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Posture, spontaneous movements, and behavioural state organisation in infants affected by brain
malformations
Fabrizio Fermi”‘“, Heinz F.R. Prechtl”, Giovanni Cionib, M. Federica Roversi”, Christa Einspieler”, Claudia Gallo”,
Paola B. Paolicellib, Giovanni Battista Cavazzutia “Institute of Paediatrics and Neonatal Medicine, University of Modena, Modem, Ztuly
bStelZa Man’s Scientific Znstitute and INPE University of Piss, Piss, Italy ‘Institute of Physiology, University of Graz, Graz, Austria
Received 10 June 1997; accepted 27 August 1997
Abstract
Posture, quantity of spontaneous movement patterns, quality of general movements (GMs), and behavioural state organisation were studied in nine infants affected by documented brain malformations. A single 1 h video recording of five infants and two or more serial video recordings of another four infants were performed after birth. The graphic representation of single movement patterns (actogram) and of behavioural states of one video recording was performed in eight out of nine infants. The quality of GMs was assessed according to Prechtl’s method in all video recordings. All nine infants showed a less variable posture than normal newborn infants and an unusual resting posture was detected in seven infants. Poor behavioural state organisation without sleep cycles was common to the nine infants and excessive wakefulness was observed in six infants. As for the quantity of single movement patterns, six infants lacked one or two movement patterns normally present in healthy newborn infants. An abnormal quality of GMs was noted in all nine infants and distinct motor abnormalities were observed in single infants. A monotonous and sometimes stereotyped sequence of different body parts involved in the movement (i.e. poor repertoire GMs) was common to all infants. In the four infants of whom two or more video recordings were available, initial poor repertoire GMs were followed by a further deterioration in movement quality. No relationship was found between the quantity of defective brain tissue, lack of a specific part of the brain, type and severity of GM and posture abnormalities. 0 1997 Elsevier Science Ireland Ltd.
*Corresponding author. Tel.: + 39 59 422178; fax: + 39 59 424583; e-mail: ferrarif@C220.unimo.it
0378-3782/97/$17.00 0 1997 Elsevier Science Ireland Ltd. All rights reserved. PZZ SO378-3782(97)00095-9
88 F. Ferrari et al. I Early Human Development 50 (1997) 87-11.3
Key~ods: Newborn infant; Brain malformation: Spontaneous movements; General movement quality; Posture; Behavioural states
1. Introduction
A number of studies on fetuses and newborn infants [ 1,3,4,9,11,17,19,22,24] have shown that spontaneous motor activity is affected by brain lesions or impairment. Of the whole motor repertoire, attention has been focused on a specific motor pattern i.e. general movements (GMs) which, when observed repeatedly, can be used as an early marker for brain dysfunction [16]. GMs are gross body movements involving head. trunk and limbs with variable amplitude, speed, and force: they can be recognised in fetal life from 9-10 weeks postmenstrual age (PMA) [7] onwards, and after birth the! continue to be present until 16-20 weeks post-term age [ 171.
In the case of brain damage a number of GM abnormalities have been recognised. namely poor repertoire of GMs, cramped-synchronised GMs and chaotic GMs 191 (for definitions see below). The most severe lesions (i.e. extensive cystic periventricu- lar and/or subcortical leukomalacia, severe hypoxic-ischaemic encephalopathy ) are usually accompanied by the cramped-synchronized GM t:ype [4.9,19]. Less severe lesions, like germinal matrix/intraventricular haemorrhages (GMH-NH) and/or non-cystic leukomalacia, as well as localised periventricular leukomalacia with small cysts, are usually accompanied by poor repertoire GMs of variable duration [4,9,19]. Chaotic GMs are also observed transiently in Iarge GMH-IVHs and in anencephalic fetuses [9,24]. From previous findings it is evident that fetuses with major brain malformations will not produce GMs of normal quality.
Which are the motor abnormalities, if any, observed in infants affected by more 111 less severe brain malformations?
The present study examines posture, spontaneous movements and behavioural srate organisation in infants affected by distinct brain malformations.
The following questions are specifically addressed:
1. what is the repertoire of spontaneous movements and postures in a variety of brain malformations?
2. does the lack of specific parts of the brain specifically influence GM quality and posture?
3. is there a relationship between the quantity of defective brain tissue and the degrw of abnormality of GMs?
4. is the state organisation affected in infants with brain malformations?
2. Subjects
Posture, quantity of spontaneous movement patterns, quality of general move- ments, and behavioural state organisation were studied in 6 full-term and in 3 preteml infants selected on the basis of documented brain malformation. All the infants were born between 1985 and 1996 either in Modena or in Pisa. Parents gave their informed consent for the video recordings. Clinical data of the cases are provided in Table 1.
Table
1
Clin
ical
data
of
the
stud
y gr
oup
CaSe
Se
x and
ka
ryotvp
e
GA
Grow
th Pm
- an
d
pstna
taI
data
Neuro
logica
l
exam
inatio
n
PMA
38 w
:
neck
an
d m
mk
hype
rexten
sion,
exten
sor
hype
rtonia
of
the
limbs
, kn
ee
jerks
exag
gera
ted,
cons
isten
t
SpOt
ltanW
US
Babin
ski.
EBG
i-tmdin
gs
Gutco
me
Post-
mor
tem
brain
exam
inatio
n TP
I N.
1
38
1800
(<5)
Twin
pregn
ancy
(in
traute
rine
death
40
(<5)
of
the o
ther
fetus
), CS
, Ap
gar
scor
e:
7 at
1’, 9
at
5’, g
ood
dhica
l
CT (
30
d):
cond
itions
at
bii an
d du
ring
the
first
mon
ths
of life
awnc
qhdy
, ex
tensio
n
of bra
in tis
sue
and
CSF
throu
gh
a de
fect
in the
skull
ba
se
in the
reg
ion
of the
crib
riform
pla
te
and
c&a
galli
Dece
ased
at 4
m
(St.
epid.
seps
is)
Hypo
plasia
of
the
;a pa
&al
bone
s of
the
3 sk
ulk
mark
ed
2.
cere
bmm
hy
popla
sia;
2 a m
inim
al sh
rimp
of the
?
hemi
sphe
res;
thinn
ing
G
of the
cor
tex
of the
f:
cereb
ellum
, wh
ich
was
a
of no
rmal
size.
is
Fron
to-na
sal
4 en
ceph
aloce
le.
F s Ma
rked
asym
metr
ical
F;-
dilata
tion
of the
later
al P
ventr
icles
(L CR
) E 3 2
N. 2
Fe
male
46xX
de
K4)(p
15.1)
42
2240
(<5)
LateF
HRJJ
A~pg
arsw
e: 7a
t I’,
8
49 (
25)
at 5’;
fac
ial
dysm
orph
isms:
low-se
t
33.8
(25)
ears
with
bilate
ral
pream
icolar
asgu
s lis
tuIas
, Ink
mph
thslm
ia,
hype
rtelor
ism
and
epica
nthus
, lar
ge
rwt
of the
no
se,
small
m
outh,
micm
gnath
ia.
Apath
y s.,
sev
ere
hypo
tonia
and
mild
RD
S (1
st d)
;
mult
ifoca
l clo
nic,
gene
raliz&
ton
ic
and
atypic
al (or
al au
tomati
sm)
&ures
(4’
b-7’h
d).
