A long-term fluoroscopic study was performed
on pregnant ewes over several lambing seasons to
determine the nature of sheep fetal behaviour.
This study led to the recognition of the
phenomenon of fetal pandiculation, which
is essentially similar to the post-natal
pandiculation now seen as a comparative
phenomenon of systematic stretching. The
characteristic features of fetal
pandiculation have now been studied in
general form and as specific components in the
fetuses of 22 ewes. Thirty-three events of full
pandiculation were detected in 25
episodes in 222 observations. The extant
definition of pandiculation was used as
the frame of reference for the phenomenon as
follows: "An instinctive movement, consisting in
the extension of the legs, the raising and
stretching of the arms and the throwing back of
the head and trunk, accompanied by
yawning". In addition, extension of the
axial skeleton and vigour were taken as further
definitive features of full
pandiculation.
The phenomenon has both form and
composition. In form, various salient features
can be identified as typical. In the order
approximating their consistency of expression in
the phenomenon, they include: (I) pattern; (II)
direction; (III) elongation and extension; (IV)
polarity; (V) episodic occurrence. Since these
features occur in the majority of cases, they
can be taken as identifying the general form of
major pandiculation.
No episode of fetal pandiculation
incorporated all of the characteristic
components. A score was made of the numbers of
components occurring per episode; scores ranged
from 6 to 8, to a maximum of 9. The modal
average was 7. Additional features included: (a)
temporal distribution distribution was even
throughout the period of gestation studied (2-20
days pre-partum); (b) incidence per fetus - full
pandiculation was usually encountered in
each fetus on only one or two occasions; (c)
partial pandiculation - this was
recognised when the components were reduced in
expression of vigour or in number. Partial,
incomplete and minor pandiculations collectively
numbered 63, and exceeded full pandiculations in
incidence.
Fetal pandiculation could be related
to the ends of fetal somnolent states and may be
a marker of transitional phases between sleep
and alert states. It can therefore indicate that
the phasic nature of fetal processes is being
sustained normally and may thus indicate that
the status of the fetus is satisfactory in
general respects. Viewed in a wider, comparative
light, fetal pandiculation could be
regarded as a simple signal of adequate
well-being which could be identified by
non-invasive methods. It is clear that the
phenomenon calls for appropriate attention in
further work The pursuit of research into fetal
behaviour can be a profitable branch of
fetology.
Introduction
In the finite space of the uterus, the fetus
is able to produce remarkable and various
movements. The features of fetal movement call
for appreciation since they probably relate to
fetal well-being and perinatal competence.
Contemporary studies on fetal respiratory
movements have overshadowed other forms of fetal
movement (Bowes et al., 1981; Harding and Poore,
1982), but all activity has significance in the
course of fetal development (Liggins and
Gluckman, 1984). In particular, fetal kinesis
indicates forms of movement in confined space
essential to normal physical function. In the
course of practical situations in veterinary
obstetrics, the gross kinetic movements and
attitudes of the maturing fetus require to be
identified so that appraisal of the fetal status
can be made. Additionally, in comparative
obstetrical work there is flow an
acknowledgement of "the need for a simple
non-invasive test of fetal wellbeing" (Harding,
1984). This may lie in fetal movement in some
form (Truclinger et al., 1979). Fetal kinetics
warrant more study.
The sheep has been a traditional and
suitable model for both human and animal
fetology, and parturient physiology from the
studies of Barcroft and Barron (1937) to the
present (Hecker, 1983). Some later studies on
fetal kinetics were based on Doppler ultrasound
before real-time ultrasound was used (Goodman
and Manteli, 1980; Wittman et al., 1981). As an
alternative to ultrasound, an earlier
radiographic study on the principal features of
fetal kinesis in the sheep reported simple and
complex movements, and postural steps prior to
parturition (Fraser and Terhune, 1977 a,b). At
the conclusion of that report, it was stated
that: "In future studies of this nature,
fluoroscopy and possible cine-radiography could
prove of value" (Fraser and Terhune,
1976b).
Cine-radiography was subsequently found to
have technical difficulties relating to film
development, but fluoroscopy proved suitable and
a long-term fluoroscopic programme was embarked
upon in sheep. The video-taped records from this
work were accumulated over several breeding
seasons before being thoroughly studied. From
this work, an observation on overall sheep fetal
posture at birth, including elbow flexion
intrapartum, has been reported by Husa et al.
