Children and adolescents with Down syndrome, physical fitness and physical activity

Available online at www.sciencedirect.com

Journal of Sport and Health Science 2 (2013) 47e57 www.jshs.org.cn

Review

Children and adolescents with Down syndrome, physical fitness and physical activity Ken Pitetti a,*, Tracy Baynard b, Stamatis Agiovlasitis c a

Department of Physical Therapy, College of Health Professions, Wichita State University, Wichita, KS 67260-0043, USA b Department of Kinesiology & Nutrition, University of Illinois at Chicago, Chicago, IL 60612, USA c Department of Kinesiology, Mississippi State University, Mississippi State, MS 39762, USA Received 8 July 2012; revised 7 September 2012; accepted 26 September 2012

Abstract Children (5e12 years) and adolescents (13e19 years) with Down syndrome (DS) possess a set of health, anatomical, physiological, cognitive, and psycho-social attributes predisposing them to limitations on their physical fitness and physical activity (PA) capacities. The paucity of studies and their conflicting findings prevent a clear understanding and/or substantiation of these limitations. The purpose of this article was to review the measurement, determinants and promotion of physical fitness and PA for youth (i.e., children and adolescents) with DS. The existing body of research indicates that youth with DS: 1) have low cardiovascular and muscular fitness/exercise capacity; 2) demonstrate a greater prevalence of overweight and obesity; 3) a large proportion do not meet the recommended amount of daily aerobic activity; and 4) their PA likely declines through childhood and into adolescence. Future research should focus on: 1) strength testing and training protocols; 2) methodologies to determine PA levels; and 3) practical interventions to increase PA. Copyright Ó 2012, Shanghai University of Sport. Production and hosting by Elsevier B.V. All rights reserved. Keywords: Activity; Adolescents; Children; Down syndrome; Fitness

1. Introduction 1.1. Background and genetics The condition of Down syndrome (DS) was first described in a clinical lecture report delivered in 1866 by the British physician, John Langdon Down, entitled “Observation on the ethnic classification of Mongoloid idiots”.1 Dr. Down used the derogatory term “Mongoloid” because children with DS

* Corresponding author. E-mail address: [email protected] (K. Pitetti) Peer review under responsibility of Shanghai University of Sport

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displayed facial features (e.g., epicanthal fold) that shared similarities with the prevailing erroneous ethnic theory established by the German anatomist, Johann Friedrich Blumenbach.2 Catalyzed by editorials in The Lancet, together with political pressure by advocacy groups and parental organizations in the 1960s, the term “mongolism” was dropped from medical references by the World Health Organization and replaced by “Down syndrome” during the 1970s.3 The cause of DS remained unknown until the 1950s when it became possible to identify chromosomal abnormalities with the discovery of karyotype techniques. In 1959 the French geneticist, Dr. Jerome Lejeune, reported that DS was caused by an extra 21st chromosome, an aneuploidy condition known as trisomy 21.4 The vast majority of cases of DS are due to full trisomy 21, with every somatic cell in the body having an extra 21st chromosome (Table 1). A smaller percentage of persons with DS are due to mosaic trisomy (2%e4%) and Robertsonian translocation (3%e4%).5 Reports have suggested that children with mosaic

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DS have similar health and developmental difficulties as children with full trisomy 21, but to a lesser degree6 and those with DS caused by Robertsonian translocation have increased frequency of psychiatric disorders.7 1.2. Demographics In the United States the incidence of DS at birth from 1979 to 2003 increased from 9.0 to 11.8 per 10,000 births (Table 1).8 It is suggested that the probable cause for the increase in DS is related to the trend toward later child bearing, with women over 35 being five times more likely than younger women to have children with DS.5 1.3. The intellectual and health profiles of persons with Down syndrome Although about one-third of the causes of intellectual disabilities (ID) remain unknown, the three major known causes of ID are DS, Fetal Alcohol Spectrum Disorder, and Fragile X syndrome.6 As is the case for all persons with ID, the degree of ID in persons with DS is determined by limitations in both cognitive function and in adaptive behavior (e.g., conceptual, social, and practical adaptive skills).7-9 The degree of cognitive impairment is variable, with the majority classified as mild (IQ: 50e55e69) or moderate (30e35 to 50e55) while a smaller percentage (<10%) are severe (IQ < 20e25 to 30e35).10,11 Adaptive behavior encompasses conceptual skills (language, reading and writing, self directions), social skills (self esteem, gullibility, naivete´, avoids victimization) and practical adaptive skills (dressing, toileting, preparing meals, using transportation, occupational skills) that allow individuals to be functional in their everyday life.10,11 Adaptive behavior may improve with early intervention but the level of function varies according to innate capacities and social support systems (Table 1).10,11 Table 1 Description, demographics, and health profiles of persons with Down syndrome. Characteristic

Description

Description and demographics

1. 2. 3. 4. 5.

Health profiles Childhood

Adulthood

Caused by trisomy 21 11.8 per 10,000 births (USA) Mild/moderate intellectual disability Limited adaptive skills Life span near 60 years

1. Congenital heart disease (septal and valvular defects) 2. Respiratory illnesses (pneumonia and chronic bronchitis) 1. Deterioration of functional capacities due to dementia of Alzheimer’s type 2. Recurrent pneumonia 3. Sensory impairments (hearing and vision) 4. Musculoskeletal disorders (joint instability and osteoporosis)

Although ID affects every day functioning, the health profiles of children and adolescents with ID without DS are unremarkable. In contrast, the effects of DS involve a range of medical conditions in addition to ID that may be identified at birth or develop during the life span (Table 1). These conditions include increased risk of congenital heart disease (50%), hearing loss (75%), eye disease (60%), obstructive sleep apnea (75%), gastrointestinal conditions (10%), thyroid (hypothyroidism) disease (15%), and atlanto-axial/atlanto-occipital instability (10%e30%).8,9 Excluding birth, nearly half of children with DS are hospitalized before age 3, with the principle causes for hospitalization being congenital heart disease (e.g., septal and valvular anomalies) and respiratory illnesses (pneumonia, acute, and chronic bronchitis).10 These medical conditions increase demands on the health care system that can be as much as 13 times higher than for children (0e4 years) without DS.11 Health care costs have been reported to decline with age, and by adolescence the cost of health care services have been reported to decrease to 1.1e1.7 times of those without disabilities.12,13 However, diagnosis of congenital heart disease and level of independence influence total health care cost, independent of age.12 These health care estimates do not address overall cost to families affected by DS, such as special education, individual transport needs, housing modifications, and related cost to family members (e.g., employment opportunities). Survival for persons with DS has improved over the past few decades with life expectancy nearing 60 years paralleling the improvement in social and medical support systems.14e16 However, mortality rates of persons with DS remain higher overall than those of the general population with the leading causes of death being congenital anomalies (e.g., heart defects), Alzheimer’s disease, pneumonia, leukemia, and all circulatory diseases (e.g., ischemic heart disease, cerebrovascular disease).14,17,18 Death rates for persons with DS increase significantly after age 40.19 The main cause for the upsurge in mortality in middle-aged adults with DS is the deterioration in functional abilities and rise in behavioral problems due to Alzheimer’s disease.20e23 Because of early onset of menopause, women with DS are four times more likely to develop Alzheimer’s disease than their male counterparts.24 Other disorders of aging in DS are pulmonary disorders (recurrent pneumonia caused by recurrent aspiration), sensory impairments (hearing and vision), and musculoskeletal disorders (e.g., osteoporosis and orthopedic complications caused by joint instability).23 2. Physical fitness: cardiovascular, muscle, and body composition 2.1. Cardiovascular fitness 2.1.1. Cross-sectional studies Uniformly, peak aerobic capacity (VO2peak) in both youth and adults with DS is reduced in comparison to their peers without disabilities (WOD) and with ID but without DS.25e27 This is accompanied by lower peak work rates as well as

