Research in Developmental Disabilities 55 (2016) 197–206

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Review article

Effects of Neuromuscular Training on Children and Young

Adults with Down Syndrome: Systematic Review and
Meta-Analysis
Dai Sugimoto a,b,d,∗ , Samantha L. Bowen e , William P. Meehan III a,b,d , Andrea
Stracciolini a,b,c,d
a
The Micheli Center for Sports Injury Prevention, Waltham, MA, United States
b
Division of Sports Medicine, Department of Orthopedics, Boston Children’s Hospital, Boston, MA, United States
c
Division of Emergency Medicine, Department of Pediatrics, Boston Children’s Hospital, Boston, MA, United States
d
Harvard Medical School, Boston, MA, United States
e
Northeastern University, Boston, MA, United States

a r t i c l e i n f o a b s t r a c t

Article history: Purpose: To synthesize existing research evidence and examine effects of neuromuscular
Received 19 March 2015 training on general strength, maximal strength, and functional mobility tasks in children
Received in revised form 29 March 2016 and young adults with Down syndrome.
Accepted 5 April 2016
Methods: PubMed and EBSCO were used as a data source. To attain the aim of this study,
literature search was performed under following inclusion criteria: (1) included partici-
Keywords: pants with Down syndrome, (2) implemented a neuromuscular training intervention and
Trisomy 21
measured outcome variables of general strength, maximal strength, and functional mobil-
Motor skill development
ity tasks, (3) had a group of participants whose mean ages were under 30 years old, (4)
Resistance training
Balance training employed a prospective controlled design, and (5) used mean and standard deviations to
Functional performance express the outcome variables. Effect size was calculated from each study based on pre- and
post-testing value differences in general strength, maximal strength, and functional mobil-
ity tasks between control and intervention groups. The effect size was further classified in
to one of the following categories: small, moderate, and large effects.
Results: Seven studies met inclusion criteria. Analysis indicated large to moderate effects
on general strength, moderate to small effects on maximal strength, and small effect on
functional mobility tasks by neuromuscular training.
Conclusions: Although there were limited studies, the results showed that neuromuscular
training could be used as an effective intervention in children and young adults with Down
syndrome.
What this paper adds: Synthesis of seven reviewed studies indicated that neuromuscular
training could be beneficial to optimize general and maximal muscular strength develop-
ment in children and young adults with Down syndrome.
© 2016 Elsevier Ltd. All rights reserved.

Abbreviations: SE, summary effect; CIs, confidence intervals; PEDro, Physiotherapy Evidence Database; SORT, Strength of Recommendation Taxonomy;
1RM, one-repetition maximum.
∗ Corresponding author at: The Micheli Center for Sports Injury Prevention/Boston Children’s Hospital, 9 Hope Ave., Suite 100, Waltham, MA 02453,
United States.
E-mail address: dai.sugimoto@childrens.harvard.edu (D. Sugimoto).

http://dx.doi.org/10.1016/j.ridd.2016.04.003
0891-4222/© 2016 Elsevier Ltd. All rights reserved.
198 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198
2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
2.1. Literature search and criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
2.2. Evaluation of risk of bias in individual studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
2.3. Level of evidence and strength of recommendation assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
2.4. Data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
2.5. Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 199
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
3.1. Summaries of reviewed studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
3.1.1. Shields, Taylor, and Dodd (2008) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
3.1.2. Shields and Taylor (2010) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.1.3. Cowley et al. (2011) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.1.4. Ulrich, Burghardt, Lloyd, Tiernan, and Hornyak (2011) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.1.5. Lin and Wuang (2012) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.1.6. Shields et al. (2013) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.1.7. Eid (2015) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.2. The effect of neuromuscular training on general strength (knee extension and flexion) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.3. The effect of neuromuscular training on maximal strength (1RM of leg press and chest press) . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
3.4. The effect of neuromuscular training on functional mobility tasks (grocery shelving and timed up- and-down stairs) . . . 202
3.5. Heterogeneity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202
3.6. Evidence synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203
4.1. Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Contributor’s statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Financial disclosure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

