼ 4 yrs                                                       status. Controls had significantly more
                                                                                                                           admittances for acute hospital care
Hansen et al. [86]                         75 RA          DS ¼ 45–90 min                    Normal treatment               No effect of training on disease activity and          2
                                           EG ¼ 45        Frequency ¼ 3 d/wk                                               damage progression
                                           CG ¼ 15        PD ¼ 2 yrs
Minor and Hewett [113]                     42 RA          DS ¼ NS                           Received no attention          Improved aerobic capacity and exercise                 No randomization
                                           EG ¼ 20        Intensity ¼ NS                    apart from the testing         tolerance
                                           CG ¼ 22        Frequency ¼ 3 d/wk
                                                          PD ¼ 12 wk
Rintala et al. [114]                       34 RA          DS ¼ 45–60 min                    Normal daily activities        Improved muscle strength and mobility                  1
                                           EG ¼ 18        Intensity ¼ individualized                                       No increases in aerobic capacity
                                           CG ¼ 16        Frequency ¼ 2 d/wk
                                                          PD ¼ 24 sessions

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Hall et al. [109]                          139 RA         DS ¼ 30 min                       Seated immersion               Physical (AIMS2) and psychological ben-                2
                                                          Intensity ¼ NS                                                   efits (mood and tension) were apparent in
                                                          Frequency ¼ 2 d/wk                                               all groups
                                                          PD ¼ 3 months                                                    Hydrotherapy resulted in the greatest
Sanford-Smith et al. [111]                 24 RA          DS ¼ 25–60 min                    ROM and isometric              Increase in both grip strength and exercise            2
                                                          Intensity ¼ 70% of HRmax          exercises                      tolerance and decrease in ESR
                                                          Frequency ¼ 3 d/wk                                               Trend for improved HAQ
                                                          PD ¼ 10 wk
Bilberg et al. [107]                       46 RA          DS ¼ 45 min                       Normal activities              No changes in aerobic capacity                         3
                                           EG ¼ 20        Frequency ¼ 2 d/wk                                               Increased perception of physical function
                                           CG ¼ 26        PD ¼ 12 wk                                                       and muscular function

  d/wk, day/week; n, number of participants; RA, rheumatoid arthritis; EG, intervention for experimental group; CG, intervention for control group; DS, duration of session in minutes; PD, programme
duration; NS, not specified; HRmax, maximal heart rate in beats per minute; ROM, range-of-motion; AIMS2, arthritis impact measurement scales 2; ESR, erythrocyte sedimentation rate; HAQ, health
assessment questionnaire.

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

                                                                            Dancing programmes

Author [reference]                    n                            EG                                    CG                                       Results                               Quality
Perlman et al. [118]          43 RA                 DS ¼ 30–60 min                                                             Increase in performance of 50 ft walk              No randomization
                                                    Intensity ¼ 60–70% of HRmax                                                Decrease in pain and depression
                                                    Frequency ¼ 2 d/wk
                                                    PD ¼ 16 wk
Noreau et al. [115]           29 RA                 DS ¼ 30–60 min                         Counselling sessions                Increase in performance of 50 ft walk,             No randomization
                                                    Intensity ¼ 50–70% of HRmax                                                aerobic power, hamstring strength and
                                                    Frequency ¼ 2 d/wk                                                         mood state
                                                    PD ¼ 12 wk                                                                 Decrease in pain, depression and
Noreau et al. [116]           10 RA                 DS ¼ 25–60 min                                                             Increase in 6 min walk distance and                No randomization
                                                    Intensity ¼ 50–70% of HRmax                                                improved psychological state
                                                    Frequency ¼ 2 d/wk                                                         No significant changes in aerobic
                                                    PD ¼ 8 wk                                                                  capacity, disease activity
Neuberger et al. [117]        25 RA                 Low impact aerobic dance                                                   Decreased fatigue in the patients who              No randomization
                                                                                                                               participated the most
                                                                                                                               Increased aerobic fitness and grip
                                                                                                                               Decreased pain and walk time
                                                                                                                               No significant increases in joint count
                                                                                                                               or ESR
Westby et al. [119]           53 RA women           DS ¼ 45–60 min                         Habitual physical activities        Improved functional capacity and                   2
                              EG ¼ 23               Intensity ¼ NS                         and therapy                         activity level
                              CG ¼ 30               Frequency ¼ 3 d/wk                                                         BMD did not differ significantly
                                                    PD ¼ 12 months                                                             between groups
                                                                                                                               No change in disease activity
Moffet et al. [120]           10 RA                 DS ¼ 45–60 min                                                             Significant improvement in locomotion              No randomization
                                                    Intensity ¼ 50–70% of HRmax                                                ability and walking ability
                                                    PD ¼ 8 wk

