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Physiotherapy Theory and Practice

An International Journal of Physical Therapy

ISSN: 0959-3985 (Print) 1532-5040 (Online) Journal homepage: https://www.tandfonline.com/loi/iptp20

Characteristics of general movements in preterm


infants assessed by computer-based video
analysis

Lars Adde, Hong Yang, Rannei Sæther, Alexander Refsum Jensenius, Espen
Ihlen, Jia-yan Cao & Ragnhild Støen

To cite this article: Lars Adde, Hong Yang, Rannei Sæther, Alexander Refsum Jensenius, Espen
Ihlen, Jia-yan Cao & Ragnhild Støen (2018) Characteristics of general movements in preterm
infants assessed by computer-based video analysis, Physiotherapy Theory and Practice, 34:4,
286-292, DOI: 10.1080/09593985.2017.1391908

To link to this article: https://doi.org/10.1080/09593985.2017.1391908

Published online: 24 Oct 2017.

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PHYSIOTHERAPY THEORY AND PRACTICE
2018, VOL. 34, NO. 4, 286–292
https://doi.org/10.1080/09593985.2017.1391908

RESEARCH REPORT

Characteristics of general movements in preterm infants assessed by


computer-based video analysis
Lars Adde, PhD, PTa,b, Hong Yang, PhD, MDc, Rannei Sæther, PhD, PTa,d, Alexander Refsum Jensenius, PhD e
,
Espen Ihlen, PhDf, Jia-yan Cao, PhD, MDc, and Ragnhild Støen, PhD, MDa,d
a
Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway; bClinics of Clinical
Service, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway; cRehabilitation Department, Children’s Hospital of Fudan
University, Shanghai, China; dDepartment of Pediatrics, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway; eDepartment
of Musicology, University of Oslo, Oslo, Norway; fDepartment of Neuroscience and Movement Science, Norwegian University of Science and
Technology, Trondheim, Norway

ABSTRACT ARTICLE HISTORY


Background: Previous evidence suggests that the variability of the spatial center of infant move- Received 12 November 2015
ments, calculated by computer-based video analysis software, can identify fidgety general move- Revised 31 October 2016
ments (GMs) and predict cerebral palsy. Aim: To evaluate whether computer-based video analysis Accepted 1 February 2017
quantifies specific characteristics of normal fidgety movements as opposed to writhing general KEYWORDS
movements. Methods: A longitudinal study design was applied. Twenty-seven low-to moderate- General movement
risk preterm infants (20 boys, 7 girls; mean gestational age 32 [SD 2.7, range 27–36] weeks, mean assessment; Fidgety
birth weight 1790 grams [SD 430g, range 1185–2700g]) were videotaped at the ages of 3–5 weeks movements; Computerized
(period of writhing GMs) and 10–15 weeks (period of fidgety GMs) post term. GMs were classified GM assessment; Cerebral
according to Prechtl’s general movement assessment method (GMA) and by computer-based palsy
video analysis. The variability of the centroid of motion (CSD), derived from differences between
subsequent video frames, was calculated by means of computer-based video analysis software;
group mean differences between GM periods were reported. Results: The mean variability of the
centroid of motion (CSD) determined by computer-based video analysis was 7.5% lower during the
period of fidgety GMs than during the period of writhing GMs (p = 0.004). Conclusion: Our
findings support that the variability of the centroid of motion reflects small and variable move-
ments evenly distributed across the body, and hence shows that computer-based video analysis
qualifies for assessment of direction and amplitude of FMs in young infants.