1. Introduction

Down syndrome is one of the most common developmental disabilities. It is estimated that approximately 5500 children
with Down syndrome are born annually in the United States (United States Centers for Disease Control and Prevention,
2014). Children with Down syndrome often demonstrate deficits in muscular strength, muscular endurance, and motor skill
development (Cowley et al., 2011; Horvat, Croce, Tomporowski, & Barna, 2013; Shields & Taylor, 2010). It is theorized that
the cognitive constraints hinder the ability of the children with Down syndrome to learn and execute appropriate tasks
associated with activity of daily living and general physical exercises. Furthermore, it is challenging for children with Down
syndrome to perform an additional task simultaneously (Horvat et al., 2013), which further leads to a difficulty to adapt
in the environment (de Mello Monteiro et al., 2014). Additionally, a series of negative impacts including reduced strength,
decreased balance, and delayed reaction time on the ability to perform various tasks is reported. (Angelopoulou, Tsimaras,
Christoulas, Kokaridas, & Mandroukas, 1999; Gupta, Rao, & Sukriti, 2011; Tsimaras & Fotiadou, 2004).
Limited ability to perform activities of daily living and participation in the routine physical exercises during childhood can
potentially lead to inadequate neuromuscular development among children with Down syndrome as compared to that of
geno-typically normal children. Evaluation of general motor skill deficits in early childhood is important because established
lifestyle habits during childhood may continuously lead to their adulthood (Telama, 2009). Studies identified an association
between sedentary behaviors and poor motor skill development during early childhood (Ford, van den Bogert, Myer, Shapiro,
& Hewett, 2008; Lopes, Santos, Pereira, & Lopes, 2013; Myer et al., 2013). Additionally, it has been documented that children
with a low level of physical activities tend to develop serious health complications including obesity, cardiovascular disease,
and diabetes (Arango et al., 2014; Stephens et al., 2014). In contrast, physically active children and adolescents demonstrate
greater musculoskeletal strength, superior cardiorespiratory function, and more desirable metabolic health compared to
their inactive counterparts (Lambourne & Donnelly, 2011; Strong et al., 2005).
In order to improve deficits in motor function, neuromuscular training has been developed. Neuromuscular training
is defined as stimuli that are provided by physical exercises and aims to enhance various neuromuscular components
including muscular strength, physical coordination, and functional movements (Di Stasi, Myer, & Hewett, 2013; Filipa, Byrnes,
Paterno, Myer, & Hewett, 2010; Myer, Brent, Ford, & Hewett, 2008; Myer, Chu, Brent, & Hewett, 2008). In recent studies,
neuromuscular training is often employed for a purpose of sports-related injury prevention among physically active children
and adolescents. Several investigations demonstrated prophylactic effects of neuromuscular training on traumatic knee
injury reduction (Sadoghi, von Keudell, & Vavken, 2012; Sugimoto, Myer, Foss, & Hewett, 2014; Sugimoto, Myer, McKeon, &
Hewett, 2012). Because reduced motor abilities are reported in individuals with Down syndrome, neuromuscular training
 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206 199

may be beneficial. However, the effects of neuromuscular training on children with Down syndrome have been understudied.
A study performed by Shields et al. (2013) showed an increased in muscle mass and functional performance among children
and young adults with Down syndrome after 10 weeks of a series of exercises. However, the magnitude of increases and
parameter of measurements are diverse within the past reports, and there remains no consensus regarding the effectiveness
of neuromuscular training on motor skill development among children and young adults with Down syndrome. Therefore,
the synthesis of published data may help generating evidence of how well neuromuscular training intervention facilitates
the well-being of motor skill development among children and young adults with Down syndrome. Thus, the objective of
this study was to synthesize existing research evidence and determine effects of neuromuscular training on general strength,
maximal strength, and functional mobility tasks among children and young adults with Down syndrome. We hypothesized
that neuromuscular training would demonstrate moderate to large effects on general strength, maximal strength, and the
functional mobility task execution among children and young adults with Down syndrome.

