Abstract
Background: Many patients with Down syndrome (PWDS) have poor cardiometabolic risk profiles, aerobic capacities and weak hypotonic muscles, primarily because of physical inactivity and poor diet.
Objectives: This study discusses the benefits of exercise therapy on body composition, aerobic capacity, muscle strength, proprioception and cardiometabolic profiles of PWDS.
Methods: A literature review using the Crossref metadatabase, following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA), focusing on the period 2007-2018, was undertaken. Each record was judged adopting the modified Downs and Black Appraisal Scale. The literature investigation identified 15 701 records. Records were excluded if they were published before 2007, pertained to the impact of exercise on intellectual disabilities beyond Down syndrome or the impact of medical, pharmaceutical, nutrition and psychological interventions among PWDS and were published in languages besides English. Nineteen articles were synthesised into this commentary.
Results: PWDS have a heightened cardiometabolic risk profile and high oxidative stress associated with elevated insulin resistance, poor insulin sensitivity, atherosclerosis and hypertension. PWDS have low aerobic capacity (VO2max), peak heart rates, muscle strength, agility and balance. Regular physical activity is beneficial to improve their VO2max and muscle strength. Moreover, regular physical activity reduces lipid peroxidation and arterial cell wall damage, the pathogenesis of atheroma is limited.
Conclusion: Exercise therapy compliance seems to have a positive impact on the cardiometabolic risk profile, muscle strength and aerobic work capacity of PWDS. Nonetheless, additional vigorous experimental investigations are necessary to better understand the effect of exercise therapy on the aerobic, strength, proprioception and cardiometabolic risk profile of PWDS.
Keywords: cardiometabolic; Down syndrome; exercise; muscle strength; proprioception; obesity.
Introduction
The longevity of patients with Down syndrome (PWDS) has chronologically extended over the course of the last century (Vis et al. 2009). In 1929, the average lifespan of PWDS was 9 years; this later increased to 12 years (1949), and then progressively extended to 35 years (1982) and reaching 55 years (2007) a decade ago (Barnhart & Connolly 2007). The increased longevity among PWDS is quite possibly because of improved medical and pharmaceutical management (Duffels et al. 2009). Vis et al. (2009) reported that one to two babies out of every 1000 live births are identified with Down syndrome (DS). The increased longevity of PWDS is of concern as this increases the demands placed on parents and caregivers who act as resident guardians (Barnhart & Connolly 2007). Because of the generally poor cardiometabolic risk profile and aerobic capacity of PWDS, they are doubly dependent on their caregivers for whom the burden of care only increases as both caregivers and patients age.
Patients with Down syndrome have an increased risk of acquiring secondary physiological pathologies due primarily to a physically inactive lifestyle and poor nutritional choices (Heller et al. 2008). These pathophysiological conditions include cardiovascular diseases, pulmonary hypoplasia, muscle hypotonia, osteoporosis, arthritis, osteoarthritis, diabetes mellitus and obesity (Heller et al. 2008). Muscle atrophy as well as poor muscle strength and endurance are co-maladies of physically inactive (sedentary) living and are frequently observed in PWDS (Dishman, Heath & Lee 2013). Heller et al. (2008) reported that the average longevity of PWDS is 55 years – 11 years fewer than individuals with other intellectual disabilities and 15 years shorter than the general populace. Rimmer, Braddock and Fujiura (1995) reported that only 10% of intellectually disabled individuals engage in a minimum of 3 days of physical activity weekly; the sedentary lifestyle adopted by the majority of intellectually disabled individuals adversely contributes to their poor fitness status, further contributing to the higher rates of obesity that are found among PWDS.
The cardiovascular diseases that have been identified among PWDS include mitral value prolapse, endocarditis, atherosclerosis and congestive heart failure (Vis et al. 2009). Patients with Down syndrome have an incidence of obesity that ranges from 31% to 47%; the high level of obesity has been associated with their sedentary lifestyle and poor eating habits (Vis et al. 2009). Abnormally high lipid profiles among PWDS are correlated with atherosclerosis (Wallen et al. 2009). The physically inactive lifestyle adopted by PWDS is furthermore associated with lower cardiorespiratory capacity, higher adiposity and reciprocal lower muscle mass, poor muscular strength, endurance, hypotonic muscles, and lower sympathetic nervous system response to physical activity and exercise (Izquierdo-Gomez et al. 2015).
