Polygraphic features of a victim of sudden infant death syndrome and of infants with apparent life-threatening event

CASE REPORTS

Polygraphic Features of a Victim of Sudden Infant Death Syndrome and of Infants with Apparent Life-Threatening Event Jun Kohyama, MD and Y oshihide Iwakawa, MD

We analyzed a polygram of a victim of sudden infant death syndrome (SIDS) which had been taken five weeks prior to his death. The findings are discussed in association with the serial polygraphic observations of four infants who had suf fered from apparent life-threatening event (ALTE), and twenty neurologically normal infants. Frequencies of respiratory pauses were high in SIDS, and average durations of respiratory pauses showed higher values in ALTE than in the controls. Normal paradoxical motions between chest and abdominal wall during active sleep period (AS) were completely abolished in the records of SIDS and of one ALTE. Normal developmental decreases of localized movements (LMs) on mental muscle with age were insufficient in ALTE. The numbers of twitch movements (TMs) were low in SIDS and in two of ALTE, while those of gross movements in the subjects were identical with those in the controls. Dissociation indexes (ratio of the number of TMs against the sum of the numbers of TMs and LMs) were low in SIDS and in two of ALTE. These findings seemed to be the physiological reflection of the impairment of arousal responsiveness and of the developmental disturbance of the brainstem in SIDS and ALTE. Polygraphic evaluations on the respiratory pattern during AS and the dissociation state ofTMs from LMs may be helpful in the early detection of SIDS and/or ALTE in asymptomatic infants. Key words: Polygram, SIDS, ALTE, body movement, respiratory pattern. Kohyama J, Iwakawa Y. Polygraphic features of a victim of sudden infant death syndrome and of infants with apparent life-threatening event. Brain Dev 1989;11:186-90

The hypothesis that apnea is the cause of sudden infant death syndrome (SIDS) [1] has been widely discussed, and the importance of polygraphic assessments has been emphasized. The polygrams recording apnea and heart rates, however, have been proved to be insufficient to predict SIDS [2-4], and an impairment in arousal responsiveness has been suggested as the cause of SIDS [3, 5- 7] . A baby who had been born at our hospital recently died of a suspected SIDS episode. A polygram obtained five weeks prior to his death was examined from a new point of view by comparing it with serial records of four infants suffering from apparent life-threatening event (ALTE) [8]. From the Department of Pediatrics, Tsuchiura Kyoudou Hospital, Tsuchiura, Ibaraki (JK); Department of Pediatrics, School of Medicine, Tokyo Medical and Dental University, Tokyo (YI). Received for publication: November 15, 1988. Accepted for publication: March 8, 1989. Correspondence address: Dr. Jun Kohyama, Department of Pediatrics, Tsuchiura Kyoudou Hospital, Manabe-Shinmachi 11-7, Tsuchiura, Ibaraki 300, Japan.

SUBJECTS AND METHODS A case of SIDS A baby boy, born after 28 gestational weeks, weighing 1,256 gm, with asphyxia, was under controlled ventilation for 47 days due to primary apnea of prematurity and sepsis. A routine polygram was recorded on the 108th day of his life (Fig 1); he was discharged on the 110th hospital day, weighing 3,070 gm, and was in good condition. On the 145th day of his life, he drank breast milk well at 5 pm, and his mother noticed him sleeping well at 9 pm. Thirty minutes later, his father noticed his pale appearance and respiratory arrest. Postmortem examination was not performed. Cases of ALTE (Table 1) The subjects were the four infants (designated ALTE 1, 2, 3, 4) who had required intensive resuscitation for unexpected apneic event with cyanosis. No medical cause for the event had been found after a systematic clinical investigation, and the first polygrams were recorded within two weeks of ALTE. Serial records were per-

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Fig 1 Sleep diagram of a victim of SIDS five weeks prior to his death. No specific polygraphic features are found only from this diagram. Aw: awakefulness, A: active sleep, I: indeterminate sleep, Q: quiet sleep, HR: hour.