2. Methods

2.1. Literature search and criteria

A literature search was performed using PubMed and EBSCO (CINAHL, MEDLINE and SPORTDiscus) databases, and the
search period was set from January 1, 1985 to December 31, 2015. The search was performed in January 8, 2016. The litera-
ture search was conducted by applying a combination of the following key words: ‘Down syndrome,’ ‘trisomy 21,’ ‘strength,’
‘coordination,’ ‘functional task’; “neuromuscular training,” ‘pediatric,’ and ‘adolescents.’ All literature was screened with a
step-by-step procedure; and a further cross-reference search was executed to find additional studies. The following inclu-
sionary criteria were applied: (1) included participants with Down syndrome; (2) implemented a neuromuscular training
intervention and measured outcome variables of general strength; maximum strength; and functional mobility tasks; (3)
had a group of participants whose mean ages were younger than 30 years old; (4) employed a prospective controlled design;
and (5) used means and standard deviations to express outcome variables. The prospective controlled design was defined as
a group of individuals who were classified into an experimental group and a control group over time. Studies were limited
to English language and human subject investigations. Abstracts; posters; and unpublished data were not included in the
final analysis. Irrelevant studies that dealt with different interests; topics; or variables such as heart rate; aerobic capacity;
and oxidative stress were excluded.

2.2. Evaluation of risk of bias in individual studies

The Physiotherapy Evidence Database (PEDro) scale was used to rate the quality of the methods in the included studies
(Moseley, Herbert, Sherrington, & Maher, 2002; Moseley, Sherrington, Elkins, Herbert, & Maher, 2009). The PEDro scale
consists of a total of 11 criteria, which include: (1) reporting of eligibility criteria, (2) random assignment to intervention
groups, (3) concealment of allocation, (4) similarity of relevant variables at baseline, (5) the blinding of participants, 6) the
blinding of investigators/therapists, (7) blinding of investigators measuring outcomes, 8) proportion of participants to have
key outcome measured, (9) compliance with assigned intervention, (10) reporting of between groups statistical comparisons,
and (11) reporting of point estimates and variability for key measures. When the criterion of each category was met, with
the exception of (1), one point was awarded.

2.3. Level of evidence and strength of recommendation assessment

To evaluate the quality of the current analysis, the Strength of Recommendation Taxonomy (SORT) was implemented
(Ebell et al., 2004). The SORT was designed to assess a quality of the reviewed studies and generate a rating of the evidence
using a letter grade. The following scales were used to determine the strength of the current analysis and evidence: A
(consistent evidence), B (inconsistent evidence), and C (consensus).

2.4. Data extraction

Pre-and post-testing values of general strength, maximal strength, and functional mobility tasks were extracted from
control and intervention groups of the reviewed studies. The number of study participants in each control and intervention
group was also extracted. The variables for general strength, maximal strength, and functional mobility tasks were defined
as follows. For general strength, knee extension and flexion variables were extracted. For maximal strength, one-repetition
maximum (1RM) values of leg press and chest press were used. To evaluate functional mobility performance, grocery shelving
tasks and timed up-and-down stairs were chosen because those tasks simulate real life-like maneuvers and are considered
as a representative of cognitive planning, physical mobility, and motor coordination. When the necessary information for
the analyses was not documented in the original study, an email was sent to a corresponding author of the reviewed studies,
and a request for the necessary information was sought.
200 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206

Table 1
PEDro scores of the reviewed studies.

Reviewed Studies Total Scores PEDro scale

1 2 3 4 5 6 7 8 9 10 11

Shields et al. (2008) 8 – X X X X X X X X

Shields and Taylor (2010) 8 – X X X X X X X X
Cowley et al. (2011) 4 – X X X X
Ulrich et al. (2011) 3 – X X X
Lin and Wuang (2012) 7 – X X X X X X X
Shields et al. (2013) 8 – X X X X X X X X
Eid (2015) 8 – X X X X X X X X

X “yes” score. Blank “no” score. PEDro scale is optimized for evaluation of randomized control trails, thus the PEDro assessment score for the non-randomized
control should be interpreted with caution. (1) Eligibility criteria specified, (2) random allocation of subjects, (3) allocation concealed, (4) similar groups at
baseline, (5) blinding of subjects, (6) blinding of intervention providers, (7) blinding of outcome assessors, (8) outcomes obtained from 85% of subjects, (9)
use of intent-to-treat analysis if protocol violated, (10) between group statistical comparison, (11) point measures and measures of variability.