(1988) which confirmed the radiographic findings
of Fraser and Terhune (1977b). Review and
synthesis of these fluoroscopic records led to
the recognition of the phenomenon of
pandiculation in the sheep fetus.
The general form of pandiculation can
be given briefly as a vigorous overall extension
of the body with upward and forward extension of
the head, forward extension of the forelimbs and
stretching of the spinal column. In some
instances, there is also hind limb extension.
Wide yawning is also included in some
instances. This stretching behaviour in the
fetus is essentially similar to the post-natal
and adult pandiculation, which itself has
only recently been recognised as a comparative
phenomenon of systematic stretching (Fraser,
1989a). Characteristic fetal
pandiculation has now been studied, in
its general form and specific components, in an
extensive review, involving 222 observations on
22 ewes.
Various components can be recognised in
fetal pandiculations. In the order of their
apparent occurrences they are as follows: (1)
elbow extension; (2) elbow advance; (3) carpal
and digital extension; (4) cervico-occipital
extension; (5) head elevation; (6) pandiculated
pose; (7) intention movements; (8 and 9)
yawning and jaw movement.
Animals, materials and methods
The recordings on which this report is based
were made during three sheep breeding seasons.
All the ewes were of the Newfoundland breed type
and were taken as available from an adjacent
research flock. Each chosen animal had been
previously screened to ensure that it was
pregnant. In as many cases as possible, ewes
were selected which carried only a single fetus.
They were monitored by the fluoroscopic method
on a loose schedule daily, or on alternate days,
throughout the period estimated as the final 2-3
weeks of gestation. Each sampling period was of
10 min duration, during which all the
fluoroscoped skeletal images on the monitor
screen were also recorded on video tape by a
video cassette recorder coupled to the monitor.
On some occasions, repeat observations were
carried out later in the same day to determine
the persistence of some feature of interest,
such as pre-partum orientation.
All ewes were placed, with minimal
restraint, on the X-ray table in left lateral
recumbency. This position was chosen to minimise
any effect from rumenal weight and bulk
overlying the fetus, and possibly impeding its
movement, since fetal activity can be
compromised by maternal forces (Harding et al.,
1981). A canvas binder was used over the ewe's
body to provide stability for the ewe on the
table. Rope hobbles were placed on paired
forelimbs and hind limbs, and secured to the
side rail of the table. Blindfolds over the eyes
of the ewes were found to quieten them. Ewes
soon adapted to the procedure and after the
initial few sessions there was little struggle
during fluroscopy.
When the recordings were subsequently
reviewed, very specific features, such as limb
movements which have been noted by others
(Natale et al., 1981; Rigatto et al., 1982),
were the initial focus of attention. However,
after the holistic phenomenon of
pandiculation was discovered, all further
reviews were aimed at singling out and
interpreting this special feature. Since it was
only occasionally shown by the fetus and had not
been specifically sought out in the initial
monitoring, locating the episodes of
pandiculation required thorough searching
of all the recordings. Although some of these
lacked focus, many examples were discernible and
complete. They were present in real time on the
tapes and existed as a short phase of activity
which might be analogous to the short-term
cycles of activity which have been reported in
the human fetus (Granat et al., 1979). The taped
material did not always bridge the entire
shortterm episode owing to the cut-off time of
the original taping or loss of target. Viewing
both fore and hindquarters at the same point in
the observation was difficult, except in those
cases where curving of the fetal spine brought
them together.
Definitions
The definition of pandiculation, as
given in the Oxford English Dictionary, was used
as the frame of reference for the phenomenon as
follows: "An instinc tive movement, consisting
in the extension of the legs, the raising and
stretching of the arms and the throwing back of
the head and trunk, accompanied by
yawning". In addition, extension of the
axial skeleton and vigour were taken as
definitive features of full
pandiculation. It became apparent that
some episodes of this phenomenon lacked some
degree of quality or some components. These
instances were designated as partial
pandiculation, a term which also included
minor pandiculation. The phenomenon was
therefore classified into full or partial
categories. The definition given to the latter,
for the purposes of this study, was as follows:
"A bodily extension which lacks some property of
major pandiculation but which retains
some of its salient features such as full limb
and axial extension".