Although a plethora of literature extolling the virtues of adopting a physically active lifestyle exists, few review articles describing the empirical findings of the benefits of physical activity and exercise among individuals with DS have been published (2007–2017). The commentary offered by Barnhart and Connolly (2007) suggests that as PWDS age they have higher cardiometabolic risk profiles, and that, consequently, the adoption of regular physical activity would be beneficial. The study undertaken by Barnhart and Connolly (2007) is, however, limited in so far as they failed to describe their literature gathering technique. A further limitation of the study lies in the absence of an explanation of the manner in which exercise could improve the health of PWDS.
Similarly, the clinical commentary of Fernhall, Mendonca and Bynard (2013) does not reflect the manner in which the literature was sourced; the authors, however, postulate that poor aerobic capacity in PWDS is attributed to their autonomic dysfunction. The systematic literature review by Bertapelli et al. (2016) focused on the prevalence of obesity among young PWDS, and upon interventions within this population, noting the high occurrence of obesity among young PWDS. They further highlighted the inconsistent impact of interventions that sought to curtail the obesity of young PWDS. However, Bertapelli et al. (2016) only reviewed five exercise and physical interventions, unlike this commentary, which has identified 11. This review sought to determine whether subsequent experimental studies had been conducted after the Bertapelli et al. (2016) review, and whether these studies provided evidence to substantiate the claim that regular physical activity decreases obesity among PWDS, thereby improving their cardiometabolic risk profile. The present review further sought to determine whether exercise therapy improved the cardiometabolic risk profile of PWDS, whereas Shields et al. (2018) focused on the impact of exercise induced oxidative stress on PWDS. The findings detailed by Shields et al. (2018) did not relate to the cardiometabolic risk profile of PWDS. The aforementioned empirical studies were reviewed according to Mill’s Canons to ascertain the vigour of causal relationship between regular exercise interventions and improved health among the PWDS.
This review offers two unique characteristics differentiating it from previous reviews: (1) a description of the pathogenesis of obesity, diabetes mellitus and atherosclerosis common among PWDS, and (2) a description of the physiological mechanism of how regular aerobic exercise and physical activity improve the cardiometabolic profile of PWDS.
Methods
The literature review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) practices. This was done to ensure that all pertinent literature was sourced and synthesised into the drafting of this commentary.
Literature surveillance
An exploration of peer-reviewed literature within the Crossref metadatabase was completed. The Crossref metadatabase is an educational databank, which is composed of the PubMed, Science Direct, Ebscohost, CINAHL and Google Scholar search engines (Figure 1). The keywords used in the literature search were Down syndrome, exercise, cardiometabolic, muscle strength, agility, balance, proprioception and obesity. The selection criteria of the literature were accomplished in the subsequent three phases: (1) title review, (2) abstract review and (3) full text review. The records were screened by T.J.E. and Barnard M.B.
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FIGURE 1: Conceptualisation of the review process. |
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Admissibility standards
Participants were records pertaining to PWDS and exercise. The interventions were the recorded results of exercise interventions on the cardiometabolic risk profile, aerobic capacity and muscle strength of PWDS. Applicable findings included (1) the influence of exercise on the cardiometabolic profile of PWDS, (2) the influence of exercise on the muscle strength and endurance of PWDS and (3) aerobic capacity (the effect of exercise on the ease of performing daily activity of PWDS). The elimination benchmarks included (1) the literature preceding 2007, (2) evidence relating to exercise with regard to individuals with other intellectual disabilities, (3) the literature related to the impact of medical, pharmaceutical, nutritional and psychological interventions among PWDS, (4) non-English articles and (5) the literature concerning the impact of exercise on physiological, cognitive and behavioural aspects outside the domain of the prescribed outcome interests of this article.