Table 1 Cases of ALTE

ALTE ALTE ALTE ALTE

1 2 3 4

formed three times in ALTE 1 and once for the other three infants.

Birth

Apgar score

Sex

The day of ALTE

34 weeks/2,384 gm 41 weeks/3,300 gm 39 weeks/2,872 gm 37 weeks/3,002 gm

6 9 8 9

Male Female Male Male

34 20 22 30

Polygraphic procedures Polysomnograms were recorded for three to eight hours from natural sleep onset to natural arousal. The records of subjects with a conceptional age of more than 45 weeks were all-night ones. Each polygram involved electroencephalograms, bipolar horizontal electrooculogram, respiratory monitorings around the chest and abdominal region both setting to record upward tracing during expansion, and surface electromyograms (sEMG) on the mental muscle, abdominal rectal muscle, and one or two limb muscles. Sleep states were classified according to Parmelee et al [9]. The standard of the Association for Psychophysiological Study of Sleep [10] was also applied to the records taken for the infants who were more than three months of age.

Table 2 Respiratory pauses, and body movements during sleep

Conceptional age (wks) Controls ALTE SIDS (mean ± SD) 1 234 39-41 (n = 5) 39 42-44 (n = 5) 42 42 43 44 45-52 (n = 5)

Respiratory pauses Average Frequency duration TST TST (AS or SREM) (ASorSREM) sec NIM

46 52 52 56-72 (n = 5) 68 76

GMs TST (ASorSREM) NIH

LMs TST (AS or SREM) NIH

TMs TST (ASorSREM) NIH

DI TST

0.27 ± 0.07

0.7 ± 0.9 (0.9 ± 1.2)

3.6 ± 0.6 (3.2 ± 0.2)

16.7 ± 6.6 (22.8 ± 5.9)

60.5 ± 8.3 (110.8 ± 53.8)

24.0 ± 9.9 (35.8 ± 12.4)

0.6 (0.7)

6.1* (4.1*)

18.3 (33.0)

74.2 (76.5)

10.0 (13.7)

0.12*

0.3 ± 0.1 (0.5 ± 0.2)

3.1 ± 0.4 (2.9 ± 0.4)

21.1 ± 6.0 (26.4 ± 5.6)

23.5 ± 4.8 (29.6 ± 6.9)

0.27 ± 0.05

0.6* 0.3 0.8* 0.3

4.0* 3.4 3.8 4.0*

21.2 21.2 23.0 27.3

(0.8) (0.3) (1.4*) (0.3)

0.5 ± 0.3 (0.9 ± 0.4) 50

Body movements

(3.7) (2.8) (3.7) (2.9)

(23.4) (30.8) (29.8) (34.7)

3.3 ± 0.2 (3.1 ± 0.3)

16.7 ± 4.0 (21.8 ± 8.6)

3.9* 3.4 3.8* 3.2

(3.7) (3.0) (3.5) (2.8)

17.0 15.0 13.0 17.7

0.4 ± 0.2 (0.5 ± 0.4)

3.6 (3.4

±

0.4 (0.9) 0.2 (0.4)

4.0 (3.9) 4.2 (3.5)

0.5 0.3 0.5 0.5

(0.7) (0.5) (0.8) (0.9)

±

0.5 0.5)

(24.7) (19.2) (19.9) (25.5)

11.9±3.1 (18.2 ± 2.7) 10.4 (15.2) 12.2 (13.2)

66.5 ± 22.4 (81.5 ± 19.3) 78.6 74.8 71.1 82.7

(80.3) (94.3) (92.6) (107.1)

50.8 ± 13.1 (84.6 ± 20.7) 31.7 70.7 76.1 71.6

(56.5) (129.3*) (134.3*) (148.8*)

42.4 (93.1

± ±

7.3 24.7)

51.6 (88.7) 91.0* (129.0)

15.0 23.3 10.3* 19.1

(11.4*) (32.3) (18.5) (24.4)

29.3 ± 6.8 (56.7 ± 15.0) 15.2* 17.7 40.8 35.8 50.1 (108.4

(26.8) (32.8) (70.0) (73.5) ± ±

15.7 34.0)

30.5 (84.7) 38.8 (86.7)

0.16* 0.24 0.13* 0.19 0.37 ± 0.06 0.32 0.20* 0.35 0.33 0.53

±

0.06

0.37* 0.30*

* Deviation over 2.0 SD from the mean of the controls. N/M: number per minute, N/H: number per hour, DI: dissociation index [TMs/(TMs+LMs»).

