The effect of deep hypothermia and total circulatory arrest on the electroencephalogram in children

Electroencephalography and Clinical Neurophysiology, 1974, 36" 661-667 , ) Elsevier Scientific Publishing Company . . . . . . . . . . . . . . . . . . . ,,,~,., in , ,,,~ N-th "-~'''~-

CLINICAL

661

NOTE

THE EFFECT OF DEEP H Y P O T H E R M I A A N D TOTAL C I R C U L A T O R Y ARREST ON THE E L E C T R O E N C E P H A L O G R A M IN C H I L D R E N 1 EDWARD L. REILLY2, JAMES A. BRUNBERG 3 AND DONALD B. DOTY 4 University Hospitals and Clinics, arid The lou'a Psrchopathic Hospital, Iowa City, Iou'a / U S.A. )

{Accepted for publication: December 31, 1973)

Surgical repair of complicated congenital heart defects in children has been facilitated by combined deep hypothermia and total circulatory arrest (Mohri et ai. 1969; Barratt-Boyes et ol. 1971; Subramanian et al. 1971: Mort et al, 1972). Excellent exposure and precise repair of intracardiac defects in a bloodless field are possible and under deep hypothermia all perfusion can be eliminated for as long as 70 min. The duration and complications of bypass perfusion are reduced by this technique (Gilman 1965; Tufo et ai. 1970; Aguilar et aL 1971 ). This study was one part of the investigation of CNS effects of this surgical technique (Brunberg et al. 1973, 1974a).

in all operative recordings. Fast activity provoked by halothane anesthesia was prominent in the fronto-central region (F3-C3 or F4-C4). Five sec epochs of this activity were selected visually and the voltage and frequency measured at specific points in the procedure: (!) after the induction of general anesthesia: (2) at the completion of surface cooling to 26°-30°C; during further more rapid cooling utilizing cardiopuimonary bypass with a mixture of (3) 930o 02 and 7?;o CO2 (4) 90°,'0 02 and 10°,'o CO2; and (5)just before total circulatory arrest while 1 0 0 ° 0 0 z was being given (17°-23°C); (6) at the end of circulatory arrest; (7)after ! min of bypass rewarming; and (8) at the end of bypass rewarming (35°C).

METHO D A N D MATERIAL RESULTS Electroencephalograms (EEGs) wer,c obtained from 28 patients less than 2 years of age who underwent complete intracardiac correction of their anomalies using deep hypothermia, a limited period of extracorporeal circulation, and total circulatory arrest for I 1-54 min (Brunberg et al. ! 974b). Twenty-one sikcr .~ikcr chloride disc electrodes (Grass E5SH) were applied w,tth collodion to the scalp according to the International 10-20 System (Jasper 1958). In one operative record, only 14 scalp electrodes were placed due to time limitations. Maximum amplification (!.25 pV = I mm pen deflection) was used during circulatory arrest

Supported in part by the Neurosensory Center Program, Project Grant No. NS03354 from NINDS. "Formerly Assistant Professor, Division of EEG and Clinical Neurophysiology, Department of Psychiatry, University of Iowa. Reprints to: EEG and Clinical NeurophysioIogy, University of Texas Medical School at Houston. Hermann Hospital, 1203 Ross Sterling Avenue, Houston, Texas 77025. 3Former!y Instructor, Departments of Pediatrics and Neurology. University of Iowa. Present address: David Grant Medical Center, Travis Air Force Base, Santa Rosa, California. "~Associate Professor, Division of Thoracic and Cardiovascular Surgery Department of Surgery, University of Iowa.

Pre- and posteratire records

Twenty-two EEGs were obtained preoperatively from 20 patients (Table I). Fourteen of these patients had both preoperative and early postoperative EEGs. Four of this group had abnormal preoperative records. Two (patient 12 and 13) had two EEGs prior to surgery. Patient 12 initially had nonfocal spikes and multiple spikes, but no evidence of this activity 2 weeks later on the day prior to surgery. Patient 13 at 2.5 months of age had shifting spike-and sharp-waves, but just prior to surgery at 5 months of age the recording was normal. Two other patients had dominant activity slower than normal. Following surgery, patient 12 demonstrated abnormality similar to his first preoperative record, but the other 3 patients had normal records. Two additional patients developea excessive slow activity for their age only after surgery. Five patients died during or shortly after surgery. Four had normal preoperative EEGs while the fifth had demonstrated bilateral independent sharp waves in the temporal and parietal region. Patient 24 also had preoperative temporal sharp waves, but this child did well. He was discharged without a postoperative EEG. Seven patients had only postoperative recordings because the surgery was done on an emergency basis. Three of these children had excessive slow activity. Thus 7 acutely ill patients were respon~btz for three of the six i:l.l_l . . . !.i.{ .I !. I. i I~.il' post-

Ei Li ~ L L Y et ai.

