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Ann Thorac Surg 1998;65:S65-S70
© 1998 The Society of Thoracic Surgeons

Neurologic Sequelae Associated With Deep Hypothermic Circulatory Arrest

^a Department of Anesthesia, Children’s Hospital, Boston, Massachusetts, USA

Address reprint requests to Dr Hickey, Department of Anesthesia, Children’s Hospital, 300 Longwood Ave, Boston, MA 02115

Presented at Risk Assessment of Major Perioperative Issues in Pediatric Cardiac Surgery, Washington, DC, May 7, 1997.

	Abstract

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
Background. Earlier studies of the incidence of neurologic disturbances after deep hypothermic circulatory arrest produced conflicting results. This article reviews the results of the Boston Circulatory Arrest Study, and another study undertaken to compare neurologic outcome in infants after deep hypothermic circulatory arrest using alpha-stat and pH-stat strategies.

Methods. The study population in the Boston Circulatory Arrest Study consisted of 171 infants less than 3 months of age. Neurologic outcomes were evaluated perioperatively, at 1 year, and at 4 years. The study population in the alpha-stat versus pH-stat study consisted of 182 infants no older than 9 months of age. Patients were evaluated for postoperative electroencephalographic (EEG) and clinical seizures, recovery time to first EEG activity, and postoperative mortality and morbidity.

Results. After about 30 minutes of circulatory arrest there was increasing probability of perioperative clinical seizures, EEG seizures, and increased time to recovery of EEG activity. One-year evaluations showed a significant relation of duration of circulatory arrest to lowered psychomotor developmental index and increased neurologic abnormalities. Four-year evaluations showed no difference between low-flow and circulatory-arrest patients in results of neurologic examination or in full-scale general IQ, although there was an effect of circulatory arrest duration on various subscores of cognitive function. Compared with the pH-stat strategy, the alpha-stat strategy tended to be associated with more EEG seizures and higher postoperative morbidity and mortality, and was significantly associated with longer recovery time to first EEG activity.

Conclusions. These studies strongly suggest that in infants undergoing open heart operations for complex congenital heart defects, low-flow bypass is associated with better neurologic outcome than is circulatory arrest and that the pH-stat strategy is associated with a better outcome than the alpha-stat strategy when circulatory arrest is used.

	Introduction

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
The many improvements achieved in bypass technology, surgical anesthesia technology, and postoperative care have resulted in significantly improved survival of children with congenital heart disease. This development has focused increased attention on the neurologic sequelae associated with cardiac surgical procedures occurring in young children, with potential adverse effects that have an impact on subsequent long lifetimes.

The study of neurologic sequelae in this patient population is difficult because there are many possible causes of intraoperative brain injury during the repair of congenital heart disease. Injury due to air and particulate emboli, which may occur regardless of whether or not circulatory arrest is used, and flow-related injury are risks in all cardiopulmonary bypass procedures. Unique to the repair of congenital heart disease in young children are the potential adverse neurologic sequelae related to the use of deep hypothermic circulatory arrest (DHCA).

	Incidence of neurologic disturbances

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
Early investigation of the incidence of functional and structural disturbances after DHCA found clear evidence of choreoathetosis. A reported incidence of 19% comes mostly from the 1960s and 1970s; during the last decade the incidence of choreoathetosis, typically occurring 2 to 6 days postoperatively, has been 1% or less at most institutions. The incidence of transient seizures ranged from 4% to 25%, depending on the institution and the thoroughness of the surveillance for seizures. A number of studies looked at the effects of DHCA on cognitive function. Wells and associates [1] found that DHCA patients scored worse than siblings, with effects related to the duration of DHCA, but that patients subjected to moderate hypothermic circulatory arrest scored comparably with siblings. Blackwood and colleagues [2] found no difference in preoperative and postoperative cognitive scores among patients who underwent DHCA. Multiple other studies also produced conflicting results. All studies had many methodologic flaws, which included diversity of age, diagnoses, and preoperative conditions in patient populations, among other issues that we now know have an impact on cognitive neurologic outcome.

Over the past decade, low-flow bypass, which maintains a continuous cerebral circulation at a low flow rate (eg, 0.75 L · min^-1 · m²), has been advocated as preferable to circulatory arrest with respect to neurologic outcome. However, this procedure prolongs bypass time, thereby potentially increasing exposure to pump-related sources of brain injury. Advocates of low-flow bypass simply accepted on faith that the provision of some perfusion during deep hypothermia would improve neurologic outcome; there were no rigorous clinical studies that tested this hypothesis.