PB f
rom
the
4’h
d; pe
rsis
tent
ge
neral
ized
hypo
tonia
and
apath
y s.
1 w:
retm
flexio
n of
the
head
, m
arked
gene
ralize
d
hypo
tonia,
apath
y s.
5 d:
oo
sleep
organ
izatio
n, low
volta
ge
EEG,
isolat
ed
par&
o-
occip
ital
EBG
disch
arges
, no
distin
ct EE
G pa
tterns
(no
TA,H
VS,LV
I)
CT (
1 d)
:
dilata
tion
of the
late
ral
ventr
icles
(L >
R),
large
su
barac
hnoid
haem
orrha
ge
Dece
ased
at 2
m
(poeu
ma-
nia)
Q
Tabl
e I
(con
tinue
d)
CW
Sex
and
GA
iirowt
b he
- an
d Ne
urolo
gical
EEG
Im
agin
g O
utco
me
Post
-mor
tem
WW
pe
posm
atal
data
ex
amina
tion
reco
rding
s re
sults
br
ain
exam
inatio
n
N.
3 Fe
mal
e
46,xX
41
2310
( <
5)
45.5
(
< 5)
32.5
(IO
)
Late
FH
RD,
CS,
resu
scita
tion
bag
and
mas
k,
Apga
r sc
ore:
4
at l
’, 7
at
5’.
Facia
l dy
smor
phism
: lo
w-se
t
em,
loose
sk
in at
the
back
of
th
e
neck
, po
sterio
r pa
late
cleft.
M
ultipl
e
mal
form
atio
ns:
pulm
onar
y ar
tery
steno
sis,
ostiu
m
prim
nm,
pate
nt
ducm
s m
terio
sns,
R
card
iac
vent
ricle
hype
rtmph
y,
hypo
plasia
of
the
R
kidne
y, hy
popla
sia
of
the
tbym
us.
card
io-re
spira
tory
dis
tress
,
hepa
tom
egaly
an
d oe
dem
a,
cyan
osis.
N. 4
M
ale
46,X
Y
17
2095
(5
)
46
(IOj
27.5
(C
S)
Out
bom
. Tw
in
preg
nanc
y: ba
g an
d
mas
k re
susc
itatio
n,
Apga
r sc
ore:
7
at
I’,
8 at
5’.
Tran
sfer
red
to N
ICU
at 2
!! hp
C~U%
Y cf
f?ck
! dy
$mor
pl%
m.
Labiu
m
palat
osch
isis.
pate
nt
ductu
s
arte
riosn
s. Hy
perth
erm
ia ep
isode
s,
stat
us
epile
pticu
s (o
ral-b
ucca
l
auto
mat
ism,
polyp
nea,
abno
rmal
eyes
m
ovem
ent,
myo
clonic
-tonic
fit
s
of
the
limbs
), re
curre
nt
pneu
mon
ia
from
bif
ib up
to
th
e 8’”
m
Id:
neck
an
d tru
nk
hype
rexte
nsion
,
flexo
r hy
perto
nia
of
the
limbs
5 m
: tru
nk
and
neck
by
poto
nia,
limb
hype
nonia
,
hypix
Gtk&
y
and
poor
vis
ual
resp
onse
s,
exag
gera
ted
knee
ierks
.
I, 2.
2.5
. 3,
5 m
:
pers
isten
t EE
G
asym
met
ry
(R <
L),
iwk
of
mam
rado
nai
teat
ures
(i.
e.
enco
ches
front
ales,
sleep
spind
les,
etc.
), no
norm
al EE
G
patte
rns.
abno
rmal
bilate
ral
fast
activ
ities
and
shar
p
wave
s es
pecia
lly
on
the
R he
mts
phe~
MRI
(1
5 d)
:
cotp
us
callo
sum
.
falx
cere
bri
and
mte
rhen
usph
eric
lissu
re
agen
esis.
Fuse
d th
alam
i. th
ird
vent
ricle
not
pres
em.
A cr
esce
nt-s
hape
d
holov
entric
le
surro
unds
fu
sed
thal
ami.
Pach
ygyr
ia.
tvh-
k@ti
thinn
iog
of
the
hem
isphe
ric
white
mdt
er
wig
I !
Dece
ased
at
2 m
(he
art
failu
re)
Left
eye
colob
oma,
polym
icrog
yria
,
agen
esis
of
the
olfac
tory
bu
lbs
Dece
ased
at 8
m
(sta
tus
cprle
pticu
s)
Micr
ocep
haly;
bilate
ral
agen
esia
of
the
olfac
tory
bu
lbs;
front
al lob
es
are
fnse
d
by m
eans
of
men
inge
s,
a sh
rimp
of
sepa
ratio
n
of
the
hem
isphe
res
is
dete
ctable
;
pach
ygyr
ia;
bilate
ral
hypo
plasia
of
th
e
parie
tal
and
occip
ital
IOkS
CaSe
se
x an
d
karym
pe
GA
GIOW
th Pm
an
d
postn
atal
data
Neuro
logica
l
exm
i”ati0
”
EEG
record
ings
Imag
ing
result
s
outco
me
Post-
mor
tem
brain
exam
inatio
n
N. 5
Fe
male
38
24
80
(10)
CS,
Apga
r sc
ore:
9 at
l’, 9
at 5’.
46,
xx
45
(5)
Good
clin
ical
cond
ition
and
gmwt
h
28.5
(<5)
du
ring
the n
eona
tal
perio
d.
N. 6
Ma
le
46,X
Y4p
40
3185
(10
) Ou
thorn,
Ap
gar
scor
e: 9
at 1’,
9 a
t
50 (
25)
5'.
Tran
sferre
d to
NICU
on
2”d
d.
31.5
(95)
beca
use
of clo
nic
jerks
. Fa
cial
dysm
otpbis
m:
micm
g”ath
ia,
high
foreh
ead,
wide
op
en
fontan
elles
,
low-se
t ea
rs, R
at roo
t of
the
nose
,
cly”&
ctyly
of the
fifth
lin
ger,
shor
t
limbs
. He
pat~g
aly,
hypx
tmpb
y
of ca
rdiac
i”te
mtlia
l se
ptmn
and
of
the v
e”tlicu
laI
walls
, tm
pr,
small
ampli
tude
trem
ors,
mult
ifoca
l clo
nic
seizu
res,
swea
ting
and
irritab
ility
episo
des
obse
rved
d”rin
g the
“em
atd
pmiod
. Iso
l&d
epilep
tic
S&IR
S (to
nic
and
clonic
jer
ks)
throu
ghou
t the
firs
t m
onths
of
life;
stahts
e@
pticu
s fm
m 8
m. C
linica
l
and
metab
olic
(incre
ased
ve
ry-lon
g-
chain
fa
tty
acids
) ind
icatio
ns
for
zellw
eger
s.
