Detection of damage during open-heart surgery · platinum needle electrodes2 situated in -the...

Thorax (1973), 28, 464.

Detection of neurological damage duringopen-heart surgery

M. A. BRANTHWAITE

Bromptan Hospital, London

Branthwaite, M. A. (1973). Thorax, 28, 464-472. Detection of neurological damage during open-heart surgery. Cerebral activity during open-heart surgery has been recorded in 140 patientsusing a heavily filtered electroencephalograph, the Cerebral Function Monitor (CFM).Unlike the conventional electroencephalogram the CFM record is recorded at slow speeds,is filtered to minimize electrical interference, and is easy to interpret.A high incidence (62 9%) of alteration in electrical activity was noted at the onset of

perfusion, and several different patterns of change are described.Ten patients suffered neurological damage to a degree which produced physical signs in the

postoperative period. In eight of these 10 cases, abnormal depression of the CFM record wasnoted during perfusion; the depression occurred at the onset on five occasions. Equivocalchanges were noted at the onset of perfusion in one patient whose neurological lesion mayhave been related to a postoperative cardiac rhythm disorder. One patient sustained a mid-brain lesion, probably at the onset of perfusion, and the CFM record during operation wasunremarkable.The incidence of both neurological damage and depression of the CFM record at the onset

of perfusion has decreased since filters for microemboli have been included in the perfusioncircuit.

It is concluded that the CFM is a useful means of detecting acute changes in corticalactivity during open-heart surgery. The risk of cerebral damage is high at the onset ofperfusion when both hypotension and microemboli from the extracorporeal circuit maycontribute to the neurological lesion.

A previous study of neurological damage duringopen-heart surgery revealed an incidence ofapproximately 20% (Branthwaite, 1972). Threefactors appeared to be associated, namely age,duration of perfusion, and the presence of pre-existing neurological disease. It proved impossibleto identify precise causes with any certainty.

Recording the electro-encephalogram (EEG)throughout the procedure has been advocated asa means of monitoring cerebral function (Fischer-Williams and Cooper, 1964), and previous studieshave noted events which are commonly associatedwith EEG changes, such as cannulation orobstruction of the superior vena cava (Pam-piglione and Waterston, 1961) and acidosis(Brazier, 1961). Conventionally, the EEG is re-corded from multiple sites at fast speed. Inter-ference due to artefacts is common (Sadove,Becka, and Gibbs, 1967), and considerable skilland experience are required for accurate inter-pretation. Recently, a cerebral function monitor

(CFM) has been developed which records aheavily filtered EEG signal at slow speeds(Maynard, Prior, and Scott, 1969). Acute changesin cerebral activity cause a change in either themean value or amplitude of the tracing and areeasily recognized by the observer; interference iseliminated to a large extent by the filter system.

Relative freedom from interference togetherwith the ease of interpretation and slow speed ofrecording form a combination which is particu-larly suitable for monitoring cardiac surgery, andPrior et al. (1971) have described its use for thispurpose in 49 cases. In the present study, anattempt has been made to identify the timing andhence the presumptive nature of neurologicaldamage by recording the EEG throughout theoperation using the CFM.

MATERIAL AND METHODS

One hundred and forty patients have been studiedduring open-heart surgery for a wide variety of con-

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Detection of neurological damage during open-heart surgery

genital and acquired heart disease. Their ages rangedfrom 3 months to 74 years.

In the majority of cases anaesthesia consisted ofpremedication with omnopon and scopolamine fol-lowed by a thiopentone, nitrous oxide-oxygen-relaxantsequence, supplemented when necessary with eitheromnopon or low concentrations (less than 1 %) ofhalothane.There was considerable variation in perfusion tech-

nique and apparatus; four types of oxygenator wereused (rotating disc, Rygg, Temptrol, and membrane)and different degrees of haemodilution were employed.The pH of the perfusate was adjusted to approximately7-4 with sodium bicarbonate before the onset of per-fusion. In the first 33 cases the arterial return wasfiltered through a 150 mesh and bubble trap, butin later cases a Swank filter for microemboli wasincorporated into the cardiotomy suction and bloodpriming line; more recently, a 40 ,t Barrier filter' hasbeen used in addition on the arterial return.

