Research in Developmental Disabilities 67 (2017) 1–8

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Research in Developmental Disabilities

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The motor repertoire in 3- to 5-month old infants with Down MARK

syndrome
⁎
Dafne Herreroa,1, Christa Einspielerb, ,2, Carolina Y. Panvequio Aizawac,
Akmer Mutlud, Hong Yange, Alice Nogolováf, Jasmin Pansyg, Karin Nielsen-Sainesh,
Peter B. Marschikb,i, GenGM Study Group
a
School of Public Health, University of São Paulo, São Paulo, Brazil
b
Research Unit iDN, Interdisciplinary Developmental Neuroscience, Department of Phoniatrics, Medical University of Graz, Graz, Austria
c
Department of Physical Therapy, Communication Science & Disorders and Occupational Therapy, School of Medicine, University of São Paulo, São
Paulo, Brazil
d
Developmental and Early Physiotherapy Unit, Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Hacettepe University,
Ankara, Turkey
e
Rehabilitation Department, Children’s Hospital of Fudan University, Shanghai, China
f
Children’s Department, City Hospital of Ostrava, Ostrava, Czech Republic
g
Division of Neonatology, Department of Pediatrics and Adolescent Medicine, Medical University of Graz, Graz, Austria
h
Division of Infectious Diseases, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
i
Center of Neurodevelopmental Disorders (KIND), Department of Women’s and Children’s Health, Karolinska Institutet, Stockholm, Sweden

AR TI CLE I NF O AB S T R A CT

Keywords: Background: Even though Down syndrome is the most common chromosomal cause of in-
Down syndrome tellectual disability, studies on early development are scarce.
Fidgety movements Aim: To describe movements and postures in 3- to 5-month-old infants with Down syndrome and
General movements assess the relation between pre- and perinatal risk factors and the eventual motor performance.
Infant
Methods and procedures: Exploratory study; 47 infants with Down syndrome (26 males, 27 infants
Motor optimality score
born preterm, 22 infants with congenital heart disease) were videoed at 10–19 weeks post-term
(median = 14 weeks). We assessed their Motor Optimality Score (MOS) based on postures and
movements (including fidgety movements) and compared it to that of 47 infants later diagnosed
with cerebral palsy and 47 infants with a normal neurological outcome, matched for gestational
and recording ages.
Outcomes and results: The MOS (median = 13, range 10–28) was significantly lower than in
infants with a normal neurological outcome (median = 26), but higher than in infants later di-
agnosed with cerebral palsy (median = 6). Fourteen infants with Down syndrome showed
normal fidgety movements, 13 no fidgety movements, and 20 exaggerated, too fast or too slow
fidgety movements. A lack of movements to the midline and several atypical postures were ob-
served. Neither preterm birth nor congenital heart disease was related to aberrant fidgety
movements or reduced MOS.
Conclusions and implications: The heterogeneity in fidgety movements and MOS add to an un-
derstanding of the large variability of the early phenotype of Down syndrome. Studies on the
predictive values of the early spontaneous motor repertoire, especially for the cognitive outcome,
are warranted.
What this paper adds: The significance of this exploratory study lies in its minute description of

⁎
Corresponding author at: Department of Phoniatrics, Medical University of Graz, Auenbruggerplatz 26, 8036 Graz, Austria.
E-mail address: [email protected] (C. Einspieler).
1
These authors contributed equally to this work.
2
See Appendix A for name of the authors of GenGM Study Group.

http://dx.doi.org/10.1016/j.ridd.2017.05.006
Received 18 January 2017; Received in revised form 21 April 2017; Accepted 21 May 2017
Available online 03 June 2017
0891-4222/ © 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
D. Herrero et al. Research in Developmental Disabilities 67 (2017) 1–8

the motor repertoire of infants with Down syndrome aged 3–5 months. Thirty percent of infants
with Down syndrome showed age-specific normal fidgety movements. The rate of abnormal
fidgety movements (large amplitude, high/slow speed) or a lack of fidgety movements was ex-
ceedingly high. The motor optimality score of infants with Down syndrome was lower than in
infants with normal neurological outcome but higher than in infants who were later diagnosed
with cerebral palsy. Neither preterm birth nor congenital heart disease were related to the motor
performance at 3–5 months.

