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J Thorac Cardiovasc Surg 1995;110:934-943
© 1995 Mosby, Inc.

SURGERY FOR CONGENITAL HEART DISEASE

CEREBRAL BLOOD FLOW VELOCITY IN PEDIATRIC PATIENTS IS REDUCED AFTER CARDIOPULMONARY BYPASS WITH PROFOUND HYPOTHERMIA

New York, N.Y.

Received for publication Dec. 16, 1994. Accepted for publication March 10, 1995. Address for reprints: Amy E. Jonassen, MD, The Department of Anesthesiology, Columbia University College of Physicians and Surgeons, 622 West 168th St., New York, NY 10032.

Abstract

Transcranial Doppler sonography of the middle cerebral artery was used to determine whether cerebral perfusion was detectable in low flow states during operations with cardiopulmonary bypass in pediatric patients. Quantitative and qualitative differences in cerebral blood flow velocity after rewarming in patients treated with continuous low-flow bypass or deep hypothermic circulatory arrest were assessed. To determine whether the alterations in cerebrovascular resistance pattern observed in our patients undergoing profound hypothermia was more a function of perfusion technique than of minimum temperature during operation, a third group of patients treated with moderate hypothermia was studied. The three patient groups were the arrest group (N = 16), comprised of patients undergoing circulatory arrest at 18° to 20°C; the low-flow group (N = 16), patients treated with continuous low-flow (cardiac index 0.5 L/min per square meter) bypass at 18° to 20°C; and the moderate group (N = 5), patients treated with moderate hypothermia at 24° to 28°C. Flow velocity was detectable in all patients in the low-flow group, with mean arterial pressures as low as 15 mm Hg. Mean flow velocity was reduced after bypass as compared with prebypass values in both the arrest and low-flow groups (p = 0.0001). Mean flow velocity increased after bypass in the moderate group (p = 0.0001). A Doppler waveform pattern consistent with high cerebrovascular resistance was found in 67% of patients in the arrest group and 44% of those in the low-flow group. None of the patients in the moderate group exhibited such a pattern. Patients treated with profound hypothermia who underwent a period of cold full-flow reperfusion before rewarming did not exhibit this high resistance pattern after rewarming. The present findings indicate that profound hypothermia may evoke changes in the cerebral vasculature that result in decreased mean cerebral blood flow velocity after cardiopulmonary bypass rewarming. A period of cold full-flow reperfusion before rewarming may prevent these alterations and improve cerebral perfusion during rewarming. (J THORACCARDIOVASCSURG1995;110:934-43)

Despite improvements in cardiopulmonary bypass (CPB) technology, neurologic injury remains a physically, emotionally, and economically disastrous complication in up to 10% of pediatric patients undergoing cardiac operations. ^1-3 Preexisting brain anomalies, intraoperative hypoperfusion, embolization or thermal injury, and postoperative low cardiac output states may all contribute to this phenomenon. ^1-3 Two forms of CPB management, deep hypothermic circulatory arrest and continuous hypothermic low-flow CPB (low-flow CPB), are commonly used to provide a bloodless surgical field during correction of complex congenital heart defects. Presently, anatomic considerations such as type of repair and the presence of aberrant venous drainage often dictate which CPB technique is used, although at times the surgeon does have a choice. Attention has been focused on these differing forms of CPB management and their impact on cerebral metabolism and perfusion, as well as on long-term neurologic outcome, in an effort to determine whether one technique is clearly preferable to another when a choice can be made. ^4-11 The ideal method remains a matter of controversy.

Animal ^4-6 and human ⁷ studies have demonstrated the adequacy of low-flow CPB in maintaining cerebral perfusion, whereas deep hypothermic circulatory arrest was shown to result in prolonged decreases in cerebral blood flow and metabolism after recirculation ⁹ and in depletion of intracellular energy stores. ⁵ A large prospective investigation comparing results in patients treated with deep hypothermic circulatory arrest or low-flow CPB associated deep hypothermic circulatory arrest with a higher prevalence of clinical and subclinical seizure activity and higher serum creatine kinase brain isoenzyme fraction (a marker for cerebral injury) in the postoperative period. ¹⁰ In contrast, an earlier study determined serum creatine kinase BB levels to be similarly elevated in patients after both deep hypothermic circulatory arrest and low-flow CPB. ¹¹ A recent study of pediatric patients during low-flow CPB found that under conditions of low perfusion pressure cerebral blood flow velocity (CBFV) was not detectable by transcranial Doppler sonography (TCD). ¹²

The purpose of this investigation was (1) to determine whether blood flow is detectable by TCD in the middle cerebral artery during periods of extremely low pump flow rates and mean arterial pressure and (2) to determine whether there is a difference in CBFV and intracranial resistance patterns on rewarming from profound hypothermia (temperature <20°C) after either low flow CPB or deep hypothermic circulatory arrest.

