This article is commented on by Apkon on page 490 of this issue.
A 21-week bone deposition promoting exercise programme increases bone mass in young people with Down syndrome
Article first published online: 13 MAR 2012
© The Authors. Developmental Medicine & Child Neurology © 2012 Mac Keith Press
Developmental Medicine & Child Neurology
Volume 54, Issue 6, pages 552–556, June 2012
How to Cite
GONZÁLEZ-AGÜERO, A., VICENTE-RODRÍGUEZ, G., GÓMEZ-CABELLO, A., ARA, I., MORENO, L. A. and CASAJÚS, J. A. (2012), A 21-week bone deposition promoting exercise programme increases bone mass in young people with Down syndrome. Developmental Medicine & Child Neurology, 54: 552–556. doi: 10.1111/j.1469-8749.2012.04262.x
- Issue published online: 10 MAY 2012
- Article first published online: 13 MAR 2012
- PUBLICATION DATA Accepted for publication 29th December 2011. Published online 13th March 2012.
Aim To determine whether the bone mass of young people with Down syndrome may increase, following a 21-week conditioning training programme including plyometric jumps.
Method Twenty-eight participants with Down syndrome (13 females, 15 males) aged 10 to 19 years were divided into exercise (DS-E; n=14; eight females, six males mean age 13y 8mo, SD 2y 6mo) and non-exercise (DS-NE; n=14; five females, nine males mean age 15y 5mo, SD 2y 6mo) groups. Total and regional (hip and lumbar spine [L1–L4]) bone mineral content (BMC) and total lean mass were assessed by dual energy X-ray absorptiometry at baseline and after a 25-minute training session performed twice a week. Repeated-measures analyses of variation were applied to test differences between pre- and posttraining values for BMC and total lean mass. Differences between increments were studied with the Student’s t-test. Linear regression models were fitted to test independent relationships.
Results After the intervention, higher increments in total and hip BMC, and total lean mass, were observed in the DS-E group (all p<0.05). A time×exercise interaction was found for total lean mass (p<0.05). The increment in total lean mass, height, and Tanner stage accounted for almost for 60% in the increment in total BMC in the DS-NE group (p<0.05).
Interpretation Twenty-one weeks of training have a positive effect on the acquisition of bone mass in young people with Down syndrome.
Bone mineral content
Down syndrome, exercise group
Down syndrome, non-exercise group
Total lean mass
What this paper adds
- •Young people with Down syndrome may increase their bone mass following a physical exercise programme.
- •The increment in bone mass could be mediated by an increment in total lean mass, which is also detectable.
Down syndrome is a genetic condition accompanied by intellectual disability and more than 80 clinical manifestations, some of them affecting body composition.1 Lower levels of bone mineral content (BMC) have been observed not only in adults2–6 but also in children and adolescents with Down syndrome7,8 compared with their counterparts without Down syndrome. The acquisition of high bone mass during childhood and adolescence is an important factor in preventing osteoporosis later in life.9,10 Because life expectancy of persons with Down syndrome has increased over recent decades to over 55 years, the incidence of osteoporosis, bone fragility, and related fractures is expected to increase in the coming years.
It is well established that physical activity and, specifically, participation in sport during growth has an osteogenic effect on the growing skeleton in children and adolescents without disabilities;12–14 however, studies have not yet been made of children and adolescents with Down syndrome,15 who might also benefit from osteogenic exercising. Plyometric training is a type of exercise that requires various jumps in place or rebound jumping, which may increase peak bone mass during adolescence.16 This type of exercise has been shown to be an effective method for increasing lean mass in adolescents with Down syndrome,17 and as bone mass is closely associated with lean mass this is a positive finding. It has also been suggested that in young people the mechanical impact resulting from plyometric exercise is one of the most osteogenic activities,12 and could enhance the levels of osteocalcin,18 which is an established and extensively used biochemical marker of bone formation.19
Thus, the aim of the present study was to determine whether young people with Down syndrome are able to increase their bone-related variables (total and regional BMC) following a 21-week training programme consisting of two 25-minute sessions per week of conditioning and plyometric jump training.