1, 3.5
, 6
m:
postu
ral
delay
,
mild
hy
petto
nia
of
the l
imbs
, po
or
intera
ctive
perfo
rman
ces
1, 3,
5, 9
m:
squin
t, bil
ateral
eyelid
pto
sis,
poor
visua
l ori
entat
ion,
neck
an
d tm
nk
hypo
tonia,
increa
sed
lib
tlexo
r by
perto
nia,
trem
ors;
no
signs
of m
ental
or
moto
r
deve
lopme
nt
8d:
lack
of m
aturat
ional
featur
es,
no n
ormal
EEG
patte
rns,
bilate
ral
low
volta
ge
fast
activ
ities
thrw
ghwt
differ
ent
beha
vioura
l
states
; iso
lated
sh
arp
wave
s in
the L
hemi
sphe
re
Durin
g the
firs
t 8
mon
ths
of life
: po
or
mahu
ation
al fea
tures
,
poor
EEG
patte
rns.
Isolat
ed
E!xi
disch
arges
at
the L
hemi
sphe
re on
two
occa
sions
.
At 9
m:
slow
back
groun
d EE
G
activ
ity
and
repeti
tive
2-2.5
Hz
spike
s slo
w
wave
s dis
charg
es
CT(I5
d)
:
mode
rate
dilata
tion
of
the s
obara
cbno
id
SpC.
3
CT (
1 m
):
occip
ital
horn
of the
latera
l ve
ntricle
s
dilate
d, co
rpus
callo
sum
hypo
plasia
8 ye
ars:
seve
re
men
tal
retard
ation
Dece
ased
at 10
m
Macro
ceph
aly
and
pach
ygyri
a, co
rpus
callo
sum
and
cereb
ellum
hypo
plasia
, dila
ted
latera
l ve
ntricle
s,
delay
ed
myeli
natio
n
Tabl
e 1
(con
rinue
d)
GP.
Wth
Pr
e-
and
Neur
ologic
al
postn
atd
data
ex
amina
tion
EEG
reco
rding
s
lmag
ing
resu
lts
Out
com
e PO
St-ll
lOIte
lIl
brain
21
ex
amina
tion
2
N. 7
Fe
mal
e
46,xX
36
26
10 (
50)
44 (
10)
31.5
(10)
Out
born
, lat
e FH
RD,
CS,
Apga
r
scor
e: 7
at
I’,
9 at
5’,
go
od
clinic
al
cond
itions
du
ring
the
neon
atal
perio
d.
Recu
rrent
cy
stopy
elitis
an
d
pneu
mon
ia in
the
first
ye
ar.
N. 8
Fe
mal
e
46,X
x 25
75
0 (S
O)
33 (5
0)
19.5
( <
5)
Solut
io pla
cent
ae,
CS,
intob
ated
at
birth
, Ap
gar
scor
e:
6 at
IO
7
at 5
’,
mec
h.
vent
ilatiw
(IP
PV
for
25
d,
CPAP
fo
r 4
d).
Incr
ease
d int
racra
nial
pres
sure
, ve
ntricu
loper
itone
al sh
unt
perfo
rmed
at
39
w.
bilate
ral
ROP
2, 3
, 5,
9 m
: m
icroc
epha
ly,
limb
flexo
r
hype
rtonia
,
impa
ired
men
tal,
mot
or
and
postu
ral
deve
lopm
ent,
evide
nce
of s
pasti
c
dipleg
ia.
1, 2
, 4.
6 m
: se
vere
ne
ck
and
trunk
hy
poto
nia.
spon
taneo
us
&bin&
i.
!!%%
SS!g
exte
nsor
lim
b
hype
rtonia
. No
visua
l or
ienta
tion.
PMA
40
w:
exce
ss
of
slow
wave
s
and
fast
acti
vities
in
state
4, LV
I in
stat
e 2.
MRI
(4
m
):
vast
oc
cipita
l
men
ingo
-
ence
phalo
cele:
hype
rinte
nsity
of
its
pare
nchy
mal
pti
in
T&we
ight
ed
imag
es
MRI
(P
MA
33
w)
hydr
anen
ceph
aly:
cere
bral
hem
isphe
res
near
ly co
mple
tely
repla
ced
by
cere
bros
pmal
lhud.
A
min
imal
po
rtion
of t
he
R fro
nto-
tem
pora
l, R
and
L oc
cipita
l lob
es
is co
nser
ved.
Th
aiam
i
and
cere
bellu
m
are
pres
ent
(Fig
. 2
a an
d h)
Lost
at th
e fo
llow-
up
at
the
age
of
II m
.
3 ye
ars:
tll%XO
-
ceph
aly.
swer
e
men
tal
reta
rdat
ion
(unt
esta
ble)
spas
tic
tetra
plegia
,
CW
sex
and
karyo
tvpe
GA
Grow
th Pm
- an
d
postn
atal
data
EEG
record
ings
Imag
ing
rewl
ts
0tltco
me
Post-
mon
em
brain
exam
inatio
n
N. 9
Ma
le
46,
XY
40
2980
(10
) Ap
gar
scor
e: 9
at I’,
9 at
5’.
49 c
m
Neon
atal
conv
ulsion
s an
d sta
tus
35 W
) ep
ilepticu
s wi
th L
hemi
conv
ulsive
focal
clonic
se
izures
un
respo
nsive
to
therap
y. Pa
rtial
R he
misp
herec
tomy
at 4
m,
no m
ore
clinica
l se
izures
,
EEG
focal
disch
arges
on
the
left
hemi
sphe
re on
ly.
3 m
:
mild
ne
ck
and
trunk
hy
poton
ia,
tonus
as
ymm
etry
(L>R
): go
od
visua
l ori
entat
ion
and
socia
l
intera
ction
2 an
d 4
w: in
terict
al
disco
ntinu
ous
EEG
and
focal
R pa
rietal
sharp
-wav
es,
repeti
tive
EEG
disch
arges
at
the
R he
misp
here
not
alway
s as
socia
ted
with
ictal
clinica
l
MRI
(2 w)
mark
ed
mag
nifica
tion
of the
R h
emisp
here
with
thick
ening
of
the
corte
x. Th
e R
fronta
l
lobe
is no
rmal.
6m
mild
postt
d an
d
men
tal
delay
, m
ild
tonus
w-w
CL>@
Abbre
viatio
ns:
h: ho
ar;
d: da
y; W
: wee
k; m
: mon
th;
y: ye
ar:
L: lef
t; R:
tigh
t; d&
delet
ion.
Grow
th:
the t
hree
value
s of
the t
able
refer
to
: bir
thweig
ht (pe
rcenti
les
in gr
ams)
acc
ording
to
the R
&ian
perce
ntile
grow
th
char
ts;
length
(pe
rcenti
les)
at bir
th;
head
cir
cum
feren
ce
in cm
(pe
rcenti
les)
at bir
th.
Pm-an
d po
st-na
tal
data:
FH
RD:
fetal
heart
rat
e de
celer
ation
; CS
: ce
sarea
n se
ction
: RD
S:
mpi
mor
y dis
tress
sy
ndro
me;
s:
syn
dmne
; RO
P:
Ietin
Opat
by
of pr
ematu
rity:
CPAP
: co
ntinn
os
posit
ive
airwa
y pre
ssure
; IP
PV:
inter
mitte
nt po
sitive
pre
ssure
ve
ntilat
ion;
max
. bil
. lev
el:
max
imal
bilim
bin
level;
PB
: Ph
enob
arbita
l; NI
CU:
neon
atal
inten
sive
cam
unit
; PM
A:
post-
men
strua
l ag
e. EE
G re
cord
hgs:
TA:
trac6
alte
mao
t; HV
S:
high
volta
ge
slow;
LV
I: low
vo
ltage
irre
gular
. Ou
tcom
e: St
. ep
id,:
Stap
hyloc
cxco
s ep
idomi
dis.