1. Introduction

Even though Down syndrome is the most common chromosomal cause of intellectual disability, with 20–22 individuals per
10,000 births affected (e.g., Kurtovic-Kozaric et al., 2016; Loane et al., 2013), studies on early development are scarce. Infants with
Down syndrome are known to be socially competent but show a delay in the acquisition of motor milestones and deficits in early
gesture production (Grieco, Pulsifer, Seligsohn, Skotko, & Schwartz, 2015; Özcaliskan, Adamson, Dimitrova, Bailey, & Schmuck,
2016; Saito & Watanabe, 2016). As early as the first months of life they scored lower than typically developing infants on both the
Test of Infant Motor Performance (Cardoso, Campos, Santos, Santos, & Rocha, 2015) and the Alberta Infant Motor Scale (Tudella,
Pereira, Pedrolongo Basso, & Savelsbergh, 2011). They kicked less often (Ulrich & Ulrich, 1995) and their arm movements were less
accurate when reaching for objects of different sizes (de Campos, Cerra, Silva, & Rocha, 2014). Repeated assessments of their
spontaneous general movements revealed a heterogeneous movement quality, although the fluency and complexity tended to im-
prove between 1 and 6 months of age (Mazzone, Mugno, & Mazzone, 2004).
Initially designed for infants with acquired brain injuries, the Prechtl assessment of general movements (Einspieler & Prechtl,
2005; Prechtl et al., 1997) has recently also been applied to infants with genetic syndromes (Einspieler, Hirota, Yuge,
Deijima, & Marschik, 2012; Einspieler, Kerr, & Prechtl, 2005; Einspieler et al., 2014; Marschik, Soloveichick,
Windpassinger, & Einspieler, 2015; Mazzone et al., 2004) and infants later diagnosed with autism spectrum disorders (Einspieler
et al., 2014; Zappella et al., 2015). The assessment is based on visual Gestalt perception of normal vs. abnormal movements in the
entire body (i.e. general movements). It is applied in foetuses, preterm infants, and newborn infants from term to 5 months post-term
(Einspieler, Prechtl, Bos, Ferrari, & Cioni, 2004; Prechtl & Einspieler, 1997). The excellent predictive power of general movement
assessments (Bosanquet, Copeland, Ware, & Boyd, 2013; Einspieler et al., 2004) is mainly attributable to fidgety general movements,
which occur from 3 to 5 months post-term age (Einspieler & Prechtl, 2005; Prechtl et al., 1997). Infants with normal fidgety
movements are very likely to develop normally in neurological terms, whereas infants who never develop fidgety movements have a
high risk for neurological impairment (Einspieler & Prechtl, 2005; Prechtl et al., 1997). Adding a detailed assessment of concurrent
movements and postures to the assessment of fidgety movements, for example, showed a reduced motor optimality score (MOS) to be
associated with a limited activity in children who were later diagnosed with cerebral palsy (Yang et al., 2012), or with lower
intelligent quotients during school age (Butcher et al., 2009). We therefore assumed that determining the MOS (Einspieler et al.,
2004, p. 26) by assessing fidgety movements as well as concurrent movement and postural patterns would enable us to systematically

Table 1
Clinical characteristics of 47 infants with Down syndrome.

Median, Interquartile (P25, P75) and Range; or N (%)

Maternal age Median = 35 years

P25 = 31 years; P75 = 39 years; range: 17–45 years
Paternal age Median = 37 years
P25 = 32 years; P75 = 42 years; range: 23–50 years
Parity Median = 2
P25 = 1; P75 = 3; range: 1–5
Pregnancy complications 22 (47%)
Preterm birth 27 (57%)
Caesarean section 31 (66%)
Birth weight Median = 2585 g
P25 = 2000 g; P75 = 2980 g; range: 1400–3680 g
Apgar Score at 1 min Median = 8
P25 = 7; P75 = 8; range: 6–10
Apgar Score at 5 min Median = 9
P25 = 8; P75 = 9; range: 8–10
Hyperbilirubinaemia 26 (55%)
CHD: (Atrio)ventricular septal defects and/or patent ductus arteriosus 22 (47%)
Duration of mechanical ventilation Median = 0 days
P25 = 0 days; P75 = 3 days; range: 0–19 days
Age at discharge from the hospital Median = 12 days
P25 = 4 days; P75 = 30 days; range: 3–90 days

Key: CHD, congenital heart disease.

