Early Human Development 40 (\994) 39-49

Observation of movements during sleep in AL TE (apparent life threatening event) and apnoeic

infants - a pilot study

Christa Einspieler*a, Heinz F.R. Prechtla,b, Leo van Eykern b, Bart de Roos b

aDepartment of Physiology, Karl-Franzens-Universiry of Graz, Harrachgasse 21/5, A-801O Graz, Austria bDepartment of Developmental Neurology, University Hospital of Groningen,

Groningen, The Netherlands

Received 20 June 1994; revision received 2 September 1994; accepted 5 September 1994

Abstract

Fourteen infants of 2 months or 6 months of age were video-recorded during polysom­nography . Four were normal infants, five had a history of ALTE (apparent life threatening event) and five had repeated and prolonged apnoea during sleep. Two AL TE infants have been recorded at 2 months as well as at 6 months of age. Movements during sleep could be classified into general movements, isolated movements of the upper extremity, startles, head rotations, and trunk rotations. In the AL TE cases at 2 months of age, the motility was quan­titatively not different from the control infants but was markedly reduced at 6 months of age. (All cases had their event before 8 weeks of age.) In contrast to these findings, infants with repeated apnoea did not show a clear change in the quantity of their movements. With the exception of one AL TE case at 2 months, all observed cases of AL TE and apnoeic infants showed an abnormal quality of their spontaneous movements during sleep. As reported in a previous study [3], all these cases had also been found moving abnormally during wakefulness. It is suggested that the abnormal motility is a sequelae of the event (AL TE or repeated apnoeas) with as a consequence, an impairment of neural functions.

Keywords: AL TE; Apnoea, general movements; Quality assessment; Sleep; Sudden infant death, video observation

• Corresponding author.

0378-3782/94/$07.00 © 1994 Elsevier Science Ireland Ltd. All rights reserved SSD10378-3782(94)01588-G

40 C. Einspieler et al. I Early Hwn. Dev. 40 (1994) 39-49

1. Introduction

In a previous study [4], it was found that parents of victims of sudden infant death syndrome (SIDS) reported, retrospectively, a low incidence of movements in their sleeping infants. It was conjectured that cases who have survived an apparent life threatening event (AL TE) may also show a similar phenomenon.

In addition, infants with repeated apnoea during sleep show signs of neurological dysfunction expressed in deviant neurological findings [12] and in the abnormal quality of their general movement during wakefulness [3].

The assessment of spontaneous motor behaviour has proven to be an important method for assessing the integrity of the central nervous system in infants [14,15]. The study by Ferrari et al. [6] showed the high predictive value of observations of general movements. According to Prechtl [14] the definition of general movements is as follows: "They are gross movements involving the whole body. They may last from a few seconds to a minute. 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. Despite this variability, general movements must be considered as a distinct co­ordinated pattern, easy to recognise each time they occur again." (pp. 152-153). In normal cases, their appearance is fluent, elegant, and complex and they are variable in speed, amplitude, and intensity. However, in cases of brain lesions, e.g. periven­tricular haemorrhages and leucomalacia [6], in preterm infants under intensive care treatment [I], in infants with hypoxic-ischaemic encephalopathy after birth asphyxia [16], and in infants with repeated sleep apnoeas [3], general movements become monotonous, lose their complexity and particularly, they lose their fluency and elegance.

In normal infants, these general movements can be observed during wakefulness until the third month of life. It is not yet known how these movements occur during sleep and especially how they are quantitatively and qualitatively affected in cases with repeated sleep apnoea and after AL TE.

Hence, the aim of the present pilot study is to attempt to answer the following questions, based on accidentally available recorded material from another study. (I) Which distinct movement patterns occur during sleep in normal infants? (2) Are there age differences in normal infants in respect to their motor repertoire during sleep? (3) Is it true that infants who have suffered an AL TE move less during sleep than normal infants? (4) If there is a reduction in quantity of movements in ALTE cases, is there also a change in the quality of the remaining movements? (5) Do in­fants with more apnoeic spells differ from infants with less respiratory pauses con­cerning quantity and quality of movements during sleep? (6) Is there any correlation between the quality of general movements during wakefulness and the quality of movements during sleep?