Youth with DS: Fitness and activity

a faster time to exhaustion (Table 2).27 Such findings were first reported by Eberhard et al.28 in 1989, whereby they demonstrated a 15% lower VO2peak using bicycle ergometry compared to age-matched children WOD. In 1990, Fernhall et al.,26 using a validated treadmill protocol, reported lower VO2peak in adolescents with DS when compared to adolescents WOD and that lack of motivation or understanding protocol instructions in participants with DS did not contribute to their findings. Following these initial contributions, the literature has consistently demonstrated lower VO2peak values when individuals with DS are compared to individuals WOD and with ID but without DS. In the largest sample to date (total n ¼ 635; n ¼ 133 with DS, n ¼ 180 with ID, n ¼ 322 WOD), Baynard et al.25 reported that VO2peak (absolute and relative values) is lower in children and adolescents with DS through young adulthood and into middle age, regardless of the comparison group. Furthermore, the authors also demonstrated VO2peak does not significantly change after the age of w16 years.25 Interestingly, the average VO2peak at this age in individuals with DS is similar to normative values found in middle-aged to older persons WOD, yet individuals with DS do not appear to experience the age-related decline in VO2peak as is expected in those WOD (Table 2).25 Three physiologic factors that potentially contribute to low VO2peak values in persons with DS are autonomic dysfunction, reduced ventilatory capacity, and metabolic dysfunction. When considering autonomic dysfunction, lower peak heart rate (HR) responses have been consistently reported across all age groups for persons with DS.25 The cause of lower peak HR in persons with DS is still not completely understood at this time, but Fernhall et al.29 demonstrated in a group of young Table 2 Physical fitness in youth with Down syndrome (DS). Characteristic

Description

Cardiovascular fitness

1. Low peak aerobic capacity/time to exhaustion 2. Low peak heart rate 3. Peak aerobic capacity does not change significantly with age after w16 years 4. Autonomic dysfunction a primary factor related to low fitness 5. Field tests largely support laboratory findings 6. Responsive to aerobic endurance training, particularly with improvements in work capacity

Muscular strength

1. Lower strength compared to individuals without disabilities 2. Resistance training appears safe and beneficial for improving strength 3. Improved leg strength does not appear improve aerobic capacity

Body composition

1. Youth with DS in North America and Europe are more obese/overweight vs. counterparts without disabilities 2. Cause of high rate of overweight/obesity is multifactorial (physiological, societal, environmental, psychological, etc.) 3. Studies show no improvement in body composition from exercise training alone, likely due to lack of dietary control

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adults with DS (mean age 24 years) a blunted to non-existent catecholamine response to peak exercise. This suggests that some portion of the autonomic pathway is dysfunctional and contributes to the lower HR response. Although diminished sympathoexcitation in adults with DS has been reported,30,31 to date no studies have included youth with DS (Table 2). Further, with higher obesity levels generally observed in persons with DS, the interaction between autonomic control and obesity may be an important avenue to investigate in this population. It was also postulated that due to the relatively large tongues (macroglossia) compared to the bony confines of the oral cavity in persons with DS, ventilation would be restricted at high work levels and thus limit peak performance. Indeed, adolescents and young adults with DS have been reported to have low peak ventilation.26 However, Fernhall and Pitetti27 concluded that peak ventilatory parameters (e.g., ventilatory equivalents, and peak minute ventialation) were appropriate for a given VO2peak. In addition, imaging work has established that children with DS do not have true macroglossia, although they have relatively large tongues compared to their oral cavity volume.32 Therefore, ventilation capacity does not appear to restrict the peak performance of youth with DS. However, gaps do exist in the literature with little to no data available for additional ventilatory parameters, such as peak minute ventilation/maximal ventilatory volume or peak tidal volume/ventilatory capacity. This type of data would broaden our understanding of potential limitations to exercise in persons with DS. Metabolic limitations have also been suggested to constrain the physical capacity of youth and young adults with DS. However, only two studies actually measured ventilatory threshold in adolescents and young adults with DS.33,34 Collectively, these two studies reported that ventilatory threshold was difficult to detect (e.g., V-slope method); however, in those participants where it was detectable, normal ventilatory thresholds were observed when expressed as a percentage of VO2peak. Given that the respiratory exchange ratio is related to substrate utilization and exercise intensity, collection of blood lactate would assist in determining the role that metabolic function may have in limiting exercise performance in youth with DS. However, submaximal and maximal exercise blood lactate levels have not been reported in the literature for youth with DS. In line with this, supramaximal testing (e.g., Wingate testing) is not reliable enough to date to help complete a metabolic profile in youth with DS.35 It is important to note that several studies using field tests also report lower predicted VO2peak and/or exercise performance in youth and young adults with DS compared to peers WOD (Table 2).36,37 The largest field study to date to measure run performance (20-m shuttle run) had 119 youth (11e18 years) with DS, 394 youth with ID but without DS, and 80 youth WOD.38 Children and adolescents with ID but without DS had better run performance than their peers with DS independent of age, sex, and body mass index (BMI).38 Furthermore, those WOD had better run performance than their peers with ID, again independent of age, sex, and BMI.38

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Thus, poor running performance of children and adolescents with ID, with and without DS, is not a consequence of age, sex, or BMI. Furthermore, Fernhall et al.39,40 produced a regression equation from the results of the 20-m shuttle run to predict VO2peak in children and adolescents with ID, with and without DS. This equation was cross-validated in 2003 by Guerra et al.,41 however, this study consisted of a greater percentage of children and adolescents with DS and they were not able to validate Fernhall’s39,40 original equation designed for persons with ID to a sample with DS alone. The prediction of VO2peak, from a 20-m shuttle run test, was further examined by Agiovlasitis et al.,42 whereby they reported that while shuttle performance was a predictor of VO2peak in youth with DS, the equation had low predictability at the individual level. Therefore, the use of the regression equation developed by Fernhall et al.39,40 to predict VO2peak in persons with ID does not appear to be specific for youth with DS. 2.1.2. Training studies There are relatively very few longitudinal training studies in persons with DS, particularly in youth. For this reason, training studies in young adults with DS will be utilized here with the understanding that it would be likely that youth with DS would experience similar findings. A meta-analysis was conducted by Dodd and Shields43 that included four papers, which met their inclusion criteria.44e47 They reported that aerobic training programs, which conformed to the American College of Sports Medicine guidelines, were effective for improving VO2peak, peak ventilation, time to exhaustion, and/ or maximum workrate.43 One of the first training studies in adolescents with DS was conducted by Millar et al.,45 with 14 individuals participating in a 10-week walking/jogging program, 3 days/week at 65%e 75% peak HR, which resulted in no change in VO2peak, but did improve treadmill test time by 9%.45 Training studies that have measured VO2peak since the report by Millar et al.45 have supported those initial findings, in that improvements have been seen in exercise/work capacity without significant improvements in VO2peak with training interventions lasting 12e16 weeks (Table 2).9,48 Further evidence of positive training effects stems from an often overlooked study, whereby HR recovery following a 3-min step test and resting HR were decreased in a group of 10 individuals with DS (8e18 years) after a 13-week training program.49 Lastly, an interesting case study reported that a young 10.5-year-old female with DS following 6 weeks of training did not alter her estimated VO2peak, but her submaximal HR was lower during the treadmill test, as was her respiratory rate, indicating improved work capacity and capacity for change.50 While aerobic training studies are limited in persons with DS, let alone youth, previous work suggests exercise training is beneficial in youth with DS even if VO2peak itself is not necessarily an expected outcome. It is especially important to consider training studies in youth with DS in that early intervention to improve their work/exercise capacity could impact the health anomalies specific to the condition of DS.