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document the motor repertoire of infants with Down syndrome. The MOS makes it possible to quantitatively relate pre- and perinatal
data to the motor repertoire of an infant and to data obtained from follow-up studies.
The aims of our study were (1) to describe movements and postures in 3- to 5-month-old infants with Down syndrome; (2) to
compare their MOS with the MOS of two matched samples, one of which was later diagnosed with cerebral palsy, while the other had
a normal neurological outcome; and (3) to analyse to what extent clinical risk factors during pregnancy, at delivery, and during the
neonatal period were related to the motor performance in 3- to 5-month-old infants with Down syndrome.

2. Methods

2.1. Participants

This exploratory study comprised a convenience sample of 47 infants with Down syndrome − 21 females (45%) and 26 males
(55%) − who had been admitted to (a) the Darcy Vargas Public Hospital, São Paulo (17 individuals); (b) the Department of
Physiotherapy and Rehabilitation at the Hacettepe University in Ankara (ten individuals); (c) the Associação de Pais e Amigos dos
Excepcionais at São Paulo University (seven individuals); (d) the Rehabilitation Department of the Children’s Hospital of Fudan
University in Shanghai (four individuals); (e) the Children’s Department at the City Hospital of Ostrava (three individuals); (f) the
Clinic of Early Intervention at the University Hospital São Paolo (three individuals); and (g) the Medical University of Graz (three
individuals) between June 2015 and May 2016. In order for the infants to be included in the study, the infants’ motor performance
had to be recorded between 9 and 20 weeks post-term. The infants’ gestational ages at birth ranged from 29 to 41 weeks
(median = 37 weeks), with a birth weight range of 1440 g to 3680 g (median = 2585 g). Twenty-seven infants were born preterm
(57%), including two monozygotic twin pairs. Other clinical characteristics obtained from the medical histories are presented in
Table 1. Three infants were diagnosed with mosaic Down syndrome, one with Robertsonian translocation (14;21).
For comparison we used data of our international, MOS-based data bank (N = 365 as of January 15, 2017), picking (i) 47
individuals with a normal neurological outcome at 3–5 years of age, whose gestational age and age of video recording matched our
study cases; and (ii) 47 individuals with a comparable gestational age at birth and post-term age at the time of the video recording

Table 2
The motor optimality score (MOS) and its subcategories in 47 infants diagnosed with Down syndrome, 47 infants diagnosed with cerebral palsy, and 47 infants with a
normal neurological outcome at 3 to 5 years of age.

Down Syndrome (DS) Cerebral Palsy (CP) Normal Neurological Outcome (N) p-values

Preterm birth 27 (57.4%) 27 (57.4%) 27 (57.4%)

Recording age
9–12 weeks 12 (25.5%) 16 (34%) 12 (25.5%)
13–16 weeks 30 (64%) 24 (51%) 30 (64%)
17–20 weeks 5 (10.5%) 7 (15%) 5 (10.5%)
MOS Median = 13 Median = 6 Median = 26 DS vs. CP
P25 = 12 P25 = 6 P25 = 21 p < 0.01a
P75 = 23 P75 = 8 P75 = 28 DS vs. N
Range: 10–28 Range: 5–20 Range: 10–28 p < 0.01a
Fidgety movements DS vs. CP
Normal 14 (30%) 1 (2%) 44 (93.5%) p < 0.01b
Abnormalx 20 (42.5%) 0 (0%) 0 (0%) DS vs. N
Absent 13 (27.5%) 46 (98%) 3 (6.5%) p < 0.01b
Repertoire DS vs. CP
Age-adequate 12 (25.5%) 0 (0%) 27 (57.5%) p < 0.01b
Reduced 20 (42.5%) 4 (8.5%) 15 (32%) DS vs. N
Not age-adequate 15 (32%) 43 (91.5%) 5 (10.5%) p < 0.01b
Movements DS vs. CP
N > A 39 (83%) 6 (12.5%) 36 (76.5%) p < 0.01b
N=A 5 (10.5%) 11 (23.5%) 8 (17%) DS vs. N
N < A 3 (6.5%) 30 (64%) 3 (6.5%) p = 0.67b
Posture DS vs. CP
N > A 22 (47%) 8 (17%) 31 (66%) p < 0.01b
N=A 10 (21%) 5 (10.5%) 6 (13%) DS vs. N
N < A 15 (32%) 34 (72.5%) 10 (21%) p = 0.17b
Movement character DS vs. N
Smooth, fluent 3 (6.5%) 0 (0%) 19 (40.5%) p < 0.01b
Abnormal, not CS 44 (93.5%) 34 (72%) 28 (59.5%) DS vs. CP
CS 0 (0%) 13 (28%) 0 (0%) p < 0.01b