C. Einspieler et al. / Early Hum. Dev. 40 (1994) 39-49 41

2. SUbjects

In a poly graphic study supported by the Austrian Science Foundation (Project S49/03) as a part of the European COMAC-BME project 'Methodology for the Analysis of the Sleep - Wakefulness Continuum', 26 infants participated from Oc­tober 1989 to June 1990. Video-recordings were made in 14 cases and have been analysed for this pilot study. All parents gave informed permission for the procedure.

These infants underwent a polygraphic recording for three reasons: 1. In four cases (cases 01-04), the parents volunteered their infants because they

had heard about this study. These infants were healthy and had no prenatal or peri­natal risk factors. In the following, they will be referred to as 'control-infants'. Case 01 and case 02 were observed at an age of 2 months, case 03 and case 04 at 6 months of age.

2. Five infants (cases 05-09) were referred for a sleep recording at the Paediatric Department of the University of Graz because they had experienced an apparent life threatening event (ALTE). In these infants, an unexpected event was reported by the caretaker during which the infant was apnoeic, pale or cyanotic, and limp and re­quired either vigorous stimulation or cardiopulmonary resuscitation. Three infants were given mouth to mouth resuscitation by a parent before reaching the hospital. In all cases, no obvious clinical cause could be found for this event. In their polygraphic recordings they had no signs of respiratory problems such as prolonged apnoeas and drops in oxygen saturation. They will be referred to as 'ALTE infants'. The age of the occurrence of the AL TE is given in Table 1. Case 05 and case 06 were recorded twice at 2 and at 6 months of age, whereas case 07, 08 and 09 were observed only at 6 months of age.

3. Five infants (cases 10-14) were referred for a sleep recording at the Paediatric Department because they had prolonged and/or frequent respiratory pauses and drops in transcutaneous P02 during sleep in a previous recording performed few days before at the Paediatric Department. In the following, they will be referred to as 'apnoeic infants'. The cases 10, 11, 12, and 13 were observed at 2 months of age and only case 14 at 6 months of age.

None of the above mentioned infants had a history which would indicate a risk of perinatal brain damage. For additional clinical data, see Table I .

3. Methods

At 19:00 h, the infants were admitted to the sleep laboratory for an 8-h night mon­itoring session. Monitoring was carried out in a quiet and semi-dark room, at a tem­perature ranging between 20 and 22°e. The infants were first fed by their mothers and were then allowed to sleep in their usual position.

During polygraphic recording the following variables were simultaneously record­ed: four EEG derivations, EOG, ECG, EMG, heart rate, respiration (thoracic and

42 C. Einspieler et al. / Early Hum. Dev. 40 (1994) 39-49

Table I Clinical data of subjects

Case Group Recording age Sex Gestational age Birth-weight (weeks) (weeks) (g)

01 Control 7.5 F 40 3280 02 Control 8 M 41 3840 03 Control 26 F 40 3000 04 Control 27 F 38 3300 05 AL TE (8 weeks) 9 and 26 M 40 4100 06 ALTE (7 weeks) 9 and 26 M 42 3400 07 AL TE (5 weeks) 26.5 M 41 3560 08 AL TE (8, 10 days) 26 M 41 3150 09 AL TE (7.5 weeks) 27 M 38 3320 10 Apnoea 8 F 40 3100 11 Apnoea 8 F 38 3300 12 Apnoea 8 M 40 3150 13 Apnoea 6.5 F 40 2940 14 Apnoea 26 F 39 3900

abdominal excursions with strain gauges, and nasal air flow), oxygen saturation, Lc.­Po2, t.C.-PC02, micro-vibration, blood pressure, and temperature [10,11].

All infants participated in a previously reported study [3] concerning spontaneous movements during wakefulness. Hence it was possible to compare their spontaneous motor activity during wakefulness with those during sleep.

3.1. Recording of spontaneous movements during sleep

The infants were video-recorded during several hours of the polygraphic recor­dings. All infants were used to sleeping covered up to the mid thorax with blankets. Uncovered, which would have been preferable, the babies would have protested and not slept.