K. Pitetti et al.

2.2. Muscular strength Few studies exist that have employed strength testing and/ or training in youth with DS. Strength decrements were first characterized in youth with DS in 1994 by Cioni et al.,51 in which children and adolescents with DS (n ¼ 25) exhibited weak knee extensor strength compared to a WOD control group. Furthermore, these authors concluded that adolescents with DS generally do not show improvements in strength beyond the age of 14 years.51 These findings can be extended to the hip abductors as well.52 Interestingly, Pitetti and Fernhall53 explored the relationship between VO2peak and strength in youths aged 10e17 years with ID (n ¼ 29), including eight children with DS, and found a significant relationship between knee flexion/extension strength and aerobic capacity (r ¼ 0.56e0.62). Their data suggest that leg strength may be a limiting factor in both work and aerobic capacity in persons with DS, which is also supported by similar work in adults (Table 2).54 There is a small body of literature in young adults with DS (mean age w24e25 years) that further extends the limited findings in youth. Several studies have demonstrated lower muscle strength in young adults with DS for both knee, and/or elbow extensors/flexors compared to participants WOD.55e58 In those studies that distinguished between individuals with ID with or without DS, no general differences in strength were observed between these two groups, whereas the control group WOD was always stronger (65%e225% stronger). However, it should be noted that while not different, Croce et al.57 have reported lower hamstring to quadriceps ratios in adults with DS (20%) vs. those WOD and 10% lower compared to adults with ID without DS. This may suggest reduced muscular performance and knee joint stability. The number of strength training intervention studies that included individuals with DS is even smaller, with two studies known to have specifically trained youth with DS.59,60 Weber and French59 found that resistance training improved overall muscular strength in adolescents with DS (e.g., 10 muscular tests performed), yet this study lacked a control group. Recently, Shields and Taylor60 demonstrated that a 10-week community-based progressive resistance training intervention was successful in increasing lower limb strength (as well as muscle endurance) in 23 adolescents with DS, with no changes in upper limb strength. Unfortunately, no measure of work and/or aerobic capacity was performed in these studies.59,60 Lastly, a case study demonstrated that a young girl with DS improved general muscle strength (e.g., trunk, hip, knee, and shoulder) following a 10-week combined aerobic and resistance program.50 These data collectively suggest that strength training in youth is beneficial. Little to no data exist on the relationship between strength training and improving work capacity in youth with DS (Table 2). A recent study by Cowley et al.61 reported a small, but significant increase in relative VO2peak following a 10-week strength training program in young adults with DS, yet no difference in absolute VO2 was observed, suggesting this improvement was mediated by weight loss (w5 kg).

Youth with DS: Fitness and activity

A group of progressive resistance exercise training studies clearly demonstrate that strength training is a safe and important component of exercise prescription in young adults with DS (24e29 years).61e64 These studies lasted 10e12 weeks and all employed a 2e3 days/week training of large muscle groups, with improvements found in both upper- and/ or lower-body strength. Interestingly, Cowley et al.61 concomitantly measured aerobic capacity and reported no change in absolute VO2peak and a small but significant decrease in relative VO2peak (Table 2). 2.3. Body composition Equivocal evidence exists regarding body composition in persons with DS. The lack of consistency may involve methodological issues for measuring body composition (e.g., skinfolds vs. dual energy X-ray absorptiometry) or perhaps comparing weight status using different vehicles, such as a laboratory measures versus BMI. Another possible contributor may be ethnic and/or environmental issues as well. Caution is urged when interpreting global statements on body composition in DS for these reasons. Numerous investigations have reported that the prevalence of overweight and obesity are substantially higher in individuals with DS compared to their age-matched peers WOD and with ID but without DS.65,66 Prasher67 reported that w48% of adults with DS were obese, with w27% being overweight (both sexes averaged) and that being overweight and/or obese was associated with living at home compared to group-home situations. This is consistent with Rubin et al’s65 report of w48% for men and w56% of women being overweight/ obese. Interestingly, BMI was found to decrease throughout the lifespan in males and females with DS, whereas BMI increases through the lifespan in the general population.67 This is in contrast to Baynard et al.,25 whereby they reported BMI increases not only in the control group, but also in groups of ID, with and without DS, up through middle-age. Prasher67 was unable to adequately explain why BMI would decrease from young adulthood (16e19 years) through the 20 s into the 60 s. Perhaps the Alzheimer’s issues that individuals with DS often experience could provide a possible explanation. Early work by Sharav and Bowman68 demonstrated that young children with DS (w4e5 years) were not different from their siblings WOD in BMI. Additionally, Luke et al.69 reported non-significant but higher BMI and lower fat-free mass in children with DS (9 years old) versus a control group WOD, whereas other investigators have observed higher BMIs and/or percentage of body fat in youth with DS compared to peers WOD.52,70 However, these studies also included adults in their samples.52,70 In contrast to Luke et al.,69 others have observed lower total muscle mass in persons with DS versus individuals WOD.70 This has been further substantiated recently in Spanish youth with DS that did exhibit higher body fat content and lower lean mass than peers WOD.71 In Greece, researchers observed that 22% of adolescents in their sample were obese and that percent body fat, BMI, fat mass and fat-free mass were also greater in