Key: N > A, more normal than abnormal patterns; N = A, an equal number of normal and abnormal patterns; N < A, fewer normal than abnormal patterns; CS,
cramped-synchronised movement character, i.e. spontaneous general movements appear stiff; limb and trunk muscles contract almost simultaneously and then relax
almost simultaneously (Einspieler et al., 2004).
a
Mann-Whitney-U test.
b
Pearson Chi-square test.
x
this category also includes infants with fidgety-like movements (large amplitude, slow).

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who were diagnosed with cerebral palsy at 3–5 years of age (Table 2). Since spontaneous (i.e. endogenously generated) movements
are not related to ethnicity (Luxwolda et al., 2014), we did not match the ethnic background.
All parents gave their written informed consent. The ethical review boards of the various centres approved the study.

2.2. Recording and evaluation of movements and postures at 3–5 months post-term age

Within the GenGM network we recorded 5-min videos of the spontaneous motility of each infant at a median post-term age of 14
weeks (P25 = 12 weeks; P75 = 15 weeks; range: 10–19 weeks). The recordings were performed during periods of active wakefulness
between feedings, with the infant partly dressed, lying in supine position (Einspieler et al., 2004). The videos were evaluated by at
least two certified raters (D.H., C.E., A.M., A.N., J.P., P.B.M.) according to the Prechtl method of global and detailed general
movement assessment (Einspieler et al., 2004 Einspieler & Prechtl, 2005). Scorers C.E. and P.B.M. were not familiar with the details of
the participants’ clinical histories apart from the fact that they had Down syndrome. In case of disagreement (four recordings; 8.5%),
the raters re-evaluated the recordings until consensus was reached on a final score.
Fidgety movements and the concurrent repertoire of movements and postures were assessed independently in separate runs of the
video recordings. Using the score sheet for the assessment of motor repertoire at 3–5 months (Einspieler et al., 2004, p. 26), we
calculated the MOS, with a maximum value of 28 (for the best possible performance) and a minimum value of 5. The score sheet
comprises the following five sub-categories: (i) fidgety movements, (ii) age-adequacy of motor repertoire, (iii) quality of movement
patterns other than fidgety movements, (iv) posture, and (v) overall quality of the motor repertoire (Einspieler et al., 2004; Yuge
et al., 2011). Fjørtoft and colleagues found a high inter-observer reliability for the MOS with intra-class correlation coefficients
ranging from 0.80 to 0.94 (Fjørtoft, Einspieler, Adde, & Strand, 2009).

2.3. Statistical analysis

Statistical analysis was performed using the SPSS package for Windows, version 23.0 (SPSS Inc., Chicago, IL). The Pearson Chi-
square test was used to evaluate associations between nominal data. To put the medians of non-normally distributed continuous data
(e.g. motor optimality score) in relation to nominal data (e.g. preterm birth), we applied the Mann-Whitney-U test or, if there were
more than two categories, the Kruskal-Wallis test (e.g. repertoire). To assess the relative strength of the association between variables,
we computed the following correlation coefficients: Cramer’s V coefficient was applied when at least one of the two variables was
nominal (e.g. preterm birth and age-adequacy of the repertoire). To assess the relation between two continuous variables (e.g.
gestational age and motor optimality score), we applied the Pearson product-moment correlation coefficient. Throughout the ana-
lyses, p < 0.05 (two-tailed) was considered to be statistically significant.