Introduction GMA was required to support its use in clinical routine


(Darsaklis et al., 2011).
Early identification of cerebral palsy (CP), the major
A complementary thinking on GMA has evolved
motor disability caused by preterm birth (Serenius
based on recent studies which assessed general move-
et al., 2013), is important for early intervention and
ments (GMs) with computer-based methods (Adde
specific follow-up, but also to give certainty to parents
et al., 2013; Kanemaru et al., 2013; Karch et al., 2012,
whose children are unlikely to develop CP (Novak,
2010; Marcroft et al., 2015; Valle et al., 2015). For a
2014). Prechtl’s qualitative assessment of general move-
comprehensive evaluation of the integrity of the devel-
ments (GMA) can be used as a tool for early identifica-
oping nervous system, observation and computer-based
tion of infants with neurodevelopmental disabilities,
analysis of GMs may complement each other
especially during the period of fidgety movements
(Einspieler and Marschik, 2013).
(FMs; 9–18 weeks post-term age) (Burger and Louw,
Most motion capture systems use on-body markers
2009; Einspieler et al., 2004; Noble and Boyd, 2012;
or sensors. They provide very precise and accurate data
Prechtl et al., 1997; Yang et al., 2012). GMA is based
about the kinematics and kinetics of human motion,
on visual Gestalt perception, which requires well-
often in combination with force plates and physiologi-
trained and experienced observers; wherever these are
cal sensors. However, there are also a number of draw-
not available, widespread clinical use of GMA is not
backs to such motion capture systems: they tend to be
feasible. One of many systematic reviews concluded
very expensive; must be installed in a controlled envir-
that more detailed evidence of the predictive value of
onment; require subjects to wear sensors (sometimes

CONTACT Lars Adde, PhD, PT lars.adde@ntnu.no Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology,
Trondheim 7491, Norway.
© 2017 Taylor & Francis
PHYSIOTHERAPY THEORY AND PRACTICE 287

connected to cables); and they require calibration as for their quality at 3–5 weeks post term (period of
well as experts for advanced analyses and interpretation writhing movements) and at 10–15 weeks post term
of the recorded data (Marcroft et al., 2015). Such sys- (period of FMs) by means of observation and compu-
tems are especially difficult to use in high-risk infants, ter-based video analyses. The same video-clips were
who may be sensitive to instrumentation that might used for both assessment methods.
influence their behavioral state and well-being, and
consequently the quality of their GMs. Our group has
Subjects
carried out three studies on a novel computer-based
video software system developed to detect FMs at a Preterm infants with a low to moderate risk of adverse
post-term age of 10–18 weeks, and for the prediction neurological outcome were recruited between
of CP (Adde et al., 2013, 2010, 2009). The software September 2012 and August 2013 at the Children’s
calculates differences in pixel values between subse- Hospital of Fudan University. Inclusion criteria were:
quent video frames, and exports motion variables 1) preterm birth at 27–36 weeks gestational age (GA);
reflecting the amount of motion and distribution of and 2) existing videos of the infant recorded during
the infant’s movements in the video. This type of both the writhing and the fidgety periods of GMs.
non-invasive computer-based video analysis requires a Infants diagnosed with a syndrome or intraventricular
standard, commercially available video camera but no hemorrhage grade II-IV according to Papile et al.
instrumentation on the infant, which makes it prefer- (1978) were excluded. Ultimately, 30 participants and
able to other computer-based methods. 60 video recordings were included. The study protocol
GMs involve the whole body in a variable sequence of was approved by the ethics board of the Children’s
arm, neck and trunk movements (Prechtl, 1990). At term Hospital of Fudan University. Written informed con-
age and until about 6–9 weeks post-term age, they are sent was obtained from parents/legal guardians of all
called writhing movements and are characterized by an participating infants.
ellipsoid form. At 6–9 weeks post term, these writhing,
ellipsoid GMs are replaced by FMs (Prechtl, 1997). FMs
are small movements of moderate speed and variable Video recordings
acceleration of the neck, trunk and limbs in all directions; All infants were placed supine on a standard bed/mattress
they are continual in the awake infant, except when wearing a diaper and a bodysuit to make them comfor-
fussing and crying; their absence is a particularly strong table. All recordings were performed during active wake-
marker for later CP (Einspieler et al., 2004). Our previous fulness using a stationary digital video camera (Panasonic
studies (Adde et al., 2010, 2009) suggest that some aspects HX-DC2, resolution: 1280 × 720). To ensure camera
of the movement pattern relevant for the identification of consistency, the camera was placed at the foot end of
FMs and later CP are reflected in the computer-based the bed/mattress and the set-up was standardized for all
movement parameter “Variation of the centroid of video recordings. Both assessment techniques were based
motion” (i.e. the variable displacement of the spatial on video recordings trimmed according to Prechtl’s GMA
center of the infant’s movements). Because the transfor- methodology (Einspieler et al., 2004).
mation from writhing to FMs involves their decrease in
amplitude and change in character from ellipsoid to
small and circular, it has been hypothesized for infants Observation of general movements
displaying normal GM patterns that the displacement of GMs were classified by two certified observers accord-
the spatial center should also decrease in this process. ing to Prechtl’s method of GMA (Einspieler et al.,
The aim of the present study was to determine whether 2004), both of whom had successfully completed GM
computer-based video analysis can quantify specific char- Trust training courses. One observer, who had not been
acteristics of normal FMs as opposed to writhing involved in the recruitment of the participants, was
movements. blinded to the infants’ medical histories. The two obser-
vers performed their assessments independently. In
case of disagreement, they re-assessed questionable
Methods videos together to reach consensus. GMs during the
writhing period were classified as normal if variable,
Design
complex and fluent movement patterns were observed,
The present study is a longitudinal cohort study of and as abnormal if the subcategories poor repertoire,
preterm infants in China whose GMs were assessed cramped-synchronized or chaotic were applied. FMs
288 L. ADDE ET AL.

