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Review

Paediatric exercise training in prevention and treatment Guido E Pieles,1,2 Richard Horn,3 Craig A Williams,3 A Graham Stuart1 1

Congenital Heart Unit, Bristol Royal Hospital for Children/ Bristol Heart Institute, Upper Maudlin St, Bristol, UK 2 National Institute for Health Research (NIHR) Cardiovascular Biomedical Research Unit, Bristol Heart Institute, Bristol Royal Infirmary, Bristol, UK 3 Children’s Health & Exercise Research Centre (CHERC), College of Life and Environmental Sciences, St. Luke’s Campus, University of Exeter, Exeter, UK Correspondence to Dr Guido E Pieles, Congenital Heart Unit, Bristol Royal Hospital for Children/Bristol Heart Institute, Upper Maudlin Street, Bristol BS2 8BJ, UK; [email protected], [email protected] Received 7 October 2013 Revised 22 November 2013 Accepted 27 November 2013 Published Online First 18 December 2013

To cite: Pieles GE, Horn R, Williams CA, et al. Arch Dis Child 2014;99:380–385. 380

ABSTRACT Exercise training is an underused intervention in paediatric healthcare. This is surprising, since initial evidence demonstrates its effectiveness and safety; furthermore it confers socioeconomic benefits for healthcare systems. Pilot studies have assessed and confirmed the feasibility of exercise training in many paediatric disease settings. However, more research is needed to understand the pathophysiology, quantify treatment effects and monitor outcomes. A concerted effort from researchers, health professionals and police makers will be necessary to make exercise training an evidence-based and cost-effective intervention in paediatric care.

INTRODUCTION Physical activity and health Play and exercise form an essential part of children’s daily life and innumerable skills are acquired during physical activity (PA). PA contributes significantly to the development of motor and sensory skills, bone strength, a healthy body composition, reduced incidence of metabolic risk factors and improved mental health. A proportion of the recent decline in regular daily activity levels has been attributed to increases in electronic media use,1 2 creating a so called urban ‘activity toxic’ home environment with less space and increased safety risks3 and a decrease in free or discretionary play time.4 The trend towards an inactive lifestyle over the last years is most pronounced in teenagers with only 32% of teenage boys and 15% of girls meeting government activity targets.5 6 Numerous studies have established strong links between reduced PA and all-cause mortality in adults.7 In the UK inactivity is the cause of 3% of disability-adjusted years of life lost (DALY) which amounts to a health-economic burden to the National Health Service (NHS) of £1.06 billion.8 Taken together, diet and physical inactivity amount to a disability-adjusted years of life loss of 14·3% according to the most recently published UK health performance survey.9 It is generally accepted that physical exercise contributes significantly to child wellbeing, health and development.1 However, more evidence is required to define the specifics of exercise prescription that is, frequency, intensity and duration applicable to healthy and children with disease. Furthermore, our understanding of the mechanisms underlying exercise training benefits in specific diseases is limited. Although the morbidity associated with an inactive lifestyle in children and adolescents is gradually being appreciated by paediatric health professionals,3 10 more work is needed. Currently, fewer

than 25% of inner city children reach government recommended levels of PA.11

Definition and assessment of physical activity PA is a complex set of behaviours encompassing any bodily movement which results in energy expenditure above the resting level.12 Exercise and physical fitness are terms which are often used interchangeably with PA but they are not identical. Exercise refers to PA which is planned and repetitive often with the intent to improve a particular component of physical fitness. Physical fitness is a conceptual term referring to attributes which relate to the ability to perform PA for example, strength, speed, aerobic fitness.13 Despite methodological challenges such as the control of the environment, inhomogeneous and small study cohorts and the confounding effects of growth and maturation, several organisations have published activity recommendations for healthy children (table 1).