[mqia
g re
sults
: CS
F:
cem
bm-sp
inal
flui&
CT,
Comp
uted
Tom
ogra
phy;
MRIz
Mag
netic
Re
sona
nce
Imag
ing
8
94 F. Ferrari et al. I Early Human Development 50 (1997) 87-113
3. Method
3.1. Neurological examination
Neurological assessment was performed in the neonatal period according to the Dubowitz and Dubowitz protocol [S] during the preterm period and to the PrechtJ protocol [ 141 at term age. During the following months neurological examination was performed according to Amiel-Tison’s and Grenier’s examination protocols 121 or to an extension of Touwen’s criteria [23].
3.2. Brain imaging, EEG recording
Brain imaging was carried out in eight infants: Computed Tomography in four infants (Case 1, 2, 5, 6) and Magnetic Resonance Imaging ( I,5 Tesla) in four infants (Case 4, 7, 8, 9). One infant (Case 3) was not subjected to brain imaging study because of her severe clinical conditions; post-mortem examination revealed poly- microgyria.
All five infants who died underwent post-mortem examination. One or more EEG and/or EEG-polygraphic recordings of I h or longer were
performed in six infants. Eight active electrodes (Fpl, Fp2. C3, C4, T3, T4. 01, 02 of the international lo-20 system) were applied to the scalp. Nasal respiration (termistor), abdominal respiration (strain gauge), chin-EMG (electromyogram), limb- EMG, EOG (electrooculogram) and electrocardiogram were recorded along with the electroencephalogram. The EEG description took into accotint maturational features (e.g. temporal theta, encoches frontales, delta brushes), normal EEG patterns like TA (trace altemant), H (high voltage slow), M (mixed), LVI (low voltage irregular) at term age and specific EEG abnormalities (e.g. electrical discharges, persistent interhemispheric voltage asymmetry, absence of spatial organisation, poor inter- hemispheric synchrony, severely depressed EEG) [lo].
3.3. Methods of recording general movements and posture
Each infant was filmed at least once and at most 4 times during their stay in the hospital, each video recording lasting 1 h. During the video recordings the infants were lying naked and supine in an incubator or in a cot free to move and without infusion. The video camera was one metre above the incubator or cot, at an angle of 45”. Opening and closing of the eyes, crying and regularity of respiration wet-e continuously observed and verbally recorded on the audio-channel of the videotape.
Spontaneous movements were analysed from the replay of the video recordings. Occurrence and duration of the different types of movements in eight of the nine infants (Case 9 was video recorded for 15 min only) were noted on pre-coded sheets in order to produce actograms for the visual display of all events occurring during the first (or the fourth in Case 8) video recording.
Posture was assessed when the baby remained quiet for at least 5 s and a sketch was made every time a new posture was obtained; the two most frequently occurring
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 95
resting postures per baby were considered. Preference postures were defined as the position of head, trunk and limbs assumed by the infant for the largest percentage of observation time [ 181. In the present study we used the term “dominant” posture when the infant displayed no more than one posture and the term “unusual” posture when the infant showed a type of posture not observed in healthy fullterm infants [5,6]. Abnormal posture during the first 3 to 4 month of life [2] were also considered as unusual.
3.4. Assessment of behavioural states
Regularity of respiration, opening or closing of the eyes, body movements, and crying were used for identification of Prechtl’s five behavioural states [13]. A 3 min moving window was employed over the four variables to indicate the onset and offset of each state. A state was present if throughout the 3 min period its configuration met all the criteria required for the sleeping states 1 and 2 or the awake states 3 to 5. If criteria for a particular state were lacking, “dissociated state” was recorded.
3.5. Quantitative assessment of spontaneous movements patterns
The quantitative assessment of spontaneous motility took into account the motor patterns observed in healthy newborn infants. The actograms of the infants of this study were compared with those observed in normal fullterm (5) and preterm infants (6).
3.6. Qualitative assessment of general movements
According to the definition [16], general movements are “gross movements involving the whole body. They may last from a few seconds to several minutes. What is particular about them is the variable sequence of arm, leg, neck and trunk movements. They wax and wane in intensity, force and speed and their onset and end are gradual. The majority of extension or flexion of arms and legs is complex, with superimposed rotations and often slight changes in direction of the movement. These additional components make the movement fluent and elegant and create the impression of complexity and variability”. In the first 4 to 5 weeks after term age GMs are called “writhing movements”, changing at the age of 6 to 9 weeks into so-called “fidgety movements” which disappear around 16 to 20 weeks. Fidgety movements are defined as an ongoing stream of small, circular and elegant movements of neck, trnnk and limbs [ 171. Fidgety movements are judged as abnormal if they are absent or if their amplitude, speed and jerkiness are moderately or greatly exaggerated.
As in previous studies [4,9,19] we assessed the quality of GMs in two steps. We first scored normal or abnormal quality of GMs on the basis of a global visual Gestalt-perception of the complexity, fluency and elegance or monotony and awkwardness of the single GM. Three major categories of abnormal GMs, described in previous papers [4,9,17,19], were distinguished as follows: 1) poor repertoire GMs:
96 F. Ferrari et al. I Early Human Development 50 (1997) 87-I I3
the sequence of successive components is monotonous and movements do not occur in the complex manner observed in normal GMs; 2) crarqed-synchronkd GMs: general movements look rigid and lack the normal smooth and fluent character; all limb and trunk muscles contract and relax almost simultaneously; 3) chaotic GMs: general movements look chaotic in their sequence.
As a second step we performed a semi-quantitative scoring of the single aspects of GMs by repeated replay of the videotape (Table 2) [9]. Eight criteria dealing with amplitude, speed, movement character, sequencing, range in space, fluency and elegance and onset and offset of gross movements, as well as with subtle distal movements are given a score of 2 for every optimal aspect while the non-optimal aspects are only given a score of 1. Hence, the optimality score ranges from a maximum of 16 to a minimum of 8 points (Table 3) [9].
This kind of evaluation cannot replace the overall judgement and needs to he carried out independently. It provides details of those components which may have changed in abnormal GM, identifying differences from the normal.
4. Results
Case 1: aueucephaly, fronto-nasal encephalucele
Video recording at 38 weeks PMA Actogram (Fig. 3 a): the state profile shows state 4 followed by state 2 and
dissociated state. No sleep cycles. Movement patterns: rare isolated arm movements, no isolated leg, hand and foot movements. Movement patterns other than GMs and sobs are rare through all behavioural states. GMs tend to occur in burst-pause patterns, GMs in sleep have a short duration.
Posture (Fig. 4 Case 1, a and b): unusual posture with neck and trunk arching, head and trunk lying on the left side (a); posture with flexed limbs is occasionally seen (b). Posture on the left side restricts the limb movements to one spatial plane. Poor posture variability.