were defined as normal if present (N) and as abnormal To visualize the entire movement sequences, we
if absent (FM-), sporadic (FM±) or exaggerated with used motion average images and motiongrams
respect to speed and amplitude (Fa). Infants with GMs exported from the videos, with infants represented in
classified as cramped-synchronized (limb and trunk a frontal view so as provide us with coherent spatial
muscles contract and relax almost simultaneously), and temporal movement information, respectively
chaotic (limb movements of large amplitude that (Jensenius, 2013). A motiongram can be seen as a
occurs in a chaotic order) or with abnormal FMs representation of the motion image. Each motion
(absence of FMs/sporadic FMs that is interspersed image is averaged to a one-pixel-wide or -tall matrix
with long pauses/FMs that is exaggerated with respect and plotted over time. The results are displayed either
to speed and amplitude) were excluded from the study in a horizontal or a vertical motiongram. An average
because their movement patterns clearly differ from image, as shown in Figure 1, combines all motion
infants with normal movement patterns that was images into a single display, thus giving an impression
needed for this study. of the spatial distribution of motion during the entire
recording. A horizontal motiongram like the one in
Figure 2 shows the temporal characteristics of an
Computer-based video analysis of general infant’s movements during the writhing and fidgety
movements movement periods.
Quantitative variables used in previous studies
The video analysis software was described in detail in
(Adde et al., 2013, 2010, 2009) were derived from the
previous articles (Adde et al., 2013, 2010, 2009; Valle
motion image by means of computer-based video ana-
et al., 2015). The videos contain 25 frames per second
lysis. Quantity of motion (Q) is the calculated sum of
with 1280 × 720 pixels. By subtracting subsequent
all pixels with positive values (i.e. active pixels) in the
frames in the video stream (frame differencing), the
motion image divided by the total number of pixels in
number of pixels that change between frames is calcu-
the image. The mean and standard deviations of the
lated to create the “motion image.” A motion image
quantity of motion (Qmean, QSD) were used as indepen-
thus represents the motion between two video frames
dent variables in further statistical analysis. The
(Jensenius, 2013), which allowed us to export quantita-
Centroid of motion (C) is the spatial center of pixels
tive data based on pixel values in the motion image. A
with positive values in the motion image. This variable
motion image with a value of zero indicates that no
reflects the center point of the infant’s total movement;
movement occurred between the frames; one with posi-
its position changes continuously during a video
tive values represents movement (Adde et al., 2010,
sequence. The mean value and standard deviation of
2009). All videos in the present study were cropped so
the centroid of motion in horizontal (X) and vertical
as to remove any movements by sources other than the
(Y) directions were calculated (Cxmean, Cymean, CxSD,
infants (e.g. interfering parents), leaving for analysis
CySD). The variability of the centroid of motion (CSD)
only a window with the standard bed/mattress and
was derived from the CxSD and CySD. Evenly
the infant.