METHODS

With Institutional Review Board approval, 37 patients (aged 1 day to 9 years) undergoing operation with hypothermic CPB for repair of complex congenital heart defects were entered into the study.

Anesthesia was induced with intravenous fentanyl 35 to 50 µg/kg and muscle relaxation was achieved with either pancuronium 0.15 mg/kg intravenously or vecuronium 0.1 mg/kg intravenously. The anesthetic was supplemented with additional muscle relaxant, fentanyl (total 50 to 100 µg/kg), and midazolam 0.05 to 0.1 mg/kg as needed. At the discretion of the attending anesthesiologist, sodium thiopental 5 to 10 mg/kg was administered at the onset of rewarming for its cerebral metabolic depressant effect. Nasotracheal intubation was followed by controlled mechanical ventilation of the lungs with oxygen in air to maintain arterial carbon dioxide tension within normocapnic ranges. Arterial pressure (MAP) and oxyhemoglobin saturation; end-tidal carbon dioxide concentration; and rectal, esophageal, and tympanic membrane temperatures were monitored continuously.

CBFV was measured with a 2 MHz, range-gated, pulsed-wave pediatric transcranial Doppler sonographic probe affixed over the left temporal window. Blood flow velocity (mean, systolic, and diastolic) was determined with use of the Transpect or CDS device (Medasonics, Fremont, Calif.). The low-pass filter, which removes signals at velocities of 4 cm/sec or less, was disabled in the CDS model, allowing resolution down to 2 cm/sec. The M1 segment of the left middle cerebral artery was insonated at depths of 25 to 38 mm to obtain a maximal signal and no changes in gain or power were made during the study period.

Nonpulsatile CPB was established with use of an ascending aortic cannula and either a single venous cannula or inferior and superior venous cannulas. A standard roller pump was used with a 0.8 m ² Capiox membrane oxygenator (Terumo, Tokyo, Japan) and arterial line filter (Pall Biomedical Products, Glen Cove, N.Y.). The pump prime consisted of electrolyte solution (Normosol R; Abbott Laboratories, Chicago, Ill.), albumin (12.5 gm/400 ml), mannitol (0.5 gm/kg), NaHCO₃ (10 mEq plus 1 mEq/kg), CaCl (100 mg), heparin (300 µg/kg plus 3 µg/ml of prime), and washed packed red cells to maintain a hematocrit value of approximately 25%. Full-flow CPB was considered to be a cardiac index (CI) 2.2 to 2.4 L/min per square meter (approximately 120 to 150 ml/kg per minute). Cooling proceeded at 1° to 2° C per minute and was facilitated in all patients by peripheral vasodilation with sodium nitroprusside, 1 to 3 µg/kg per minute. Alpha-stat acid-base management was used.

Patients were assigned to one of three groups on the basis of the anatomic necessities of the surgical correction. In 16 patients (low-flow group), the operation was done during low-flow CPB with CI of 0.5 to 0.8 L/min per square meter (25 to 50 ml/kg per minute) at a rectal temperature less than 20° C. Circulatory arrest was instituted in another 16 patients at a rectal temperature less than 20° C (arrest group). In a third group of five patients, the operation was conducted under moderately hypothermic conditions at a rectal temperature of 24° to 28° C and CI of 1.0 to 1.2 L/min per square meter (moderate group).

Results of blood gas analysis; hematocrit, MAP, CBFV, and CI values; and esophageal, rectal, and tympanic membrane temperatures were recorded (1) after induction of anesthesia before CPB (PRE), (2) at the onset of rewarming from hypothermia (HYPO), and (3) just after separation from CPB (POST). In addition, CBFV, MAP, rectal and esophageal temperatures, and CI were recorded at all changes in pump flow. Thiopental administration and the presence of a postoperative central shunt, that is, one created to provide pulmonary blood flow from the systemic circulation (see Fig. 1), were also noted. The flow pattern during rewarming was determined (normal was a diastolic flow velocity within 50% of baseline values and high resistance was a diastolic flow velocity <50% of baseline values) (Figs. 2 and 3). To distinguish between patients with anatomic reasons for low diastolic flow velocity and those without such structural causes of diastolic runoff, patients with postoperative central shunts such as those created in the Norwood I procedure were excluded from the analysis of flow pattern on rewarming.