GMs: Variable sequence and movement character from GM to GM. Onset is generally gradual, offset is dominantly sudden. Some GMs look chaotic, dominantly large, fast and abrupt; some consist of prolonged flexion-extension of the trunk, flexion-adduction of the limbs: others start with poorly organ&d and fragmented limb movements and end with frozen posture in AexionIextension of the four limbs. Various brief, convulsive episodes consist af rhythmical myoclonic jerks of the trunk and limbs (3 to 7 jerks in a row) during GMs. Global evaluation: chaotic, cramped, poor repertoire GMs, myoclonic seizures.
Optimulity score: 9 (Table 3, Case 1). Peculiar is the variety of distinct abnormal GMs observed in this severe brain
malformation: chaotic GMs, cramped-synchronized GMs and poor repertoire GMs were present at different times of the recording in the Siune infant; convulsive phenomena (myoclonic jerks) were often superimposed on GMs.
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 91
Table 2 Evaluation sheet of general movement quality
NAME: POSTMENSTRUAL AGE: Recording times (or counter no.) from
&*TE I
Tape Nr:
I R-A CYCLE i 1
I
I Amplitude
II
III
IV
V
VI
VII
Speed
Movement character
Sequencing
1.a 1.b 1s
2
Predominantly small range Predominantly large range Small and large, no intermediate range Variable in full range
1.a 1.b 1.c 1.d 2
1.a 1.b 1.c 1.d 1.e 2
1.a 1.b 1.c
1.d
1.e
2
Monotonously slow Monotonously fast Slow and fast, no intermediate Invariable Variable
Cramped PlOPPY Flapping Tremulous Poor repertoire Variable and complex
Only synchronized movements Disorganized Monotonous sequence within single GM Some body parts are not involved in the mov. Repetition of same sequence from GM to GM Variable sequence
Spatial sectors of the movements 1 Not variable 2 Variable
Fluency and elegance 1.a 1.b 2
Not fluent, no rotations Not fluent, few rotations Fluent and elegant, many rotations
Onset-offset of GMs. 1.a 1.b
2
Abrupt Minimal fluctuations in intensity Smooth crescendo and decrescendo
98 F. Ferrari et al. I Early Human Drvelopmcnt 50 (1997) 87-113
Table 2. Continued Evaluation sheet of general movement quality
VIII Subtle distal movements 1 .a l.b 1 .c
1 .d 2
Continual fisting No or rare finger movement.\ Only synchronized opening and closing finger movements Few variable finger movements Large variety of finger and hand movements (including hand rotation)
Global Evaluation: (N-A-Hypokinesia)
Date
Optima@ score: (maximal 16) Examiner
Case 2: chromosomal abnormality [de1(4)(p15.1)] and congenital asymmetrical hydrocephalus
Video recording at 43 weeks PMA Actogram (Fig. 3 b): the state profile displays state 1 and 4, no state 2 and 3. no
sleep cycles.
Fig. 1. Alobar holoprosencephaly. MR coronal MPGR 500/9/2 I,5 T image of Case 4 at 15 days: abnormal gyral configuration (pachygyria), marked thinning of the hemispheric white matter, absence of the corpus callosum and of the interhemispheric fissure, fused thalami, absence of the third ventricle and presence of a crescent-shaped holoventricle.
Tabl
e 3
Scor
es
of
the
eight
GM
cr
iteria
an
d m
otor
op
timali
ty sc
ore
in
the
nine
infa
nts
Newb
orn
PMA
SCOR
E SH
EET
PARA
METE
RS
Optim
al@
infan
ts sc
ore
I II
Ampli
tude
Spee
d
UI
Move
ment
chara
cter
IV
Sequ
encin
g
V Spa&
l
secto
rs
of the
mov
emen
ts
VI
FhW
lCY
and
elega
nce
VII
onse
t-
offse
t of
GMs
VIII
Subtl
e
distal
mov
emen
ts
Case
1
38 w
ks
1C
1C
la lb
2 la
la Id
9
Case
2 43
wks
2
la lb
Ic 2
lb 2
2 12
case
3
case
4
case
s
Case
6
Case
1
45
wks
39 w
ks
42
wks
39wk
s
43 w
ks
44 w
ks
38 w
ks
40 w
ks
49 w
ks
la la la la la Ic 2 la la
la la la lb lc Ic la la la
le
1.Z
le
le
Id la le le la-k
1C
le la IC-le
IC-le
la 1C
lc Ic-le
la
lb lb lb la la la la la
lb lb la lb la la 2 2 2
lb 8
2 9
Id 8
lb 8
Ic
8
la-k
8
Id 10
Id 9
Id
9
54 w
ks
lb la
la-le
la-k
1 la
la Id
8
Case
8
3owk
s la
la Id-
le lc-
le I
la 2
la 9
34W
kS
1C
Ic 1C
lb
I lb
lb Id
8
35 w
ks
2 2
2 2
2 lb
2 2
15
41 w
ks
lb lb
la la
1 la
la la
8
Case
9
40 w
ks
la la
le 1C
1
lb lb
lb 8
F. Ferrari et al. / Early Human Development 50 (1997) 87-113
(a) (b) Fig. 2. (a and b): Hydranencephaly. MR Axial SE 600/20/2 1,5 T images of Case 8 at 33 weeks PMA: absence of a vast portion of the cerebrum replaced by cerebrospinal fluid, presence of the thalami and residual portion of the right fronto-temporal, right and left occipital lobes.
Movement patterns: large amount of twitches and isolated arm movements in contrast with no isolated leg movements.
Posture (Fig. 4, Case 2, a and b): unusual preference postures with scoliosis of the neck and retroflexion of the head. No other postures.
GIws: monotonous repetition of extrarotations of the arms and of fragmented movements of the limbs, mainly in the horizontal plane; movements are floppy, onset-offset of GMs is gradual, amplitude, spatial sectors and subtle distal movements are variable. Global evaluation: poor repertoire GMs.
Optima&y score: 12 (Table 3, Case 2). The unusual posture and the floppy character of GMs are peculiar to this baby.
Case 3: polymicrogyria and multiple malformations
Video recording at 45 weeks PMA Actogram (Fig. 3 c): the state profile shows a brief state 2 episode followed by
alternation of state 4 and 3, no sleep cycles. Movement patterns: startles and trunk movements are not observed during the video recording.