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adolescents with DS (10e18 years) than in children with DS (2e9 years).72 It is important to note that several studies do suggest that children and adults with developmental disabilities in the United States and Australia have greater prevalence rates of overweight and obesity compared to non-disabled agematched controls. Yet these studies only have a small portion of individuals with DS included.65,66 However, the prevalence of overweight/obesity has recently been questioned and it may not be as high as previously thought.73 It is also possible international differences exist that need further examination. More work will need to be conducted not only at the physiological level, but work at the environmental, community, societal and psychological levels to fully delineate the numerous factors involved in obesity (Table 2). 3. Physical activity (PA) in youth with DS Apart from physical fitness, PA has the potential to improve health in youth with DS. Although the relationship of PA and health outcomes has not been directly examined in youth with DS, it is reasonable to assume that the findings in the general population of youth also apply to those with DS. PA may improve the cardiovascular, metabolic, musculo-skeletal, and psychosocial health profiles of all youth.74e76 For this reason, the 2008 Physical Activity Guidelines for Americans devoted a section to children and adolescents.76 Specifically, it is recommended that youth older than 6 years perform 60 min of PA daily. Most of aerobic activity should be of either moderate or vigorous intensity, defined as 3.0e5.9 and >5.9 metabolic equivalent units (METs), respectively; however, vigorous-intensity activity should be performed at least 3 days/week. Muscle- and bone-strengthening activities are important components of the recommended 60 min of daily activity and each should be performed at least 3 days/ week. Importantly, the Guidelines call for the promotion of physical activities that are age-appropriate, enjoyable, and offer variety. Recent evidence, however, suggests that most American youthdespecially adolescentsddo not meet the required amount of daily PA and that their activity levels decline as they grow.77 The issues of interest therefore are: (a) whether the PA levels of youth with DS differ from those of youth WOD, and (b) whether youth with DS meet the current recommendations for PA. Answering these questions is difficult because research on PA in youth with DS is limited. In a review of research published prior to 2008,78 the authors could not conclude whether the PA levels of youth with ID, including those of youth with DS, are different from those of children WOD. As the authors explained, this was due to methodological problems of previous research such as insufficient description of samples and questionable applicability of objective or subjective measurements of PA to youth with ID. 3.1. Measurement of PA in youth with DS Subjective PA assessments using questionnaires are not as accurate as objective ones.77 This difficulty is magnified in

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youth with DS by the need to use parental or caregiver/teacher proxy reports.78 One study demonstrated questionable accuracy of PA measurement by proxy reports for adults with ID.79 It is possible that subjective assessment of PA in youth with DS may benefit if questionnaires are obtained from both parents and teachers or caregivers; such practice may offer a more accurate representation of the activities youths with DS engage in throughout the day. Nevertheless, to our knowledge, the psychometric properties of subjective measures have not been examined in youth with DS. Finally, in-depth interviewsdtypically with parentsddo not allow for a quantification of the amount of PA performed by youth with DS. Objective PA measurements with accelerometers or pedometers are preferable, but they should be used carefully in youth with DS. Pedometers appear valid and reliable during locomotion in youth with intellectual or developmental disabilities,80,81 but their accuracy may be compromised during games and sport activities conducted in physical education.82 Additionally, spring-levered pedometers are less accurate than piezoelectric in people with DS.83 Furthermore, using step-rate cut-points to estimate moderate- and vigorousintensity activity in youth with DS may be problematic. Adults with DS have lower step-rate cut-points for activity intensity even when accounting for their shorter height compared to adults without DS84dthis may potentially apply to youth with DS. Similarly, accelerometry-determined cut-points for moderate- and vigorous-intensity activity developed for youth WOD may not be applicable to youth with DS. This has been demonstrated for adults with DS85 and it has been suggested to be partially due to an altered gait pattern that increases the energy expenditure.86 It is possible that this also applies to youth with DS who also exhibit altered gait patterns,87,88 potentially duedat least in partdto deficits of the cerebellum.89 Additionally, cut-offs developed in youth WOD may be inappropriate for those with DS because the latter have very low cardiovascular fitness. Finally, there have been some reports of compliance issues with accelerometers secured at the hip in youth with DS.90,91 Although these difficulties are not extensive, they highlight the need for adequate familiarization and parental supervision. Alternately, researchers could consider other placement sites, such as the wrist, where the accelerometer could be secured with an irremovable strap. These measurement issues should be collectively considered when evaluating previous reports of PA in youth with DS. 3.2. What are the PA levels of youth with DS? In infants with DS, movementdespecially of the legsdmay be important for motor development. Children with DS appear to reach stages in motor development with some delay.92 A notable example is the onset of independent walking which occurs about a year later (wage 2) in children with DS than children with typical development.93,94 It is possible that low levels of motor activity during early infancy may contribute to this phenomenon. One study found that, during the first 6 months of life, infants with DS show lower levels of general movements as measured by observation than

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infants with typical development.95 In contrast, analyzing video recordings, others reported no differences between infants with and without DS in the total amount of leg movements93 which are presumably more relevant for the development of walking. Subsequently, infants with DS were found to show more low-intensity and less high-intensity leg motor activity than infants with typical development.96,97 Furthermore, greater amount of high-intensity activity at about 1 year of age was associated with earlier walking onset in infants with DS.96,97 Finally, a randomized controlled study showed that infants with DS, who underwent home-based stepping training while supported over customized treadmills, achieved independent walking by an average of 101 days earlier than infants with DS not undertaking this intervention; the intervention was initiated once infants with DS could sit independently and it was conducted 5 days/week, 8 min/day, until the onset of independent walking.94 Taken together, these data suggest that alterations in PA patterns in infants with DS are associated with their motor development, thus supporting the need for early interventions.96 The objective data on PA levels of children and adolescents with DS are limited and provide somewhat conflicting results. Non-resting total energy expenditure measured with doublylabeled water did not differ between 5- and 11-year-old children with DS from the U.S. and peers WOD of similar age and BMI.98 In another U.S. study, the amounts of total, lowintensity, and moderateeintensity activity, as well as time spent sedentary measured with hip-accelerometry over 7 days did not differ between children with DS aged 3e10 years and similarly-aged siblings WOD;90 however, the children with DS participated in less and shorter bouts of vigorous-intensity activity than their siblings. Notably, children both with and without DS in that study exceeded the recommendations for total and vigorous-intensity aerobic activity. Similarly, Australian children and adolescents with DS met on average the recommended amounts of moderate- and vigorous-intensity activity as measured by hip-accelerometry91 and also appeared more active than U.S. youth.77 But there was large between-person variability in activity levels and 58% of the children with DS did not meet the recommended amount. In the same study, youths with DS aged 13e17 years showed lower total, moderate-, and vigorous-intensity activity than those aged 7e12 years, indicating a possible age-associated decline in PA. Recent acceleromety-derived data from the U.S. demonstrated that, on average, children and adolescents with DS did not engage in moderate-to-vigorous PA for 60 min/ day.99 Furthermore, PA was lower and sedentary behavior was higher in older youths with DS compared to younger ones. Another U.S. study using accelerometry100 showed that, prior to an intervention, youth with DS aged 8e15 years were active at moderate-to-vigorous levels for an average of about 43 min, although there was significant between-people variation in this value. Finally, cross-sectional accelerometry-determined data from England demonstrated lower amount and faster ageassociated decline of moderate-to-vigorous activity in people with DS than people with ID but without DS across the lifespan (Table 3).101

Youth with DS: Fitness and activity Table 3 Physical activity in youth with Down syndrome (DS). Characteristic

Description

Physical activity

1. Likely declines during the growing years 2. A large proportion of youth with DS does not meet the recommendation for daily aerobic activity 3. Youth with DS participate in a wide variety of culturally-relevant leisure activities

Barriers to physical activity Within the person 1. 2. 3. Environmental 1. 2. 3. 4. 5. 6.