62 TABLE !

Patient I 2 3 4 5 6 7 8 9 10 11 12

Age

Diagnosis

Preoperative EEG

Early postoperative EEG

20 mo. 20 mo. 19 mo.

VSD DORV DORV

N Slow for age N

N N N

22 14 16 7 6 3 3 9 2

AV Canal Anom pul ven conn ASD VSD PDA Coar TGA TGA VSD PS ASD VSD TET ASD

N N Left > fight delta N N N Left hemisph, delta N Par sh & muir sp

N Left > right delta N

14 15 16 17 18 19 20 21

!1 2.5 4 10 II 23 22 I

mo. mo. mo. too. mo. too. too. yr.

VSD TGA VSD PDA Coar TGA PS Mitral valve atr TGA VSD TET VSD

N N N N N N N Slow for age Ist sh, sp & mult sp; 2nd N I st temp-par sp & sh; 2nd N N N N N N .... .... ....

22 23 24 25 26 27 28

19 22 5 4 5 16 5

da. too. too. da. too. da vok.

TGA TET TED TGA TGA VSD PS VSD ASD ASD VSD PDA Coar

.... .... .... .... .... Temp-par sh Temp-par sh

13

mo. mo. mo. wk. mo. mo. mo. mo. mo.

5 mo.

TGA

N N

i

Multifocal delta N Slow for age

N

Diagnosis: VSD, ventricular septal defect; ASD, atrial septal defect: DOR~, double outlet right ventricle: PDA, patent ductus arteriosus: TET, tetralogy of Fallot; TGA, transposition of the great arteries: PS, pulmonary stenosis: Coar, coarctation. EEG: N, normal; sh, sharp; sp, spike; temp, temporal: par, parietal: mult, multiple: - . - not done:*, died, operative recordings obtained from a total of 21 patients. Twenty late postoperative records were obtained from 17 children i-9 months after the operation. Fourteen patients had normal records but, 7-9 months after surgery, 2 developed epileptiform discharges and a third developed 14 and 6/see positive spikes. All 3 patients had earlier postoperative records witho~tt spikes of any type.

Operativerecords Recordings were obtained from 14 patients during surgery. At the onset of surface cooling theaverage frontocentral voltage was 45/aV (SE _+7/~V), During cardiac bypass cooling (! 7°-23°C) the voltage dropped to 19/~V (SE +7/~V). This was a significant change from the initial voltage (P< 0.01). The voltage of the fronto-centrai activity in 6 of the 14 children was less than 10/JV prior to circulatory arrest but in no case was there a sustained total absence of electrical

activity during the pre-arrest period. During circulatory arrest voltage rapidly dropped below I0/iV in the remaining 8 cases. Fronto-central activity disappeared earlier than that recorded in the parietal occipital area. Frequency did not change significantly except during circulatory arrest, but 9 of 14 patients showed no fronto-central activity and the average is not representative of those 5 individuals who still had fronto-central activity (range 4-7 c/sec). Residual occipital activity in some cases became intermittent, trailing off into the background "noise" so that the time of total loss of cerebral electrical activity was often approximate. From the rapid voltage drop to either the loss of all activity or to the restoration of the blood supply the persisting occipital activity was mostly I-2,5/~V with some 4 IN activity (Fig. I). Occipital activity persisted in 8 patients throughout the total circulatory arrest (Table II) which averaged 29 min