Posture (Fig. 4, Case 3, a): unusual dominant posture with head and trunk lying on
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 101
T/i
RJ IllIll III1 II II Ill I I lllll uu II II I III III II ST I III I/ / I HF
MW HR I I y? TF
TA TR II II I I I
: I II I I II I II IIlIImIlllPI III/l I I II so II I IF 1 l I I’,,
I I I IIIII aI II II I II /
II-I I I I I /I I III II II III1 I MM Ia I II I I I I YA FC I III I /Ill I 1
Fig. 3. (a) Behavioural state profile and actogram of Case 1, GA 38 weeks, at 38 weeks of PMA (CP, change posture; SR, stretch, TM, tremulous movement; CL, clonus; TW, twitch; ST, startle; HF, head retroflexion; HR, head rotation; TF, trunk flexion; TA, trunk arching; TR, trunk rotation; IL, isolated leg movement; IA, isolated arm movement; SO, sob; IF, isolated foot movement; IH, isolated hand movement; MM, mouth movement; YA, yawn; FC, hand-face contact; SM, smile). Periods of dissociated state are indicated by interrupted lines. The horizontal axis shows time in minutes. (b) Behavioural state profile and actogram of Case 2, GA 42 weeks, at 43 weeks of PMA. (c) Behavioural state profile and actogram of Case 3, GA 41 weeks, at 45 weeks of PMA. (d) Behavioural state profile and actogram of Case 4, GA 37 weeks, at 39 weeks of PMA. (e) Behavioural state profi~e and actogram of Case 5, GA 38 weeks, at 39 weeks of PMA. (f) Behavioural state profile and actogram of Case 6, GA 40 weeks and 5 days, at 43 weeks of PMA. (g) Behavioural state profile and actogram of Case 7, GA 36 weeks, at 38 weeks of PMA. (h) Behavioural state profile and actogram of Case 8, GA 25 weeks and 3 days, at 41 weeks of PMA
102 F. Ferrari et al, I Early Human Development .li(l (1997) 87-113
5 4
STATE 3 2- 1 - GENERAL ’
MOVEMENTS - 4M n n nn - r!nrl L
SR TM CL w ST HF
MAIN HR
y;” TF TA TR IL
To IF IH MM YA FC
STATE
II
I I II I
II I Ii
I II i
I I
I I lllll
(di
_-__- I-----“---7---
GENERAL ’ MOVEMENTS n nn nn ru-trln r-l--
SR TM I
& II ’ I, I It I I ST I II I I /
HF MAIN HR I m II Ill I llli I ii
“;;F TF TA TR IL I I I I 1 i II
IA I II I SO IF IH MM I I IIU PW / III il il YA
It I Ii
FC I11 I
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 103
5 4
/--
--___- STATE 3
* 1
GENERAL ‘1 MOVEMENTS
m
SR TM CL Tw ST HF
h@.lN HR M;;;. TF
TA TR IL IA SO IF
I I ill I I
I I I I II IllI I I II
I’ I I
I I
I II I
IH MM II II I I II III I I
I II I I
YA I FC I II Ml I Ill I Ill I11 I II Ill III1 IU I
SM 11 1 GdE IN LIN. 16 I6 66 26 66 II 66 66 66 66 60
6 1.
STATE 3 2 [ I (f)
I
GENERAL d,,,,,nnn u - MOVEMENTS r-ti-a 81 n
MAIN MOVEM.
PATT.
SR TM CL l-w
iz HR TF TA TR IL
& IF
L4
2 SM
II I II I III I
I I I I I I I II II II I 1 I I I III I I I II I I I
I I I I I II I Ill II
III I Illi II I I I
III/ I II II/II I I II I II II I R II I
I I I I
I I I III I I I II I
I I I II UIIII I
t-ME IN “,I,. 16 $6 26 66 30 66 66 46 66 66 66
Fig. 3. (continued)
104 F. Ferrari et al. I Early Human Development 50 i1997) 87-113
STATE
GENERAL MOVEMSNTS
SR
T Tw ST I-IF
t.wN HR y;F TF
TA TR IL
:o IF IH MC YA FC SM
ll-lRnlu u -L--.
II I I I I I I
II /
II I II I II Ill I I i I I llill IU I ! I ii Ill I !
Ill II II I I if ! I I I I I I I
I II I
I ;I I I I i
0 10 10 20 20 so 35 IO 40 00 56 60 ME IN MN.
5 II_
4 STATE 3 (h)
2 1
GENERAL ‘1 n m0vEmENT.s r-ulnnn nnan_r -.
SR TM II II II III I Ill I llil bl I /t/i ill IO/ II iii
%d II I
I/ I I ST / II I HF 1111 II III il II Ill! I ! IU
MAIN HRII 1 I II I I’ll! I II “;z&?, TF I I
TA /\I I I ! I ! / II I II
TR I II
IL
& IF IH
SM 1 ;lMS 0 MIN. 10 lo I 20 so a0 4 40 50 00 00 IN
Fig. 3. (continued)
F. Ferrari et al. I Early Human Development 50 (1997) 87-113
106 F. Ferrari et al. / Early Human Development 50 (1997) 87-113
the right side, flexed limbs, extension of neck and trunk. Limb movements are limited to the horizontal plane.
GMs: predominantly slow and small amphtude movements, repetition of the same movement sequence. Global evaluation: marked poor repertoire GMs.
Optimality score: 8 (Table 3, Case 3). Body posture is peculiar; monotony of the motor sequencing is the main feature oi
GM quality.
Case 4: holopmsencephaly
Video recording at 39 weeks PMA Actogram (Fig. 3 d): the state profile shows a long phase of state 1 and dissociated
state followed by state 4 and 3. No state 2 episodes and no sleep cycles. Movement patterns: no trunk movements, no isolated hand and foot movements.
Posture (Fig. 4, Case 4, 39 weeks, a and b): preference posrures with flexed or semiflexed limbs. Poor posture variability.
GMs: repetition of small amplitude head movements, elegant wrist rotations, hand face contact. Global evaluation: Poor repertoire GMs.
Optimality score: 9 (Table 3, Case 4, 39 weeks). No posture and movement peculiarities, extreme monotony of the movement
sequence.
Video recording at 42 weeks PMA Posture: (Fig. 4, case 4, 42 weeks, a): dominant ATN posture. GMs: stereotyped pedalling, frequent asymmetric tonic neck (ATN) posture during
GM, abrupt, synchronous, stereotyped, short-lasting limb movements. Limb move- ments, small in amplitude, similar to myoclonic jerks. Tremors are often superim- posed on limb movements. Global evaluation: marked poor repertoire GMs.
Optima&y score: 8 (Table 3, Case 4, 42 weeks). Small, synchronous movements of the limbs, similar to myoclonic jerks and no
trunk movements are unusual and peculiar features.
Case 5: congenital microcephaly
Video recording at 39 week PMA Actogram (Fig. 3 e): the state profile shows all 5 behavioural states, predominance
of state 4, no sleep cycles. Movement patterns: no twitches, startles, cloni. tremors, trunk, isolated foot and isolated hand movements. Many hand-face-contact move- ments in contrast to a lack of subtle distal movements.
Posture (Fig. 4, Case 5, a and b): unusual postures with head and trunk lying on the left side, flexed upper and flexed or extended lower limbs. No other postures. Limb movements are limited to the horizontal plane.
GMs: stereotyped adduction-abduction of the forearms, repetitive rowing and pedalling movements, no wrist rotations, poor trunk movements, abrupt and jerky
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 107
head rotations, no fluency or elegance, monotonous sequencing. Crying does not change the movement patterns. Global evaluation: Poor repertoire GMs,
Optimality score: 8 (Table 3, Case 5). Continual ongoing of GMs, stereotypy of the movement sequence within single
GM and from GM to GM and a limited repertoire of the movement patterns are the main features of the motor activity.
Case 6: macrocephaly
Video recording at 43 weeks PMA Actogram (Fig. 3 f): the state profile shows periodical transitions from wakefulness
to sleep (state 1 or 2) and again from sleep to wakefulness without a single sleep cycle. Movements, and GMs in particular, tend to occur in burst-pause patterns rather than being scattered over the record.
Movements patterns: cloni, trunk movements and isolated hand movements are not observed.
Posture (Fig. 4, Case 6, 43 weeks, a and b): unusual postures with flexed wrists and elbows. Poor posture variability.