  n, number of participants; RA, rheumatoid arthritis; EG, intervention for experimental group; CG, intervention for control group; DS, duration of session in minutes; PD, programme duration; NS, not
specified; HRmax, maximal heart rate in beats per minute; BMD, bone mineral density; d/wk, day/week.
                                                      Exercise and rheumatoid arthritis                                                     243

in RA. Interestingly, a case study has described a female with RA        improves long-term adherence and goes on to improve cardio-
who completed a whole marathon run following a training                  vascular outcomes for these patients.
programme [128].
                                                                         RA, cardiovascular disease and exercise
  Combination of aerobic and strength training. The com-
bination of intensive aerobic and strength training has been the         Suggestions for future practice and research
most widely used exercise regimen in recent research in RA and
produces an effective physical stimulus to achieve desirable             We propose the systematic introduction of exercise training as
physiological adaptations (Table 4). An RCT by van den Ende              part of the routine multidisciplinary care of patients with RA,
and colleagues [129] has highlighted that combining intense              with the specific aim of reducing cardiovascular risk and
aerobic and resistance training can lead to significant enhance-         preventing or managing CVD. This will require further research,
ment in both cardiorespiratory capacity and muscular strength.           adaptation of existing knowledge and resources where available,
Other RCTs support the beneficial effects of this type of                as well as development of new services.
exercise in patients with recent-onset [95], active [129] or inactive        Education on the cardiovascular aspects of rheumatoid disease
RA [130]. As a result of these findings, the American College of         and the role of exercise in preventing CVD and managing RA
Rheumatology updated the treatment guidelines to introduce               itself is a major area for future research and clinical practice
dynamic exercise as an effective means for the management of             development; this needs to be targeted both to patients and to
RA [131].                                                                healthcare professionals, aiming to achieve not just improved
                                                                         knowledge but mainly sustained lifestyle changes. This may
                                                                         require a combination of approaches, including behavioural