A sample of 28 children and adolescents with Down syndrome (13 females, 15 males) aged 10 to 19 years at baseline were recruited from different schools and institutions in Aragon, Spain. Participants were randomly assigned to the no exercise control group (DS-NE; n=14: five females, nine males) or to the exercise group (DS-E; n=14: eight females, six males), who followed the training programme. Seven participants were taking medication (levothyroxine sodium) during the study, four in the DS-NE group and three in the DS-E group. Parents and children were informed about the aims and procedures, as well as the possible risks and benefits of the study. Written informed consent was obtained from all the participants and their parents or guardians. The study was performed in accordance with the Helsinki Declaration of 1961 (revised in Edinburgh, 2000) and was approved by the Research Ethics Committee of the Government of Aragon (CEICA, Spain).
All participants were measured with a stadiometer without shoes and minimum clothing to the nearest 0.1 cm (SECA 225; SECA, Hamburg, Germany), and weight to the nearest 0.1kg (SECA 861; SECA). The body mass index was calculated as weight (kilograms) divided by height squared (square metres).
Pubertal status assessment
Pubertal development was determined by direct observation by a physician according to the five stages proposed by Tanner and Whitehouse.20
Bone and lean masses
The bone and lean mass of the participants were measured with dual-energy X-ray absorptiometry using a paediatric version of the software QDR-Explorer (Hologic software version 12.4, Bedford, MA, USA). Dual-energy X-ray absorptiometry equipment was calibrated with a lumbar spine phantom following the manufactures guidelines. Participants were scanned in supine position and the scans were performed in high resolution. Three scans were performed in each participant: whole body, left hip, and lumbar spine. Total lean mass (TLM; kilograms) and BMC (grams) were obtained from the whole body scan; BMC was obtained from lumbar spine (L1–L4) and left hip (proximal region of the femur) scans.
Those participants allocated to the DS-E group exercised twice a week, and each session was conducted with a maximum of 10 participants. One researcher (an experienced exercise practitioner) and one to three assistants supervised the exercise sessions. Each session consisted of combined conditioning and plyometric jump training. The first week was used as familiarization on how to use the material/equipment and how to perform the exercises. Each training session consisted of 5 minutes warm-up activities, 10 to 15 minutes for the main part of the session, and 5 minutes cool-down. In the final stage of training (the last 5 wks), training was sometimes extended by 5 minutes. Training consisted of one or two rotations in a four-stage circuit. The training protocol is summarized in Figure 1.
The exercises performed in each stage were as follows:
Stage 1. Jumps: standing vertical jump, jump with run-in, drop jump (height jumped between 40 and 50cm), drop jump+horizontal jump (height jumped between 40 and 50cm). From the third week onwards, participants carried adapted medicine balls while performing the jumps.
Stage 2. Press-ups against the wall: place hands on a wall and perform press-ups standing with feet apart 30 to 50cm from the wall.
Stage 3. Elastic-fitness bands: (a) lateral rows: steps onto the band; grasp ends with a neutral grip, arms hanging down to sides with elbows slightly bent. Raise band to side of body at shoulder height keeping elbows only slightly bent, then return to start position. (b) Bicep curls: stands with feet shoulder-width apart, knees slightly bent, and at a staggered stance. Grasp ends of band with underhand grip, arms hanging down at sides, elbows close to sides. Flex at the elbows and curl band up to approximately shoulder level. Elbows kept close to sides throughout movement. Return to start position. (c) Frontal rows: stand upright, knees slightly flexed, grasping band with hands held close in front of chest, arms straight. Row one arm back until elbow is behind shoulders. Flex shoulders and back. Return, keep arm slightly flexed. Continue with opposite side.
Stage 4. Adapted medicine balls: Standing, throw and catch medicine balls, with a distance between participants of 3 to 4m.
The DS-E group was divided into four intensity-groups (quartiles), depending on the body weight of each participant, and they worked out individually within each group. When participants showed excessive facility for performing exercises, they were transferred to the next intensity-group. There were four fitness band colours (yellow, green, blue, and purple) of increasing resistance and four medicine balls (1, 2, 3, and 4kg), each one being assigned to a group depending on the strength demanded to perform the exercises.