	The Boston Circulatory Arrest Study

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
In 1987, we began to study effects of circulatory arrest and low-flow bypass on neurologic outcome, including the outcome effect of the duration of circulatory arrest. Figure 1 illustrates the difficulty and the resource demands of doing these types of studies. We first did some pilot studies in 1987. With the receipt of a large grant from the National Institutes of Health, we began to enroll patients. Patient enrollment continued for about 4 years, during which time we began to bring patients back for 1-year evaluations. Patients then were brought back for 4-year evaluations. The results of our 4-year evaluations of this cohort of patients initially studied between 1988 and 1992 are still unpublished. Of course, in terms of the evolution of techniques, 1992 represents almost another era. In 1992 we were not using ultrafiltration, and bypass circuits and oxygenators were much different from what they are currently, as were many other techniques. What was done then is still only now being assessed, after a lag time of about 10 years, the expenditure of about $10 million, and a huge institutional commitment.

View larger version (29K): [in this window] [in a new window]   Fig 1. Illustration of the demands on time and resources required by this type of study.

We enrolled 180 of the 191 patients eligible for the study during the 3-year enrollment period. Nine patients were shunted to other procedures because of coronary artery anatomy or other issues. Arterial switch was the operation of choice in 171 patients, and these were all studied. Early death at less than 30 days occurred in 3 patients, for a 1.8% hospital mortality rate. All remaining patients entered the outcome study.

Perioperative results
Perioperative results [3] showed that there was increasing probability of clinical seizures after about 30 minutes of circulatory arrest as the predominant perfusion strategy (Fig 2). The probability was somewhat higher in the presence of a ventricular septal defect, which was an independent risk factor, compared with an intact septum. The incidence of seizures as detected by 48-hour continuous 16-lead electroencephalographic (EEG) monitoring was about three times greater than the incidence of seizures seen clinically (Fig 3). But again the same general effect held, in that there was significant probability of EEG seizures after about 30 minutes of circulatory arrest time. A prolonged latency to first EEG activity was another marker of neurologic injury. We found a very significant straight-line relation between duration of circulatory arrest time and the time to redevelopment of EEG activity during the intraoperative period (Fig 4).

View larger version (15K): [in this window] [in a new window]   Fig 2. Relation of incidence of postoperative clinical seizures to duration of circulatory arrest. (IVS = intact ventricular septum; VSD = ventricular septal defect.)

View larger version (16K): [in this window] [in a new window]   Fig 3. Relation of incidence of postoperative seizures detected by electroencephalographic monitoring to duration of circulatory arrest. (IVS = intact ventricular septum; VSD = ventricular septal defect.)

View larger version (14K): [in this window] [in a new window]   Fig 4. Relationship of time to postoperative redevelopment of electroencephalographic activity to duration of circulatory arrest.

Four-year evaluation
A first analysis of the 4-year evaluations has just been completed. The primary outcomes were IQ, as measured by the Wechsler Preschool Primary Scale of Intelligence-Revised index, and a neurologic examination. Secondary outcomes were measured by very rigorous assessments of motor function, speech, and language by developmental psychologists.

There was no statistically significant difference between low-flow and circulatory-arrest patients on the 4-year neurologic examination or on full-scale IQ. Overall, IQ scores tended to be lower than the norm in this patient population. The impact of circulatory arrest on cognitive function that was apparent at the 1-year evaluations seems to have been blurred as the patients grew older. The plasticity of the central nervous system and the ability of parts of the brain to assume the functions of other parts appear to have modified the early findings of neurologic damage. Ventricular septal defect was an independent risk factor both for abnormality on neurologic examination and for lower IQ at 4 years of age.

Circulatory arrest did have long-term impact on various subscores of cognitive function: fine motor function, gross motor function, and speech apraxia. The use of a predominant circulatory-arrest strategy was not significantly associated with language per se at 4 years of age but did have a highly significant impact on the index of speech apraxia. There was a significantly higher incidence of speech apraxia in the group that underwent circulatory arrest than in the group that underwent low-flow bypass (Fig 5).

View larger version (11K): [in this window] [in a new window]   Fig 5. Incidence of speech apraxia among circulatory (Circ.) arrest and low-flow bypass patients at 4-year evaluations. (IVS = intact ventricular septum; VSD = ventricular septal defect.)

	Alpha-stat versus pH-stat strategy

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

In 1992, we undertook a study to compare cardiovascular and neurologic outcomes in infants after deep hypothermic CPB using the alpha-stat versus pH-stat strategy [5]. We used the same protocols and paradigms that we had developed for our earlier DHCA study, ie, the same kind of randomized, blinded, carefully stratified protocols and randomization schemes. Previous studies on central nervous system outcome in children and infants (retrospective studies mostly done at our institution) had shown worse cognitive outcomes after the Senning procedure with alpha-stat. Also, a somewhat loose association had been observed between the use of alpha-stat and a miniepidemic of postoperative choreoathetosis that occurred in the late 1980s and early 1990s in our institution, an epidemic that has fortunately since subsided.