3. Results

3.1. The motor performance of infants with Down syndrome at 3–5 months postterm age (Table 2, first column)

Fourteen infants had normal fidgety movements (30%); six infants (12.5%) displayed abnormal fidgety movements (i.e. they look
like normal ones though with a greater amplitude, speed and jerkiness); 13 infants (27.5%) displayed no fidgety movements, which
were therefore classified as absent; 14 infants (30%) showed fidgety-like movements whose amplitude was too great and whose pace
was too slow. Abnormal and absent fidgety movements as well as fidgety-like movements were grouped as aberrant fidgety move-
ments (33 infants; 70%).
Twelve infants (25.5%) displayed an age-adequate movement repertoire. The repertoire was found to be reduced in 20 infants
(42.5%; mainly due to a lack of movements to the midline), and age-inadequate in 15 infants (32%).
The quality of the various movement patterns (other than fidgety movements) was scored as predominantly normal in 39 infants
(83%) and predominantly abnormal in three infants (6.5%); five infants (10.5%) showed an equal number of normal and abnormal
movements. On average the infants demonstrated three normal movement patterns (range: 0–8) and one abnormal movement pattern
(range: 0–3). The most frequent normal movement patterns included visual scanning (32/47; 68%), side-to-side movements of the
head (22/47; 47%), foot-to-foot contact (14/47; 30%), hand-to-mouth contact (12/47; 25.5%), and kicking (10/47; 21%). Smiling
(9/47; 19%), fiddling (9/47; 19%), hand regards (8/47; 17%), swipes (7/47; 15%), hand-to-hand contact (6/47; 13%), arching (6/
47; 13%), and leg lifting (5/47; 11%) were observed in fewer than ten individuals. Other movement patterns such as wiggling-
oscillating arm movements, hand-to-knee contact, or rolling to the side were observed in fewer than five individuals (< 10%). The
most frequent abnormal movement pattern was long-lasting and/or repetitive tongue protrusion (26/47; 55%). In a few infants we
observed hand-to-hand contact with no mutual manipulation (4/47; 8.5%), long lasting wiggling-oscillating arm movements (3/47;
6%), repetitive kicking (3/47; 6%), and monotonous side-to-side movements of the head (1/47; 2%).
Posture was rated as predominantly normal in 22 infants (47%) and predominantly abnormal in 15 infants (32%); ten infants
(21%) showed an equal number of normal and abnormal postures (Table 2). Infants with predominantly normal postural patterns
were able to hold their head in midline (31/47; 66%), showed a symmetrical body posture (25/47; 53%) and variable finger postures
(23/47; 49%); a persistent asymmetric tonic neck response was absent in all individuals. On average the infants demonstrated three
normal postural patterns (range: 1–4) and two abnormal postural patterns (range: 0–7). The most common abnormal pattern was a
lack of variable finger postures (24/47; 51%) with just a few monotonous finger postures, finger spreading and/or predominant
fisting. Twelve infants (25.5%) kept both arms predominantly extended, while seven infants (15%) kept their legs extended most of

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the time. Hyperextension of the neck and trunk was seen in three individuals (6.5%). The following two postural atypicalities were
observed, but are not captured by the MOS sheet: nine individuals (19%) showed an internal rotation and pronation of one or both
wrists, and 22 infants (47%) showed an external rotation and abduction of the hips (which was also the reason why most of them
were unable to show foot-to-foot contact).
Only three infants (6.5%) exhibited a normal, smooth and fluent overall movement character, while 44 infants (93.5%) displayed
a monotonous, stiff, jerky and/or tremulous movement character.
The median MOS was 13 (P25 = 12; P75 = 23; range: 10–28).

3.2. The MOS of infants with Down syndrome compared to infants later diagnosed with cerebral palsy and infants with a normal neurological
outcome (Table 2)

The MOS of infants with Down syndrome was significantly lower than that of infants with a normal neurological outcome
(p < 0.01) but significantly higher than that of infants later diagnosed with cerebral palsy (p < 0.01). Similar results were obtained
for fidgety movements, the age-adequacy of the motor repertoire, and the overall movement character (p-values < 0.01). The
quality of movement and postural patterns of infants with Down syndrome were similar to those of infants with a normal neurological
outcome (p-values > 0.10), while infants later diagnosed with cerebral palsy scored lower (p-values < 0.01; Table 2).