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Adherence to exercise in RA                                              approaches, involving several healthcare professionals [161].
Consistent engagement in an exercise regimen is essential to reach       It can link in with the further research required into ways of
improvements in fitness and physical well-being as well as               optimising long-term adherence to an active lifestyle and exercise
psychological benefits in people with RA. We therefore carried           regimes in this population.
out a systematic investigation of the evidence as to whether RA              The short- and longer-term effects of different exercise regimens
patients adhere to exercise regimens and what factors may                on important metabolic factors and on vascular function need to
influence this. In general, adherence/compliance has either been         be specifically investigated in the RA population. These have
mentioned in relation to lack of long-term continuation of exercise      never been researched in any populations characterized by ‘high
after an intervention [139] or has been investigated in exercise         grade’ systemic inflammation, where their regulation may be
regimes not specifically targeted at RA patients [99, 140–148].          under overwhelming pressure from inflammatory networks [4]
This has made it difficult to reach any definitive conclusion [139,      rendering them less susceptible to beneficial change through
149–158]. The Ottawa Panel’s meta-analysis [154] reviewing               exercise. Ultimately, long-term RCTs are needed to show whether
previous RCTs of exercise regimens for RA patients demonstrated          structured exercise programmes can be adhered to in the long
that adherence/compliance was included as an outcome only in             term, provide sustained cardiovascular benefits and reduce CVD
two studies [148, 159]; the first was excluded from the meta-            mortality in RA.
analysis for being a head-to-head study rather than a fully                  In the meantime, a pragmatic approach can be taken, build-
controlled study (it assessed dynamic muscle training vs progres-        ing upon existing infrastructure, knowledge and expertise.
sive muscle relaxation) [148]; the second was excluded for having        Rheumatology clinical nurse specialists [162], liaising with their
adherence as the sole outcome with little specific detail of the         cardiology counterparts and local cardiac rehabilitation services,
content of the (hand only) exercise intervention [159]. Other            can incorporate the important role of exercise in their RA patient
studies can also be criticized for inadequate-sized samples, short       education programmes. Equipment and expertise available in
follow-up, inappropriate control conditions and poor conformity          cardiac rehabilitation centres and community fitness clubs can be
with the interventions [151]. Long-term adherence may be                 adopted to provide exercise opportunities and classes for people
particularly important as a 12-week RCT comparing dynamic                with variable (and changing) degrees of physical disability, such as
exercise with isometric and range-of-motion exercises among RA           those with RA. Exercise can then be ‘prescribed’ on the basis of a
patients found that benefits for aerobic capacity and strength were      person’s exact needs.
lost another 12 weeks after the intervention [129]. O’Grady et al.           In Fig. 1, we propose a general schema of the factors that need
[153] also stated that long-term adherence would be required for         to be considered in any patient with RA, and their possible
sustained cardiovascular benefits in RA patients, but none of the        operationalization, with regard to the main objectives of their
studies they reviewed had addressed this.                                personalized exercise regimen. This includes two main categories
   General patient education has been reported to be effective in        of factors: (i) cardiovascular status and objectives; and (ii) overall
increasing the time spent exercising [141, 142]; however, this is not    and specific physical ability to exercise, related to RA status. We
a consistent finding [146]. It seems that increased adherence to         suggest as general principles that: (i) exercise is part of the general
exercise associates with lower baseline functional disability and        management of the RA patient and can be facilitated by other
disease activity [160] as well as the baseline levels of physical        interventions (e.g. pharmacological, educational, behavioural);
activity and fatigue [99]. Social factors, such as support of friends,   (ii) its main targets are first the attainment and maintenance of
significantly contribute to increased adherence to exercise regi-        optimal (for the individual patient) function of the musculoske-
mens [145]. This suggests that appropriate regimens should be            letal system, which can then facilitate exercises focused on
chosen for patients with more severe disease; dance sessions,            cardiorespiratory fitness; and (iii) exercise is tailored to the
for example, have high attendance [120], which is potentially due        individual (although it can be delivered in a group environment),
to the relatively low demands of this mode of exercise together          taking into account their baseline fitness and physical ability as
with its social component. Indeed, tailoring exercise regimens has       well as their personal preferences and objectives, so that ideally
been suggested to improve adherence [144, 153].                          a concordance of objectives can be achieved between the patients
   In summary, adherence to exercise has not been adequately             and the therapist [162].
studied in RA. High-quality evidence is rare, and appears to
suggest that well-controlled disease, better functional ability and         Cardiovascular status. We suggest a schematic division into
strong social structure may facilitate adherence to exercise by          those in whom exercise is aimed at reducing/managing CVD risk
patients with RA. Rigorous investigations are required to test           and those in whom it is incorporated in the management of
whether tailoring exercise regimens around these considerations          existing CVD (before or after an acute coronary syndrome).
244                                                                      G. S. Metsios et al.

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


Author [reference]                     n                           EG                             CG                           Results                       Quality
Nordemar et al. [132]        10 RA                  DS ¼ 23 h/wk                                                  Small increase in muscle               No randomization
                                                    Aerobic ¼ 50–70%                                              fibre size
                                                      of VO2max                                                   Decrease in pain
                                                    Strength ¼ NS                                                 Increase in muscular strength
                                                    PD ¼ 7 months                                                 No changes in VO2max
Nordemar et al. [83]         46 RA                  DS ¼ 30–60 min                       Pharmaceutical           EG less progression of joint           1
                             EG ¼ 23                Intensity ¼ varied                   therapy                  damage than CG
                             CG ¼ 23                   according to the patient                                   Increase in walking ability and
                                                    PD ¼ 4–8 yrs                                                  quadriceps torque
                                                                                                                  No changes in oxygen
                                                                                                                  consumption and heart rate
Stenstrom [133]              42 RA                  DS ¼ NS                              Same as EEG group        Better self-efficacy, functional       2
                                                    Intensity ¼ NS                       with different           capacity, less pain, lowered
                                                    Frequency ¼ 5 d/wk                   instructions             Ritchie index and increased
                                                    PD ¼ 12 wk                                                    mobility in the EEG group
van den Ende et al. [129]    100 RA 3 EG            DS ¼ 60 min                          ROM home                 Intensive dynamic training is          2
                               each n ¼ 25          Intensity ¼ 70–85% of HRmax          exercises                more effective than all other