Evaluation of records
The literature was reviewed according to the suitability of the title and adherence of each article to the inclusion criteria. The merit of each record was evaluated using a modified Downs and Black Appraisal Scale which inspects the value of randomised controlled trials, non-randomised, pseudo-randomised controlled articles, comparative studies with and without concurrent controls, and case series and/or studies with either post-test or pre-test/post-test outcomes (Downs & Black 1998) (Tables 1 and 2). These measures were undertaken to eradicate researcher bias. The modified checklist comprises 16 questions with a maximum score of 16 points. Answers were given a score of either 0 (no) or 1 (yes). The questions adopted from the Downs and Black Appraisal Scale were 1, 3, 4, 5, 6, 10, 11, 12, 13, 14, 18, 20, 21, 22, 23 and 27. These questions were categorised into four subdivisions, which evaluate the whole value of each record (Table 2). The categorising included reporting prowess (n = 6 questions), external validity (n = 3 questions), internal validity (n = 6 questions) and power of significance (n = 1 questions) (Downs & Black 1998). All authors were able to query the scoring of each record and would then discuss the scores adopting the jointly accepted score. The summation of these scores was then transformed to a percentage to rate the overall value of the individual records (Downs & Black 1998). The overall value of the records was categorised using a scale demarcated as follows: < 50% (weak), 50% – 69% (fair), 70% – 79% (good) and ≥ 80% (very good) (Downs & Black 1998). The mean rating of the selected papers was fair.
| TABLE 1: Appraisal of the hierarchy of records. |
Ethical consideration
This article is an overview or clinical commentary; therefore, no subjects were involved.
Results
A total of 1331 participants were enrolled across the 19 studies with a mean age of 18.1 ± 6.8 years, a mean body mass of 61.8 kg ± 13.3 kg, a mean height of 1.53 ± 0.09 m and a mean BMI of 25.2 kg/m2 ± 4.0 kg/m2. The 19 studies comprised 2 systematic reviews, 1 case study, 10 observational cross-sectional and 6 randomised controlled trials (Table 1). Eleven studies reviewed the influence of exercise and physical activity on the health status of PWDS. Regular aerobic exercises reduced lipid peroxidation, oxidative stress, arterial cell wall damage and body fat all while enhancing insulin sensitivity, which was favourably associated with lowering the metabolic risk profile of participants. Regular muscle strengthening improved lower limb strength and improved daily habitual activities (walking upstairs and grocery shelving), motor skills and posture (Table 3).
| TABLE 3: Sequential summary of the characteristics and conclusions of the records (n = 19). |
Discussion
The discussion of findings will follow the interest outcomes of the literature search, namely the impact of exercise on the cardiometabolic profile of PWDS, as well as on their muscle strength, agility and balance. The discussion of the effects of exercise on the cardiometabolic profile of PWDS will detail the role of oxidative stress on the pathogenesis of diabetes mellitus and atherosclerosis and underline the favourable impact of exercise on the improvement of the cardiometabolic profile of PWDS. Finally, the articles synthesised into this commentary will be reviewed according to Mill’s Canons (Dishman et al. 2013) so as to ascertain the strength of the relationship between exercise and the change in health status of PWDS.