Health problems Low fitness levels Low motor skills Lack of accessible, inclusive, and properly designed programs Transportation difficulties Negative attitudes towards people with disabilities Competing family responsibilities Parental education and income Lack of friends

Facilitators of physical activity Within the person 1. Knowledge on physical activity and health 2. Positive attitude towards exercise 3. Determination to succeed Environmental 1. Positive social and familial attitudes 2. Knowledgeable professionals 3. Structured programs that . 1) Are adapted to the needs of youth with DS 2) Provide knowledge on physical activity and health 3) Are inclusive 4) Promote social interaction and enjoyment

Some subjective datadobtained with parental reports or indepth interviewsdsupplement the literature on PA of youth with DS. Canadian children with DS aged 2e14 years were rated by their parents as less active and as spending more time indoors compared to siblings without DS,68 although all youth in this study with DS participated in organized sports at least once per week.69 Among 38 Australian youth with DS aged 11e18 years, only two engaged in PA more than 3 days/ weekda finding suggestive of low PA levels.102 In a second Australian study, less than one third of 208 youth with DS aged 5e18 years were found to be active at moderate-tovigorous intensity for 60 min/day, although most participated in sports.103 Finally, during in-depth interviews, parents of U.S. preschoolers with DS perceived their children as naturally active. In contrast, parents of elementary-school students perceived a gradual decrease in their children’s interest for PA, supporting the possibility for an age-associated decline among youth with DS.104 The existing objective and subjective data do not allow us to conclude with confidence whether youth with DS have lower PA levels than youth WOD, but this appears likely. Additionally, it is not known if youth with DS meet the required amounts of muscle- and bone-strengthening activities. Although there are no longitudinal data on the developmental course of PA in youth with DS, it is likely that PA declines with age in this population. Furthermore, a large

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proportion of children and adolescents with DS may not meet the recommended amount of daily aerobic activity. 3.3. Determinants of PA The study of the determinants of PA in youth with DS is still in its infancy. Following the approach of the International Classification of Functioning, Disability and Health,105 PA may be influenced by a child’s health status, functional profile, participation in life activities, and contextual factorsdeither within the person or in the environment. DS is associated with many health conditions, but there is great variability in the number and extent of conditions that youth with DS exhibit. In one study, medical issues were not associated with function among youth with DS.106 It is reasonable, however, to assume that acute health problems might present barriers to PA for youth with DS and that, when medical issues are efficiently overcome, PA may be facilitated. The functional profiles of youth with DS may also be related to their PA levels. Quantitative and qualitative data suggest that lower cognitive, behavioral, and motor skills may present barriers to PA of youth with DS.103,104,107,108 Some theorists also argue that people with DS may have a tendency for slower, safer, and more accurate movement patterns due to interactions between neurological, environmental, and taskassociated constraints.109 Additionally, the very low aerobic and muscular fitness of youth with DS may potentially affect their involvement in physical activities, especially of higher intensities, but this has not been directly examined (Table 3). Contextual factors within the person may also be at play. In support of this argument, the aforementioned lower participation in vigorous-intensity activities of children with DS compared to their siblings90 was collectively explained by age, sex, race, ethnicity, income, maternal education, and BMI. It is difficult, however, to determine the individual contributions of these factors to PA of the children in that study. As previously discussed, PA in youth with DS may decline with age,91,101,104 although one study did not find differences in sport participation between children and adolescents with DS.103 Furthermore, whether PA differs between sexes in youth with DS, as in youth WOD,74,77 is not known. Data from Taiwan, China showed no difference in recreational and sport participation between boys and girls with DS.108 In contrast, another study conducted in Taiwan, China demonstrated that, among youth with ID including DS, boys and those who had positive attitudes towards exercise were more likely to be regularly active after school.110 It is also very likely that the social and physical environment contributes to the PA levels of children and adolescents with DS (Table 3). This is supported by a wide variation in types of leisure participation among youth with DS around the world.68,102,103,108,110,111 Furthermore, it has been argued that inactivity among youth with DS may be a learned behavior partially resulting from exclusionary practices.112 Importantly, lack of accessible, inclusive, and appropriately-designed programs, as well as negative attitudes, transportation problems, competing family responsibilities, parental education

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and income, and lack of friends, all reportedly present barriers to PA for youth with DS.90,104,107 3.4. PA promotion Youth with DS reportedly participate in a wide range of recreational activities. Examples include walking, swimming, bowling, dancing, and team sports.68,102,103,108,110,111 The types of leisure participation among youth with DS likely vary around the world; for example, swimming appears common in Australia,102,103 ice-skating in Canada,68 and bicycling in Taiwan, China.108 Notably, walking is one of the most commonly performed activities among youth with DS,108,110,111 suggesting that their altered gait pattern87,88 may not present a barrier to PA. Supporting this proposition, children and adolescents with DS exhibit functional independence in locomotion tasks.106 Therefore, youth with DS have the potential to participate in all types of culturally-relevant physical activities. Unfortunately, very little data exist on interventions to promote PA in youth with DS. A randomized-controlled study found that youth with DS who learned to ride a bicycle increased their PA levels about 1 year after the intervention,100 suggesting that motor skill development may improve longterm PA. Furthermore, well-designed school programs allow students with ID including those with DS to meet the PA recommendations.113 It should also be considered that 12 weeks of exercise training, combined with health education, improves the attitudes towards exercise and psycho-social well being of adults with DS,114 but, to our knowledge, similar studies in youth with DS have not been conducted (Table 3). It has been recommended that PA promotion in all youth aimed at ameliorating the age-associated decline in PA, suppressing the development of pathological processes, and creating life-long PA habits.74 To achieve these goals in youth with DS, PA promotion should be multi-factorial. Welldesigned programs should take into account the physical, cognitive, and psycho-social health profiles of children with DS as well as their need for enjoyment and participation. But at the same time, the environmental contexts in which PA, exercise, and recreation occur must be appropriately designed. Parents tell us that the PA of their children with DS may be facilitated by positive familial and social attitudes, and structured programsdones that are adapted to the abilities of their children, offer youth with DS knowledge on PA and health, utilize their determination to succeed, and promote social interactions and enjoyment.104,107,111 4. Summary and future directions 4.1. Physical fitness Youth with DS have low peak aerobic capacity coupled with low peak HR, suggesting autonomic dysfunction may be a primary reason explaining low work performance in this population. Furthermore, persons with DS also have low muscular strength compared to individuals WOD. Exercise