3.3. The neonatal period and its relation to the motor performance at 3–5 months post-term age (Table 3 and 4)

None of the clinical characteristics was related to the MOS or fidgety movements. Preterm birth was not associated with the MOS
or its subcategories (Table 3), nor was any other clinical variable. We would particularly like to mention that congenital heart disease
(CHD) was not related to the motor performance at 3–5 months. Cranial ultrasound data were only available for a small proportion of
the sample (eight infants, 17%). Two infants with abnormal cranial ultrasound findings had abnormal fidgety-like movements.
Among the six infants with normal cranial ultrasound findings three showed normal fidgety movements, one infant did not develop
fidgety movements, and two infants had slow abnormal fidgety-like movements ().
Table 4 only lists significant associations between clinical variables and items of the MOS. A jerky movement character (observed
in 26/47 infants; 55%) was associated with caesarean section and hyperbilirubinaemia, although the two clinical variables were not
related to each other (Pearson Chi-square test, p = 0.58). Delivery by caesarean section was also related to a higher occurrence of a
particular atypical posture at 3–5 months: in many cases external rotation and abduction of the hips led to a lack of (especially lower
limb) movements to the midline.
No difference was observed between twins and singletons (Fisher sign test, p > 0.05). Neither the three infants with mosaic
Down syndrome (two with absent fidgety movements, one with normal fidgety movements; MOS = 10, 12 and 24, respectively) nor
the one with Robertsonian translocation (normal fidgety movements, MOS = 23) showed any sort of specific features in their motor
performance at 3–5 months post term.

Table 3
The motor optimality score (MOS) and its subcategories in 47 infants diagnosed with Down syndrome according to preterm or term birth.

Preterm Born Term Born p-values

n = 27 n = 20

MOS Median = 13 Median = 13 p = 0.71a

P25 = 12 P25 = 12
P75 = 24 P75 = 16
Range: 10–26 Range: 10–28
Fidgety movements 10 (37%) 4 (20%) p = 0.65b
Normal 10 (37%) 10 (50%)
Abnormalx 7 (26%) 6 (30%)
Absent
Repertoire 4 (15%) 8 (40%) 8 (40%) 4 (20%) p = 0.11b
Age-adequate 12 (44%)
Reduced 11 (41%)
Not age-adequate
Movements 22 (81.5%) 17 (85%) p = 0.41b
N > A 4 (15%) 1 (5%)
N=A 1 (3.5%) 2 (10%)
N < A
Posture 14 (52%) 8 (40%) 3 (15%) p = 0.24b
N > A 7 (26%) 6 (22%) 9 (45%)
N=A
N < A
Movement character 2 (7.5%) 1 (5%) p = 0.56b
Smooth, fluent 25 (92.5%) 19 (95%)
Abnormal, not CS

Key: as in Table 2.

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Table 4
Significant associations between clinical characteristics and specific motor patterns in 47 3- to
5-month-old infants with Down syndrome.

Caesarean section Jerky movement character

Cramer’s V = 0.32; p < 0.05
External rotation and abduction of hips
Cramer’s V = 0.34; p < 0.05
Hyperbilirubinaemia Jerky movement character
Cramer’s V = 0.30; p < 0.05

a
Key: Mann-Whitney-U test.