Figure 1. Motion average images of an infant from the writhing movement period (left) and the fidgety movements’ period (right).
Legend: A darker gray scale color tone closer to the infant’s body indicates movements with predominantly smaller amplitudes during the
fidgety movements’ period compared to the writhing movement period.
PHYSIOTHERAPY THEORY AND PRACTICE 289

Figure 2. Motiongrams of infant movements.


Legend: Motiongrams (and motion average images to the left) of the vertical movements of infant with time running from left to right.
Upper and lower limits on the y-axis represent upper and lower boarders of the mattress, respectively. Upper panel from the writhing
movements’ period and lower panel from the fidgety movements’ period of the same infant. The upper part of the motiongrams displays
vertical movements of the upper extremities and head, while the lower part of the motiongrams displays vertical hip and lower extremities
movements. In the writhing period, the infant predominately moved upper extremities (seen as a darker greyscale color) with a stiller period
in the middle part of the recording, while a continual movement structure in all body parts is observed in the fidgety movements’ period
(continual motiongram with higher degree of density in the upper and lower part of the motiongram).

distributed movements in all body parts and all direc- power of abnormal outcome in such cases (Einspieler
tions find expression in a low variability of the centroid et al., 2004), so all infants were included for further
of motion (CSD), regardless of the amplitude of move- analysis. During the writhing period, 12 videos were
ment. Unsteady limb movements (i.e. uneven lateral classified as poor-repertoire, 15 as normal and none as
activity of the upper and lower limbs) will typically cramped-synchronized or chaotic. The observers dis-
yield higher CSD values. agreed on one (1.8%) video clip but then discussed it
and reached consensus.
Statistics
Data were analyzed using SPSS Statistics version 21.0 Participants and video recordings
(IBM SPSS Statistics, Chicago, IL, USA) and variables
The study group consisted of 20 boys and 7 girls, with a
were examined for normality using the Kolmogorov-
mean gestational age of 32 weeks (SD 2.7, range 27–36)
Smirnov test. Because all values were small and con-
and a mean birth weight of 1790 grams (SD 430g, range
tained many decimals, they were multiplied by 1000. To
1185–2700g). Table 1 shows neonatal morbidities in all
correct for the increase in body size between the wri-
participating infants. The mean duration of the edited
thing and fidgety movement periods, all variables were
video recordings used for observation and computer-
normalized for trunk area (TA), which was calculated
ized GM assessment was 5 minutes (range
by multiplying the trunk length by the trunk width
3–10 minutes and 3–11 minutes for the periods of
measured from the video image, and given in cm2.
writhing and FMs, respectively).
The computer-based variables showed normal dis-
tribution, and parametric statistics were employed. The
estimated group means for infants assessed during the Computer-based video analysis of general
writhing and fidgety movement periods were calcu- movements
lated. Between-group differences were determined in a
paired sample t-test, and variable differences were Table 2 shows the infants’ motion image variables dur-
reported including percentages. ing the writhing and fidgety movement periods. All
variables showed lower values in the period of FMs