Table 2
Summary of reviewed studies including participants, mean ages, intervention, frequency, duration, and level of evidence.

Study Participants Mean Ages† (years old) Intervention Frequency Duration Level of Evidence*

Shields et al. (2008) Intervention = 9 25.8 Strength 2 times/week 10 weeks I

Control = 11 27.6

Shields and Taylor (2010) Intervention = 11 15.9 Strength 2 times/week 10 weeks I

Control = 12 15.3

Cowley et al. (2011) Intervention = 19 29.0 Strength 2 times/week 10 weeks II

Control = 11 27.0

Ulrich et al. (2011) Intervention = 19 12.4 Balance 5 days 5 days II

Control = 27 12.0

Lin and Wuang (2012) Intervention = 46 10.6 Strength and Balance 3 times/week 6 weeks I
Control = 46 11.2

Shields et al. (2013) Intervention = 34 17.7 Strength 2 times/week 10 weeks I

Control = 34 18.2

Eid (2015) Intervention = 15 8.9 Whole-body Vibration 3 times/week 6 months I

Control = 15 9.3
*
Level of Evidence: I: Randomized controlled study design and II: Non-Randomized controlled study design.
†
Mean ages were expressed separately in intervention and control groups.

2.5. Data analysis

To analyze effects of neuromuscular training intervention on general strength, maximal strength, and functional mobility
tasks, effect size (Hedges’s g) with 95% confidence intervals (CIs) was calculated from each study. The extracted effect sizes
with 95%CIs were further analyzed through a meta-analysis to obtain a summary effect (SE). The SE of effect sizes from each
outcome variable in the general strength, maximal strength, and functional mobility tasks was classified into the following
three categories: small (0.1–0.3), moderate (0.3–0.5), and large (>0.5) (Cohen, 1992). Because studies that have a larger
sample size are more influential in a fixed-effect model, a random-effect model was chosen to minimize variability among
the included studies. I2 statistics was employed to examine if the total variation across the included studies was due to
heterogeneity, as opposed to random chance. Statistical significance level (␣ level) was set, a priori, at 0.05 for all analyses.
Analyses were performed using the comprehensive meta-analysis software (Biostat, Englewood, NJ, USA).

3. Results

Seven studies met the inclusion criteria, and Table 1 displays results of the PEDro scores of the individual study. Table 2
provides data on participant number, mean ages, intervention details, and level of evidence of the each study.

3.1. Summaries of reviewed studies

3.1.1. Shields, Taylor, and Dodd (2008)

This randomized control trial included 20 Down syndrome patients with the mean age of 26.8 years. Participants in
intervention group were asked to perform a set of six weight machine exercises twice per week for a 10-week period while
participants in control group maintained their normal activity levels. The participants in the intervention group showed
improvements in upper limb endurance compared to the participants in the control group. Lower limb performance or
 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206 201

physical function was not measured. This study concluded that resistance training can improve upper limb endurance
among adults with Down syndrome.

3.1.2. Shields and Taylor (2010)

This randomized control trial implemented a series of resistance training and assessed muscle strength among 23
teenagers with Down syndrome. Muscle strength was measured at baseline, and post-intervention, using 1RM leg press
and 1RM chest press. The exercise intervention was conducted twice a week for a period of 10 weeks and consisted of six
exercises: three for upper limb strength and three for lower limb strength (seated leg press, knee extension and calf raise).
There was a 42% increase from baseline in lower limb muscle strength in the intervention group.

3.1.3. Cowley et al. (2011)

Thirty adults with Down syndrome participated in a non-randomized control trial. Participants who were allocated
to the intervention group performed resistance training two days per week for 10 weeks. Isometric and isokinetic knee
extension and flexion strength, aerobic capacity, and timed performance on chair rise, walking and stair ascent and descent
were measured. Participants in the intervention group showed significant increases in both isometric and isokinetic knee
extension and flexion strength compared to participants in control group.