Impact of exercise on the cardiometabolic profile of patients with Down syndrome
Patients with Down syndrome have a high incidence of metabolic syndrome, which has been related to heightened cardiometabolic risk profiles (diabetes mellitus, poor insulin sensitivity and high insulin resistance, obesity, atherosclerosis, high low-density lipoprotein cholesterol, hypertension and poor aerobic capacity) (Wallen et al. 2009). Furthermore, high oxidative stress has been related to elevated insulin resistance, poor insulin sensitivity, atherosclerosis and hypertension (Flore et al. 2008). Oxidative stress impairs β-cell function, which reduces the production of insulin by impairing glucose-stimulated insulin secretion, thereby creating a state of hyperglycaemia, which ultimately leads to the development of diabetes mellitus (Tangvarasittichai 2015). Abnormal lipid metabolism has been related to premature risk for the development of atherosclerosis among PWDS (Vis et al. 2009). Aguiar et al. (2008) and Silva et al. (2017) reported that consistent physical activity or exercise lowers body fat, suggesting that regular exercise and physical activity can improve the cardiometabolic risk profile of PWDS. One of the principal benefits of regular aerobic exercises is the use of fats (lipids) for energy, reducing fat content and thereby improving the individual’s cardiometabolic risk profile (Durstine et al. 2011). A further benefit of regular aerobic exercise is the earlier use of lipids, thereby conserving muscle and liver glycogen stores, which has a carbohydrate sparing effect. The use of lipids as an energy fuel yields more ATP than the decomposition of carbohydrates. The catabolism of lipids occurs through the process of lipolysis. The more lipids used, the greater the reduction in fat stores, thereby lowering body fat (McArdle, Katch & Katch 2000). Ulrich et al. (2011) reported that PWDS who exercise regularly reduce body fat, but the authors did not explain the exercise induced physiological mechanism behind the fat loss and how this relates to obesity. Aguiar et al. (2008) reported on the oxidative stress benefits of physical activity, which may positively influence unhealthy cardiometabolic risk profiles, but did specifically explain its use in combating obesity. The study undertaken by Aguiar et al. (2008) was not a randomised control, thereby limiting the significance of the findings and Ulrich et al. (2011) in a single randomised controlled study further showed the paucity of validation in the aforementioned studies. More empirical randomised controlled studies that discuss the biochemical exercise induced mechanism of fat loss relating to reduction in obesity levels among PWDS are therefore required to validate these findings. Such studies would further encourage PWDS and their caregivers to become involved in regular physical activity and exercise.
Impact of aerobic exercise on the pathogenesis of atherosclerosis
Patients with Down syndrome have been identified as having high oxidative stress, which serves as a pathogenic mechanism for the development of atherosclerosis, neurodegeneration, cell aging, cancer and immunological disorders (Ordonez & Rosety-Rodriguez 2007). Oxidative injuries in cardiovascular tissue such as arteries provide opportunities for the development of atheroma (cholesterol plaque), facilitating the pathogenesis of atherosclerosis (the build-up of low density lipoprotein cholesterol, fat, triglycerides and macrophages forming an atheroma/plaque, which reduces blood flow) and arteriosclerosis (the process whereby the arterial walls thicken and harden, losing their elasticity and reducing blood flow) (Tangvarasittichai 2015). Regular endurance exercise and physical activity decrease lipid peroxidation and arterial cell wall damage, which limits the pathogenesis of atheroma (Rosety-Rodriguez et al. 2010). Regular exercise furthermore facilitates the release of nitrate oxide, vasodilating blood vessels and thereby enhancing blood flow (Durstine et al. 2011). These findings demonstrate the benefit of regular aerobic exercise for the reduction of the cardiometabolic risk profile of PWDS. However, more experimental investigations are required to validate the findings of Rodriguez et al. (2010), among PWDS.
Aerobic capacity of patients with Down syndrome
Fernhall et al. (2013) and Wee et al. (2015) indicated that PWDS have low aerobic capacity, characterised by low VO2max and peak heart rates. Fernhall et al. (2013) postulate that autonomic dysfunction is the principal contributor to the poor aerobic capacity and maximal oxygen consumption of PWDS, which may lead to their poor cardiometabolic risk profiles. The poor catecholamine (epinephrine and norepinephrine) response to peak exercise among PWDS suggests that this may be the principal reason for the low peak heart rates and poor aerobic capacity during exercise of PWDS (Fernhall et al. 2009). Shields et al. (2017) reported that PWDS who were aerobically fitter had smaller waist circumferences and a lower BMI. Although the evidence provided by Shields et al. (2017) suggests that body composition is inversely associated with aerobic fitness, the research study design (observational) limits the significance of the findings. Despite this, the findings of Shields et al. (2017) nevertheless motivate exercise interventions for PWDS. Silva et al.’s (2017) study is the only randomised controlled study that was included in this review; the study demonstrates that regular aerobic exercise increased the aerobic capacity of PWDS and thus warrants validation through more randomised controlled trials. Although the physiological mechanism has been identified, more empirical investigations are required to determine the manner in which the aerobic capacity of PWDS can be improved. This data can then, in turn, assist in the improvement of the cardiometabolic risk profile of PWDS.