4. Discussion

Apart from one individual reported in the context of a larger sample of high-risk infants in Japan (Yuge et al., 2011), this is the
first study to use the MOS to describe fidgety movements and the concurrent motor repertoire in infants with Down syndrome.
Mazzone et al. (2004) applied the detailed scoring for writhing general movements (observable from birth to 1–2 months post-term)
up to the age of 6 months rather than for fidgety and concurrent motor patterns, which occur from 3 months onwards.
The motor coordination and performance of children, adolescents and adults with Down syndrome has been found to be highly
heterogeneous (Latash, 2007). Interestingly, we already observed this heterogeneity at a much younger age: 30% of our 3- to 5-
month-old infants with Down syndrome showed normal fidgety movements, 27.5% had no fidgety movements, and 42.5% showed
abnormal fidgety movements. These highly diverse findings are reflected in the MOS, which range from 10 to the highest possible
score of 28. Fifty percent of the infants scored between 10 and 13, which is significantly lower than infants with a normal neuro-
logical outcome and higher than infants who were later diagnosed with cerebral palsy. So far, two studies carried out in children with
cerebral palsy in China, Italy, and the Netherlands demonstrated the lower the MOS at 3–5 months, the more severely limited their
gross motor function (Bruggink et al., 2009; Yang et al., 2012). As we intend to monitor our sample of children with Down syndrome
for at least 2 more years, we shall also assess the relation between the MOS and the motor, cognitive and language outcomes.
The one infant with Down syndrome described by Yuge et al. (2011) displayed abnormal fidgety movements and an MOS of 13.
Abnormal fidgety movements, exaggerated in amplitude, speed and jerkiness, were also observed in six infants in the present study.
This is an exceptionally high rate of occurrence, as abnormal fidgety movements are usually rare (see also Table 2). It has been a
matter of debate whether or not infants with a low muscle tone are more likely to show abnormal fidgety movements (Einspieler,
Peharz, & Marschik, 2016; Yuge et al., 2011). Although this may not be consentaneously defined, a low muscle tone is a general
feature in infants with Down syndrome (Latash, 2007; Morris, Vaughan, & Vaccaro, 1982). A number of studies have documented an
association between abnormal fidgety movements and coordination difficulties and/or disabilities in fine manipulative skills at
school age (Einspieler et al., 2007; Einspieler et al., 2016); others describe an exceedingly high rate of abnormal fidgety movements in
infants who were later diagnosed with autism spectrum disorders or Rett syndrome (Einspieler et al., 2005; Einspieler et al., 2014).
However, most so-called abnormal fidgety movements in infants later diagnosed with autism spectrum disorders or Rett syndrome
did not correspond with the category of abnormal fidgety movements described in infants with brain injuries, which were ex-
aggerated in amplitude and speed (Einspieler & Prechtl, 2005; Einspieler et al., 2016; Prechtl et al., 1997). Several infants with a later
diagnosis of autism spectrum disorders or Rett syndrome showed continual fidgety activity which was exaggerated in amplitude but
too slow (Einspieler et al., 2005; Einspieler et al., 2014; Zappella et al., 2015). We also observed this pattern in 14/47 (30%) infants
with Down syndrome (see the abnormal fidgety movements’ category in Table 2). It remains unclear whether this pattern is related to
low muscle tone, another early atypicality in autism spectrum disorders (Flanagan, Landa, Bhat, & Bauman, 2012) and Rett syndrome
(Nomura & Segawa, 1990), as video analysis does not allow for an assessment of active muscle strength or resistance to passive
movements. Data on neurological examinations were not available in 44 of 47 individuals. In any case, the low rate of movements to
the midline (i.e., foot-to-foot contact in 30% and hand-to-hand contact in only 13% of our sample) and the lack of kicking (21%) are
in line with previous studies, where they have also been discussed as possible consequences of low muscle tone (Tudella et al., 2011).
The same is true of the frequent external rotation and abduction of the hip (observed in 47% of infants with Down syndrome) as well
as the uni- or bilateral internal rotation and pronation of the wrist(s) (19%). Unfortunately we are unable to confirm this association
for lack of information about our infants’ muscle tone (see section 4.1.).
Several research groups have reported a significant impact of pre- and perinatal variables on the MOS at 3–5 months. For
example, prenatal exposure to environmental pollutants or selective serotonin reuptake inhibitors, and perinatal hypoxic events
resulted in a reduced MOS (Berghuis, Soechitram, Hitzert, Sauer, & Bos, 2013; de Vries, van der Veere, Reijneveld, & Bos, 2013; Yuge
et al., 2011). No such association was established in our study. Neither gestational age nor birth weight or any other perinatal risk
factor was found to be significantly related to the MOS or fidgety movements, notwithstanding the fact that 27 infants (57%) were
born preterm. Nor was the percentage of aberrant fidgety movements and/or a lower MOS increased in the 22 infants with CHD,
although toddlers with Down syndrome and CHD were reported to have a higher percentage of motor, language and cognitive deficits
at 12–14 months than toddlers with Down syndrome and a normal heart structure (Alsaied et al., 2016; Visootsak et al., 2016). In our
study, neither aberrant fidgety movements nor a reduced MOS were attributable to preterm birth or CHD.
Only two variables were shown to affect movements and postures at 3–5 months: caesarean section and hyperbilirubinaemia were
related to a jerky movement character, and external rotation and abduction of hips was more common among infants born by