View larger version (107K): [in this window] [in a new window]   Fig. 1. Diastolic flow reversal after CPB in presence of central shunt. Note flow away from TCD probe (below zero line) during diastole.

View larger version (122K): [in this window] [in a new window]   Fig. 2. Normal diastolic flow velocity pattern after CPB with circulatory arrest.

View larger version (120K): [in this window] [in a new window]   Fig. 3. Absence of diastolic forward flow velocity after CPB with profound hypothermia.

RESULTS

Demographic data for the three patient groups are presented in Table I. Both profoundly hypothermic groups (low-flow and arrest) consisted mostly of infants younger than 6 months old, with one or two older infants (maximum age 8 months) in each group (see Table I). There was no significant difference in the prevalence of preoperative cyanosis between the two profoundly hypothermic groups. By nature of the difference in surgical correction and thus CPB management, the moderate hypothermic group included more older children. Those patients did not have cyanosis before operation, as a function of a difference in cardiac lesions and previous palliative operations. There was no significant difference in age, weight, or CPB and crossclamp times between the two profoundly hypothermic groups. Although crossclamp time was shorter in the moderate group (p = 0.21), total CPB time was the same as that in the other two groups (p = 0.65). The mean period of reduced CI in the low-flow group was significantly longer (53 minutes) than that of circulatory arrest (35 minutes) in the arrest group (p < 0.001).

View larger version (69K): [in this window] [in a new window]   Fig. 4. Loss and recovery of middle cerebral artery flow during low-flow CPB at 18° C. Point A, CI 1.8 L/min per square meter, MAP 18 mm Hg; note roller head artifact. Point B, CI 0.5 L/min per square meter, MAP 20 mm Hg; loss of detectable flow. Point C, CI 0.5 L/min per square meter, MAP 20 mm Hg; return of middle cerebral artery flow. Slashes denote time lag of 13 seconds.

View larger version (16K): [in this window] [in a new window]   Fig. 5. Mean middle cerebral artery flow velocity for three study groups (low-flow, arrest, and moderate hypothermia) over three study measurement points (PRE, HYPO, and POST). mCBFV, Mean CBFV; #p < 0.05 difference between moderate versus arrest and low-flow; *p = 0.0001 difference from PRE baseline value.

All patients survived the operation. One patient in the arrest group who underwent the Norwood I procedure for hypoplastic left heart syndrome and had a complicated preoperative and postoperative course exhibited choreiform movements at age 3 months. Intraoperatively, the patient underwent 58 minutes of circulatory arrest at 19° C and had low-flow velocity (mean velocity 8 cm/sec) with diastolic reversal on rewarming (central shunt present). There were no discernible abnormalities on computed tomographic scan at age 3 months, and the movements abated by age 9 months. None of the patients in the low-flow or moderate groups had any gross neurologic abnormalities (clinical seizure, posturing, or focal deficit) in the postoperative period.

DISCUSSION

In this study we have shown that cerebral blood flow is detectable during low-flow CPB at MAP and CI values lower than those previously reported. We have found that despite hemodilution during CPB, cerebral perfusion is decreased after CPB with profound hypothermia. A significant proportion of patients treated with profound hypothermia and either low-flow CPB or circulatory arrest exhibited a TCD pattern consistent with increased cerebral vascular resistance in the early postoperative period, whereas this pattern was not present in patients treated with moderately hypothermic CPB. There was a tendency for this pattern to occur with greater frequency in patients who had a period of circulatory arrest.

TCD sonography is well suited to intraoperative evaluation of the cerebral circulation. TCD allows real-time, noninvasive measurement of relative alterations in CBFV. Changes in CBFV correlate well with changes in cerebral blood flow as measured by tracer washout techniques. ^13,14

With the use of TCD sonography we have demonstrated detectable cerebral blood flow at pump flow rates and MAP values lower than those previously reported in pediatric patients undergoing low-flow CPB. The minimum mean flow velocity we detected was 3 cm/sec. These data are in agreement with those of van der Linden and associates, ⁷ who measured mean flow velocities at 33% of baseline values during low-flow CPB, albeit at somewhat higher flow rates and MAP values (CI 0.8, MAP 27 mm Hg).