Subjects were enrolled in a randomized study from July 1992 through June 1996. All subjects were no older than 9 months of age undergoing reparative heart operations, although not restricted to transposition of the great arteries as in our earlier study, and without any associated congenital or acquired extracardiac disorders or history of a previous operation. Of the 216 eligible patients, 190 were enrolled and 182 were studied; 8 were excluded for various reasons, mostly for lack of temperature compliance with the protocol.

In our earlier study of neurologic outcome after DHCA done between 1988 and 1992, the overall incidence of postoperative clinical seizures was about 6.0% to 6.5% and of EEG seizures about 20%. In this study, the incidence of clinical seizures was about 3% and of EEG seizures about 6% to 7%. So while we were studying neurologic outcome, the neurologic outcome was improving. The power analysis that we used in this study assumed the same level of neurologic injury, particularly seizure disorders, that we had encountered earlier. Consequently, with 180 patients, we were left without sufficient power to be able to make a definitive statement about neurologic outcome. However, there was a fairly impressive tendency toward more EEG seizures with alpha-stat than with pH-stat (Fig 6). There also was a statistically significant shorter recovery time to first EEG activity and a trend toward lower postoperative morbidity and mortality in the pH-stat group.

View larger version (12K): [in this window] [in a new window]   Fig 6. Incidence of postoperative seizures with use of alpha-stat and pH-stat strategies in infants undergoing reparative heart operations. (EEG = electroencephalogram.)

	Pharmacologic intervention

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
Our experience in these DHCA studies clearly indicates that it is going to be difficult to demonstrate significant preservation of neurologic function with use of an antiinflammatory agent, such as aprotinin, given the present low level of neurologic damage that we are seeing. The introduction during just the past few years of ultrafiltration, use of a very small bypass circuit with very limited prime volumes, alternative drugs, and other advances will make it quite difficult to demonstrate the additional increment of improvement that may be attributed to the use of an antiinflammatory agent. Very long outcome studies and considerable resources will be required.

Nevertheless, we are actively investigating a number of antiinflammatory agents, particularly those centered on adhesion molecules. We are just now starting clinical trials with one antiadhesion agent. We are beginning with a study of its pharmacokinetics, so that we can be fairly clear as to what level of agent we must have in the patient and in the bypass circuit before proceeding to a full clinical trial.

	Discussion

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 
QUESTION FROM THE AUDIENCE: There have been some reports in the adult literature of adverse outcomes with the use of circulatory arrest in ascending aortic arch repairs. Are you concerned about the risk of thrombosis when using an antithrombinolytic during circulatory arrest?

DR HICKEY: We do not consider circulatory arrest an issue with the use of an antithrombinolytic at the present time.

QUESTION FROM THE AUDIENCE: Do you operate on adult patients at all?

DR HICKEY: We operate on adults with congenital heart disease, but rarely use circulatory arrest in these patients.

QUESTION FROM THE AUDIENCE: In your study of alpha-stat versus pH-stat, did you avoid circulatory arrest in your patients?

DR HICKEY: No, those patients all had circulatory arrest for some period. With the pH-stat group, we maintained the pH-stat strategy throughout the cooling period, the rewarming period, and 5 minutes of reperfusion. Then we switched to an alpha-stat strategy. If we used low-flow, we used the pH-stat strategy throughout the cooling period and the low-flow bypass until we started rewarming.

QUESTION FROM THE AUDIENCE: On the basis of this study, would you now extend the pH-stat strategy to all patients or only use it in infants?

DR HICKEY: We now generally use it for all patients for whom we use deep hypothermia, whether or not we use low-flow or circulatory arrest. If we are using only moderate levels of hypothermia, the question becomes largely academic.

QUESTION FROM THE AUDIENCE: It appears that your low flow is not very low flow.

DR HICKEY: We use 0.7 L · min^-1 · m^-2, or about 50 mL · kg^-1 · min^-1 in the neonates. That is about a third of our normal flow level. Parenthetically, the question of how low "low flow" should be is still completely open. It has been shown that you can go as low as 5 to 10 mL · kg^-1 · min^-1 and still seem to cover the minimal amount of all bleeds to the brain at 15° to 18°C. But I do not think anyone wants to push the limits that low clinically, and I do not know of any group actively doing that.

QUESTION FROM THE AUDIENCE: What I find most interesting in your original study is that there is a 10% incidence of neurologic injury even when you have essentially no circulatory arrest.

DR HICKEY: Absolutely. Even when everything is done completely right, as far as we know about what is right at the present time, there is still a baseline incidence of neurologic injury. This may be related to the embolic load, the inflammatory response to bypass, and reperfusion injury, among other factors.