EEG IN HYPOTHERMLA AND CIRCULATORY ARREST

663

TABLE !! Intra-operative recordings. Patient

Paroxsymal activity

Duration of circulatory arrest (mini

Occurrence of electrocerebral silence

¢5 7 9 10 II 12 13 14 15 22 25 26 27 28

no yes no yes no yes no no yes yes yes yes no no

_'29 36 II 25 31 II 38 25 54 41 33 46 23 43

no yes no yes yes no yes no yes no yes no no no

(range 11-.46 mini. Six children lost all electroeerebral activity after an average of 19 minutes (range 4 to 32 rain). Electrocerebral silence penisted for the remainder of the arrest period (average of 16,3 min and range 6-32 mini, Once mwarming bypass was re-established the occipital activity (if lost) and fronto-central activity returned and increased in voltage, After I rain of warming the fronto-central activity was of higher voltage in those children who had demonstrated persistent occipital activity during the arrest than in those with electrocerebral silence, At the end of rewarming (35 °) voltages tended to be higher and frequencies slower than during early anesthesia but the values were not significantly changed from early anesthesia values. Paroxysmal cerebral electrical activity was observed during the operative procedure in 7 ofthe 14 patients (Fig. 2). Three had epileptiform activity during surface cooling and lost it when placed on cardiopulmonary bypass for more rapid cooling, Four patients developed paroxysmal activity only after bypass was initiated, Six of the 7 again transiently demonstrated paroxysmal activity during bypass r~warming. The occurrence of paroxysmal activity and/or electrical silence during operative recordings appeared to be of no postoperative clinical significance in this group of patients. Two of 7 with, and 2 of 7 without paroxysmal discharge during surgery died shortly after the operation. DISCUSSION The most striking feature observed during this surgical procedure was the persistance of cerebral electrical activity in some children in spite of total arrest of the blood supply. Harden et al. (1966) had reported loss of EEG activity early in circulatory arrest, but this was not the case in the present ~ries. The earlier study was carried out with amplification of 10 #V/mm and electrode positions not completely analogous to the O! and 02 electrodes of the 10-20 System (PampiOione 1956). Such variations in technique could account

Duration of electrocerebral silence (mini 6 16 27 6 32 -14 .w -----

for the different results, The abrupt voltage drop during cooling could be construed to represent loss of all electrical activity if adequate amplification was not used. The hazards involved in the study of low voltage activity without adequate amplification have been discussed in detail by Siiverman et ol. (1970). in early studies of EEGs during bypothermia considerable variation was observed with respect to the temperature at which cerebral activity was lost. it was initially reported that frequency and amplitude decreased until all activity was lost at 20°C (McQueen 1956). Kenyon (1961)and Drew (1961) reported loss of EEG activity at 18°-20°C and a return as the temperature rose above 20°C. In contrast Weiss and Arfel (1960I reported total extinction of activity at 13°-14°C and Belsey et al. (1968) reported activity persisting to 12°C. Pagni and Courjon (1964) observed activity in some individuals at 7°C while others lost activity at 17°C. Harden et al. (1966) observed persistent activity until circulatory arrest in children cooled to !8.5-24.3°C. Activity was not lost prior to circulatory arrest in any of 14 patients on whom operative recordings were obtained in this present series. Paroxysmal activity and spike-and-wave complexes have been noted in deep hypothermia with a variable suggested relationship to prognosis (Weiss and Arfel 1960; Pagni and Courjon 1964}. Seven of 14 patients in the present series demonstrated epileptifonn activity during the operative recording. A relationship between this activity and rapid temperature change was suggested by 4 patients who developed such complexes during rapid bypass cooling and the 6 patients with such activity in rapid rewarming. Three patients developed paroxysmal activity during surface cooling, but it ceased during bypass cooling, suggesting that in these patients the paroxysmal activity represented anoxia which resolved with the perfusion of oxygenated blood. The presence of paroxysmal discharge did not appear to change prognosis significantly.

E. L. REILLYet aL

PATIENT26, 5 MO. OLD, 2/4/75 BALOTHA L.F. 1 H.F. 70

PATIENT 26, 5 MO. OLD, 2/4/73 18 MINUTESOF CIRCULATORYAI~qBST 180 CENTIGRADE L.F, 1

z~-.~

.H,F, 35

I

PATIENT 26, 5 MO. OID, 214//3 45 MINI.ITKBOF CIHCUIATORYAI~SST L,F. 1 B.F, 35 &

1~.~ I

1

see.