The effect of exercise on the muscle strength, agility and balance of patients with Down syndrome
Patients with Down syndrome have poor muscle strength, agility and balance as compared to similarly age-matched peers (Izquierdo-Gomez et al. 2015). Shields and Taylor (2010) and Gupta and Singh (2011) reported that regular strengthening exercises improve the muscle strength of PWDS. Shields and Taylor (2010) also demonstrated that the increase in muscle strength served to enhance both daily functional activities (such as walking upstairs with greater ease) and the performance of rudimentary tasks (such as packing shelves). Gupta and Singh (2011) illustrated that regular strength training improves muscle strength and proprioception (balance). However, Gupta and Singh (2011) did not explain how improved muscle strength was associated with improved balance. Empirical investigations explaining the relationship between the improvement in muscle strength and the consequent improvement in balance in PWDS are advised. Silva et al. (2017) also reported that computer games (namely, the Nintendo Wii) assisted in increasing lower limb muscle strength, aerobic capacity and motor coordination. The merit of the above-mentioned studies is their randomised controlled design that validates each other’s findings: regular resistance training- and physical activity-based electronic games do have the potential to improve muscle strength and balance, thereby providing daily functional benefits. The effects of different types of strength training and exercises, such as circuit training, swimming and basic plyometric drills on the health profile of PWDS, should be investigated through randomised controlled trials. The adoption of alternate strengthening activities, such as circuit training, plyometric and swimming, will add variety to the exercise regime of PWDS, thereby helping to maintain adherence to exercise therapy. Furthermore, regular resistance training does have cardiometabolic benefits, which needs to be explored in the context of this particular population, in so far as obesity is associated with the development of diabetes mellitus. Regular strength training has been reported to lower insulin resistance and improve insulin sensitivity, thereby improving the cardiometabolic profile of diabetic patients (Durstine et al. 2011). Although these findings are yet to be validated for PWDS, they show promise in so far as strengthening can also serve to improve the cardiometabolic risk profiles of PWDS. More empirical randomised controlled trails are, however, needed. Over and above this, Gupta and Singh (2011) and Berg et al. (2012) have documented that regular exercise can improve postural stability among PWDS.
Strength of evidence supporting the beneficial effects of regular exercise in improving the cardiometabolic risk profile, muscle strength and proprioception of patients with Down syndrome
The authors adopted Mill’s Canons (Dishman et al. 2013) to determine the strength of evidence supporting the causal inference relating to the impact of exercise interventions on chronic diseases. Mill’s Canons have the following five criteria:
- Temporal sequence refers to the sequence of the exposure of the intervention, which must precede the change of the diseased condition within a sufficient time frame to make a plausible conclusion. Ten of the 11 studies demonstrated that regular exercise improves the health status of PWDS. Six of these 11 studies focused on the effect of exercise on the cardiometabolic risk profile of PWDS. Five studies (83.3%) out of the six indicated that regular exercise improves the cardiometabolic risk profile of PWDS (Aguiar et al. 2008; Ordonez & Rosety-Rodriguez 2007; Ordonez et al. 2012; Rosety-Rodriguez et al. 2010; Silva et al. 2017). Of the five studies, two were randomised control studies (Ordonez et al. 2012; Silva et al. 2017) and three were observational cross-sectional studies (Aguiar et al. 2008; Ordonez & Rosety-Rodriguez 2007; Rosety-Rodriguez et al. 2010). Four randomised control trials indicated that regular exercise improves the strength and proprioception of PWDS, thereby addressing the patients’ hypotonic muscle deficits (Gupta & Singh 2011; Lin & Wuang 2010; Shields & Taylor 2010; Silva et al. 2017). Shields and Taylor (2010) also associated increased muscle strength with improved daily functional activities such walking and packing shelves among PWDS. Two randomised controlled trials and one case study demonstrated that regular physical activity improves the postural stability of PWDS (Berg et al. 2012; Gupta & Singh 2011; Ulrich et al. 2011).
- Strength of association refers to the clinical meaningful difference between the disease and the intervention. Ten of the 11 studies indicated a strong association between the exercise and physical activity interventions and improved cardiometabolic risk profile, strength, proprioception and postural balance (Table 3).