Every group followed the same schedule of exercises with a different band colour and ball (Fig. 1).
A minimum attendance of 70% was required to be included in the exercise group. If minimum assistance was not achieved, the participant was excluded from the statistical analyses.
All statistical analyses were performed with the Statistical Package for the Social Sciences (SPSS) version 15.0 for Windows (SPSS, Chicago, IL, USA). Means and standard deviations are given as descriptive statistics unless otherwise stated. Normal distribution of the variables was established using the Kolmogorov–Smirnov test; the assumption of homoscedasticity was also confirmed. The χ2 test was used to evaluate the differences in Tanner stage. Student’s t-tests were used to evaluate the differences between groups for physical characteristics. Repeated measures analyses of variance were performed to evaluate whether sex×training interactions were present and to determine the time×exercise interactions for BMC and TLM, including as covariates the increments in TLM (only for BMC variables), in height, and in Tanner stage. Every adjusted value of pre- and posttraining, BMC (total, hip, and spine), and TLM was recorded in the database and the percentage of change (increment of each variable, Δ) calculated; a Student’s t-test was used to evaluate the differences between groups. To test the independent relation between the increments in BMC and the increments of possible confounders, multiple linear regression models were applied including TLM (model 1), TLM+height (model 2), TLM+height+Tanner stage (model 3) and TLM+height+Tanner stage+age at baseline (model 4). Statistical significance was set at p<0.05.
Adherence to training and possible adverse effects
The median for training assistance was 83.8% with 15.5 as the interquartile range. Only one participant (female) did not achieve the minimum 70% attendance at the intervention programme (she attended 45% of the training sessions) and her data were excluded from the analyses. At the end of the training programme, five participants progressed to a higher intensity-group. No withdrawals from the DS-E or DS-NE groups occurred. Noticeably, no adverse effects and no health problems were noted in the participants of both groups over the 21-week period.
Age, Tanner stage, and physical characteristics of the participants are summarized in Table I. Participants in the DS-E group showed lower body mass index than the DS-NE group at baseline (p<0.05; Table I). Participants in both groups showed similar age, height, weight, and Tanner stage distribution at both baseline and post-intervention points.
|Down syndrome, non-exercise (DS-NE; n=14)||Down syndrome, exercise, (DS-E; n=13)|
|Pretraining, mean (SD)||p||Posttraining, mean (SD)||p||Pretraining, mean (SD)||Posttraining, mean (SD)|
|Age (y)||15.4 (2.5)||0.067||16.0 (2.5)||0.067||13.7 (2.6)||14.3 (2.6)|
|Weight (kg)||48.7 (10.7)||0.057||49.5 (10.6)||0.095||40.1 (9.6)||41.8 (9.8)|
|Height (cm)||146.8 (10.7)||0.299||148.3 (10.2)||0.243||141.9 (12.5)||142.8 (12.4)|
|Tanner stage (I, II, III, IV, V)||1/1/1/5/6||0.361||0/2/1/3/8||0.407||3/0/3/2/5||3/1/1/3/5|
|BMI (kg/m2)||22.4 (3.4)||0.028||22.3 (3.2)||0.136||19.6a (2.7)||20.2 (2.6)|
Effects of training on body composition
As no sex×training interactions were found (data not shown), analyses were performed including males and females as a whole.
Overall, the DS-E group showed greater increments in total BMC, TLM, and in the hip BMC (all p<0.05; Table II). Repeated measures analysis of variance showed a time×exercise interaction for TLM (p<0.05; Table II), but no interactions were found for BMC variables.