Kohyama et al: Polygrams in SIDS and ALTE 187

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Fig 3 Polygrams during active sleep in patients with ALTE 1 and SIDS. The dissociations of TMs from LMs are not obvious. The motions of chest and abdominal walls are synchronized.

188 Brain & Development, Vol 1l,No 3, 1989

Frequencies and average durations of respiratory pauses lasting two seconds or more were calculated. Body movements during sleep (BMs) were detected by sEMG, and classified into three types: gross movements (GMs), localized movements (LMs), and twitch movements (TMs). GMs comprised movements including the trunk, lasting two seconds or more. LMs and TMs comprised those localized on mental muscle. LMs were those lasting more than 0.5 seconds and TMs those lasting 0.5 seconds or less. The numbers of BMs were examined_ RESULTS (Table 2) Percent sleep stages of the subjects were within 2.0 standard deviation (SD) from the mean of the controls, except for ALTE 2 (46 wks: decrease of indeterminate sleep stage) and 3 (52 wks: increase of slow wave sleep stage). Frequencies of respiratory pauses during total sleep time (TST) were beyond 2.0 SD from the mean of the controls in SIDS and ALTE 1 (42 wks). Average durations of respiratory pauses during TST were beyond 2.0 SD from the mean of the controls in ALTE 1 (39, 42 wks), 2 (46 wks), and 3. During the active sleep period (AS) or stage REM (S REM) , chest and abdominal walls moved paradoxically in the controls (Fig 2), while this phenomenon was not observed in SIDS and ALTE 1 (Fig 3). The numbers of GMs in the subjects were all within 2.0 SD from the mean of the controls both during AS (SREM) and TST. LMs during TST showed gradual decreases with age in the controls, while these decreases were insufficient in ALTE, and in particular, they were increased with age in ALTE 1 and 2. TMs during both AS (SREM) and TST increased with age in the controls, whereas these increases were insufficient in ALTE 1. The values during TST in SIDS and ALTE 2 (46 wks) were below 2.0 SD from the mean of the controls. DISCUSSION Bentele and Albani reviewed the functional studies on SIDS [2], summarizing prospectively obtained polysomnographic data on a total of 23 SIDS victims from the former literature, and supported the conclusion by Monod et al [11] that polygraphic data had no predictive value for SIDS. In these studies, however, respiratory pattern and BMs, which are studied in the present report, were neither considered nor evaluated. Though our patient could not be termed a definitive SIDS and the smallness of the number of the subjects could not allow us to make a precise statistic analysis, difficulties and scantiness of prospective polygraphic studies in SIDS may give some significancies to our report. Chest and abdominal walls have been known to move paradoxically during AS until the early childhood period [12]. Interestingly, this phenomenon was completely