Fig. I. Top: S-rface cooling with halothane anesthesia. Middle: Persistence o f occipital activity in channels 4 and 8, higher voltage on the l~l't. Bottom: Occipital activity is more evident over the left hemisphere.

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Figi 2; Top: Recurrent paroxysmal activity in early surface cooling. Middle: Paroxysmal activity developing during cooling bypass. Bottom:Return of paroxysmal activity during warming bypass.

E.L. REILLY et aL

666 SUMMARY

REFERENCES

The EEGs from 28 children less than 2 years of age who underwent cardiac surgery utilizing deep hypothermia and circulatory arrest are reported. There was no increase in the number of abnormal EEGs following this procedure when both pre- and postoperative records were available. The subgroup requiring surgery on an emergency basis had only postoperative records and accounted for a disproportionate number of the abnormal postoperative EEGs. Recordings were made on 14 patients during surgery. In no case was electrical activity lost on the basis of temperature alone. EEG voltage decreased significantly with little change in frequency as the patient's temperature fell. In spite of sustained total circulatory arrest, low voltage activity persisted in the occipital area t'lroughout the procedure (! !--46 min) in 8 children while all cerebral activity was lost for 6-32 rain in the other 6. Intraoperative paroxysmal activity was observed in 7 children but neither this nor temporary loss of activity during circulatory arrest appeared related to the subsequent clinical course. Recovery of the EEG activity was prompt. When temperatures returned to 35°C, frequencies and voltages were similar to those of the early anesthesia period.

AGUILAR, M. J., GERBODE, F. and HILL, J. D. Neuropathologic complications of cardiac surgery. J. thorac, cardiovasc, Suro., 1971, 61". 676-685. BARRATT-BOYES, B. G., SIMPSON, M. and NEUTZE, J. M, Intracardiac surgery in neonates and infants using deep hypothermia with surface cooling and limited cardiopulmonary bypass. Circulation, 1971, Suppl. !: 43 and 44:

RESUidE LES EFFETS DE L'HYPOTHERMIE PROFONDE ET DE L'ARRET CIRCULATOIRE TOTAL SUR L'ELECTROENCEPHALOGRAMME DE L'ENFANT Ce travail concerne l'6tude EEG de 28 enfants de moins de 2 ans, soumis "~ chirurgie cardiaque sous hypothermie profonde et arr6t circulatoire. Lorsque les trac6s pr6 et postop6ratoires sent disponibles, on ne note pas d'augmentation du hombre d'EEGs anormaux apr6s cette intervention. Le sous-groupe n6cessitant une intervention d'urgente et ,.'ayant que des trac~s post-op~ratoires montre au contraire un nombre disproportionn6 d'EEGs post-op6ratoires anormaux. Les trac6s ont i:t6 r~alis6s chez 14 malades au cours de l'intervention. Dans aucun de ces cas on n'a observ6 de perte de l'activit6 61ectrique sur ia base de la seule temp6rature. Le voltage EEG diminue de fa¢on significative, avec de petites modifications de fr6quences, au fur et it mesure de la chute de la temp6rature. En d6pit d'un arr~,t circulatoire total prolong6, une activit6 de bas voltage pers~ste au niveau de raire occipitale tout au long de cet arr6t circulatoire (! ! ',i 46 rain) chez 8 enfants, alors que toute activit6 c6r6brale est abolie pendant 6/~ 32 min chez les 6 autres malades. Une activit6 paroxystique a 6t6 observ~e en cours d'op6ration chez 7 enfants, mais ni cette donn6e, ni la perte temporaire d'actiPit6 au cours de l'arr6t circulatoire n'apparaissent li6es 1'6volution clinique ult6rieure. La r6cap6ration de ractivit6 EEG est rapide. Quand la temperature revient ~ 35~C, les fr6quences et les voltages sent similaires .~ crux du d6but de I'anesth~sie. The authors acknowledge the assistance of Dr. John R. Knott and Mr. Jon F. Peters in the complet.ion of this study.

1-25.

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EEG IN HYPOTHERMIA AND CIRCULATORY ARREST cerebral silence. Neurology (Minneap.), 1970, 20: 525533. StmRAMAmAN, S., W^G~R, H., Vt.AD, P. and LA~rdtT, E. Surface-induced deep hypothermia in cardiac surgery. Pediat. Surg., 1971, 6: 612.

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