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training utilizing endurance and/or resistance exercise appears beneficial for youth with DS. The role of overweight/obesity in youth with DS does not currently explain lower aerobic capacities in persons with DS, yet more work needs to be conducted to completely understand its role with regards to aerobic capacity and PA in this population. Studies involving multi-factorial issues (e.g., physiological, environmental, etc.) common to youth with DS are necessary to understand how to optimize quality of life in this population. 4.2. PA Cross-sectional data suggest that PA likely declines with growth in youth with DS and that a large proportion of these youths do not meet the recommended amount of daily aerobic activity. Effective PA promotion should be multi-factorialdit should be adapted to the physiological, cognitive, and psychosocial profiles of youth with DS, but should also consider environmental modifications. There is a need to improve the assessment of PA with objective and subjective approaches. Furthermore, longitudinal research is needed to examine how PA levels change and what factors contribute to them during growth in youth with DS. Finally, it is also important to examine the effectiveness of specific interventions aimed at increasing PA. References 1. Down JLH. Observations on an ethnic classification of idiots. London hospital reports 1866;3:259e62. 2. Bhopal R. The beautiful skull and blumenbach’s errors: the birth of the scientific concept of race. BMJ 2007;335:1308e9. 3. Classification and nomenclature of morphological defects. Lancet 1975;305:513. 4. Lejeune J, Gautier M, Turpin R. Study of somatic chromosomes from 9 mongoloid children. C R Hebd Seances Acad Sci 1959;248:1721e2. 5. Shin M, Besser LM, Kucik JE, Lu C, Siffel C, Correa A, et al. Prevalence of Down syndrome among children and adolescents in 10 regions of the United States. Pediatrics 2009;124:1565e71. 6. Schalock RL, Borthwick-Duffy SA, Buntinx WHE, Coulter DL, Craig EM. Intellectual disability: definition, classification, and systems of supports. 11th ed. Washington, DC: American Association on Intellectual & Develomental Disabilities; 2010. 7. Edwards WLR. Mental retardation: definition, classification, and systems of support. Washington, DC: American Association on Mental Retardation; 2002. 8. American Academy of Pediatrics. Health supervision for children with Down syndrome. Pediatrics 2001;107:442e9. 9. Cohen W. Health care guidelines for individuals with Down syndrome. Down Syndrome Q 1996;1:1e10. 10. So SA, Urbano RC, Hodapp RM. Hospitalizations of infants and young children with Down syndrome: evidence from inpatient person-records from a statewide administrative database. J Intellect Disabil Res 2007;51:1030e8. 11. Boulet SL, Molinari NA, Grosse SD, Honein MA, CorreaVillasenor A. Health care expenditures for infants and young children with Down syndrome in a privately insured population. J Pediatr 2008;153:241e6. 12. Geelhoed EA, Bebbington A, Bower C, Deshpande A, Leonard H. Direct health care costs of children and adolescents with Down syndrome. J Pediatr 2011;159:541e5.

Youth with DS: Fitness and activity 13. Goldstein H. One year of health and social services for adolescents with down’s syndrome. A calculation of costs in a representative area of Denmark. Soc Psychiatry Psychiatr Epidemiol 1989;24:30e4. 14. Day SM, Strauss DJ, Shavelle RM, Reynolds RJ. Mortality and causes of death in persons with Down syndrome in California. Dev Med Child Neurol 2005;47:171e6. 15. Glasson EJ, Sullivan SG, Hussain R, Petterson BA, Montgomery PD, Bittles AH. The changing survival profile of people with down’s syndrome: implications for genetic counselling. Clin Genet 2002;62:390e3. 16. Yang Q, Rasmussen SA, Friedman JM. Mortality associated with Down’s syndrome in the USA from 1983 to 1997: a population-based study. Lancet 2002;359:1019e25. 17. Hermon C, Alberman E, Beral V, Swerdlow AJ. Mortality and cancer incidence in persons with Down’s syndrome, their parents and siblings. Ann Hum Genet 2001;65:167e76. 18. Hill DA, Gridley G, Cnattingius S, Mellemkjaer L, Linet M, Adami HO, et al. Mortality and cancer incidence among individuals with Down syndrome. Arch Intern Med 2003;163:705e11. 19. Strauss D, Eyman RK. Mortality of people with mental retardation in california with and without Down syndrome, 1986-1991. Am J Ment Retard 1996;100:643e53. 20. Day S. Estimators of long-term transition probabilities in multistate stochastic processes. Riverside CA: University of California; 2001 [dissertation]. 21. Esbensen AJ, Seltzer MM, Greenberg JS. Factors predicting mortality in midlife adults with and without Down syndrome living with family. J Intellect Disabil Res 2007;51:1039e50. 22. Strauss D, Zigman WB. Behavioral capabilities and mortality risk in adults with and without Down syndrome. Am J Ment Retard 1996;101:269e81. 23. Torr J, Strydom A, Patti P, Jokenen N. Aging in Down syndrome: morbidity and mortality. J Policy Prac Intell Disabil 2010;2:70e81. 24. Schupf N, Winsten S, Patel B, Pang D, Ferin M, Zigman WB, et al. Bioavailable estradiol and age at onset of alzheimer’s disease in postmenopausal women with Down syndrome. Neurosci Lett 2006;406:298e302. 25. Baynard T, Pitetti KH, Guerra M, Unnithan VB, Fernhall B. Age-related changes in aerobic capacity in individuals with mental retardation: a 20year review. Med Sci Sports Exerc 2008;40:1984e9. 26. Fernhall B, Millar AL, Tymeson GT, Burkett LN. Maximal exercise testing of mentally retarded adolescents and adults: reliability study. Arch Phys Med Rehabil 1990;71:1065e8. 27. Fernhall B, Pitetti KH. Limitations to work capacity in individuals with intellectual disabilities. Clin Exerc Physiol 2001;3:176e85. 28. Eberhard Y, Eterradossi J, Rapacchi B. Physical aptitudes to exertion in children with down’s syndrome. J Ment Defic Res 1989;33(Pt 2):167e74. 29. Fernhall B, Baynard T, Collier SR, Figueroa A, Goulopoulou S, Kamimori GH, et al. Catecholamine response to maximal exercise in persons with Down syndrome. Am J Cardiol 2009;103:724e6. 30. Baynard T, Pitetti KH, Guerra M, Fernhall B. Heart rate variability at rest and during exercise in persons with Down syndrome. Arch Phys Med Rehabil 2004;85:1285e90. 31. Fernhall B, Otterstetter M. Attenuated responses to sympathoexcitation in individuals with Down syndrome. J Appl Physiol 2003;94:2158e65. 32. Guimaraes CV, Donnelly LF, Shott SR, Amin RS, Kalra M. Relative rather than absolute macroglossia in patients with Down syndrome: implications for treatment of obstructive sleep apnea. Pediatr Radiol 2008;38:1062e7. 33. Baynard T, Unnithan V, Pitetti K, Fernhall B. Determination of ventilatory threshold in adolescents with mental retardation with and without Down syndrome. Pediatr Exerc Sci 2004;16:126e37. 34. Mendonca GV, Pereira FD, Fernhall B. Oxygen uptake kinetics during exercise in adults with Down syndrome. Eur J Appl Physiol 2010;110:575e83. 35. Guerra M, Gene´-Barriga, Fernhall B. Reliability of wingate testing in adolescents with Down syndrome. Pediatr Exerc Sci 2009;21:47e54.