Benefits of training and recommendations Despite considerable evidence for the health benefit of PA14 15 there is increasing concern that physical fitness and exercise have become sidelined in paediatric practise.12 16 Individualised exercise training programmes can play an important role in reducing physical inactivity and aid in rehabilitation. In particular, the association between poor cardiovascular fitness and risk of cardiovascular disease has led to the use of aerobic training as a key component of cardiac rehabilitation for adults with acquired heart disease.17 In a similar manner, regular exercise can reduce cardiovascular risk factors in children.18 19 It is noteworthy that, at least in the UK, no formal programme of exercise rehabilitation exists for children with congenital heart disease (CHD). A possible reason for this observation is that methodologies for assessing the outcome of exercise interventions vary widely; often focusing on the measurement of physiological parameters and focusing less attention to overall health status.20 21 General recommendations of the American College of Sports Medicine for aerobic training in healthy children were published in 1998, but these do not include advice on mode, length and intensity of training. More recent guidelines are targeted towards elite adolescent athletes but the recommendations of 3–4 exercise sessions lasting 40–60 min at an intensity of 85–90% of maximum heart rate could equally apply for the healthy paediatric population and promote ‘optimal lifetime health’.22 However, there are no clear guidelines on what exercise should be prescribed for children with a chronic illness. Research is urgently needed to identify the optimum mode, intensity and duration of

Pieles GE, et al. Arch Dis Child 2014;99:380–385. doi:10.1136/archdischild-2013-303826

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Review Table 1

Summary of current guidelines for physical activity (PA) in childhood

Guidelines

Year

Key recommendations

Canadian Society for Exercise Physiology (5–17 years)

2012

UK Department of Health PA Guidelines for Children and Young People (5–18 years)

2011

World Health Organisation Global Recommendations on PA for Health (5–17 years old)

2011

US Department of Health and Human Services (HHS) 2008 PA Guidelines for Americans (children and adolescents)

2008

Australian Government Department of Health and Ageing (5–18 years)

2005

Children aged 5–17 years should engage daily in 60 min of moderate to vigorous PA. This should include: vigorous-intensity activities at least 3 days per week, activities that strengthen muscle and bone at least 3 days per week. For health benefits, children aged 5–17 years should minimise daily sedentary time by limiting screen time to no more than 2 h per day, limiting sedentary (motorised) transport, extended sitting and indoor time Children and young people should engage in moderate to vigorous PA for at least 60 min and up to several hours every day. Vigorous intensity activities, including those that strengthen muscle and bone, should be incorporated at least 3 days a week. All children and young people should minimise sedentary time Children aged 5–17 years should accumulate at least 60 min of moderate to vigorous PA daily. Amounts of PA greater than 60 min provide additional health benefits. Most of the daily PA should be aerobic. Vigorous-intensity activities should be incorporated, including those that strengthen muscle and bone, at least three times per week Children and adolescents should do 60 min or more of PA daily. Most of the 60 min or more should be moderate or vigorous aerobic PA, and should include vigorous PA at least 3 days a week. As part of their 60 min daily PA, children and adolescents should include muscle and bone strengthening PA on at least 3 days of the week A combination of moderate and vigorous activities for at least 60 min a day is recommended. Children should not spend more than 2 h a day using electronic media for entertainment, particularly during daylight hours

exercise required to facilitate rehabilitation, recovery and prevention of long-term deterioration for specific diseases of childhood.

Exercise training concepts in paediatric disease Exercise training in the context of medical treatment or rehabilitation is underused at present in most healthcare systems despite widespread evidence of health benefit in children.23 24 Although preliminary knowledge of exercise limitations exists for many paediatric disease groups, the few available generic training programmes which exist address overall body systems and their use needs to be tailored to specific diseases and disease-specific targets. This has been reviewed in detail elsewhere.12 Moreover, existing paediatric exercise guidelines are based on expert consensus rather than clear evidence-based data. One such set of recommendations is by the American Heart Association which categorises exercise into dynamic and static exercise stress and can be used to advise appropriate exercise types and levels, to define training methods and also assess the safety of exercise programmes (figure 1).25 However, critical scrutiny of the guidelines as applied to children show that the logic of precisely classifying a named activity (eg, rugby or sprinting—defined as moderate) may be flawed and will be dependent on many factors not least the age, physical maturity and competitive nature of the participants. Despite the generality of the American Heart Association guidelines and controversy related to precise classifications, there is slowly accumulating evidence of the treatment benefits of exercise programmes for specific paediatric disease. In the following section we describe the level of evidence for training programmes in the specific disease setting using the Oxford Centre for Evidence Based Medicine classification (table 2).