3.1.4. Ulrich, Burghardt, Lloyd, Tiernan, and Hornyak (2011)

This study included a total of 46 children and early teenagers with Down syndrome and randomly allocated them into
intervention and control groups. This trial implemented a 2-wheel bicycle riding (balance) as an intervention for a 75-min per
day for five consecutive sessions. After the intervention, participants in the intervention group resulted in a more physically
active lifestyle at the 12 month follow-up. Also, increased strength in knee extension and flexion and decreased total body
fat were observed among participants in the intervention group.

3.1.5. Lin and Wuang (2012)

Ninety-two teenagers with Down syndrome were recruited in this randomized control trial. Participants in intervention
group were asked to complete a 5-min treadmill exercise and a 20-min virtual-reality based activity three times per week
for six weeks. The Bruininks-Oseretsky Test of Motor Proficiency was used to measure balance. Strength of knee flexors and
extensors along with hip musculature (hip extensors, hip flexors, and hip abductors) were tested by a handheld dynamome-
ter. Increases in the balance score were reported among the participants in the intervention group while the decreases
were observed in the control group. Strength increases in all muscles groups were recorded among the participants in the
intervention group.

3.1.6. Shields et al. (2013)

In this randomized control trial, a total of 68 teenagers and young adults with Down syndrome were randomly assigned to
either intervention or control group. Participants in the intervention group were asked to perform a total of seven exercises
(three exercises for upper body, three exercises for lower body, and one exercise for trunk strength) two times per week for
a duration of 10 weeks. The participants in the intervention group demonstrated significantly greater muscular strength in
comparison to participants in the control group.

3.1.7. Eid (2015)

Thirty children with Down syndrome participated in this randomized control trial. Participants in the intervention group
performed a whole-body vibration training while participants in the control group had a physical therapy program, which
consisted of stretching, muscle contraction, balance and postural control. Both interventions were designed and performed
three times per week for six months. At the end of this experiment, the participants in the intervention group demonstrated
significantly greater knee extensor strength, knee flexor strength, and postural control than their baseline values, and the
participants in the control group.

3.2. The effect of neuromuscular training on general strength (knee extension and flexion)

Four studies had a record of general strength in regards to knee extension strength (Cowley et al., 2011; Eid, 2015; Lin &
Wuang, 2012; Ulrich et al., 2011). The SE of effect sizes from each reviewed study indicated a large effect of the intervention
on knee extension strength (SE: 0.52, 95%CIs: 0.31, 0.72, p = 0.01, Fig. 1). The same four studies (Cowley et al., 2011; Eid,
2015; Lin & Wuang, 2012; Ulrich et al., 2011) demonstrated a moderate effect (SE: 0.45, 95%CIs: 0.21, 0.68, p = 0.01, Fig. 2)
of the intervention on knee flexion strength.

3.3. The effect of neuromuscular training on maximal strength (1RM of leg press and chest press)

Three studies recorded maximal strength values using 1RM leg press (Shields & Taylor, 2010; Shields et al., 2008, 2013).
The SE of effect sizes showed a moderate effect of the intervention on 1 RM leg press with statistical significance (SE: 0.40,
95%CIs: 0.03, 0.78, p = 0.04, Fig. 3). However, the same three studies (Shields & Taylor, 2010; Shields et al., 2008, 2013)
202 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206

Fig. 1. Forest plot of knee extension strength.

Fig. 2. Forest plot of knee flexion strength.

Fig. 3. Forest plot of 1RM of leg press.

indicated a small, statistically non-significant effect (SE: 0.21, 95%CIs: −0.16, 0.57, p = 0.27, Fig. 4) of the intervention on 1
RM chest press.

3.4. The effect of neuromuscular training on functional mobility tasks (grocery shelving and timed up- and-down stairs)

Two studies included data of functional mobility task execution, with grocery shelving (Shields & Taylor, 2010; Shields
et al., 2008). The results showed a small, statistically non-significant effect (SE: 0.11, 95%CIs: −0.47, 0.69, p = 0.71, Fig. 5),
of the intervention on grocery shelving. The SE of effect sizes from the same two studies (Shields & Taylor, 2010; Shields
et al., 2008) demonstrated a small, statistically non-significant effect (SE: 0.25, 95%CIs: −0.34, 0.83, p = 0.41, Fig. 6), of the
intervention on timed up-and-down stairs.
 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206 203

Fig. 4. Forest plot of 1RM of chest press.