GMs: brisk and synchronous onset of GMs, low threshold to Moro response, tremors during GM, no trunk movements, brisk head rotations, synchronous opening of the hands, dominantly slow, small range limb movements, frozen posture in extension of the lower limbs. Global evaluation: marked poor repertoire GMs.
Optima& score: 8 (Table 3, Case 6). Flexed posture of the wrists is peculiar; monotonous sequencing of the limb
movements and brisk head rotations are the main features of the motor activity.
Video recording at 44 weeks PMA Posture (Fig. 4, Case 6, 44 weeks, a and b): unusual postures with wrists still
flexed, full extension of the legs. Poor posture variability. GMs: few tremors, cramped-synchronized GMs with tremors superimposed, poor
trunk movements, frozen posture in extensions of the lower limbs, opening of the mouth synchronous to limb movements, no finger movements. Global evaluation: cramped-synchronized GMs.
OptimaEizy score: 8 (Table 3, Case 6).
Case 7: parieto-occipital encephalocele
Video recording at 38 weeks PMA Actogram (Fig. 3 g): state profile presents state 4 and 3, no sleep states. Movements patterns: GMs are so close to each other that they can hardly be
distinguished; as regards other movement patterns, head rotation, trunk movements, tremors and cloni were not observed.
Posture (Fig. 4, Case 7, 38 weeks, a and b): preference postures with head fixed to the right side because of the big parietal-occipital encephalocele. Poor posture variability.
108 F. Ferrari et al. I Early Human Development 50 (1997) 87-113
GMs: variable amplitude, smooth crescendo and decrescendo, monotonously slow speed, monotonous sequence within single GM and from GM to GM, slow flexion of the lower limbs. Global evaluation: poor repertoire GMs.
Optimality Score: 10 (Table 3, Case 7, 38 weeks).
Video recording at 40 weeks PMA Posture (Fig. 4, Case 7, 40 weeks, a and b): ATN preference postures. GMs: look similar to the previous recording with a more limited motor repertoire
and consistent monotony of the sequencing. Global evaluation: poor repertoire GMs. Optima&y score: 9 (Table 3, Case 7, 40 weeks).
Video recording at 49 weeks PMA Posture (Fig. 4, Case 7, 49 weeks, a and b): preference postures with ATN and
reverse ATN posture. Poor posture variability. GMs: cramped movements of the upper limbs, no fidgety movements, repetition of
the same motor sequence. Global evaluation: poor repertoire GMs with some cramped movements of the upper limbs.
Optimality score: 9 (Table 3, Case 7, 49 weeks).
Video recording at 54 weeks PMA Posture (Fig. 4, Case 7, 54 weeks, a): unusual dominant posture with head
retroflexion, trunk arching, no more ATN posture. Head position affects the sequence and the variability of the movements.
GMs: no fidgety movements, no hand-hand contact, no foot-foot contact, pool repertoire and synchronized movements. Global evaluation: synchronized movement< of all four limbs; lacking fidgety movements.
Optimality score: 8 (Table 3, Case 7, 54 weeks). Monotony of the movement sequence (poor repertoire GMs) in the first three video
recordings and the cramped-synchronized character at 54 weeks PMA are the main features: body and limbs posture is affected by the fixed position of the head.
Case 8: hydranencephaly
Video recording at 30 weeks PMA Posture (Fig. 4, Case 8, 30 weeks, a and b): preference postures with flexed or
semiflexed limbs, poor posture variability. GMs: very short and poorly differentiated GMs, stereotyped sequencing from GM
to GM, myoclonic jerks of the limbs. Global evaluation: marked poor repertoire GMs. Optima& score: 9 (Table 3, Case 8, 30 weeks).
Video recording at 34 weeks PMA Posture (Fig. 4, Case 8, 34 weeks, a and b): ATN preference postures, poor posture
variability. GMs: flapping and chaotic GMs, poor postural control. ATN posture, rhythmical
F. Ferrari et al. 1 Early Human Development 50 (1997) 87-113 109
tongue protrusion and mouthing, no fluency and elegance. Global evaluation: chaotic GMs.
Optima&y score: 8 (Table 3, Case 8, 34 weeks).
Video recording at 35 weeks PMA Posture (Fig. 4, Case 8, 35 weeks, a and b): preference postures with flexed limbs. GMs: variable amplitude, speed, movement character, sequencing, and spatial
sectors; smooth onset-offset; variety of subtle distal movements; lacking elegance and fluency. Global evaluation: abnormal GM quality because of lack of fluency and elegance, quality of GMs is markedly improved compared to the previous recordings.
Optimal@ score: 15 (Table 3, Case 8, 35 weeks).
Video recording at 41 weeks PMA Actogram (Fig. 3 h): the state profile identifies one short state 1, preceded and
followed by wakefulness and crying, no sleep cycles. Movement patterns: isolated leg, arm, foot and hand movements are not seen.
Posture (Fig. 4, Case 8, 41 weeks, a and b): unusual preference postures with head retroflexion and trunk arching. Limb movements take place predominantly in the horizontal plane. No other resting postures.
GMs: small amplitude, slow, forceful, synchronized GMs, synchronous opening and spreading of the fingers, fast small amplitude tremors. Global evaluation: cramped-synchronized GMs.
Optima&y score: 8 (Table 3, Case 8, 41 weeks). A change in quality of GMs is seen throughout the successive four video
recordings: initial poor repertoire GMs at 30 weeks are followed by chaotic GMs at 34 weeks and by a surprising (and to our knowledge inexplicable) improvement of GM quality at 35 weeks; a major motor abnormality, the cramped-synchronized character, appears at 41 weeks PMA.
Case 9: hemimegaluencephaly
Video recording at 40 weeks PMA No actogram was performed as the video recording was too short. Posture (Fig. 4, Case 9, a and b): two preference postures, poor posture variability. GMs: during 15 mm of video recording the newborn shows two brief GMs in state
4; amplitude is monotonously small, speed is monotonously slow, poor sequence within single GM and from GM to GM. Movements are fluent but not elegant. No clear asymmetry in posture and movement. Global evaluation: poor repertoire GMs.
Optima& score: 8 (Table 3, Case 9). The repetition of slow and small amplitude limb movements and the monotony of
the motor sequence are the dominant features. No asymmetry in posture and movement was detected despite the brain malformation being limited to the right brain hemisphere.
110 F. Ferrari et al. / Early Human Development 50 (‘1991) 87-113
4.1. Quantitative abnomurlities of movement patterns
With respect to the quantitative abnormalities, six of the eight babies who were observed with 1 h video recording lacked one (5 Cases) or two (I Case) movement patterns usually present in normal healthy newborn infants. The missing patterns were isolated leg and/or isolated arm movements in three infants, startles in two infants, twitches and head rotation in another two infants. Among the so-called inconsistently occurring movement patterns (they may be present or absent even in normal infantsj trunk movements (5 Cases), isolated foot and/or isolated hand movements (4 Cases) and cloni (2 Cases) were not observed in our study group. ‘The combination of several movement patterns differed from infant to infant: the anencephalic newborn infant lacked isolated movements of arms, legs, hands and fee:; Case 3, polymicrogyria, lacked startles and trunk movements; Case 4, holoprosencephaly, lacked trunk and isolated hand movements, Case 5, congenital microcephaly, lacked startles, twitche%. cloni, tremors, trunk movements and isolated hand and foot movements; Case 6. pachygyria (Zellweger syndrome), lacked cloni and isolated hand and trunk move- ments; Case 7, parieto-occipital encephalocele, lacked head rotations, trunk move- ments, tremors and cloni; Case 8, hydranencephaly, lacked isolated arm, leg, hand and foot movements.
