Comparing Two Strategies of Cardiopulmonary Bypass Cooling on Jugular Venous Oxygen Saturation in Neonates and Infants

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Comparing Two Strategies of Cardiopulmonary Bypass Cooling on Jugular Venous Oxygen Saturation in Neonates and Infants Frank H. Kern, MD, Ross M. Ungerleider, MD, Scott R. Schulman, MD, Jon N.

1 Comparing Two Strategies of Cardiopulmonary Bypass Cooling on Jugular Venous Oxygen Saturation in Neonates and Infants Frank H. Kern, MD, Ross M. Ungerleider, MD, Scott R. Schulman, MD, Jon N. Meliones, MD, Randall M. Schell, MD, Beatrice Baldwin, CRNA, Paul R. Hickey, MD, Mark F. Newman, MD, Richard A. Jonas, MD, and William J. Greeley, MD Departments of Anesthesiology, Surgery, and Pediatrics, Duke University Medical Center, Durham, North Carolina; and Children's Hospital and Harvard Medical School Boston, Massachusetts Background. Cerebral protection during deep hypothermic circulatory arrest is predicated on efficient and complete cerebral cooling. Institutions approach cooling quite differently. We compared two different cooling strategies in terms of measured jugular venous bulb saturations in 39 infants undergoing deep hypothermic cardiopulmonary bypass to evaluate the effect of institutional cooling practices on jugular venous bulb saturation, an indirect measure of cerebral cooling efficiency. Methods. The patients were grouped based on the method of core cooling. In group A (n = 17), core cooling was achieved rapidly by setting the water bath temperature of the heat exchanger at 4 to 5 C, and the patient was cooled until rectal temperature and nasopharyngeal temperature were 15 C or lower. In group B (n = 22), the heat exchanger was initially set at 18 C and slowly lowered to 12 C. Hypothermic temperatures of 12 C were maintained until the nasopharyngeal temperature was 18 C or less and the rectal temperature was 20 C or lower. Once cooling was complete, blood samples were ana- lyzed by cooximetry for determination of arterial oxygen saturation and jugular venous bulb saturation. Results. In group A, the measured jugular venous bulb saturation was 98.0% % and the oxygen saturation to jugular venous bulb saturation difference was 0.3% + 0.5%, measured at the time that institutional cooling objectives were achieved (total cooling time, minutes). In group B, jugular venous bulb saturation was 86.2% ± 12% and the oxygen saturation to jugular venous bulb saturation difference was 10.8% %, measured at the time that institutional cooling objectives were achieved (total cooling time, minutes) (p < 0.01). Conclusions. Differences in cardiopulmonary bypass cooling techniques may alter the rate at which jugular bulb saturations rise. We believe this represents an indirect measure of the efficiency of brain cooling and therefore of cerebral protection. (Ann Thorac Surg 1995;60: ) he use of cardiopulmonary bypass (CPB) with deep T hypothermic circulatory arrest (DHCA) has proven to be a valuable tool for the repair of complex congenital heart lesions in newborns and infants. Intricate cardiac repairs in a bloodless, cannula-free field have improved operative precision, enhanced survival, and reduced cardiac morbidity in the smallest of infants [1]. However, as overall surgical outcome has improved, neuropsychologic dysfunction is being recognized as a prominent and visible complication of neonatal heart operations ]2-4]. Recent studies support the notion that increased length of DHCA increases the incidence of postoperative central nervous system dysfunction [2, 4]. Newburger and colleagues [4] demonstrated a correlation between postoperative seizures with early developmental abnormalities and a more prolonged period of DHCA [4]. They con- Accepted for publication May 25, Address reprint requests to Dr Kern, Duke University Medical Center, Box 3046, Durham, NC cluded that DHCA should be used judiciously and its duration minimized if possible. In addition to the length of DHCA, inter-institutional variations in the incidence of neuropsychologic dysfunction have been reported [5]. Although reasons for this variability in outcome are not well elucidated, technical differences in the management of cardiopulmonary bypass and DHCA have been suggested [5-7]. One factor identified is the variability in the approach used to cool the brain of neonates and infants before initiating DHCA. Different approaches to cerebral cooling may alter the efficiency of brain cooling and may contribute to neuropsychologic dysfunction after circulatory arrest [2, 3, 8]. Differences in cooling include: (1) the duration of the cooling period, (2) the perfusion flow rate used during cooling, (3) the hypothermic temperature targeted (12 to 20 C), and (4) the temperature of the water bath used to cool the blood (4 to 18 C). We evaluated two distinct cooling strategies used at two institutions with congenital cardiac surgical pro by The Society of Thoracic Surgeons /95/$9.50 SSDI (95)

Ann Thorac Surg KERN ET AL 1199 1995;60:1198-202 BRAIN COOLING DURING CPB IN INFANTS grams: Duke University Medical Center and Children's Hospital, Boston.