Results
General form of major
pandiculations
Events of overall, holistic extension were
seen as complex fetal movements of a high order
of organisation. They were notable in a
particular state in which the fetus exhibited
maximal extension of head and neck, together
with marked forelimb extension. The limb
extensions were bilaterally symmetrical and
sometimes bipolar, i.e. affecting both fore and
hind poles of the fetal axis. The co-ordination
of all these sundry extensions showed that they
were related in one general kinetic feature of
extension, viz. pandiculation. Episodes
of this phenomenon were comparatively rare and
usually isolated events, but at other times they
occurred in a sequence of two or three instances
in close association. Thirty-three major
pandiculations were seen in a total of 22
fetuses (Table 1).
In form, various salient features can be
identified as typifying the activity. Some of
these are constant and, to that extent,
definitive; others are variable features of
general form. They are described below in the
order approximating their consistency of
expression in the phenomenon.
I Pattern
The progressive course of the actions in
pandiculation, after being effectively
initiated, exhibited a pattern. The outline of
this behavioural scheme conformed to the concept
of an action pattern, as defined by McFarland
(1987). The several movements flowed into each
other, creating one compound action of 5-10 s
duration.
II. Direction
The collective effect of these fetal
movements was distal extension, resulting in
pandiculation having a longitudinal
direction. In this, it was more often observed
that the anterior parts, namely the head, neck
and forelimbs, influenced the longitudinal
direction in the disposition of the fetus. In a
proportion of cases, both fore and hind parts
participated simultaneously in extensions. It
was taken as axiomatic that the phenomenon
required the vigorous extension of the head,
neck and forelimbs as essential features. When
extension of the hind limbs occurred alone, this
was not taken as an episode of
pandiculation, particularly since some
hind limb extensions were directed anteriorly,
rather than posteriorly, in relation to the
fetal body. As a result of the head and neck
twisting during extension, a few pandiculations
had a rotary direction. The degrees of such
rotation were often 90-180', in relation to the
long axis of the fetus.
III. Elongation and extension
The longitudinal direction resulted in the
fetus being outstretched. It follows that these
two features are related to each other, but they
are subtly different in that one characterises
the initial step of the phenomenon, while the
other describes its final form. Linear
elongation was also a consequence of rotary
pandiculation which was, incidentally,
more often observed in the fetus in a supine
position than in a prone position.
The whole activity took the form of a
vigorous action which resulted in the extension
of the fetus in its totality. Vigour was a
notable quality in the form of this kinetic
event.
IV Polarity
Pandiculation was sometimes bipolar in form,
in that both forequarters and hindquarters were
involved in the extension. This appeared to take
place in some instances with the foreparts
extending marginally before the hind parts did.
Sometimes, pandiculations appeared to involve
only the anterior end of the animal and such
extension was taken as one of the identifying
forms of this activity. Observations on this
feature were made difficult by the inability to
monitor both ends of the fetus simultaneously
unless the fetus presented these in one
radiographic field by virtue of lateral spinal
flexion.
V. Episode
It was usual for instances of full
pandiculation to occur in isolation. In
addition, these events were of low frequency and
only occurred in 25 (- 11%) of the
observations.
In five episodes, pandiculations occurred in
series, with one event following almost
immediately after another. In three of these
cases, three pandiculations occurred, while in
the two others two pandiculations occurred in
close succession forming a pair of actions
taking the form of one pandiculated
episode.
The above features occur in the majority of
cases and can therefore be taken as identifying
the general form of major pandiculation.
Within the general form, various components can
be recognised. These are listed in Table 2a and
b, and are given there and below in the order of
their apparent incidence in
pandiculation.
Components of fetal
pandiculation
1. Elbow extension This component
occurred in every instance and was considered to
be one of the definitive features of the
phenomenon. Typically, both elbows extended
simultaneously and to an equivalent degree.
2. Elbow advance Somewhat in
association with elbow extension, advance of the
elbow joint was also a notable feature and
occurred in each instance of full
pandiculation. Again, this was taken as a
definitive component. The advance of the elbow
was, of course, the consequence of the shoulder
joint extending, but the resultant shifting
forward of the elbow was the more prominent
result.
3. Carpal and digital extension In
association with extension of the elbow and the
shoulder (as given above in Nos. I and 2), full
extension of the carpal and digital joints also
occurred. This obviously resulted in the
forelimbs being extended forward to their
fullest extent.
4. Cervico-occipital extension
Together with the above three components,
this item of head and/or neck extension was also
an identifying characteristic in
pandiculation. Typically, in this the
head was extended to its fullest possible
position, chiefly as a result of maximal
extension of the atlanto-occipital joint.