|DXA measurement||Down syndrome, non-exercise (DS-NE) (n=14)||Down syndrome, exercise (DS-E) (n=13)||Interaction: group×time p|
|Pretraining||Posttraining||Adjusted percentage of change||Pretraining||Posttraining||Adjusted percentage of change|
|BMC (g)||1110.3 (76.3)||1139.2 (77.3)||2.4a||803.3 (79.9)||852.3 (81.0)||6.7||0.197|
|TLM (kg)||32.4 (1.9)||32.7 (2.1)||1.9a||26.4 (2.0)||27.9 (2.2)||5.8||0.008b|
|BMC (g)||22.7 (1.7)||24.4 (1.9)||6.2a||16.9 (1.9)||19.3 (2.2)||14.6||0.587|
|BMC (g)||44.1 (3.4)||47.6 (3.5)||6.4||28.6 (3.5)||30.1 (3.7)||6.4||0.107|
Multiple linear regression models revealed that in the DS-NE group, the ΔTLM accounted for 54%, the Δheight accounted for 5%, and the ΔTanner stage accounted for 0.6% of the variation in the increment of total BMC (all p<0.05; Table III). No associations were found for the total BMC in the DS-E group, nor for the hip or lumbar spine in either of the two groups.
|ΔTotal BMC||ΔHip BMC||ΔLumbar spine BMC|
The major finding of this study is that a 21-week training programme may help to increase the BMC of young people with Down syndrome. As far as we know, this is the first study reporting the benefits in bone-related variables of an exercise programme in children and adolescents with Down syndrome. The association between low bone mass with risk of osteoporosis and related fractures, and the fact that childhood and adolescence are the most important periods to achieve the peak of bone mass,9,10 give more relevance to our study, especially in a population characterized by reduced bone acquisition.7 The increments in total and hip region BMC in the DS-E group were two to three times higher than in the DS-NE group after the training period and after adjustments for important confounders. The fact that we did not find any significant time×exercise interaction in bone-related variables could be due to the reduced number of participants in the study. The present study is in line with previous studies that obtained benefits from using plyometric training with children and adolescents without disabilities.16,21 However, the rate of improvement in total and hip BMC was higher in the present study (6.7% vs 3.7% and 1.6% in total, and 14.6% vs 4.5% in hip) and similar improvement was obtained in the lumbar spine region (6.4% vs 6.6% and 3.1%).
Lean mass is highly correlated with bone mass12 and, as found in the present study, a time×exercise interaction was found for TLM in the DS-E group compared with the DS-NE group. The previous point could suggest that the higher increments observed in BMC may be due more to the indirect effect of muscle hypertrophy on bone than to the direct effect of exercise on bone. However, the fact that neither the increment in TLM, in height, or in Tanner stage, nor the age of the participants in the DS-E group, significantly accounts for the increments in BMC, allows us to suppose that the training could have had an effect on the bone mass of the participants. Owing to the osteogenic effect of exercise or to the higher increment in TLM, the results of the intervention were satisfactory in terms of bone mass acquisition with an intervention that was quite modest in terms of time employed. In the future, the effect of longer and/or more intense trainings may show whether the tendency of young people with Down syndrome to have reduced bone mass could be compensated.
Another important issue is the feasibility of the programme. As there were no withdrawals, it seems that the training programme was attractive and easily adhered to, which is a matter of great importance in this specific population.
A limitation to this study is that we did not perform traditional strength training based on percentages of 1-maximum repetition; however, the protocol of our training programme was well established and defined. Unfortunately, exposure to sunlight and diet were not controlled in this study. The strengths of this study were the inclusion of both sexes in the design, the use of a control group of young people with Down syndrome, and the sample size, which although not a very large one, is larger than that of any other intervention study including training with children and adolescents with Down syndrome.
To conclude, our findings suggest that physical conditioning including plyometric jumps may be a good strategy to increase BMC in young people with Down syndrome.
We thank all the children and their parents who participated in the study for their understanding and dedication to the project. We especially thank Fundación Down Zaragoza, Special Olympics Aragon, and Colegio Jesús-María El Salvador for their support. We also thank Paula Velasco Martínez from the University of Zaragoza for her technical assistance. This work was supported by the Gobierno de Aragón (Proyecto PM 17/2007) and the Ministerio de Ciencia e Innovación de España (Red de investigación en ejercicio físico y salud para poblaciones especiales-EXERNET-DEP2005-00046/ACTI).
- 18Acute effects of plyometric jumping and intermittent running on serum bone markers in young males. Eur J Appl Physiol DOI: 10.1007/s00421-011-2108-8., , , , , .