By chance, four infants were lying in supine, three in lateral position, and nine in prone position during the beginning of the video-recording. The older infants, in particular, changed position during recording by spontaneous trunk rotation.

All video-sequences had a high technical quality which permitted detailed inter­pretation. In addition, all sequences of nursing interventions, manipulations of the electrodes, episodes of fussing and crying, and wakefulness were excluded from anal­ysis. Only observations of the infants' spontaneous behaviour during undisturbed sleep with an average duration of 2.5 h (range, 1-4 h) were analysed.

3.2. Classification of sleep states

The polygraphic data from each infant were pre-processed, integrated over 30 s and a compressed record plotted on a single sheet [11]. From these recordings, the assessment of states has been performed visually using the following five criteria:

Table 2 Rate per 10 min of spontaneous movements in eight 2-month-old infants

Case Group GMs UppExt Startle HRs

NREM REM NREM REM NREM REM NREM REM

01 Control 0.31 \.65 2.54 0.75 02 Control 4.00 0.50 0.44 05 ALTE 0.51 5.16 1.10 7.26 0.95 1.24 3.91 06 ALTE 0.34 0.75 0.17 0.97 0.11 0.51 \.40 10 Apnoea \.06 4.77 3.84 0.22 3.47 11 Apnoea 0.65 4.56 2.26 2.52 \.29 0.58 12 Apnoea 1.15 3.19 0.48 2.83 0.59 0.40 1.74 13 Apnoea 0.96 3.56 0.77 1.53 0.64 1.27

GMs, general movements; UppExt, isolated movements of the upper extremity; HRs, head rotations.

Table 3 Rate per 10 min of spontaneous movements in eight 6-month-old infants

Case Group GMs UppExt Startle HRs TRs

NREM REM NREM REM NREM REM NREM REM NREM

03 Control 0.89 4.31 0.54 6.55 0.17 0.36 04 Control 0.65 2.01 0.09 3.38 0.74 \.80 0.09

05 ALTE 0.50 0.22 \.02 0.44 0.51 \.53

06 ALTE 0.47 2.44 0.70 2.20 0.12 0.49 0.12 \.46 07 ALTE 0.46 1.32 0.46 0.91 0.46 0.99 0.46 08 ALTE 1.52 0.30 0.61 0.30

09 ALTE 0.61 1.39 0.76 0.70 0.15 0.32 14 Apnoea 0.61 \.26 \.92 2.39 0.30 0.42 0.70 2.88

GMs, general movements; UppExt, isolated movements of the upper extremity; HRs, head rotations; TRs, trunk rotations.

REM

0.86 0.28 0.51

0.34 0.30 0.13

n ~ ~ ~ ~ ~ ,.... ...... ~ .., ~

~ t::::l '" :"

~ ...... .... ~ '­<..,. '0 I ~ '0

~ w

44 C. Einspieler et al. / Early Hum. Dev. 40 ( 1994) 39-49

NREM: respiration and heart rate regular, high EEG amplitude, no EOG activity and rare EMG activity.

REM: respiration and heart rate irregular, low EEG amplitude, frequent EOG and EMG activity.

The transitions have been marked manually to indicate the beginning and end of states. For each infant, there had been at least one NREM and one REM epoch but this was exceptional and in most cases, two to three epochs of each sleep state had been selected for analysis of the motor activity. As mentioned before, epochs of wakefulness and manipulation of the infant have been excluded from analysis.

3.3. Analysis, coding and data processing

Each videotape was time coded for analysis with the aid of the special program 'tape-time' which was developed by one of us (L.v.E.). This program was used to score (a) events with a beginning and end (duration) such as general movements and isolated movements of the upper extremity, and (b) single events such as startles or head rotations. In addition, the times of state transitions were added to the data. Finally, these raw data were converted into a file for statistical processing. Percen­tage of occurrence (duration of movements in relation to scored duration of state) and rate per 10 min of movements are given in median values. The individual values are given in Tables 2 and 3.