Fig. 5. Forest plot of grocery shelving.

Fig. 6. Forest plot of timed up-and-down.

3.5. Heterogeneity

The I2 statistics of all analyses, including general strength, maximal strength, and functional mobility tasks, did not
indicate a statistically significant values (knee extension strength: p = 0.51, knee flexion strength: p = 0.25, 1RM leg press:
p = 0.58, 1RM chest press: p = 0.80, grocery shelving: p = 0.97, timed up-and-down stairs: p = 0.70). Since the p-value did not
reach the a priori significance level (p < 0.05), it was concluded that heterogeneity effects were not present in the current
analysis.

3.6. Evidence synthesis

In the current analysis, five of the seven reviewed studies were rated as level I (high quality, individual randomized
control trial) while 2 studies were rated as level II (lower quality, clinical trial and cohort study) (Table 2). Because majority
of the reviewed studies were assessed as level I, the strength of recommendation grade for the current investigation was
perceived as grade A (consistent evidence). The grade A is the highest quality of evidence based on the synthesis of the
reviewed studies.

4. Discussion

The purpose of this project was to synthesize existing research evidence and investigate effects of neuromuscular training
on general strength, maximal strength, and functional mobility tasks in children and young adults with Down syndrome.
Based on synthesis of the seven reviewed studies, the current analysis demonstrated that neuromuscular training could
204 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206

be beneficial for enhancing general and maximal strength of children and young adults with Down syndrome. Compared
to general (Figs. 1 and 2) and maximal (Figs. 3 and 4) strength, effects of neuromuscular training on functional mobility
tasks were found to be small (Figs. 5 and 6). It has been theorized that executive function, which includes working memory,
problem solving, and strategic planning, is underdeveloped in individuals with Down syndrome (Horvat et al., 2013). This
deficiency in executive function likely impairs the transfer of the general and maximal strength into execution of functional
mobility tasks. In the current investigation, grocery shelving and timed up-and-down stairs were analyzed as surrogate
variables for a performance of function and mobility among children and young adults with Down syndrome. Studies that
incorporated these specific tasks aimed to make a connection with muscular strength improvement and functional mobility
task performance (Shields & Taylor, 2010; Shields et al., 2008). Although the study participants might have developed
greater general and maximal muscular strength, limited abilities in executive function such as lack of strategic planning
may have resulted in the small effect of training on functional mobility performance. Additionally, these analyses indicated
a substantial variability among the participants, which were resulted in the wide 95% CIs (Figs. 5 and 6).
Compared to functional mobility tasks, moderate to large effects were observed in general and maximal strength measures
from lower extremity. However, one measurement that did not demonstrate a statistically significant value was from an
upper body test (1RM chest press, p = 0.27). A potential explanation of the non-significant findings from upper extremity
may stem from the selection of exercises. All of the exercises incorporated in the lower extremity exercises appeared to be
directly linked to tested movements (Lin & Wuang, 2012; Ulrich et al., 2011). Conversely, upper extremity exercises seem
more focused on specific muscle groups, such as deltoids, latissimus dorsi, and upper back musculature. The test evaluated
upper body muscular power was 1 RM chest press, which is not directly related to deltoids, latissimus dorsi, and upper back
musculature groups. To perform a chest press movement, force needs to be mainly generated by pectoralis major and minor
muscles. The small effect observed in the 1RM chest press may be a result of emphasis placed on different muscle groups
during training.
Although our study population consisted of children and young adults with Down syndrome, it appeared that findings of
the current investigation are consistent with adult population with Down syndrome (Li, Chen, Meng How, & Zhang, 2013). An
investigation that synthesized 10 past studies concluded that neuromuscular training led muscular strength improvement
in adults with Down syndrome (Li et al., 2013). This investigation also reported enhancement on balance ability. We initially
intended to examine effect of neuromuscular training on balance measures. However, inconsistencies in balance outcome
measures and methods did not allow us to include several studies (Gupta et al., 2011; Jankowicz-Szymanska, Mikolajczyk, &
Wojtanowski, 2012). To summarize these excluded studies briefly, one study showed significant balance enhancement after
six weeks of neuromuscular training intervention (Gupta et al., 2011). Another study reported improvement in both static
and dynamic balance capabilities (Alentorn-Geli et al., 2014). The other study also concluded that a series of exercises led
a superior center of gravity control in single leg balance test (Jankowicz-Szymanska et al., 2012). In addition to the positive
impact on balance ability, a few studies focused on investigating physiological effects of training in individuals with Down
syndrome. A study reported lean body mass increases among adolescents with Down syndrome following neuromuscular
training (Gonzalez-Aguero et al., 2011). Furthermore, increased oxygen consumption was reported in individuals with Down
syndrome after cardiovascular training (Rimmer, Heller, Wang, & Valerio, 2004; Varela, Sardinha, & Pitetti, 2001).