Our data differ from those of Taylor, Burrows, and Bissonette, ¹² who reported absence of detectable flow in a significant proportion of patients undergoing low-flow CPB and observed minimum mean flow velocities of 6 cm/sec. Possible explanations for this difference may include our use of vasodilation with sodium nitroprusside during CPB, the increased sensitivity of our TCD apparatus by removal of the low-pass filter, and our avoidance of jugular central venous lines that theoretically may impede regional cerebral venous drainage in small infants, thus decreasing cerebral perfusion pressure and potential differences in perfusion technique. As an example of the latter, we have found CBFV to be reduced by such maneuvers as opening of the bypass pump manifold, which decreases the effective CI delivered to the patient without changing the pump speed and perceived CI. Thus we conclude that in the clinical setting low-flow CPB does provide continuous cerebral perfusion.

Immediately after CPB, mean CBFV was significantly reduced as compared with pre-CPB values in patients in both the low-flow and arrest groups. The observed reduction in arterial carbon dioxide tension from the pre-CPB to the post-CPB period would be expected to produce a roughly 12% decrease in mean CBFV. ¹⁵ On the other hand, the decrease in the hematocrit value by more than 10% with hemodilution on CPB would be expected to produce an almost 20% increase in mean CBFV. ¹⁶ The net effect of these opposing influences on cerebral perfusion should have resulted in a similar, if not slightly increased, CBFV. In contrast to our findings, Greeley and associates, ⁸ with use of the xenon clearance technique of measuring cerebral blood flow, noted return of cerebral perfusion to baseline values after CPB in patients undergoing full-flow or low-flow hypothermic CPB; however, cerebral blood flow was reduced at the conclusion of bypass in patients who had a period of circulatory arrest. With the use of TCD evaluation of cerebral perfusion, van der Linden and associates ⁷ reported return to baseline values of CBFV at the end of operation in pediatric patients treated with low-flow CPB. Patients in both of those studies underwent hemodilution by 5% to 10% during CPB, which should have resulted in a 10% to 20% increase in cerebral perfusion. Thus, given the degree of hemodilution, a mere return to pre-CPB values of cerebral blood flow demonstrates, in fact, a relative decrease in cerebral perfusion. Comparable with patients in our moderate group, patients who underwent CPB at 28°C in the study by Greeley and associates ⁸ had higher CBF values in the post-CPB period compared with baseline values. Therefore we conclude that patients treated with moderately hypothermic CPB exhibit an appropriate increase in cerebral perfusion in response to hemodilution, whereas those treated with profound hypothermia do not.

Two possible criticisms of our comparison of patients treated with profound or moderate hypothermia rest in the unavoidable difference in age and cardiac lesions between the two populations. Baseline CBFV was higher in the moderate group than in either the low-flow or arrest groups. This is to be expected as a function of age. ¹⁷ We have evaluated the change from baseline over the period of CPB in all three groups, and it is this relative change over time that illustrates the difference in response between the patients treated with profound or moderate hypothermia. TCD studies of neonates have demonstrated an appropriate increase in CBFV with partial exchange transfusion as treatment for polycythemia. ¹⁸ Thus the difference in age between the profoundly hypothermic and the moderately hypothermic populations would not be expected to affect the cerebral response to hemodilution.

Because the two temperature groups did consist of patients with varying underlying cardiac lesions, one must consider this as a possible explanation for the different CBFV responses to CPB. Although structural brain abnormalities are associated with the hypoplastic left heart syndrome, there has been no evidence to suggest that cerebral vascular function is altered in these patients. Similarly, the fact that all of the patients undergoing moderate hypothermia were acyanotic before operation does not explain the difference in CBFV response to hemodilutional CPB, because 50% of the patients undergoing profound hypothermia were also acyanotic before operation.

Our data indicate that there is a persistent relative decrease in cerebral perfusion after rewarming in patients who have undergone CPB with profound hypothermia, irrespective of the perfusion technique (low-flow or arrest) used during the repair. This may, in fact, reflect a temperature-related metabolic or vascular phenomenon, with alteration of either demand for substrate or delivery to the microcirculation. Inhomogeneous rewarming ¹⁹ with residual hypothermic metabolic suppression or decreased cerebral perfusion pressure caused by cerebral edema after profound hypothermia ^20,21 may account for these findings.