Perfusion was carried out at a normal or onlymoderately reduced temperature (30-35' C) in allbut seven cases, in five of whom hypothermic circula-lJohnson and Johnson

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tory arrest was employed at a nasopharyngeal tem-perature between 15 and 27° C. In the majority ofpatients the arterial carbon dioxide tension was main-tained between 30 and 40 mmHg throughout theoperation. Routine monitoring included arterial andsuperior vena caval pressures, nasopharyngeal tem-perature, and arterial blood gas tensions and pH.The EEG was recorded from two intradermal

platinum needle electrodes2 situated in -the parietalregion on either side of the midline, approximately5 cm apart and a little behind the level of a linejoining the external auditory meati. The impedancebetween the two electrodes was monitored contin-uously and was always well below 5 K. The CFMwas a prototype instrument, the definitive version ofwhich is now available from Devices Ltd.At first both the impedance and CFM signals were

recorded on a Devices 2-channel pen recorder run-ning at 6 mm/min; subsequently, an SE Laboratoriesmulti-channel ultraviolet recorder was used at aspeed of 10 mm/min. This enabled additional infor-mation to be recorded simultaneously, in particular,the arterial and superior vena caval pressures and thenasopharyngeal temperature.2Specialized Laboratory Equipment

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FIG. 1. (a) Normal CFM record obtained during anaesthesia. (b). Virtual abolitionof cerebral activity during an episode of ventricular fibrillation (onset at arrow).The high voltage activity preceding this represents interference due to surgical diath-ermy. (c) Depression of cerebral activity associated with hypotension due tohaemorrhage and administration ofprotamine.

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FIG. 2 (a) Acute elevation of CFM record associated with the onset of cardio-pulmonary bypass. (b) Gradual elevation of CFM record following the onset ofperfusion.

RESULTS

The appearance of normal cerebral activity duringanaesthesia as recorded on the CFM is illustrated(Fig. la). Sudden interference with cerebral per-

fusion produces an abrupt change in the record as

shown in Fig. lb and c. Surgical diathermy causesprohibitive interference if used frequently, andfor this reason the records could not be inter-preted throughout the entire operation. The per-fusion period and an interval of 15 minutes or

more before and after perfusion could always berecorded satisfactorily with only minimal inter-ference (Fig. lb).An abrupt change in cerebral activity was noted

on the CFM at the onset of perfusion in 88patients (62 9%). In two patients there was a slightincrease in the mean level of the record whencannulation of the superior vena cava was asso-ciated with an increase in caval pressure, and in40 patients there was a slight drop in mean level

at the termination of perfusion. In 16 patientschanges were noted during perfusion and wereassociated in seven of the 16 with reduction ofthe temperature to less than 30° C.

Several patterns of change were seen at theonset of perfusion. Elevation of the record was

either sudden or gradual (Fig. 2a and b) andoccurred in 46 patients; a biphasic movement(Fig. 3) was recorded in 22 patients and depressionof activity (Fig. 4) was seen in 20 patients.Thirteen patients in this series sustained neuro-

logical damage of varying severity, apparentwithin 48 hours of operation. Four adults (ages53-60 years) were hemiplegic postoperatively andthe disability has persisted for more than sixmonths in one case. In these four patients, theonly abrupt change in the CFM record was atthe onset of perfusion when there was a markedand sustained depression with slow, high-voltageactivity persisting for some minutes. Figure 5 isa representative example and also illustrates the

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; f i ... ^..'s. ..: . . ... . 4 ^ .*. ' . e . . A .... . ..... ..... ^ , ^.___........... -. . .N . . 4 ... , . . ^X _'.: s .. S .......... _._..^ 2_ ^ . ^. - . A S*. ... > ^ . ^. @ - > w _ ^+ . S... A . . 4 .. . _ _ .. .. .; . A ... ._. <. _ Sfi ., .. S,lh,. . - .. _ __A|a:_w_^w^ . . . _.t_ _.0..... ... w . . _ .. _ . S ^W.W A ... . W._.. . s . ^ < . '0 S .0 .FIG. 3. Biphasic change at the onset ofperfusion.

FIG. 4. Depression ofCFMrecordfollowing the onset ofperfusion.

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FIG. 5 Profound depression ofCFM record at the onset ofperfusion. The drop is followed by a period of high-voltage,slow activity, taking 10 minutes to recover. Tracings from above downwards are arterial blood pressure, impedancebetween the two CFM electrodes, and the CFM record itself. This patient was hemiplegic postoperatively.

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FIG. 6. Acute depression of CFM record following release of the aorticclamp during perfusion. This patient had a transitory monoplegia post-operatively.