55 36. Fernhall B, Pitetti K, Stubbs Jr NLS. Validity and reliability of the 1/2 mile run-walk as an indicator of aerobic fitness in children with mental retardation. Pediatr Exerc Sci 1996;8:130e42. 37. Varela AMPK. Heart rate responses to two field exercise tests by adolescents and young adults with Down syndrome. Adapted Phys Activity Q 1995;12:43e51. 38. Pitetti K, Fernhall B. Comparing run performance of adolescents with metnal retardationewith and without Down syndrome. Adapted Phys Activity Q 2004;21:219e28. 39. Fernhall B, Pitetti KH, Millar AL, Hensen T, Vukovich MD. Cross validation of the 20 m shuttle run in children with mental retardation. Adapted Phys Activity Q 2000;17:402e12. 40. Fernhall B, Pitetti KH, Vukovich MD, Stubbs N, Hensen T, Winnick JP, et al. Validation of cardiovascular fitness field tests in children with mental retardation. Am J Ment Retard 1998;102:602e12. 41. Guerra M, Pitetti K, Fernhall B. Cross validation of the 20-m shuttle run test for adolescents with Down syndrome. Adapt Phys Activ Q 2003;20:70e9. 42. Agiovlasitis S, Pitetti KH, Guerra M, Fernhall B. Prediction of VO2peak from the 20-m shuttle-run test in youth with Down syndrome. Adapt Phys Activ Q 2011;28:146e56. 43. Dodd KJ, Shields N. A systematic review of the outcomes of cardiovascular exercise programs for people with Down syndrome. Arch Phys Med Rehabil 2005;86:2051e8. 44. Varela A, Sardinha L, Pitetti K. Effects of an aerobic rowing training regimen in young adults with Down syndrome. Am J Ment Retard 2001;106:135e44. 45. Millar AL, Fernhall B, Burkett LN. Effects of aerobic training in adolescents with Down syndrome. Med Sci Sports Exerc 1993;25:270e4. 46. Tsimaras V, Giagazoglou P, Fotiadou E, Christoulas K, Angelopoulou N. Jog-walk training in cardiorespiratory fitness of adults with Down syndrome. Percept Mot Skills 2003;96:1239e51. 47. Rimmer JH, Heller T, Wang E, Valerio I. Improvements in physical fitness in adults with Down syndrome. Am J Ment Retard 2004;109:165e74. 48. Ordonez FJ, Rosety M, Rosety-Rodriguez M. Influence of 12-week exercise training on fat mass percentage in adolescents with Down syndrome. Med Sci Monit 2006;12:CR416e9. 49. Dyer S. Physiological effects of a 13-week physical fitness program on Down syndrome subjects. Pediatr Exerc Sci 1994;6:88e100. 50. Lewis CL, Fragala-Pinkham MA. Effects of aerobic conditioning and strength training on a child with Down syndrome: a case study. Pediatr Phys Ther 2005;17:30e6. 51. Cioni M, Cocilovo A, Di Pasquale F, Araujo MB, Siqueira CR, Bianco M. Strength deficit of knee extensor muscles of individuals with Down syndrome from childhood to adolescence. Am J Ment Retard 1994;99:166e74. 52. Mercer VS, Lewis CL. Hip abductor and knee extensor muscle strength of children with and without Down syndrome. Pediatr Phys Ther 2001;13:18e26. 53. Pitetti K, Fernhall B. Aerobic capacity as related to leg strength in youths with mental retardation. Pediatr Exerc Sci 1997;9:223e36. 54. Pitetti KH, Boneh S. Cardiovascular fitness as related to leg strength in adults with mental retardation. Med Sci Sports Exerc 1995;27:423e8. 55. Angelopoulou N, Matziari C, Tsimaras V, Sakadamis A, Souftas V, Mandroukas K. Bone mineral density and muscle strength in young men with mental retardation (with and without Down syndrome). Calcif Tissue Int 2000;66:176e80. 56. Pitetti KH, Climstein M, Mays MJ, Barrett PJ. Isokinetic arm and leg strength of adults with Down syndrome: a comparative study. Arch Phys Med Rehabil 1992;73:847e50. 57. Croce RV, Pitetti KH, Horvat M, Miller J. Peak torque, average power, and hamstrings/quadriceps ratios in nondisabled adults and adults with mental retardation. Arch Phys Med Rehabil 1996;77:369e72. 58. Horvat M, Pitetti KH, Croce R. Isokinetic torque, average power, and flexion/extension ratios in nondisabled adults and adults with mental retardation. J Orthop Sports Phys Ther 1997;25:395e9.

56 59. Weber R, French R. Downs syndrome adolescents and strength training. Clin Kinesiol 1988;42:13e21. 60. Shields N, Taylor NF. A student-led progressive resistance training program increases lower limb muscle strength in adolescents with Down syndrome: a randomised controlled trial. J Physiother 2010;56:187e93. 61. Cowley PM, Ploutz-Snyder LL, Baynard T, Heffernan KS, Jae SY, Hsu S, et al. The effect of progressive resistance training on leg strength, aerobic capacity and functional tasks of daily living in persons with Down syndrome. Disabil Rehabil 2011;33:2229e36. 62. Shields N, Taylor NF, Dodd KJ. Effects of a community-based progressive resistance training program on muscle performance and physical function in adults with Down syndrome: a randomized controlled trial. Arch Phys Med Rehabil 2008;89:1215e20. 63. Tsimaras VK, Fotiadou EG. Effect of training on the muscle strength and dynamic balance ability of adults with Down syndrome. J Strength Cond Res 2004;18:343e7. 64. Mendonca GV, Pereira FD, Fernhall B. Effects of combined aerobic and resistance exercise training in adults with and without Down syndrome. Arch Phys Med Rehabil 2011;92:37e45. 65. Rubin SS, Rimmer JH, Chicoine B, Braddock D, McGuire DE. Overweight prevalence in persons with Down syndrome. Ment Retard 1998;36:175e81. 66. De S, Small J, Baur LA. Overweight and obesity among children with developmental disabilities. J Intellect Dev Disabil 2008;33:43e7. 67. Prasher V. Overweight and obesity amongst down’s syndrome adults. J Intellect Disabil Res 1995;39:437e41. 68. Sharav T, Bowman T. Dietary practices, physical activity, and body-mass index in a selected population of Down syndrome children and their siblings. Clin Pediatr (Phila) 1992;31:341e4. 69. Luke A, Sutton M, Schoeller DA, Roizen NJ. Nutrient intake and obesity in prepubescent children with Down syndrome. J Am Diet Assoc 1996;96:1262e7. 70. Baptista F, Varela A, Sardinha LB. Bone mineral mass in males and females with and without Down syndrome. Osteoporos Int 2005;16:380e8. 71. Gonzalez-Aguero A, Ara I, Moreno LA, Vicente-Rodriguez G, Casajus JA. Fat and lean masses in youths with Down syndrome: gender differences. Res Dev Disabil 2011;32:1685e93. 72. Grammatikopoulou MG, Manai A, Tsigga M, TsiligiroglouFachantidou A, Galli-Tsinopoulou A, Zakas A. Nutrient intake and anthropometry in children and adolescents with Down syndromeea preliminary study. Dev Neurorehabil 2008;11:260e7. 73. Stancliffe RJ, Lakin KC, Larson S, Engler J, Bershadsky J, Taub S, et al. Overweight and obesity among adults with intellectual disabilities who use intellectual disability/developmental disability services in 20 U.S. States. Am J Intellect Dev Disabil 2011;116:401e18. 74. Rowland T. Physical activity, fitness, and children. In: Bouchard C, Blair SN, Haskell WL, editors. Physical activity and health. Champaign, IL: Human Kinetics; 2007. p. 259e70. 75. Strong WB, Malina RM, Blimkie CJ, Daniels SR, Dishman RK, Gutin B, et al. Evidence based physical activity for school-age youth. J Pediatr 2005;146:732e7. 76. Physical Activity Guidelines Advisory Committee. 2008 physical activity guidelines for Americans. Washington, DC: U.S. Department of Health and Human Services; 2008. 77. Troiano RP, Berrigan D, Dodd KW, Masse LC, Tilert T, McDowell M. Physical activity in the united states measured by accelerometer. Med Sci Sports Exerc 2008;40:181e8. 78. Frey GC, Stanish HI, Temple VA. Physical activity of youth with intellectual disability: review and research agenda. Adapt Phys Activ Q 2008;25:95e117. 79. Matthews L, Hankey C, Penpraze V, Boyle S, Macmillan S, Miller S, et al. Agreement of accelerometer and a physical activity questionnaire in adults with intellectual disabilities. Prev Med 2011;52:361e4. 80. Beets MW, Combs C, Pitetti KH, Morgan M, Bryan RR, Foley JT. Accuracy of pedometer steps and time for youth with disabilities. Adapt Phys Activ Q 2007;24:228e44.