TCD waveform configuration and diastolic velocity pattern can be used to dynamically assess cerebrovascular resistance and intracranial pressure. With the use of TCD sonography in patients with head injury, Hassler, Steinmetz, and Gawlowski ²² reported a high resistance flow pattern associated with intracranial hypertension. Under these circumstances, TCD diastolic forward flow becomes attenuated, if not reversed. This pattern was shown to be reversible with treatment for elevated intracranial pressure. Flow reversal caused by diastolic runoff is also encountered in the presence of a central circulatory shunt such as a patent ductus arteriosus or a surgically created shunt to provide pulmonary perfusion from the systemic circulation. ^23,24

Early in the course of our study, results in several patients exhibited a striking resemblance in flow pattern during rewarming from profound hypothermia to that described by Hassler, Steinmetz, and Gawlowski. ²² Subsequently, a TCD waveform pattern consistent with increased cerebrovascular resistance was present during rewarming in 54% of patients undergoing profound hypothermia. Although our population was not large enough to discern a statistical difference in the prevalence of this elevated resistance pattern between the two CPB techniques, there was a trend toward circulatory arrest being associated with this pattern more often (67% versus 44%).

Astudillo, van der Linden, and Ekroth ²⁵ have reported a similar pattern of low diastolic flow velocity during rewarming in infants undergoing cardiac operation under profound hypothermia. The prevalence of this pattern was similar in their population to that in our group of patients (11/22 patients), yet they found it to be present far more often (10/12) in patients after a period of circulatory arrest. Patients in their study who underwent a period of cold reperfusion before rewarming did not exhibit a decrease in diastolic flow velocity on rewarming, whereas those who were immediately rewarmed on reperfusion did show decreased diastolic flow velocity. They therefore proposed that the method of recirculation may have an impact on the development of this high resistance pattern.

This may, in fact, explain the difference between the findings in their patients and the prevalence of this pattern in our two profoundly hypothermic patient populations. Patients in our arrest group often had a period of cold reperfusion after circulatory arrest before rewarming, whereas those in the low-flow group were more commonly rewarmed at the time of increased perfusion. Indeed, all of the patients in the low-flow group in whom high resistance was exhibited did undergo immediate rewarming with the increase in pump flow after the low-flow period. All four of the patients in the arrest group who had normal diastolic flow velocity during rewarming had had at least 5 minutes of cold reperfusion before rewarming, whereas the remaining eight patients in the arrest group with high resistance underwent rewarming directly on reperfusion. Thus a period of cold reperfusion after low-flow bypass or circulatory arrest may prevent increases in cerebral vascular resistance during the rewarming phase.

In our study, low arterial carbon dioxide tension may have contributed to increased cerebrovascular resistance in two of the eight patients; however, the other six patients did not have hypocapnia. These data are consistent with the findings of Hillier, Burrows, and Bissonette ²⁶ of an elevated modified index of cerebrovascular resistance and decreased CBFV in pediatric patients after circulatory arrest. Anterior fontanelle measurements of intracranial pressure in infants after circulatory arrest have shown elevations in intracranial pressure on recirculation, with normalization after roughly 20 minutes. ^21,27 In our patients, the high resistance pattern became evident during rewarming and persisted until the conclusion of operation. Three patients with this pattern were reexamined in the intensive care unit the day after operation, and the CBFV pattern had normalized. Astudillo, van der Linden, and Ekroth ²⁵ noted resolution of the high resistance pattern 1 to 5 hours after operation.

These data suggest a transient alteration in cerebral perfusion on rewarming from profound hypothermia. Because none of the patients undergoing moderate hypothermia exhibited a high resistance pattern during rewarming or after CPB, this phenomenon may represent a cerebrovascular response to profound hypothermia. What remains unclear is whether this is a primary vasoconstrictive response to altered metabolic demands or an extrinsic compression of the microvasculature as a result of cerebral edema after profoundly hypothermic CPB. ²¹ We have encountered a similar high resistance pattern (Jonassen A, Young WL, unpublished data) during rewarming in adult patients with no cardiac pathologic conditions undergoing circulatory arrest for giant aneurysm clipping. The open cranium and dura at that time make it difficult to invoke increased intracranial pressure as the cause for this phenomenon.

In summary, we have documented with the use of TCD that cerebral blood flow is detectable in extremely low perfusion states during low-flow CPB. CBFV is reduced after rewarming from profound hypothermia, regardless of CPB technique. Reduced CBFV is not found in patients undergoing CPB with moderate hypothermia. A transient high resistance pattern of TCD waveform, indicative of increased cerebrovascular resistance, is seen in half of the patients on rewarming from profound hypothermia, but was not encountered in patients treated with moderate hypothermia. This high resistance pattern may reflect a cerebrovascular response to warm reperfusion and thus might be altered by changes in rewarming strategy. The relationship of the observed alterations in intracranial hemodynamics to patient outcome needs to be defined in future studies.

Footnotes

From the Departments of Anesthesiology, ^a Surgery, ^b Neurological Surgery, ^c and Radiology, ^d Columbia University College of Physicians and Surgeons, New York, N.Y.

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