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FIG. 7. Biphasic record at the onset of perfusion in an elderly diabetic whosuffered an epileptic fit on the second postoperative day.

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FIG. 8. Depression of CFM record associated with circulatory arrest at a nasopharyngeal temperature of270 C in a 1-year-old child. Records from above down are arterial blood pressure, superior vena cavalpressure,nasopharyngeal temperature, and the CFM record. Duration of circulatory arrest was 14j minutes.

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FIG. 9. Complete perfusion record at very slow speed (1-5 mm/min) in apatient who sustained a mid-brain lesion during surgery. Total perfusion time:35 minutes. Upperpanel: impedance; lowerpanel: CFMrecord.

drop in systemic pressure which occurs frequentlyat the onset of perfusion. Three of these fourpatients were known to have arterial diseasepreoperatively, either coronary or cerebral.A similar record, showing marked depression

at the onset of perfusion with no other remarkablefeatures, was obtained in a 6-year-old child whowas irritable and confused following operation.A short episode of cardiac arrest occurred withinthe first 12 hours and it was apparent subsequentlythat the child had sustained gross neurologicaldamage; it was impossible to determine the rela-tive importance of the various neurological insults.A further two patients (ages 50 and 64 years)

had signs of a hemiplegia and a monoplegiarespectively in the postoperative period. In boththese patients the onset of perfusion producedlittle change in the CFM record, but a markeddepression of activity occurred when the aorticclamp was removed at a time when the heart wasnot ejecting. Figure 6 is characteristic of thesetwo records.An elderly diabetic (aged 66 years) suffered an

epileptic fit on the second postoperative day.Prior to this her postoperative course had beensatisfactory with no grossly detectable neuro-logical abnormality. The possibility of a transitorycardiac rhythm change preceding the convulsioncould not be excluded. The record of this patient'scerebral function during surgery revealed a

biphasic pattern at the onset of perfusion but therest of the record was uneventful (Fig. 7).A 1-year-old child suffered from convulsions

and a left hemiparesis following circulatory arrestfor 14L minutes at a nasopharyngeal temperatureof 27° C. The only noticeable feature on the CFMrecord was a sudden change at the start of thearrest period, from an apparently normal traceto very low voltage activity which tended todiminish even further until the circulation wasrestarted, when cerebral activity recovered fairlyrapidly (Fig. 8).A mid-brain lesion was apparent postoperatively

in a 36-year-old woman. This tracing (Fig. 9) wasrecorded at an unusually slow speed (1 5 mm/min)and lacks detail, but apart from the elevation atthe onset of perfusion, which persisted throughoutthe procedure, there is no major change. Studiesof the oxygen content of blood drawn from thejugular bulb suggested that the lesion in thispatient occurred at the onset of perfusion; detailsof this case will be included in a later report.Three patients were confused for several days

following operation. In a 63-year-old woman theCFM record throughout perfusion was unremark-able. A 56-year-old man required prolonged per-fusion (203 minutes) and the mean level of thetracing fell slowly throughout this period. In thepost-perfusion period an unexpected episode ofventricular fibrillation resulted in a short (2 min)

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FIG. 10. Elevation of CFM record at the onset ofperfusion (event marker No. 5) associated with an increase in alrtelrialpressure in a 74-year-old man with severe heart failure. Records from above down: arterial blood pressure; suiperiorcaval pressure; nasopharyngeal temperature; CFM record.

record of virtually absent cerebral activity(Fig. lb) before defibrillation restored an adequatecirculation and the CFM tracing returned to anormal level. A 74-year-old man was hypotensiveand in severe heart failure in the pre-perfusionperiod and the CFM tracing was low in meanlevel and amplitude. Following the onset of per-fusion, the CFM record increased in both meanvoltage and amplitude and remained unremark-able throughout the rest of the procedure (Fig. 10).