Results
Table 1. Neonatal morbidities.
Observation of general movements Diagnoses (n = 27*)
Hyperbilirubinemia 17
Three infants with abnormal GMs during the FMs’ Respiratory distress syndrome 6
period (i.e. two with sporadic FMs and one with absent Apnea 3
Wet lung disease 1
FMs) were excluded from further analysis. Hence, the Anemia 2
final analysis sample comprised 54 video recordings of Sepsis 3
Infection 2
27 infants, all of whom were classified as normal during Hypoglycemia 2
the FMs’ period (i.e. all infants with a poor repertoire of Hypocalcemia 1
Hypoproteinemia 1
writhing movements had normalized by the period of ABO hemolytic disease 1
FMs). A poor repertoire has a very low predictive * Some infants could have more than one risk factor.
290 L. ADDE ET AL.

Table 2. Estimated means and differences of computer-based results were consistent across all parameters related to
video analysis variables for infants during the fidgety and the the variability of the centroid of motion. Lower mean
writhing movement period. and variability of the centroid of motion in the hori-
Writhing
movement period Fidgety Differences zontal and vertical directions (Cxmean, CxSD, Cymean
Computer- (3–5 weeks post movement’s period between GM CySD) during the FMs’ period suggest smaller and
based term age) Mean (10–15 weeks post periods
variable (SE) term age Mean (SE) Differences (%)
variable movements distributed evenly across the
Qmean 0.0292 (0.0018) 0.0273 (0.0027) −0.0019(−3.4) body. In a previous study, the variability of the centroid
QSD 0.0290 (0.0013) 0.0280 (0.0017) −0.001(−1.8) of motion (CSD) showed lower values in infants with
Cxmean 1.3824 (0.0457) 1.0671 (0.0282) −0.3153(−12.9)*
Cymean 1.5129 (0.0622) 1.0895 (0.0340) −0.42348(−16.3)* normal FMs than in infants with abnormal FMs (Adde
CxSD 0.2726 (0.0119) 0.2264 (0.0136) −0.0462(−9.3)** et al., 2009). This was also the case in a study predicting
CySD 0.3549 (0.0121) 0.3101 (0.0132) −0.0448(−6.7)***
CSD 0.4498 (0.0145) 0.3874 (0.0160) −0.0624(−7.5)** CP in high-risk infants, which found lower CSD values
* p < 0.001, **p < 0.005, ***p < 0.05 in non-CP children than in CP children (Adde et al.,
All computer-based variable values are multiplied with 1000 and divided by 2010). The frequent changes in the small movements of
Trunk Area for normalization. Qmean = quantity of motion mean;
QSD = quantity of motion standard deviation; Cxmean = centroid of motion the neck, trunk and limbs in all directions, typically
in the X-direction mean; Cymean = centroid of motion in the Y-direction observed during the period of FMs, results in variable
mean; CxSD = centroid of motion standard deviation in the X-direction;
CySD = centroid of motion standard deviation in the Y-direction;
movements distributed evenly in the motion image
CSD = centroid of motion standard deviation; SE = standard error of mean. (Adde et al., 2013, 2010, 2009). Infant movement pat-
terns with hands and feet tucked in towards the mid-
line, which is more typical of the FMs’ period than of
than during that of writhing movements. The differ- the writhing movements’ period, could potentially con-
ence was statistically significant in all centroid-of- tribute to a low CSD value, but in most cases this
motion variables (p < 0.05). The biggest difference behavior occurred only sporadically throughout the
was recorded for the mean centroid-of-motion vari- video, which would clearly not have had a significant
ables of movements in horizontal and vertical direc- effect on the CSD value. This is supported by the
tions, with 12.9% and 16.3% lower values during the motion average image in Figure 1, where movements
period of FMs, respectively. The variability of the cen- with small amplitudes (darker grey scale close to the
troid of motion (CSD) was 7.5% lower during the FMs’ infant’s body) are more common during the FMs’ per-
period than during the writhing movements’ period of iod than during the writhing period.
GMs (p = 0.004). There were no significant differences The motiongrams in Figure 2 also show that FMs are
in any of the motion image variables between infants continuous over time across all body parts and in all
with abnormal (i.e. poor-repertoire) GMs and those directions (lower panel), which does not apply to wri-
with normal GMs during the writhing movements’ thing movements (upper panel). There were no differ-
period. ences between the writhing and FMs’ periods with
regard to the mean and variability values of the quan-
tity of motion (Qmean, QSD). The quantity-of-motion
Discussion
value in our sample represents FMs as well as concur-
In the present study we identify quantitative movement rent movements such as wiggling-oscillating, swiping
differences between the writhing and fidgety GM peri- and kicking movements, which occur in both GM
ods in preterm infants assessed by computer-based periods (Einspieler et al., 2004). Figure 2 thus indicates
video analysis. In consistence with our hypothesis, the that the differences between FMs and writhing move-
computer-based video analysis showed the variability of ments apply to movement characteristics other than the
the centroid of motion (CSD) to be low, with small and amount of movement quantified by Qmean and QSD.
variable movements evenly distributed across the body One limitation of our computer-based video analysis
– a typical FM pattern. is that it mainly reflects spatial aspects of general move-
The random selection of infants was based on an ments but does not include specific temporal character-
estimated low-to-moderate risk of adverse develop- istics, which are just as likely to be relevant for an
ment. The study was designed to explore the develop- accurate computer-based classification of GMs. The
mental trajectory of previously described, computer- moderate speed, variable acceleration and waxing and
based motion variables; its results cannot be extrapo- waning intensity of FMs are complex phenomena
lated to a specific patient group. Although the present recorded and interpreted by the GM observer during
study included only 27 infants, results were highly sig- Gestalt perception. In order to include temporal aspects
nificant and consistent with our hypotheses which was of FMs in the computer-based video analysis it is
based on expert knowledge of GMA. Furthermore, necessary to continue searching for additional
PHYSIOTHERAPY THEORY AND PRACTICE 291