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                             CG ¼ 25                Frequency ¼ 3 d/wk                                            groups in increasing aerobic
                                                    PD ¼ 12 wk                                                    fitness, joint mobility and strength
Komatireddy et al. [134]     49 RA                  Circuit training                     Habitual activities      Increase in functional capacity        2
                             EG ¼ 25                DS ¼ 20–27 min                                                No significant change in aerobic
                             CG ¼ 24                Strength ¼ NS                                                 fitness
                                                    Frequency ¼ 3 d/wk
                                                    PD ¼ 12 wk
Hakkinen et al. [74]         65 RA                  DS ¼ 45 min                          Recreational physical    Increases of EG in all muscle          2
                             EG ¼ 32                Aerobic ¼ NS                         activities and ROM       groups examined greater than
                             CG ¼ 33                Strength ¼ 50–70% of MVC             exercises                that in CG
                                                    Frequency ¼ 2 d/wk                                            No effect in disease activity
                                                    PD ¼ 12 months                                                No changes in BMD between
van den Ende et al. [130]    64 RA                  DS ¼ NS                              ROM and isometric        EG: physical and muscular              3
                             EG ¼ 34                Aerobic ¼ 60% of HRmax               exercises                strength improvement, decrease
                             CG ¼ 30                Strength ¼ 70% of MVC                                         in disease activity
                                                    Frequency ¼ 3–5 d/wk                                          CG: decrease in disease activity,
                                                    PD ¼ 24 wk                                                    muscular strength improvement
                                                                                                                  (less than EG)
Hakkinen et al. [135]        70 RA                  DS ¼ 30–45 min                       ROM and stretching       Increased strength, HAQ,               3
                             EG ¼ 35                Aerobic ¼ NS                         exercises                walking speed more pronounced
                             CG ¼ 35                Strength ¼ 50–70% of MVC                                      in EG
                                                    Frequency ¼ 2 d/wk                                            BMD increased in EG and
                                                    PD ¼ 24 month                                                 decreased in CG
de Jong et al. [73]          309 RA                 DS ¼ 90 min                          Habitual physical        Significant improvement in             3
                             EG ¼ 151               Frequency ¼ 2 d/wk                   activity                 functional ability in EG
                             CG ¼ 158               Aerobic ¼ 70–90% of HRmax                                     No radiological damage in any
                                                    Strength ¼ NS                                                 group
                                                    PD ¼ 2 yrs
Hakkinen et al. [136]        70 RA                  DS ¼ NS                              ROM and stretching       Improvement in strength, HAQ           3
                             EG ¼ 35                Frequency ¼ 2 d/wk                   exercises                and overall function capacity
                             CG ¼ 35                Aerobic ¼ NS
                                                    Strength ¼ 50–70% of MVC
                                                    PD ¼ 24 months
Hakkinen et al. [137]        23 RA                  DS ¼ 45–60 min                       The same interven-       Significant muscular strength,         No randomization
                                                    Frequency ¼ 3 d/wk                   tion in healthy          walking speed, vertical jump and
                                                    Aerobic ¼ progressive load           individuals              aerobic capacity
                                                    Strength ¼ progressive load
                                                    PD ¼ 21 wk
de Jong et al. [138]         RAPIT programme        DS ¼ 90 min                          Habitual physical        Exercise results in slowing down       3
                              309 RA                Frequency ¼ 2 d/wk                   activity                 in the loss of BMD at the hip
                             EG ¼ 151               Aerobic ¼ 70–90% of
                             CG ¼ 158                 predicted HRmax
                                                    Strength ¼ NS
                                                    PD ¼ 2 yrs
de Jong et al. [84]          RAPIT programme        DS ¼ 90 min                          Habitual physical        No progression of hand and feet        3
                              309 RA                Frequency ¼ 2 d/wk                   activity                 damage is not increased
                             EG ¼ 151               Aerobic ¼ 70–90% of
                             CG ¼ 158                 predicted HRmax
                                                    Strength ¼ NS
                                                    PD ¼ 2 yrs
Hakkinen et al. [75]         70 RA                  DS ¼ 45 min                          ROM and stretching       Strength gains during the 2-yr         3
                             EG ¼ 35                Frequency ¼ 2 d/wk                   exercises                training programme were
                             CG ¼ 35                Aerobic ¼ NS                                                  maintained
                                                    Strength ¼ 50–70% of MVC                                      More favourable development of
                                                    PD ¼ 2 yrs follow-up                                          BMD in EG group
                                                      after 5 years                                               Radiological damage remained

                                                                       Exercise and rheumatoid arthritis                                                                                  245