4.1. Limitations

Our findings must be shared in light of several limitations. First, there was a wide range of variability in outcome mea-
sures, specifically balance measurements (Alentorn-Geli et al., 2014; Gupta et al., 2011; Jankowicz-Szymanska et al., 2012).
Additionally, inclusion criteria that were developed prior to literature search might have been too strict. A combination of
the two factors likely led to a low number of reviewed studies. Also, participants’ ages among the reviewed studies were
diverse, ranging from under 10 years to late twenties (Table 2). A past study indicated that neuromuscular training is more
effective in preventing injuries in athletes before puberty as opposed to post-pubertal stages (Myer, Sugimoto, Thomas, &
Hewett, 2012). Therefore, future studies are warranted to investigate the effect of neuromuscular training in specific devel-
opmental stages of pediatric and young children with Down syndrome. Lastly, findings of this investigation do not ensure
a long-term effect of the neuromuscular training even though strength of recommendation of the SORT classification rated
the current investigation as the highest level of evidence. In this light, prospective longitudinal cohort studies are needed.

5. Conclusions

Within the limited number of studies available for reviews, neuromuscular training could be considered as an effective
intervention to promote general and maximal muscular strength enhancement in children and young adults with Down
syndrome. A small effect was obtained in functional mobility tasks, which likely stem from a combination of constraints of
brain function and a wide variability within the study participants. Conducting further randomized controlled trials with
specific strength, balance, and functional performance measurements is warranted in order to develop an effective exercise
prescription for children, young adults, and adults with Down syndrome. Improvement in motor proficiency likely helps
individuals with Down syndrome to engage with greater physical adaptation, which further leads them to participate in
 D. Sugimoto et al. / Research in Developmental Disabilities 55 (2016) 197–206 205

a more physically active lifestyle. The more physically active lifestyle may bring a better quality of life in individuals with
Down syndrome.

Conflict of interest

All authors have no conflict of interest to disclose. W.P.M. receives royalties from ABC-Clio publishing for the sale of his
book, Kids, Sports, and Concussion: A guide for coaches and parents, from Springer International for the book Head and Neck
Injuries in Young Athlete and royalties from Wolters Kluwer for working as an author for UpToDate. He is under contract
with ABC-Clio publishing for a future book entitled, Concussions. His research is funded, in part, by a grant from the National
Football League Players Association and by philanthropic support from the National Hockey League Alumni Association
through the Corey C. Griffin Pro-Am Tournament.

Funding source

No honorarium, grant, or other form of payment was given to anyone to produce this manuscript.

Contributor’s statement

Dai Sugimoto: Designed the study, analyzed the data, and contributed to write initial draft* and revised the manuscript
draft.
Samantha L. Bowen: Reviewed all of the literature, collected the data, and revised the manuscript draft.
William P. Meehan III: Provided valuable input and critically reviewed the manuscript.
Andrea Stracciolini: Conceptualized the study, delivered directional guidance, and contributed to the writing and critical
review of the manuscript.
All of the named authors approved the final manuscript as submitted, and agree to be accountable for all aspects of the
work.

Financial disclosure

All authors have no financial relationships relevant to this study to disclose.

Acknowledgement

There is no endorsement or funding source from any organizations.

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