The judgement of the quality by means of visual Gestalt perception has been car­ried out by two observers (C.E. and H.F.R.P.), one observer (H.F.R.P.) was blind regarding the history of the infants. There was a total agreement in the global judge­ment between normal versus abnormal for the 14 infants.

4. Results

4.1. Movement patterns during sleep in normal infants

4.1.1. At 2 months of age General movements. These had a loose writhing character and usually started in

one hand or arm and spread to the whole body. Their duration ranged from 3 to 30 s with a median value of 5 s. Only one infant had one general movement of 30 s during NREM sleep. All the others occurred during REM sleep epochs and covered 3.3% of REM sleep time, with a rate of three per 10 min (Table 2).

Isolated movements of the upper extremity. These occurred exclusively during REM sleep (1 .5 per 10 min) and consisted of moving the fingers alone, or including hand and arm. These movements were present in 2.2% of REM sleep while isolated finger movements represented 66% of the movements and are hence the most fre­quent components.

Startles. These have not been observed in the normal infants. Head rotations. These were either from side to side or from the resting position

turning back into the starting position. They occurred rarely.

C. Einspieler et al. / Early Hum. Dev. 40 ( 1994) 39-49 45

4.1 .2. At 6 months of age General movements. It came as a surprise that, during sleep, infants of this age

showed general movements which resembled the loose writhing type while, during wakefulness, these movements had long since disappeared. Surprisingly enough, they occurred not only during REM sleep but also during NREM sleep. During the latter, they lasted even longer (median, 7 s) than during REM sleep (median,S s). The incidence was 0.7 per 10 min during NREM sleep and 3.2 per 10 min during REM epochs (Table 3). Their duration ranged from 3 to 28 s and they covered 1.2% during NREM sleep and 3.1% during REM sleep.

Isolated movements in the upper extremity. Similar to the observation at 2 months of age, isolated finger movements were relatively frequent during REM sleep (1.2%) but never occurred during NREM sleep. However, finger and hand movements and those including the arm were seen during REM sleep (1.9%) as well as during NREM sleep (0.2%).

Startles. While startles were not observed in one infant the other had only one startle during a REM epoch.

Head rotations. These movements occurred in only one infant in both sleep states. Trunk rotations. During sleep, both infants changed their position from side to

side (0.2 per 10 min), from side into prone (0.1 per 10 min), during REM as well as NREM epochs. However, during REM sleep, rotations from side into supine (0.1 per 10 min), from prone to side (0.2 per 10 min) and rotations out from the previous position and rolling back (0.3 per 10 min) were observed.

4.2. ALTE infants: quantitative aspects

4.2.1. At 2 months of age AL TE infants at 2 months of age had no reduction of the incidence or duration

of general movements. A remarkable finding in the ALTE infants was an increase in movements in the upper extremities (0.6 per 10 min during NREM and 4 per 10 min during REM) and an increase of head rotations (0.8 per 10 min during NREM and 2.7 per 10 min during REM sleep). Another peculiarity was the presence of startles during REM epochs (0.5 per 10 min) which was not found in the controls.

4.2.2. At 6 months of age In contrast to the findings in the 2-month-old infants, a clear reduction was found

in all movement patterns in this age group. The percentage of general movements in NREM sleep (0.05 %) was 24 times reduced compared with normal values while during REM sleep (0.8%) the reduction was four times. A reduction was also found in the median duration of the general movements. During NREM sleep, the duration (2.5 s) was three times shorter but only slightly reduced during REM sleep (4 s). The incidence of occurrence of general movements during REM sleep was reduced by half (l.4 per 10 min).

The reduction was not limited to the general movements but was also found in other movement patterns. Isolated movements of the upper extremities during NREM sleep were reduced to 0.1 % which is half the normal value. More striking

46 C. Einspieler et al. / Early Hum. Dev. 40 (1994) 39-49

was the reduction of these movements during REM sleep to 0.5% which is a fourfold reduction. The rate per 10 min was five times reduced (I per \0 min).

Trunk rotations were reduced by half during REM sleep (0.3 per \0 min) whereas head rotations occurred only inconsistently.