- Consistency of results refers to the consistent observation of the association between the outcome of the intervention and the disease. Of the 11 studies reviewing the effect of regular exercise and physical activity on the health status of PWDS, 10 indicated positive outcomes (90.9%) (Table 3).
- Biological plausibility refers to the clinical explanation of the observed outcome of the intervention in regard to disease. The 10 studies that showed positive outcomes described plausible explanations for these improvements (Table 3).
- Dose–response refers to the volume of intervention required to produce a specific outcome on the disease. There is, however, no consensus pertaining to the amount or volume of exercise and physical activity needed to produce beneficial outcomes. It is advised that further research investigating the dose–response concerning intensity, duration and frequency of exercise interventions and physical activity on PWDS. This new research will help medical practitioners and exercise therapists determine the adequate dose response to exercise.
Conclusion
Clinical evidence has indicated that regular exercise benefits the health status of PWDS with regard to improving their body composition, aerobic capacity, muscle strength, proprioception and postural stability. The benefits of augmented aerobic work capacity and body composition help to lower the cardiometabolic risk profile of PWDS. However, more randomised controlled trials are needed to both determine the dose–response to exercise and validate these preliminary empirical findings. Additional empirical randomised controlled studies, which discuss the biochemical exercise induced mechanism of fat loss relating to a reduction in obesity levels among PWDS, are required to validate these findings. The effects of different types of exercises, such as circuit training, swimming and basic plyometric drills on the health profile of PWDS, should be investigated through randomised controlled trials. This review showed that aerobic exercises were primarily selected to alter the cardiometabolic profile of PWDS. Resistance training has also improved the diabetic profile of patients, and this should be explored among PWDS as well.
Acknowledgements
The authors wish to acknowledge the study of Ellapen et al. (2017) that reviewed the common upper limb injuries to wheelchair users and Ellapen et al. (2018) that described the benefits of hydrotherapy to spinal cord injured patients. These studies serve as a catalyst for this article.
Competing interests
The authors declare that no competing interests exist.
Authors’ contributions
Y.P., T.J.E., M.B., H.V.H. and M.S. were responsible for conceptualisation, data gathering and drafting of the article. Y.P. was responsible for editing and payment of page fees.
Funding
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Data availability statement
Data sharing is not applicable to this article as no new data were created or analysed in this study.
Disclaimer
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of any affiliated agency of the authors.
References
Aguiar, A.S., Tuon, T., Albuquerque, M.M., Rocha, G.S., Speck, A.E., Dafre-Rui, A.L. et al., 2008, ‘The exercise redox paradigm in the Down’s syndrome: Improvements in motor function and increases in blood oxidative status in young adults’, Journal of Neurological Transmedicine 115(12), 1643–1650. https://doi.org/10.1007/s00702-008-0120-x
Barnhart, R.C. & Connolly, B., 2007, ‘Aging and Down syndrome: Implications for physical therapy’, Physical Therapy 87(10), 1399–1406. https://doi.org/10.2522/ptj.20060334
Berg, P., Becker, T., Martian, A., Primrose, K.D. & Wingen, J., 2012, ‘Motor control outcomes following Nintendo Wii use by a child with Down syndrome’, Paediatric Physical Therapy 24(1), 78–84. https://doi.org/10.1097/PEP.0b013e31823e05e6
Bertapelli, F., Pitetti, K., Agiovlasitis, S. & Guerra-Junior, G., 2016, ‘Overweight and obesity in children and adolescents with Down syndrome – Prevalence, determinants, consequences and interventions: A literature review’, Research in Developmental Disabilities 57, 181–192. https://doi.org/10.1016/j.ridd.2016.06.018
Dishman, R.K., Heath, G.W. & Lee, I.M., 2013, Physical activity epidemiology, 2nd edn., Human Kinetics, Champaign, IL.