movement variables that reflect temporal changes in bringing the first and second authors together and thus lay-
GMs. It could also be argued that the inclusion of ing the ground for this study.
infants with abnormal (poor repertoire) GMs during
the writhing movements’ period is a limitation to our Declaration of interest
study, even though they have low predictive value of
later adverse neurological outcomes (Einspieler et al., The authors report no conflicts of interest. The authors alone
are responsible for the content and writing of the article.
2004). Our findings show no significant differences
between the motion image variables of normal and
poor-repertoire infants during the writhing GM period. Funding
This may indicate that other movement variables and/
This study was supported by the Department of Clinical
or more advanced 3D spatial and temporal analyses are Services and Department of Pediatrics of St. Olavs Hospital,
required to further differentiate between movement Trondheim University Hospital, Norway, and the Norwegian
qualities during the writhing GM period. Our study University of Science and Technology (NTNU), and The
design of evaluating motion image variables by com- Natural Science Fund of Shanghai (project number:
paring writhing with FMs should of course be taken 12ZR1403600). These institutions had no involvement in
the composition of the article.
further by comparing present and absent FMs as well as
the temporal organization of FMs. Hence, the relation-
ship between variables used in the present study and ORCID
typical characteristics of GMs should be further Alexander Refsum Jensenius http://orcid.org/0000-0001-
explored in more detail. 6171-8743
Despite the mentioned limitations we believe that
the use of regular 2D video camera recordings and
computer-based video analysis without additional References
instrumentation and with limited need for user exper- Adde L, Helbostad J, Jensenius AR, Langaas M, Stoen R 2013
tise are obvious advantages over other studies Identification of fidgety movements and prediction of CP
(Kanemaru et al., 2013; Karch et al., 2012, 2010; Kim by the use of computer-based video analysis is more accu-
et al., 2009; Marcroft et al., 2015). The availability, cost- rate when based on two video recordings. Physiotherapy
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