There was a remarkable exception. Startles had not been found during NREM sleep in the normal infants, but were present in three out of five AL TE cases. All AL TE infants showed startles during REM sleep with a rate of 0.6 per \0 min.

4.3. ALTE infants: qualitative aspects

When these various movements were observed in respect to their normal or de­viant qualities, some striking features were noted. This holds true for both ages. The following peculiarities had been observed:

4.3.1. At 2 months of age Case 05. Tremulous general movements. Abrupt arm movements. Spontaneous

tremor in the arm. Frequent 'smiling'. Excessive rapid eye movements during REM sleep. Peculiar small head movements in prolonged sequences during REM sleep (1.3 per \0 min) which were not seen in any other cases.

Case 06. The quality of general movements and other movement patterns were in­conspicuous. On the other hand, in his 8-h polygraphic recording, this infant had signs of a serious disorganisation of behavioural state parameters. However, there were sufficiently long parts in which the states could be reliably scored so that the quantitative and qualitative data can be trusted.

4.3.2. At 6 months of age Case 05. This case is identical to the same case number at 2 months. Head move­

ments with abrupt onset and tremulous ending. Startles frequently elicited tremor. General movements were now without tremor.

Case 06. The same case as described at 2 months, but now the picture has changed. During REM sleep, this infant showed two prolonged episodes of repeated vertical head banging while in prone position. Prolonged full extension of all fingers which afterwards closed slowly. Symmetrical arm movements. General movements were without tremor.

Case 07. Abrupt onset of general movements. Tremulous general movements. Rare finger movements.

Case OB. Tremulous and fragmented general movements. One episode of head movements with small amplitude.

Case 09. All general movements very tremulous. 'Slow motion' head, arm, and finger movements. Slow arm movements synchronous in both arms.

In order to relate the qualitative assessment carried out at 2 months during wakefulness [3] with those at 6 months, we blindly rank ordered the degree of abnor­mality in the 6-month observation during sleep. From the 2-month observation during wakefulness, their abnormal motor optimality score was available [3], which is of course easy to rank order. Those cases who had been the worst during wakefulness at 2 months were also the worst during sleep at 6 months and the same

C. Einspieler et al. / Early Hum. Dev. 40 (1994) 39-49 47

holds true for the relative best which were also the relative best at 6 months (rank correlation coefficient of r = 0.97).

4.4. Apnoeic infants

4.4.1. At 2 months of age The question as to whether infants with repeated sleep apnoeas at 2 months of age

differ in their quantitative and qualitative aspects from normals can be answered in the sense of a mild increase in their motor activity during sleep. General movements were increased to 5.7% during REM sleep and to 0.7% during NREM sleep. The me­dian duration of general movements was 3 s during NREM sleep and 6.8 s during REM sleep. During REM sleep, the rate of general movements per 10 min was similar to the control group but during NREM sleep, general movements were con­sistently present (I per \0 min).

Isolated movements of the upper extremity were slightly increased in comparison with the controls. The real difference was in the relatively high incidence of startles (0.6 per 10 min during REM epochs) and head rotations (1 .3 per 10 min during REM sleep) at least in three out of four apnoeic infants. When these data were related to their apnoea measurements, the increase in these two movement patterns correlated with the severity of the apnoea measurements (i .e. longest apnoea, percentage of periodic breathing, drop in t.c.-Po2, and apnoeas with bradycardia).

As far as the quality is concerned, there are several aspects of movements with ab­normal quality. Three of the four infants showed a striking restlessness during sleep with many head rotations, startles and short crying spells. In one of these cases, the state organisation broke down after 2 h and hence the movement observation was then stopped. The fourth case lacked the restlessness of the other cases but had monotonous general movements and repeated spreading of the extended fingers. The latter was also observed in one of the other cases.

4.4.2. At 6 months of age Only one infant from the group with apnoeic spells was available for analysis at

this age. There were few general movements (0.8% during NREM and 0.8% during REM). The rate of occurrence of isolated movements of the upper extremities was normal but there were many startles similar to the AL TE group. This infant had a high rate of head rotations with three per \0 min during REM sleep epochs. The total absence of trunk rotations during the 4-h observation time was remarkable.