Downs, S.H. & Black, N., 1998, ‘The feasibility of creating a checklist for the assessment of the methodological quality both of randomized and non-randomized studies of health care interventions’, Journal of Epidemiology in Community Health 52(6), 377–384. https://doi.org/10.1136/jech.52.6.377
Duffels, G.J., Vis, J.C., Van Loon, R.L.E., Nieukerk, P.T., Van Dijk, A.P.J., Hoendermis, E.S. et al., 2009, ‘Effect of Bosentan on exercise capacity and quality of life in adults with pulmonary arterial hypertension associated with congenital heart disease with and without Down’s syndrome’, American Journal of Cardiology 103(9), 1309–1315. https://doi.org/10.1016/j.amjcard.2009.01.021
Durstine, L.J., Moore, G.E., Painter, P.L. & Roberts, S.O., 2011, ACSM’s exercise management for persons with chronic diseases and disabilities, 3rd edn., Human Kinetics, Champaign, IL.
Ellapen, T.J., Swanepoel, M., Hammill, H.V. & Strydom, G.L., 2017, ‘The health benefits and constraints of exercise therapy for wheelchair users: A clinical commentary’, African Journal of Disability 6(0), a337. https://doi.org/10.4102/ajod.v6i0.337
Ellapen, T.J., Hammill, H.V., Swanepoel, M. & Strydom, G.L., 2018, ‘The benefits of hydrotherapy to patients with spinal cord injuries’, African Journal of Disability 7(0), a450. https://doi.org/10.4102/ajod.v7i0.450
Fernhall, B., Baynard, T., Collier, S.R, Figueroa, A., Goulopoulou, S., Kamimori, G.H. et al., 2009, ‘Catecholamine response to maximal exercise in persons with Down syndrome’, American Journal of Cardiology 103(5), 724–726. https://doi.org/10.1016/j.amjcard.2008.10.036
Fernhall, B., Mendonca, G.V. & Bynard, T., 2013, ‘Reduced work capacity in individuals with Down syndrome: A consequence of autonomic dysfunction?’, American College of Sports Medicine 41(3), 138–147. https://doi.org/10.1097/JES.0b013e318292f408
Flore, P., Bricout, V., Van Biesen, D., Guinot, M., Laporte, F., Pepin, J.L. et al., 2008, ‘Oxidative stress and metabolism at rest and during exercise in persons with Down syndrome’, European Society of Cardiology 15(1), 35–42. https://doi.org/10.1097/HJR.0b013e3282f2bff3
Gupta, S. & Singh, S.B., 2011, ‘Effect of strength and balance training in children with Down’s syndrome: A randomized controlled trial’, Clinical Rehabilitation 25(5), 425–432. https://doi.org/10.1177/0269215510382929
Heller, T., Hsieh, K. & Rimmer, J., 2003, ‘Barriers and support for exercise participation among adults with Down syndrome’, Journal of Gerontological Social Works 38(1–2), 161–178. https://doi.org/10.1300/J083v38n01_03
Izquierdo-Gomez, R., Martinez-Gomez, D., Estenban-Cornejo, I., Hallal, P.C., Garcia-Cervantes, L., Villagro, A. et al., 2017, ‘Changes in objectively measured physical activity in adolescents with Down Syndrome: The Up & Down longitudinal study’, Journal of Intellectual Disability Research 61(4), 363–372.
Izquierdo-Gomez, R., Martinez-Gomez, D., Villagra, A., Fernhall, B. & Veiga, O.L., 2015, ‘Associations of physical activity with fatness and fitness in adolescents with Down syndrome: The UP & DOWN study’, Research in Developmental Disabilities 36, 428–436. https://doi.org/10.1016/j.ridd.2014.10.022
Krause, S., Ware, R., McPherson, L., Lennox, N. & O’Callaghan, M., 2016, ‘Obesity in adolescents with intellectual disability: Prevalence and associated characteristics’, Obesity Research and Clinical Practice 10(5), 520–530. https://doi.org/10.1016/j.orcp.2015.10.006
Lin, H.C. & Wuang, Y.P., 2012, ‘Strength and agility training in adolescents with Down syndrome: A randomized controlled trial’, Research in Development Disabilities 33(6), 2236–2244. https://doi.org/10.1016/j.ridd.2012.06.017
McArdle, W.D., Katch, F.I. & Katch, V.L., 2000, Essentials of exercise physiology, Lippincott Williams & Wilikns, Philadelphia, PA.