EXERCISE TRAINING IN SPECIFIC CONDITIONS Congenital heart disease CHD is defined as a defect in the structure of the heart and/or great vessels, which is present at birth.26 Activity levels and exercise tolerance in children with CHD are reported to be lower than in the average population.27 Exercise testing is a routine diagnostic tool in CHD and there are preliminary data on the benefit of exercise as therapy in children and adults.28 29 However, since exercise training has not been explored Pieles GE, et al. Arch Dis Child 2014;99:380–385. doi:10.1136/archdischild-2013-303826

sufficiently in the research setting, it has yet to form a key role in clinical practice.30 Moreover, there is a significant lack of knowledge of the risks and benefits of exercise in patients and families of children with CHD.31 Available studies and consensus recommendations have reported exercise training to be a safe intervention in CHD.28 32 Additionally, recommendations for participation in competitive sports have been published27 33 and it is safe for most children with CHD to compete at an amateur level. Non-randomised controlled trials and observational studies have provided data to indicate clear, sustained benefits following structured exercise training. These include an increased exercise capacity and improvements in some psychological parameters.28 Some exercise parameters have also been shown to have a high prognostic value (reviewed in ref. 28). Existing single-centre non-randomised trials observational studies provide level 3 evidence of short-term and long-term benefits in parameters such as exercise endurance, oxygen consumption, blood pressure and heart rate. Exercise training in the patient group with CHD should be tailored to take account of an individual’s disease subtype, the medical intervention used to treat them and their current fitness level.28 Programmes also need to account for deficiencies in other organ systems commonly found in children with CHD ( pulmonary, musculoskeletal, neurological and nutritional). Overprotection of the patient by carers, teachers and medical professionals can lead to the avoidance of exercise intensity at which the training effect is most pronounced. Together with the absence of easily available exercise training programmes, this can represent a significant hurdle.34 Despite level 3 treatment benefit evidence, only 10% of all adult candidates with CHD receive structured exercise training and the number is estimated to be even lower in the paediatric population.24 The recently published document from the European Association for Cardiovascular Prevention and Rehabilitation on PA and exercise prescription for adolescents and adults with CHD is a first step towards an evidenced-based approach.35

Respiratory disease Asthma Chronic impairment of the respiratory system can lead to reduced exercise capacity. The most common form, childhood 381

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Review Figure 1 Classification of sports. This classification is based on peak static and dynamic components achieved during competition. It should be noted, however, that higher values may be reached during training. The increasing dynamic component is defined in terms of the estimated per cent of maximal oxygen uptake (VO2max) achieved and results in an increasing cardiac output. The increasing static component is related to the estimated per cent of maximal voluntary contraction reached and results in an increasing blood pressure load. The lowest total cardiovascular demands (cardiac output and blood pressure) are shown in green and the highest in red. Blue, yellow and orange depict low moderate, moderate and high moderate total cardiovascular demands, respectively. *Danger of bodily collision. †Increased risk if syncope occurs. Figure and legend reproduced with permission from Elsevier. review on physical training in cystic fibrosis has highlighted the inconsistencies in methodology and outcome measures in published data and emphasised the need to investigate the optimal training programme choice and to define comprehensive outcome measures.47 Despite the benefits associated with exercise and increased PA levels, only 26% of clinics in the UK provide exercise training programmes for patients with cystic fibrosis.48

asthma has been associated with reduced exercise and endurance capacity.36 RCT evidence is scarce, but two trials have shown an increase in exercise tolerance and also quality of life.37 38 Correct preventative treatment using inhaled bronchodilators and steroids has resulted in normal activity levels in children with asthma and exercise intolerance is seen only in moderate to severe asthma.39 Many studies have shown that activity level is a stronger predictor of low exercise capacity than severity of disease and structured exercise programmes result in normalisation of cardiopulmonary endurance after exercise training in children with severe asthma.38 PA has also a preventative role as protective factor against asthma development.40 The overall evidence for the benefits of PA reaches level 2–3.