General movements, isolated movements of the upper extremities as well as head movements were all tremulous. The movements appeared to be very fragmented .

All five apnoeic infants clearly had an abnormal quality in their general move­ments during wakefulness at 2 months of age [3] . The degree of abnormality, how­ever, was not correlated with the degree of abnormality during sleep.

5. Discussion

Despite the fact that the number of cases we have studied so far is very limited, we feel it worthwhile reporting these preliminary results which indicate certain trends in the subject cases. This is especially so as our findings are based on direct video observation of movements during comprehensive polygraphic monitoring of

48 C. Einspieler et al. / Early Hum. Dev. 40 (1994) 39-49

infants and are at variance with some previous reports. In the past, spontaneous movements during sleep have been mainly based on the indirect detection of move­ments through artifacts in the recordings [18] instead of visual classification of observed movements and by counting their incidence and duration. The often reported reduction of movements during sleep in AL TE infants [2] could not be replicated in our infants at the age of 2 months but was present at the age of 6 months. This indicates rather a late effect of this event on the function of the nervous system. Korobkin and Guilleminault [9] have speculated about 'infants who present with near miss episodes may have an underlying central nervous system abnormality or may acquire some abnormality as a result of the episode'. Their neurological fin­dings were mainly based on hypotonia which is known to be a rather unspecific sign and of limited value [16]. However, the anamnestic reports on SIDS victims [4,13] and the prospective data by Schechtman et al. [18] on cases who later succumbed to SIDS indicate an earlier reduction of sleep motility (i.e. less artifactual episodes in the recording) in the fatal cases. In four cases with ALTE, Kohyama and Iwakawa [7] found no decrease in gross movements but a decrease in localised movements, all assessed from submental EMG during the recordings. In a later paper, the same authors [8] again found no decrease in the percentage of body movements during REM sleep in six ALTE cases at an age of 2-37 weeks recorded shortly after the event. It may very well be that the discrepant findings are due to the differences in the recording method and hence they still remain an open question.

The data on the changes in the quality of the general movements were more clear cut. The frequently observed tremulousness agrees with the experience in asphyx­iated fullterm infants [16] who also showed tremulous spontaneous movements for a prolonged period. The degree of abnormality compared with the normal motor repertoire of infants of the same age is a strong indication of an impaired functional integrity of the central nervous system in these cases. There is also the relationship between the abnormal quality at 2 months of age during wakefulness and the abnor­mal findings during sleep at 6 months of age.

Less clear are our findings in the few cases of apnoeic infants. Although also pre­sent are the abnormal qualitative findings consistent with the findings during wakefulness, however, they are lacking the close correlation with each other. Never­theless, the abnormal quality of movements is present in all cases which is not restricted to wakefulness. Despite these qualitative changes, there were no striking changes in the quantity of motor output which is in agreement with previous findings in infants with brain lesions [5,6,17].

Future studies will have to find an answer to the puzzling phenomenon that SIDS victims obviously have a reduced motor activity during sleep, while AL TE infants have this only after a longer delay after the event and not for a few weeks, while quantitative changes in motility are not present in apnoeic infants and in brain­damaged cases.

Acknowledgements

The authors gratefully acknowledge Professor Pfurtscheller (Department of Medi­cal Informatics, Institute of Biomedical Engineering, Graz University of Technol-

C. Einspieler et al. I Early Hum. Dev. 40 (1994) 39-49 49

ogy) and Dr Litscher (Department of Anesthesiology, University Hospital Graz) for their permission to use video-recordings made during their polysomnography pro­ject. The selection of the babies and clinical data collection were performed by the staff of the Department of Pediatrics, University Hospital Graz (Professor Kurz and Drs Kerbl, Lackner, Reiterer, and Renate Schenkeli). Recordings were carried out by Dr Eva Maria Klug (Department of Physiology, University of Graz).

The first author acknowledges the hospitality of Professor B.c.L. Touwen of the Department of Developmental Neurology, University Hospital of Groningen, the Netherlands.

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