Ordonez, F.J. & Rosety-Rodriguez, M., 2007, ‘Regular exercise attenuated lipid peroxidation in adolescents with Down syndrome’, Clinical Biochemistry 40(1–2), 141–142. https://doi.org/10.1016/j.clinbiochem.2006.09.013
Ordonez, F.J., Rosety, M.A., Camacho-Molina, A., Fornieles, G., Rosety, M. & Rosety-Rodrigues, M., 2012, ‘Aerobic training at moderate intensity reduces protein oxidation in adolescents with Down syndrome’, Scandinavian Journal of Medicine and Science in Sports 22(1), 91–94. https://doi.org/10.1111/j.1600-0838.2010.01153.x
Rimmer, J.H., Braddock, D. & Fujiura, G., 1995, ‘Health characteristics and behaviour of adults with mental retardation residing in three living arrangements’, Research in Developmental Disabilities 16(6), 489–499. https://doi.org/10.1016/0891-4222(95)00033-X
Rosety-Rodriguez, M., Rosety, I., Fornieles-Gonzalez, G., Diaz, A., Rosety, M. & Ordonez, F.J., 2010, ‘A 12 week aerobic training programme reduced plasmatic allantoin in adolescents with Down syndrome’, British Journal of Sports Medicine 44(9), 685–687. https://doi.org/10.1136/bjsm.2008.052530
Shields, N. & Taylor, N.F., 2010, ‘A student-led progressive resistance training program increases lower limb muscle strength in adolescents with Down syndrome: A randomised controlled trial’, Journal of Physiotherapy 56(3), 187–193. https://doi.org/10.1016/S1836-9553(10)70024-2
Shields, N., Downs, J., De Haan, J.B., Taylor, N.F., Torr, J., Fernhall, B. et al., 2018, ‘What effect does regular exercise have on oxidative stress in people with Dow syndrome? A systematic review with meta-analyses’, Journal of Science and Medicine in Sport 21(6), 596–603. https://doi.org/10.1016/j.jsams.2017.10.015
Shields, N., Hussey, J., Murphy, J., Gormley, J. & Hoey, H., 2017, ‘An exploratory study of the association between physical activity, cardiovascular fitness and body size in children with Down syndrome’, Developmental Neurorehabilitation 20(2), 92–98. https://doi.org/10.3109/17518423.2015.1077901
Silva, V., Campos, C., Cavadas, M., Pinto, J., Simoes, P., Machado, S., et al., 2017, ‘Wii-based exercise program to improve physical fitness, motor proficiency and functional mobility in adults with Down syndrome’, Journal of Intellectual Disability Research 61(8), 755–765.
Tangvarasittichai, S., 2015, ‘Oxidative stress, insulin resistance, dyslipidaemia and type 2 diabetes mellitus’, World Journal of Diabetes 6(3), 456–480. http://www.doi.10.4239/wjd.v6i3.456
Ulrich, D.A., Burghardt, A.R., Lloyd, M., Tiernan, C. & Hornyak, J.E., 2011, ‘Physical activity benefits of learning to ride a two-wheel bicycle for children with Down syndrome: A randomized trial’, Physical Therapy 91(10), 1463–1477. https://doi.org/10.1111/jir.12384
Vis, J.C., Duffels, M.G.J., Winter, M.M., Weijerman, M.E., Cobben, J.M., Huisman, S.A. et al., 2009, ‘Down syndrome: A cardiovascular perspective’, Journal of Intellectual Disability Research 53(5), 419–425. https://doi.org/10.1111/j.1365-2788.2009.01158.x
Wallen, E.F., Mullersdorf, M., Christensson, K., Malm, G., Ekbolm, O. & Marcus, C., 2009, ‘High prevalence of cardio-metabolic risk factors among adolescents with intellectual disability’, Acta Pediatrica 98(5), 853–859. https://doi:10.1111/j.2227.2008.01197.x
Wee, S.O., Pitetti, K.H., Goulopoulou, S., Collier, S.R., Guerra, M. & Baynard, T., 2015, ‘Impact of obesity and Down syndrome on peak heart rate and aerobic capacity in youths and adults’, Research in Developmental Disabilities 36, 198–206. https://doi.org/10.1016/j.ridd.2014.10.002
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