DISCUSSION

Previous reports of conventional EEG monitoringduring cardiopulmonary bypass have stressed thefrequency with which changes are observed duringcannulation of the superior vena cava and at theonset of perfusion (Theye, Patrick, and Kirklin,1957; Davenport, Arfel, and Sanchez, 1959;Adelman and Jacobson, 1960; Paton, Pearcy, andSwan, 1960; Storm van Leeuwen, Mechelse, Kok,and Zierfuss, 1961). Prior et al. (1971), reportingthe use of the CFM during cardiac surgery, com-mented on the frequency with which changeswere detected at the onset of perfusion and theyattributed these to alterations in the depth ofanaesthesia. In the present series, changes in the

CFM record during cannulation of the superiorvena cava were seen infrequently but there wasa high incidence of alteration at the onset ofperfusion.A number of factors could affect cerebral

function at this time, including changes in theconcentration of intravenous or inhalationalanaesthetic agents, alterations in cerebral haemo-dynamics, arterial carbon dioxide tension, tem-perature or haematocrit as well as unidentifiedfactors related to perfusion. A subsequent reportwill describe which of the patterns illustrated inthe present paper can be attributed to one orother of the factors enumerated above.

In nine of the 10 cases with physical signs ofneurological damage, an unusual degree of depres-sion of the CFM record occurred during perfu-sion; in six patients, this occurred at the onset ofperfusion and the depression was more prolongedand profound than that recorded in patients with-out neurological damage. In one of these six cases(Fig. 7), the change was slight and no greaterthan that seen in many patients whose postopera-tive course was entirely normal, and it wasuncertain whether the cerebral lesion in this casewas sustained during surgery or postoperatively.In the tenth case (Fig. 9) the cerebral lesion was

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Detection of neurological damage during open-heart slurgery

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FIG. 11. Depression of CFM record at onset of perfusion associated with slow,high-voltage activity. This patient had no grossly detectable neurological defectin the postoperative period.

at mid-brain level and it is widely recognized thatEEG abnormalities are not caused necessarily bymid-brain disorders.

It seems therefore that the CFM has providedan accurate record of the timing of cortical dis-turbances during perfusion. It is more difficult torelate the degree of detectable neurological abnor-mality to the duration or magnitude of the changesrecorded on the CFM. The tracing in Fig. 11 issomewhat similar to that reproduced in Fig. 5,but whereas the patient whose record is shown inFig. 11 had no grossly detectable neurologicaldamage, Fig. 5 was recorded from a patient whowas hemiplegic for several days postoperativelybefore making an apparently complete recovery.Depression of cortical activity probably representsa considerable disturbance but clinically obvioussequelae do not result inevitably (compare cere-bral concussion).The onset of extracorporeal circulation is

accompanied by many changes which could exertan adverse influence on cerebral function. Anobvious possibility is a sudden drop in arterialblood pressure with a change from pulsatile tonon-pulsatile perfusion. This fall in pressure iscommon in spite of high flow rates from theperfusion apparatus (80 ml/kg/min or more).Although the cerebral circulation has the capacityto autoregulate so that cerebral blood flow ismaintained in the face of wide changes in arterialpressure (Lassen, 1959), there is a limit belowwhich cerebral blood flow falls. The adjustmentscannot compensate for very rapid changes inpressure (Schneider, 1963) and the degree towhich the cerebral vessels can dilate is probablyreduced in the elderly, especially in those withcerebrovascular disease (Bromage, 1953). Acutehypotension was documented in four of the fivepatients in whom major changes in cerebralactivity occurred at the onset of perfusion; fourof these patients were aged more than 50 yearsand three had a history of arterial disease.An alternative cause for neurological damage

at the onset of cardiopulmonary bypass could beemboli from the perfusion apparatus. SinceJanuary 1971, additional filters have been addedto the perfusion system and the incidence ofdepression of the CFM record at the onset ofperfusion has changed from 7/33 (21 -2%) in 1969and 1970 to 13/107 (12-2%) in 1971 and 1972.There has also been a very obvious reduction in theincidence of important neurological injury in thisunit since early 1971, although precise figures arenot available yet. It seems difficult to deny the con-clusion that emboli from the perfusion system mayhave been responsible in part for neurological dam-age, even though acute hypotension could havebeen an additional contributory factor.

In three patients, the neurological disturbanceappeared to occur during perfusion. In one case,circulatory arrest without adequate protectionfrom hypothermia was probably responsible,whereas in the other two instances, release of theaortic clamp was associated with depression ofcerebral activity. Emboli of air, clot or calciumtrapped in the left heart or root of the aortacould have been responsible; alternatively, acutehypotension may have occurred as the aortic valvewas 'tripped' in one case, and the perfusion pres-sure fell abruptly.A notable feature has been the complete

absence of obvious changes detected during there-establishment of a spontaneous circulation,when the left ventricle is beginning to eject.Manoeuvres to remove air from the left heart arenotoriously ineffective (Padula, Eisenstat, Bron-stein, and Camishion, 1971; Lawrence, McKay,and Sherensky, 1971) and in several of the patientsin this series, air was seen frothing out of thepuncture wound in the root of the aorta withevery ventricular contraction. Although airtrapped in the circulation can cause extensiveneurological damage, the lack of change in theCFM record with the onset of left ventricularejection suggests that cerebral air embolism israrely of serious magnitude in this unit.