abolished even during AS in SIDS and ALTE 1. According to Rome et al [13], preterm infants show no asynchronous motion during about 40% of their AS period, but the values were quite high in our patients. As asynchrony during AS has been thought to be attributed to a loss of intercostal muscle activity during AS [13], synchronous motion between chest and abdominal wall during AS in our study might be due to an insufficient loss of intercostal muscle' tone. However, even in our patients, the mental muscle tones were decreased during AS as in the controls. On the other hand, paradoxical motion between chest and abdominal wall is often followed by GMs which have been considered as one of the arousal responses [14]. Therefore, we speculated that disappearances of this paradoxical movement during AS in early infancy should be taken as the impairment of the arousal responsiveness rather than the preferable maturation of respiratory control. The developmental decreases of LMs and increases of TMs observed in the controls were not obvious in ALTE. Together with the close observation of the sEMG, we consider these findings to be the impairment of the normal developmental dissociation of TMs from LMs. In the records during the neonatal period, TMs are observed as part of LMs, but gradually with age, TMs are dissociated from LMs and can thus be observed independently (Fig 2). To evaluate these quantitatively, we calculated the dissociation index [DI: TMs/(TMs + LMs)]. DI increased with age in the controls, while the values were below 2.0 SD from the mean of the controls in SIDS, ALTE 1, and 2 (68 wks) (Table 2). We recently investigated BMs in patients who had large low-density areas in the bilateral hemispheres on brain CT scanning, and speculated that the origin of LMs and TMs might be in the brainstem [15]. Muscle twitchings during AS were reported to originate from the nucleus pontis caudalis in cats [16]. And LMs can be considered to occur by the intermittent cessation of the activity of the cells related to muscle atonia during AS. These cells were reported to be located peri-locus coeruleus pars alpha in cats [17] and may descendingly cause spinal motoneuron inhibition during AS in human infants [18]. Moreover, sEMG findings describing above suggest the existence of some close neuronal interactions between these two nuclei. Therefore, DI may reflect the maturation of the above two nuclei, and the increase of DI with age observed in the controls may indicate some aspects of the developmental maturation of the brainstem function. Thus, low DI value observed in the subjects can be assumed to be a manifestation of the disturbance of the brainstem maturation. In the victims of SIDS, decreases of catecholamine synthesizing enzyme activity in the medullary C2 areas [19] , and increased dendritic spine densities in the brainstem [20] have recently been reported. The region investigated in the former report was located near the respiratory

Kohyama et al: Polygrams in SIDS and AL TE 189

neurons and peri-locus coeruleus pars alpha, and the latter report indicated an immature development of the brainstem_ Moreover, BMs are considered to depend on the catecholaminergic activities in the brain [21]. Therefore, our present findings may be the physiological reflection of the developmental disturbance of the catecholaminergic system in the brainstem of infants with SIDS and ALTE. Although the present study is a preliminary one and further broad investigations are needed, we propose that polysomnographic evaluation of the respiratory pattern during AS (synchronized motion of chest and abdominal wall) and of the dissociation state of TMs from LSMs (low dissociation index, DI) may be helpful in the early detection of SIDS and/or ALTE. REFERENCES 1. Valdes-Dapnea MA. Sudden infant death syndrome: a review of the medical literature 1974-1979. Pediatrics 1980; 66:597-614. 2. Bentele KHP, Albani M. Are there tests predictiv~ for prolonged apnoea and SIDS? A review of epidemiological and functional studies. Acta Paediatr Scand 1988;(suppl): 342. 3. Hunt CA, Brouillette RT. Sudden infant death syndrome: 1987 perspective. J Pediatr 1987;110:669-78. 4. Kahn A, Blum D, Rebuffat E, et al. Polysomnographic studies of infants who subsequently died of sudden infant death syndrome. Pediatrics 1988;82:721-7. 5. Garg M, Kurzner SI, Bautista DB, Keens TG. Clinically unsuspected hypoxia during sleep and feeding in infants with bronchopulmonary dysplasia. Pediatrics 1988;81:635-42. 6. Garg M, Kurzner SI, Bautista DB, Keens TG. Hypoxic arousal responses in infants with bronchopulmonary dysplasia. Pediatrics 1988;82:59-63. 7. Coons S, Guilleminault C. Motility and arousal in near miss sudden infant death syndrome. J Pediatr 1985;107:728-32. 8. Consensus Statement. National institute of health consensus development conference on infantile apnea and home monitoring, Sept 29 to Oct 1, 1986. Pediatrics 1987;79:292-9. 9. Parmelee AH, Wenner AHJ, Akiyama Y, Schultz M, Stern E. Sleep states in premature infants. Dev Med Child Neurol 1967;9:70-7.

]90 Brain & Development, Vol]], No 3, ]989

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