4.2. Qualitative abnormalities of general movements
These distinct brain malformations were accompanied by a variety of motor abnormalities: chaotic and cramped-synchronized GMs in anencephaly, floppy movements in congenital hydrocephalus, slow, small amplitude movements in polymicrogyria, small, synchronous, jerky movements of the limbs in holoprosence- phaly; stereotyped adduction-abduction of the forearms and abrupt head rotations in microcephaly; brisk and tremulous limb movements and brisk head rotations in macrocephaly (Zellweger syndrome); monotonous repetition of slow, small amplitude limb movements in hemimegaloencephaly; persistent monotony, throughout the first three videorecordings, of the movement sequence in parieto-occipital encephalocele.
Quality of GMs of infant with hydranencephaly changed dramatically throughout the successive observations: very short and poorly differentiated, monotonous GMs at 30 weeks PMA, flapping and chaotic GMs at 34 weeks PMA, variable GMs at 35 weeks, cramped-synchronized GMs at 41 weeks. The difference in quality from one recording to the next was striking, as well as the transient improvement of GM5 quality at 35 weeks: we could not find a reasonable explanation for them.
5. Discussion
As expected, infants affected by severe brain malformations exhibited abnor- malities of posture and of movements. The preference resting posture varied from infant to infant, but in all cases was less variable than in normal newborn infants. An unusual posture, not seen in healthy full-term infants 151. was observed in seven out
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 111
of the nine infants. A dominant posture was present in three infants (Cases 3, 4 and 7): in these three infants, as well as in two others (Case 1 and 5), who were laying on one side, posture had a clear influence on limb movements.
In 8 out of the 9 Cases, 1 h video recording enabled us to establish a behavioural state profile and assess the infant’s state organisation. In all cases, sleep organisation was very poor: sleep cycles as such were absent in all infants; six out of the eight displayed excessive wakefulness; one of the two sleep states was absent in 4 cases; the only sleep observed in one infant was a dissociated state. These findings fully agree with previous findings by Monod and Guidasci [12] who described newborn babies with brain malformations as poor sleepers, with high percentage of wakeful- ness, no or poor sleep cycles.
The sequence of occurrence of GMs was clearly abnormal in two infants, one being affected by anencephaly and the other by pachygyria and cerebellum hypo- plasia: GMs occurred in burst-pause patterns instead of being scattered over the recording. Similar findings were observed by Visser et al. [24] in 6 of the 8 anencephalic fetuses observed with ultrasound in utero.
Abnormality is expressed in quantity and quality of spontaneous motor activity. Once again, as in previous studies on fetuses and on newborn infants with brain
impairment [9,20,24], qualitative changes in spontaneous movement prevailed over quantitative ones.
As for the quantitative abnormalities of spontaneous movements, they consisted in the lack of one or more movement patterns but no relationship was observed between defective movement patterns (or their combination) and specific brain abnormalities.
Turning from the quantitative to the qualitative aspects of spontaneous movements, with specific reference to GMs, we set out to discover whether the absence of certain parts of the brain might have a direct influence on GM quality.
It is known from the pioneering work of de Vries et al. [7] that GMs appear very early (weeks 8-9) in fetal life, when they are slow and of limited amplitude. Later on, at lo-12 weeks, GMs become more forceful but are smooth in appearance and of large amplitude. After 12 weeks, GMs become more variable in speed and amplitude; there are no major changes in their appearance between 8 and 20 weeks. Considering the second half of pregnancy, Roodenburg et al. [21] have shown that the same holds true. Cioni and Prechtl [6] have demonstrated in preterm infants that GMs between 28 weeks and term age change very little. In other words, we know that most of the qualitative features of GMs are already present during the 4’h-5’h month of gestation, with minor changes occurring in the last trimester of pregnancy (see Prechtl, 1989 [15] for review).
We can suppose that the generating neural network responsible for GMs could be primarily located in the brain stem and spinal cord, higher structures of the brain playing a more subtle role in modulating quality and, perhaps, time patterning of the different movement patterns.
The present study failed to find any connection between the absence of a specific part of the brain and GM abnormalities, or between the quantity of defective brain tissue and the degree of GM abnormalities. Anencephaly and hydmnencephaly were the two cases with most defective brain tissue, yet GM abnormalities were no worse,
112 F. Ferrari et al. I Early Human Development 50 (1997) 87-113
in terms of GM quality, than in microcephaly, holoprosencephaly and other brain malformations where there was less defective brain tissue.
Brain malformations in our study differed greatly from each other as regards type and severity of CNS malformation. The cerebral cortex, cerebral hemispheres. s&cortical and periventricular zones, cerebellum and corpus callosum were affected to a greater or lesser extent in individual infants, whereas the brain stem and spinal cord appeared less affected or even intact but, of course, without the normal input from the higher centres.
These distinct brain malformations were accompanied by a variety of motor abnormalities. This is why we felt the need to describe in detail spontaneous motor activity case by case. No infant displayed GMs identical or similar to those of other infants: each newborn infant had a sort of a personal movement “style” that was easily recognizable. This was true in all infants with the exception of the anenceph- alit infant, who displayed different types of abnormal GMs during the same recording: poor repertoire GMs, cramped-synchronized GMs and chaotic GMs. Similarities were also present and deserve mentioning along with individual differ- ences. All our infants displayed poor repertoire GMs or marked poor repertoire GMs. Poor repertoire is characterised by monotony and lack of complexity of the sequence of successive movement components. From previous studier; on GMs of preterm and term infants affected by brain lesions of perinatal origin, i.e. intraventricular- periventricular haemorrhages and/or periventricular leukomalacia in preterm infants [4,9] and hypoxic-ischaemic lesions in full-term infants [4,19], we know that poor repertoire GMs is the most common motor abnormality. It is a sign of minor brain dysfunction when it is transient and disappears during the first months of life. However, it may be a sign of severe brain impairment when it is consistent or followed by severe motor abnormality like cramped-synchronized GMs, as in our case studies. Of the four infants with more than one video recording, three displayed poor repertoire GMs followed by cramped-synchronized GMs or, in one case (Case 4), by marked poor repertoire GM. These data once aga.in suggest the need for longitudinal observations.
The repetition of the same sequence within a single GM and from GM to GM wa\ a common feature of the brain-malformed infants of this study.
The putative role of upper structures in modulating GM quality seems confirmed by these clinical observations: one of the main features of normal GMs, along with fluency, elegance and complexity is variability. GMs are variable when. along with continuous changes in speed, force, amplitude and spaciai sectors, the sequence of the different body parts involved in movement changes within the single GM and from GM to GM. This did not occur in the infants of the present study.
Acknowledgements
The authors are grateful to Prof. Trentini and his co-workers who performed the post-mortem examinations, to Dr. Mavilla and Dr. Siotini for description of the CT and MRI findings and to Luca Ori who performed the EEG-polygraphic recordings in Modena.
F. Ferrari et al. I Early Human Development 50 (1997) 87-113 113
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