Obesity The prevalence of childhood obesity is approaching 20%,49 resulting in global initiatives led by the WHO. Obesity associated health risks previously only seen in adults are now commonly seen in the paediatric population.50 The European Youth Heart Study has demonstrated a negative association between PA and cardiovascular risk factors including obesity.51 Alongside dieting and behaviour modification, physical exercise has been proposed as a low cost, safe and effective intervention in obesity. Some studies suggest that increased activity and exercise alone can be enough to prevent obesity52 but a multiinterventional approach is considered to be most effective.53 Adolescents are a particularly important target group, since it is at this age that PA behaviour patterns and body composition become established.54 Randomised controlled trials of specific training programmes to treat obesity have demonstrated benefit on overall fitness and exercise capacity, body composition, insulin sensitivity and biochemical indices of fat metabolism.55

Cystic fibrosis

Children with cystic fibrosis participate in a similar total amount of overall PA to healthy children, however, they spend less time in vigorous intensity PA and have a significantly lower exercise capacity.41 Exercise training should therefore play an important role in treatment strategy.42 Recent data in children have shown a significant increase in respiratory and skeletal muscle strength and maximal oxygen consumption after aerobic and resistance inspiratory muscle training in short-term and long-term programmes.43–45 Low fitness parameters are associated with increased mortality46 and initial evidence for exercise training also shows a positive effect on quality of life.45 The evidence of the available studies reaches level 2–3. A recent Cochrane

Table 2 Classification of treatment benefit level Question

Level 1

Level 2

Level 3

Level 4

Level 5

Does this intervention help? (treatment benefits)

Systematic review of randomised controlled trial or n-of-1 trial

Randomised controlled trial or observational study with dramatic effect

Non-randomised controlled cohort/follow-up study

Case-series, case-control, or historically controlled studies

Mechanism-based reasoning

Adapted from: Oxford Centre for Evidence Based Medicine (OCEBM)—Levels of Evidence Working Group. ‘The Oxford 2011 Levels of Evidence’. Oxford Centre for Evidence-Based Medicine. http://www.cebm.net/index.aspx?o=5653.

382

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Review Available evidence for benefits of programmes including exercise intervention is level 1–2. Recent systematic reviews have concluded that there is moderate evidence for success of community-based or school-based prevention programmes with low success of home-based programmes.56 Interestingly the strongest impact in any antiobesity programmes has been observed if an activity or training component is part of the intervention.56–58 This is reflected in the most recent National Institute for Health and Care Excellence guidance document.59 The relationship between body mass, fitness and cardiovascular health is complex. Thus, although obesity in childhood correlates with increased cardiovascular risk, it is not correct to associate ‘thinness’ with physical fitness.

Oncology Childhood cancer treatment is associated with decreased PA levels due to hospitalisation, reduced motivation, reduced overall energy levels and deconditioning.60 Therefore guided physical training in the rehabilitation phase can have benefits. Exercise programmes have shown a positive effect on aerobic fitness but also emotional wellbeing and social reintegration and thus improve physical and mental quality of life.61 62 The evidence for this was collected in small case control studies; available studies have not assessed long-term benefits of exercise programmes or thoroughly investigated the effects of cancer treatment on exercise parameters. The role of exercise programmes in the management of side effects such as anthracycline-induced cardiomyopathy has not been investigated. The evidence of the studies conducted so far support the wide role of therapeutic exercise in paediatric oncology as level 3.60

Neuromuscular disease Studies in this area have centred on cerebral palsy. Lower limb resistance and aerobic training programmes in cerebral palsy have shown strength and gait improvement, and an increase in aerobic capacity.63 64 Secondary effects such as weight reduction were also observed. Methodology and outcome measures differ significantly as investigated in a recent systematic review65 and including five randomised controlled trials the level of evidence is 2–3. Exercise programmes for adults with muscular dystrophy have targeted muscle strength and flexibility to maintain and improve functional capacity and also improve aerobic and muscular endurance.66 Paediatric evidence is quantitatively and methodologically poor but reviews suggest a positive effect of exercise training in children with muscular dystrophies.67 The overall level of evidence for muscular dystrophies is 4. Exercise programmes can also improve general motor and coordination impairment, a feature of many genetic syndromes. For example, an assisted cycle training programme in young people with Down syndrome had beneficial effects on fine motor tasks.68