QUESTION FROM THE AUDIENCE: I am curious as to what you think is the mechanism of action of pH-stat. Is it primarily improvement of brain cooling in the prearrest period? Or does the alteration in pH affect the oxygen dissociation curve and help unload more oxygen to the tissues? Or is it a combination of both factors?

DR HICKEY: I would think both factors are involved. Certainly we believe that it probably facilitates brain cooling. But, given the other outcome effects that we saw, it is likely that still more complex issues are involved.

DR ROSS M. UNGERLEIDER (Durham, NC): There are a number of questions that I would like to raise about your study. In your first study, in the curves showing the duration of circulatory arrest related to outcome, the curves for intact ventricular septum and ventricular septal defect were very separate. But if we are just looking at injury as related to duration, those curves should be identical. The fact that they are not makes me suspect that we are looking at some other factors for injury that have nothing to do with duration, perhaps involving the complexity of the ventricular septal defect patients or other unknown factors. When you combine those patients with your other patients and draw conclusions from the combined data, you may not be seeing the impact of circulatory arrest duration but rather noise from these other factors.

Another concern that I have is the nature of the randomization of the study. Were patients randomized for the three surgeons doing the majority of the operations at your institution, or did you have different surgeons doing alpha-stat or pH-stat, depending on their practice techniques? And were patients randomized according to disease? For example, we use pH-stat for patients with lots of collaterals, believing that it offers an advantage in these patients. Did any such considerations influence the assignment of patients to either group?

Finally, it seems that there are other factors that may come into play in the intensive care unit that might influence outcomes. Take anemia for example, which might make a difference in hemodynamic outcomes.

So I would like to ask you, on the basis of this study, would you recommend that we go back to our institutions and start routinely using pH-stat during cooling for all our patients?

DR HICKEY: I think the use of pH-stat during cooling makes a lot of sense. Your questions highlight the complexity of the issues involved and the difficulty we have in sorting out the possible injury-related factors. The issues involving the pH of the brain before circulatory arrest and before a planned ischemic insult are significant and will require more study.

I think that Julie Swain’s studies and our own studies in piglets showed fairly well that the intracellular pH in the brain is quite independent of the blood pH. So, although you change blood pH when you change from alpha-stat to pH-stat, the intracellular pH that determines the intracellular milieu once you go into an ischemic period is really not altered very much at all. This is one of the reasons why the alpha-stat rationale may be somewhat flawed.

With respect to randomization, our pH study was stratified by surgeon, so that each surgeon had a reasonable selection of different diagnoses and different strategies. But when you go down to a third level of stratification, trying to stratify the group of patients who have transposition of the great vessels between patients with intact ventricular septum and patients with ventricular septal defect, you do encounter the problem of an inadequate number of patients.

I would not recommend that everyone begin using the pH-stat strategy for all patients. The data we have are not sufficiently compelling. The study has some significant results, but there are other questions about the data. The study report has not yet been peer-reviewed, so we may not be aware of possible flaws.

But I do think that we should develop a healthy skepticism about whether alpha-stat is the way to go. We are fairly convinced that pH-stat makes more sense for many patients in the high-risk categories. This may be particularly true for various subsets of patients, such as those patients with extensive collaterals that you mentioned.

Would I tell everyone to routinely use the pH-stat strategy? Not yet.

	References

Top Abstract Introduction Incidence of neurologic... The Boston Circulatory Arrest... Alpha-stat versus pH-stat... Pharmacologic intervention Discussion References

 

1. Wells F.C., Coghill S., Caplan H.L., et al. Duration of circulatory arrest does influence the psychological development of children after cardiac operation in early life. J Thorac Cardiovasc Surg 1983;86:823-831.[Abstract]
2. Blackwood J.A., Hakin-Ilse K., Stewind D.J. Developmental outcome in children undergoing surgery with profound hypothermia. Anesthesiology 1986;65:437-440.[Medline]
3. Newburger J.W., Jonas R.A., Wernovsky G.H., et al. A comparison of the perioperative neurologic effects of hypothermic circulatory arrest versus low-flow cardiopulmonary bypass in infant heart surgery. N Engl J Med 1993;329:1057-1064.[Medline]
4. Bellinger D.C., Jonas R.A., Rappaport L.A., et al. Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. N Engl J Med 1995;332:549-557.[Medline]
5. DuPlessis AJ, Jonas RA, Wypij D, et al. Perioperative effects of alpha-stat versus pH-stat strategies for deep hypothermic cardiopulmonary arrest in infants. J Thorac Cardiovasc Surg (in press).

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hickey, P. R. Search for Related Content PubMed PubMed Citation Articles by Hickey, P. R.