K. Pitetti et al. 81. Beets MW, Pitetti KH. Using pedometers to measure moderate-tovigorous physical activity for youth with an intellectual disability. Disabil Health J 2011;4:46e51. 82. Pitetti KH, Beets MW, Flaming J. Accuracy of pedometer steps and time for youth with intellectual disabilities during dynamic movements. Adapt Phys Activ Q 2009;26:336e51. 83. Pitchford EA, Yun J. The accuracy of pedometers for adults with Down syndrome. Adapt Phys Activ Q 2010;27:321e36. 84. Agiovlasitis S, Beets MW, Motl RW, Fernhall B. Step-rate thresholds for moderate and vigorous-intensity activity in persons with Down syndrome. J Sci Med Sport 2012;15:425e30. 85. Agiovlasitis S, Motl RW, Fahs CA, Ranadive SM, Yan H, Echols GH, et al. Metabolic rate and accelerometer output during walking in people with Down syndrome. Med Sci Sports Exerc 2011;43:1322e7. 86. Agiovlasitis S, McCubbin JA, Yun J, Mpitsos G, Pavol MJ. Effects of Down syndrome on three-dimensional motion during walking at different speeds. Gait Posture 2009;30:345e50. 87. Kubo M, Ulrich B. Coordination of pelvis-hat (head, arms and trunk) in anterior-posterior and medio-lateral directions during treadmill gait in preadolescents with/without Down syndrome. Gait Posture 2006;23:512e8. 88. Ulrich BD, Haehl V, Buzzi UH, Kubo M, Holt KG. Modeling dynamic resource utilization in populations with unique constraints: preadolescents with and without Down syndrome. Hum Mov Sci 2004;23:133e56. 89. Pinter JD, Eliez S, Schmitt JE, Capone GT, Reiss AL. Neuroanatomy of down’s syndrome: a high-resolution mri study. Am J Psychiatry 2001;158:1659e65. 90. Whitt-Glover MC, O’Neill KL, Stettler N. Physical activity patterns in children with and without Down syndrome. Pediatr Rehabil 2006;9:158e64. 91. Shields N, Dodd KJ, Abblitt C. Do children with Down syndrome perform sufficient physical activity to maintain good health? A pilot study. Adapt Phys Activ Q 2009;26:307e20. 92. Block ME. Motor development in children with Down syndrome: a review of the literature. Adapt Phys Activ Q 1991;8:179e209. 93. Ulrich BD, Ulrich DA. Spontaneous leg movements of infants with Down syndrome and nondisabled infants. Child Dev 1995;66:1844e55. 94. Ulrich DA, Ulrich BD, Angulo-Kinzler RM, Yun J. Treadmill training of infants with Down syndrome: evidence-based developmental outcomes. Pediatrics 2001;108:E84. 95. Mazzone L, Mugno D, Mazzone D. The general movements in children with Down syndrome. Early Hum Dev 2004;79:119e30. 96. Lloyd M, Burghardt A, Ulrich DA, Angulo-Barroso R. Physical activity and walking onset in infants with Down syndrome. Adapt Phys Activ Q 2010;27:1e16. 97. McKay SM, Angulo-Barroso RM. Longitudinal assessment of leg motor activity and sleep patterns in infants with and without Down syndrome. Infant Behav Dev 2006;29:153e68. 98. Luke A, Roizen NJ, Sutton M, Schoeller DA. Energy expenditure in children with Down syndrome: correcting metabolic rate for movement. J Pediatr 1994;125:829e38. 99. Esposito PE, Macdonald M, Hornyak JE, Ulrich DA. Physical activity patterns of youth with Down syndrome. Intellect Dev Disabil 2012;50:109e19. 100. Ulrich DA, Burghardt AR, Lloyd M, Tiernan C, Hornyak JE. Physical activity benefits of learning to ride a two-wheel bicycle for children with Down syndrome: a randomized trial. Phys Ther 2011;91:1463e77. 101. Phillips AC, Holland AJ. Assessment of objectively measured physical activity levels in individuals with intellectual disabilities with and without Down’s syndrome. PLoS One 2011;6:e28618. 102. Jobling A, Cuskelly M. Young people with Down syndrome: a preliminary investigation of health knowledge and associated behaviours. J Intellect Dev Disabil 2006;31:210e8. 103. Oates A, Bebbington A, Bourke J, Girdler S, Leonard H. Leisure participation for school-aged children with Down syndrome. Disabil Rehabil 2011;33:1880e9. 104. Menear KS. Parents’ perceptions of health and physical activity needs of children with down syndrom. Downs Syndr Res Pract 2007;12:60e8.

Youth with DS: Fitness and activity 105. World Health Organization. International classification of functioning, disability and health (ICF). Geneva: World Health Organization; 2001. 106. Leonard S, Msall M, Bower C, Tremont M, Leonard H. Functional status of school-aged children with Down syndrome. J Paediatr Child Health 2002;38:160e5. 107. Barr M, Shields N. Identifying the barriers and facilitators to participation in physical activity for children with Down syndrome. J Intellect Disabil Res 2011;55:1020e33. 108. Wuang Y, Su CY. Patterns of participation and enjoyment in adolescents with Down syndrome. Res Dev Disabil 2012;33:841e8. 109. Latash ML. Motor coordination in Down syndrome: the role of adaptive changes. In: Weeks DJ, Chua R, Elliot D, editors. Perceptual-motor behavior in Down syndrome. Champaign, IL: Human Kinetics; 2000. p. 199e223.

57 110. Lin JD, Lin PY, Lin LP, Chang YY, Wu SR, Wu JL. Physical activity and its determinants among adolescents with intellectual disabilities. Res Dev Disabil 2010;31:263e9. 111. Buttimer J, Tierney E. Patterns of leisure participation among adolescents with a mild intellectual disability. J Intellect Disabil 2005;9:25e42. 112. Jobling A. Life be in it: lifestyle choices for active leisure. Downs Syndr Res Pract 2001;6:117e22. 113. Pitetti KH, Beets MW, Combs C. Physical activity levels of children with intellectual disabilities during school. Med Sci Sports Exerc 2009;41:1580e6. 114. Heller T, Hsieh K, Rimmer JH. Attitudinal and psychosocial outcomes of a fitness and health education program on adults with Down syndrome. Am J Ment Retard 2004;109:175e85.