TABLE 4. Continued


Author [reference]                           n                                 EG                               CG                              Results                         Quality
Munneke et al. [87]         RAPIT programme 309 RA                 DS ¼ 90 min               Habitual physical activity Dynamic training accelerates                      3
                            EG ¼ 151                               Frequency ¼ 2 d/wk                                   joint damage progression in
                            CG ¼ 158                               Aerobic ¼ 70–90% of HRmax                            patients with pre-existing
                                                                   Strength ¼ NS                                        extensive damage
                                                                   PD ¼ 2 yrs
Hakkinen et al. [126]       23 RA 12 healthy matched               DS ¼ 30–45 min                   The same as EG group          Significant increases in                No randomization
                              controls                             Frequency ¼ 2–3 d/wk                                           VO2max, muscle strength and
                                                                   Aerobic ¼ NS                                                   EMG activity in both groups
                                                                   Strength ¼ 50–70% of MVC
                                                                   PD ¼ 21 wk

 n, number of participants; RA, rheumatoid arthritis; EG, intervention for experimental group; CG, intervention for control group; DS, duration of session in minutes; PD, programme duration;
NS, not specified; HRmax, maximal heart rate in beats per minute; ROM, range-of-motion; MVC, maximal voluntary contraction; BMD, ¼bone mineral density; VO2max, maximal oxygen uptake;
HAQ, health assessment questionnaire; EMG, Electromyography; d|wk, day|week.

                                                                                 Cardiovascular status

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                                                     Reducing/managing CVD Risk                           Existing CVD

                                                     Little risk           Higher risk         Pre-acute event        Post-acute event

                  Baseline cardiorespiratory fitness
                                                                                     RA patient                                          Personal preferences
                  Available infrastructure

                                    Little inflammation            Little inflammation             Active inflammation                Active inflammation
                                       Little damage                  Much damage                     Little damage                      Much damage
                                   Good physical ability                                      Limited physical ability

                                                                       Rheumatoid arthritis status
FIG. 1. Major considerations in designing individualized exercise training in patients with rheumatoid arthritis.

Exercise for the latter has already been discussed in previous                                    exercise test, during which the workload is increased at regular
sections (but will need to be adopted according to the individual                                 intervals until self-reported exhaustion) prior to starting an
patient’s physical constraints, as discussed subsequently). For the                               exercise intervention, will help to establish the appropriate
former, the ACSM has developed a risk stratification algorithm,                                   workload for each individual and to refine their personalized
in order to optimize the safety of participation in exercise                                      exercise programme.
programmes. This is based on consideration of the following
specific risk factors: total cholesterol >6.5 mmol/l; smoking;                                       Physical ability to exercise. We have schematically divided
family history of CVD; sedentary lifestyle; diabetes mellitus                                     patients into those with good overall physical ability (mostly those
(blood glucose >6.7 mmol/l); systolic blood pressure >140 mmHg                                    with little current inflammation and little accumulated permanent
and overweight or obesity with BMI >25 kg/m2: individuals with                                    joint damage); and those with limited physical ability (usually
less than three of these components are considered at low risk for                                patients with a lot of joint inflammation, a lot of structural joint
developing CVD-related complications while exercising, whereas                                    damage or both). This can help refine the overall multidisciplinary
those with three or more of these components are at higher risk                                   approach, incorporating specific exercise regimens, to their treat-
[43]. The thresholds for some of these risk factors may need to be                                ment. In the former, pharmacological therapy would be aimed at
altered for the RA population: for example, total cholesterol may                                 maintaining good disease control; some range of motion exercises
be spuriously low during periods of active RA [8] and BMI                                         and resistance training could be utilized to maintain a good level of
thresholds for overweight reduced to 23 kg/m2, as recently                                        musculoskeletal system mobility and function; and the main focus
described [10]. Based on this, exercise of appropriate mode,                                      should be aerobic training aiming at optimizing cardiovascular
intensity, duration and frequency can be designed to provide                                      fitness, to the degree determined by their current levels of fitness
adequate workload for cardiovascular benefits [68]. There is a                                    and allowed by their cardiovascular risk stratification. Patients in
wide range of options, but current ACSM guidance for optimum                                      the group with limited physical ability to exercise due to the
cardiovascular benefits and enhanced cardiorespiratory capacity                                   impact of RA have been subdivided into three subgroups: In
includes regular participation (>3 times weekly) at sufficient                                    those with a lot of current inflammation, but little structural
intensities (60–80% of VO2max) and time (at least 20–30 min) [43].                                damage, we propose aggressive pharmacological therapy to
Thus, determining the current level of fitness (usually by a graded                               quickly reduce active inflammation and prevent muscle loss, due
246                                                                        G. S. Metsios et al.

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