5. Head elevation While this
component was similar to component 4 above, it
was considered to be somewhat different in that
the exertion of the fetus appeared to cause its
head being raised as a result of elevating neck
action. The impression was gained that when this
occurred it tended to precede the forward
extension of the head.
6. Follow-up pandiculated pose In the
majority of incidences, when the
pandiculation had been completed there
was a follow-up to this with the fetus remaining
in the extended pose passively for a variable
period of time. This pandiculated pose was noted
in approximately two-thirds of cases. Some of
these were poses of partial
pandiculation. A notable example of a
pose in partial pandiculation was the
characteristic birth posture, which has general
tension, but elbow flexion (Fraser and Terhune,
1977b; Husa et al., 1988).
7. Intention movements In a number of
instances, the phenomenon of
pandiculation appeared to be preceded by
initiative movements of the forelimbs (Fig. 1).
These took the form of pedal probing or
pedalling-like actions in which the two
forelimbs alternated in performing short forward
extensions and retracting movements with carpal
flexion. On some occasions, the "pedalling" took
the form of probing with the forelimbs, in short
movements directing the feet forward with carpal
extension. These actions meet the definition of
intention movements provided by McFarland
(1987).
8 and 9. Yawning and
jaw movement Although they have not been
previously reported in the literature, it was
evident in this study that certain fetal jaw
movements were morphological yawns. These
actions took the form of slow extension of the
tempero-mandibular joints to the fullest extent.
The mouth was held opened in these instances for
- 2 or 3 s and then closed. In some instances,
such yawns occurred as a commencement to
pandiculation, while in other instances
they occurred as the conclusion of
pandiculation. They were not a constant
feature of this phenomenon, but yawning
was seen clearly in several instances of full
pandiculation. Yawning, per se,
could be considered in the category of a partial
pandiculation.
Somewhat in association with yawning,
very rapid actions of tempero-mandibular
articulation (TMA) were seen as a ninth
component at various points in fetal activity
associated with yawning and as a
component of pandiculation. Rapid TMAs
were, however, common at other times and it
would be difficult to be certain of the actual
relationship between this minor kinetic factor
and the performance of
pandiculation.
Component score
Most of the components, as listed in Table
2a, occurred in the majority of episodes of full
pandiculation. A score was made of the
numbers of components occurring per episode.
These scores ranged from 6 to 8 with a maximum
of 9. The modal average was 7; the typical
pandiculation, therefore, had 7 of these
components in its make-up. No episode of
pandiculation incorporated all of the
characteristic components (Table 2h).
Additional features
Temporal distribution Pandiculation
episodes were noted in relation to time of
subsequent birth. The distribution was even
throughout the period of gestation studied; thus
the occurrences of pandiculation ranged
from 2 to 20 days pre-partum (Table 3).
Incidence per fetus Since fetal
pandiculation is a comparatively rare
event, it was usually encountered in each fetus
on only one or two occasions. To some extent,
the instances of multi-pandiculation in
two fetuses were exceptions to this observation
(Table 1).
Partial pandiculation
Partial (minor) pandiculations were recognised.
Some of these were instances of fetal stretching
in which vigour was low and duration was brief.
In many other partial pandiculations, the
complement of components was similar to full
pandiculation, but some of these, such as
elbow extension and forward thrust of the head,
were reduced in expression. Most incomplete or
partial pandiculations were lacking in one of
the following ways: (a) absence of extension in
one forelimb, but present in the other, in
association with atlantooccipital extension; (b)
symmetrical and full extension of limbs, without
atlanto-occipital extension, but with cervical
elevation; (c) failure of followthrough in the
overall action after its initiation.
Partial, incomplete and minor
pandiculation, as one category,
outnumbered full pandiculations in incidence.
They bore a relationship to the complete form in
that they were absent, or deficient, in the five
fetuses which failed to show full
pandiculation in any observation (Table
1)
Discussion
Fetal pandiculation, with its full
characteristics, having been recognised by
observation and induction, must be assumed to be
a qualitative item in the behaviour of the
fetus. As such, the evaluation of this
phenomenon is a chal-lenge from a comparative
viewpoint. This fetal activity is not likely to
be con-fined to the sheep and compound fetal
movements at a high level of complexity,
in association with vigorous bodily
extension, can be sought in other subjects as
evidence of the same phenomenon. A first
indication of such an activity in
P another species has already emerged in a
monitored survey of kinesis and pos-ture in the
pre-partum bovine fetus, using a combination of
methods with Doppler ultrasound and manual
palpation (Fraser, 1989b).