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M. A. Branthwaite

I am grateful to the surgeons of the BromptonHospital for permission to study patients under theircare.

The work has been supported by a grant from theMedical Research Council and the results will beincluded in a thesis to be presented for the degree ofM.D. (Cantab.).

REFERENCESAdelman, M. H., and Jacobson, E. (1960). Electroencephalo-

graphy in cardiac surgery. American Journal of Cardio-logy, 6, 763.

Branthwaite, M. A. (1972). Neurological damage related toopen-heart surgery: a clinical survey. Thorax, 27, 748.

Brazier, M. A. B. (1961). The EEG in open-heart surgery andin surgery for aortic and cerebral aneurysms. InCerebral Anoxia and the Electroencephalogram, p. 256,edited by H. Gastaut, and J. S. Meyer. Thomas,Springfield, Illinois.

Bromage, P. R. (1953). Some electroencephalographicchanges associated with induced vascular hypotension.Proceedings of the Royal Society of Medicine, 46, 919.

Davenport, H. T., Arfel, G., and Sanchez, F. R. (1959).The electroencephalogram in patients undergoing openheart surgery with heart/lung bypass. Anesthesiology,20, 674.

Fischer-Williams, M., and Cooper, R. A. (1964). Some aspectsof electroencephalographic changes during open-heartsurgery. Neurology (Minneapolis), 14, 472.

Lassen, N. A. (1959). Cerebral blood flow and oxygenconsumption in man. Physiological Review, 39, 183.

Lawrence, G. H., McKay, H. A., and Sherensky, R. T.(1971). Effective measures in the prevention of intra-operative aeroembolus. Journal of Thoracic and Cardio-vascular Surgery, 62, 731.

Maynard, D., Prior, P. F., and Scott, D. F. (1969). Devicefor continuous monitoring of cerebral activity in resusci-tated patients. British Medical Journal, 4, 545.

Padula, R. T., Eisenstat, T. E., Bronstein, M. H., andCamishion, R. C. (1971). Intracardiac air followingcardiotomy. Location, causative factors, and a methodfor removal. Journal of Thoracic and CardiovascularSurgery, 62, 736.

Pampiglione, G. and Waterston, D. J. (1961). EEG observa-tions during changes in venous and arterial pressure.In Cerebral Anoxia and the Electroencephalogram, p. 250edited by H. Gastaut and J. S. Meyer. Thomas,Springfield, Illinois.

Paton, B., Pearcy, W. C., and Swan, H. (1960). The import-ance of the electroencephalogram during open cardiacsurgery with particular reference to superior vena cavalobstruction. Surgery, Gynecology and Obstetrics, 111, 197.

Prior, P. F., Maynard, D. E., Sheaff, P. C., Simpson, B. R.,Strunin, L., Weaver, E. J. M., and Scott, D. F. (1971).Monitoring cerebral function: clinical experience withnew device for continuous recording of electricalactivity of brain. British Medical Journal, 2, 736.

Sadove, M. S., Becka, D., and Gibbs, F. A. (1967). Electro-encephalography for Anaesthesiologists and Surgeons.Pitman, London.

Schneider, M. (1963). Critical blood pressure in the cerebralcirculation. In Selective Vulnerability of the Brain inHypoxaemia (A Symposium organized by the Councilfor International Organizations of Medical Sciences)edited by J. P. Schade and W. H. McMenemey pp. 7-20.Blackwell, Oxford.

Storm van Leeuwen, W., Mechelse, K., Kok, L., andZierfuss, E. (1961). EEG during heart operations withartificial circulation. In Cerebral Anoxia and the Electro-encephalogram, p. 268, edited by H. Gastaut and J. S.Meyer. Thomas, Springfield, Illinois.

Theye, R. A., Patrick, R. T., and Kirklin, J. W. (1957).The electroencephalogram in patients undergoing openintracardiac operations with the aid of extracorporealcirculation. Journal of Thoracic Surgery, 34, 709.

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