DEVELOPMENT OF EXERCISE TRAINING PROGRAMMES WITHIN HEALTHCARE SYSTEMS Exercise training as treatment intervention There is sufficient evidence to suggest an overall health benefit of exercise training programmes in the paediatric disease context. However, the effectiveness of existing exercise intervention programmes has been criticised and optimal training methods have yet to be determined. A recent systematic review concluded that existing physical intervention programmes in children had a very small effect equivalent to only 4 min additional walking per day.69 Future efforts need to be directed towards research investigating disease-specific exercise Pieles GE, et al. Arch Dis Child 2014;99:380–385. doi:10.1136/archdischild-2013-303826

limitations, their pathophysiology and exercise programmes that can address these in a tailored approach. Existing assessment tools and outcome measures methodologies are inadequate to capture and monitor long-term treatment benefits. Outcome measures will need to focus on child-specific measures for example, mental and cognitive aspects, effect on social life (peer group integration) and somatic and psychological development. Much of this knowledge is available to paediatric exercise scientists and a concerted effort is necessary for this knowledge to reach paediatric healthcare professionals. Exercise training can then take its place as an effective and evidenced treatment strategy. An ideal intervention should be provided out of hospital, directed by patient and parent, promote patient autonomy, and be a low risk and low side effect intervention—exercise training can fulfil all of these criteria. If successful this may represent a more effective and economical way to improve quality of life than pharmocotherapy.70

Socioeconomic impact and policy At present 31% of the world’s population are not meeting minimum activity recommendations.71 It has been estimated that the incidence of non-communicable diseases worldwide could be decreased by 10% if physical inactivity could be eliminated.72 Moreover, a substantial socioeconomic burden of £1.06 billion8 to the NHS alone could be decreased if healthcare professionals and policymakers worked together to create a medium and long-term strategy, to promote PA, and to establish exercise medicine as a core concept of modern healthcare systems. In this paper, we provide evidence that exercise training can also be used to reduce the effects of chronic paediatric disease as well as prevent later degenerative conditions. Existing large scale socioeconomic strategic models on how to address the alarming worldwide inactivity increase in the general population aim to promote activity orientated school programmes, transport logistics, urban infrastructure, healthcare system integration, public education and motivation using modern media (‘gamification’)73 and community and sports programmes.74 Paediatric health professionals have a central role to play, as there is now sufficient evidence that programmes to promote long-term regular PA are most successful if started at school age75 and lifestyle patterns and health risks acquired in childhood strongly influence adult morbidity and mortality.

CONCLUDING REMARKS This review gives a brief summary of the current evidence on exercise training in paediatric disease. It highlights the need for a structured and multidisciplinary approach to address the alarming increase in morbidity risk associated with childhood inactivity and the underuse of exercise prescription in long-term care of chronic childhood conditions. A worthy goal would be to make exercise assessment and prescription an integral part of the paediatric consultation. An informed exercise assessment and prescription strategy will require the development of disease-specific research programmes to evaluate the optimal exercise strategy required for benefit. This will involve a multidisciplinary approach using the skills of paediatric exercise physiologists, physiotherapists, psychologists, educationalists and paediatricians. It will also require a significant enhancement of knowledge in paediatric exercise science across the health profession and considerable political effort to embed it within healthcare structures. However, the long-term benefits of such a policy would do much to pre-emptively address the predicted significant cardiovascular and general morbidity of future 383

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Review generations and limit the health-economic burden that healthcare systems will be faced with within the next decades.

24

Contributors GEP conceptualised, performed the literature review and wrote the review.

25

RH performed the literature review and helped editing the manuscript. CAW conceptualised the paper, edited and checked the manuscript.

26 27

AGS conceptualised, edited and checked the manuscript. Funding This work was supported by the National Institute for Health Research (NIHR) Biomedical Research Unit in Cardiovascular Disease at the University Hospitals Bristol NHS Foundation Trust and the University of Bristol. RH was supported by Heart Research UK. Competing interests GEP is the holder of a NIHR Academic Clinical Lectureship in Paediatric Cardiology. AGS is Medical Director of Sports Cardiology UK, (http:// www.Sportscardiology.co.uk) a company which specialises in the assessment of the athlete with cardiovascular symptoms.

28 29 30

31

Provenance and peer review Commissioned; externally peer reviewed. 32

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Paediatric exercise training in prevention and treatment Guido E Pieles, Richard Horn, Craig A Williams, et al. Arch Dis Child 2014 99: 380-385 originally published online December 18, 2013

doi: 10.1136/archdischild-2013-303826

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Paediatric exercise training in prevention and treatment.

Exercise training is an underused intervention in paediatric healthcare. This is surprising, since initial evidence demonstrates its effectiveness and...
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