The phenomenon has substantial form and
structural detail. The components are numerous
and the majority of these are evident in each
occurrence : of the action, although no single
event incorporated every possible component in
this study. These items collectively create a
vigorous unitary movement of overall extension.
In the confined space of the uterus,
pandiculation must represent both an
achievement and a physical need. In the
post-natal circumstances of confmement husbandry
of livestock, it may be no less of a need. The
holistic nature of the action suggests that
close physical restraint could inhibit the
performance of the whole gesture and, indeed,
this impression was gained in some observations.
This phenomenon raises a fresh question of
welfare, should the accommodation of an animal
not be adequate in all dimensions to permit the
occurrence of this behavioural expression.
Viewed in a wider, comparative light, fetal
pandiculation could be related to fetal
somnolent states which are now, themselves, well
recognised (Ruckebusch, 1972; Dawes, 1973;
Ruckebusch et al., 1977; Ioffe et al., 1980;
Nathanielsz et al., 1980). If
pandiculation is a marker of transitional
phases between alert and somnolent states, it
can indicate that the phasic nature of fetal
processes is progressing normally. It may
therefore indicate that the status of the fetus
is satisfactory in general respects. Assessment
of such fetal status is an objective in
obstetrics (Trudinger et al., 1979; Manning et
al., 1981). As such, fetal pandiculation
could be regarded as a simple signal of adequate
well-being which could be identified by
non-invasive methods. Its detection in the
human, if it occurs there also, would appear to
be feasible by maternal information. Whether all
of these possibilities prove of value in due
course or not, it is clear that the phenomenon
calls for appropriate attention in further
work.
One interesting minor component of the
action is fetal yawning and this has not
been previously identified. Even in the adult
human subject, yawning has received
little research. Proctor (1964) describes the
physiological minutiae of human yawning
and adds the interesting comment that it is more
likely to be associated with vigorous stretching
after sleep than before. In addition, Proctor
adds the observation that such activity is
notable in the newborn baby.
Some current research speculation into
aspects of fetal respiration, has been focused
on so-called "gasping" (Harding, 1984). Since
errors can be made in the interpretation of
ultrasonic imaging of fetal actions (Farman et
al., 1975) it is here suggested that such
isolated gasping may be yawning, which
has a gasp-like nature. The pursuit of further
research into fetal pandiculation might
resolve other puzzles in fetology. For such a
purpose, it seems that the sheep fetus continues
to be a suitable model.
Pandiculated poses were often seen to follow
full and partial forms. These poses themselves
were variously full or partial in pandiculated
degree. Partially pandiculated poses usually
differed from fully pandiculated ones in regard
to limb involvement. In partially pandiculated
poses, the upper or proximal joints of both
pairs of limbs, namely shoulder, elbow, hip and
stifle, may be flexed. Extension of the axial
skeleton and pedal extremities, resulting in
outward thrusting of the head and feet, however,
are persistent features in most instances of
pandiculated pose. The stretching phenomenon may
exhibit such outreaching of the head alone. This
central feature of axial extension seems
appropriate in an action pattern which is a
vertebrate phenomenon. Articular exercise in
general, and vertebral exercise in particular,
may be its mechanical value.
One partially pandiculated pose was the
birth posture, which exhibited extreme extension
of the atianto-occipital joint, carpal joints
and digits. This was associated with very
positive and fixed orientation towards the
maternal pelvis in the last day of gestation. To
this extent, it might be said that
pandiculation primes the fetus for birth.
However, the wide gestational distributions of
episodes show that this is not the sole function
of this action. It is likely that the function
of fetal pandiculation is compound. Its
associated sensory component of mild pleasure is
known in the human experience. This cannot be
overlooked as a possible reinforcing factor in
this, part voluntary and part involuntary,
action. The existence of this sensation in the
animal, the fetus, can only be surmised on the
basis that many of the evident components of the
phenomenon are remarkable in their similarity
across vertebrate species. Broad physiological
benefits in the post-natal situation are
recognised in human yawning and
stretching.
CONCLUSIONS
Among its roles, fetal pandiculation
has a major function as a system of orthopaedic
behaviour. It operates in the determination of
function in the moving parts of the
musculo-skeletal system. This is performed
through regional exercise. In many cases,
several regions are involved and, not
uncommonly, the entire body is affected in
pandiculation. Articular development and
maintenance are clear outcomes of such
systematic function, which also enables the
fetus to pose for birth.