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D. Herrero et al. Research in Developmental Disabilities 67 (2017) 1–8

caesarean section. In their study on healthy full-term infants during the first week after birth, Ploegstra, Bos, and de Vries (2014)
compared the general movements of low-risk neonates born by vaginal delivery with those of neonates after caesarean section and
found no difference. So far, we cannot explain how external rotation and abduction of the hips is related to caesarean section. As for
the jerky movement character, there have no doubt been more revealing findings: Groen, de Blécourt, Postema, and Hadders-Algra
(2005) reported 11 out of 15 children to have shown a normal neurological outcome in spite of jerky movements at the age of 2–4
months.

4.1. Limitations to our study

As various motor patterns such as abnormal fidgety or fidgety-like movements, lack of movements to the midline, and external
rotation and abduction of the hips could be attributed to low muscle tone, we would also have needed to assess the infants’ muscle
tone. Yet, the assessment of muscle tone is anything but unequivocal. Definitions are not standardised and inter-scorer agreement is
prone to be low (Latash, 2007; Prechtl, 2001; Touwen, 1976) except for extremes. Diverging experience and procedures in the tonus
assessment would no doubt have been additional challenges in a multicentre approach. Training and application of the Hammersmith
Infant Neurological Examination (Haataja et al., 1999) was not available in most of the centres contributing to the study.
This being a comparative study, one might consider our participants’ varied ethnic backgrounds as problematic. However, as we
are dealing with spontaneous, i.e. endogenously generated movements, the respective care-giving practices are very unlikely to have
had an impact on the early motor patterns in question. In fact, general movements have been assessed worldwide for more than 20
years with similar cross-cultural results (e.g., Bruggink et al., 2009; Luxwolda et al., 2014; Yang et al., 2012; Yuge et al., 2011). Nor
did the various sensory stimulations affect the infants’ fidgety movements, which demonstrates their robust, environment-in-
dependent character (Dibiasi & Einspieler, 2002; Dibiasi & Einspieler, 2004).
Of course, the infants’ different cultural backgrounds could be an issue with regard to the subcategory “posture”. Infants raised in
a hammock, for example, seem to be faster in acquiring the “head in midline” position and/or a “symmetric body posture” (D.H. and
C.E., personal observations), but none of our participants had experienced such exceptional practices, and this goes for all three
groups.

5. Conclusion

The significance of this exploratory study lies in its minute description of the motor repertoire of infants with Down syndrome
aged 3–5 months. During this time window, fidgety movements are the predominant spontaneous movement pattern and an excellent
marker for the neurological outcome (Bosanquet et al., 2013; Einspieler et al., 2004; Einspieler et al., 2016). Infants with Down
syndrome already show motor impairments at this early age, as evidenced by a significantly low MOS. Reassessing the same children
as toddlers will show whether the high predictive power of fidgety movements found in infants with and without acquired brain
injury (Bosanquet et al., 2013; Einspieler & Prechtl, 2005; Einspieler et al., 2004; Prechtl et al., 1997) also holds true for infants with a
genetic disorder. A particularly important aspect will be whether the early spontaneous motor repertoire will also assist to predict the
cognitive development of individuals with Down syndrome. A particularly important aspect that needs to be studied is the predictive
power of the early spontaneous motor repertoire for the cognitive development of individuals with Down syndrome. But quite apart
from this important aspect for clinicians and researchers, atypical postural features such as external rotation and abduction of the
hips and/or internal rotation and pronation of the wrists call for earlier intervention.

Acknowledgements

The authors are grateful to all families who contributed to this study. Some members of the GenGM study group were funded by
the Bill and Melinda Gates foundation (Project OPP112887). We would also like to thank Miha Tavcar (scriptophil) for proofreading
the paper.

Appendix A

GenGM Study Group: Fernanda F. Genovesi (São Paulo), Renata Hydee Hasue (São Paulo), Magdalena Krieber (Graz), Zan
Mustacchi (São Paulo), Anna Scheuchenegger (Graz), Xiu-shu Shen (Shanghai), Iris Tomantschger (Graz), Berndt Urlesberger (Graz),
Bilge N. Yardımcı (Ankara), Dajie Zhang (Graz).

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