2 Ann Thorac Surg KERN ET AL ;60: BRAIN COOLING DURING CPB IN INFANTS grams: Duke University Medical Center and Children's Hospital, Boston. The two institutional cooling strategies were evaluated by comparing their ability to cool the brain efficiently as judged by jugular bulb oxygen saturation and arterial venous oxygen differences across the brain. We hypothesized that different cooling strategies would have a distinct effect on cerebral cooling efficiency. Material and Methods Patients After receiving Institutional Review Board approval and informed parental consent, we studied 39 infants undergoing deep hypothermic CPB with or without circulatory arrest (17 patients at Children's Hospital, Boston [group A] and 22 patients at Duke University Medical Center [group B]). The patients were all less than 1 year of age, ranging from 3 days to 7 months with a mean age of 1.2 months. Patients with preexisting neurologic dysfunction were excluded from the study. Anesthesia Management No premedication was administered to the study patients. Anesthetic agents were uniform in all patients and consisted of fentanyl 100 to 150 ~g/kg, midazolam 0.0 to 0.2 mg/kg, incremental doses of pancuronium for neuromuscular blockade, and controlled mechanical ventilation. No additional inhalation anesthetic drugs or cerebral vasoactive agents were administered. Cardiopulmonary Bypass Management The patients were cooled based on institutional preferences. In both groups, a combination of passive surface cooling and core cooling was used. In group A patients, surface cooling began in the prebypass period and consisted of a room temperature lowered to 15 C, a cooling blanket set at 4 C, and ice bags placed on each side of the patient's head. Core cooling began with the initiation of CPB. Group A patients were cooled rapidly by setting the water temperature of the heat exchanger at 4 to 5 C. Patients were cooled actively until all monitored temperatures were 15 C or lower. In group B, surface cooling began in the prebypass period and consisted of a room temperature set at 15 C and a cooling blanket set at 32 C. With commencement of CPB, the cooling blanket temperature was lowered to 4 C. The head was not packed in ice during the prebypass period, but ice was applied after the initiation of core cooling. Core cooling began with initiation of CPB. Group B patients were cooled gradually by initially setting the water temperature of the heat exchanger at 18 C and slowly lowering it to 12 C. Hypothermic temperatures of 12 C were maintained until the nasopharyngeal temperature (TNp) was 18 C or less and the rectal temperature (TR) was 20 C or less. In both groups, arterial blood gas management, extracorporeal systems, and priming solutions were similar. Arterial blood gas management was directed at maintaining a ph of 7.35 to 7.40 and an arterial carbon dioxide tension of 35 to 40 mm Hg, uncorrected for body temper- ature using the principles of alpha stat blood gas management. Oxygen (inspired oxygen fraction = 1.0) was administered through the fresh gas inlet of the oxygenator. Arterial oxygen tension was monitored throughout CPB and maintained between 400 and 700 mm Hg. The extracorporeal circulation was maintained using nonpulsatile pump flow and a membrane oxygenator in both groups. The pump oxygenator system in group A was primed with normosol-r (250 to 650 ml), heparin (150,000 to 170,000 U), whole blood (200 to 500 ml to achieve a hematocrit of 20% -+ 2% during CPB), mannitol (0.5 to 1 g/kg), sodium bicarbonate (to achieve a ph of 7.35 to 7.45 ph units), and methyl prednisolone (30 mg/kg). In group B patients, the pump oxygenator was primed with lactated Ringer's solution, 700 to 800 ml; heparin, 1,000 U; albumin, 50 to 100 ml; mannitol, 0.5 to 1 g/kg; THAM, 50 to 100 meq; sodium bicarbonate to achieve a ph of 7.35 to 7.45 ph units; and packed red blood cells calculated to achieve a hematocrit of 20% + 2% during CPB. Study Protocol Two temperature probes (TNp and TR) were placed in all 39 infants and monitored continuously throughout the study period. Jugular venous saturation monitoring was accomplished with a 3F catheter placed into the jugular venous bulb. The catheter was either placed percutaneously through the internal jugular vein and advanced to the jugular venous bulb before surgical incision or placed surgically through the superior vena cava after the chest and pericardium were opened. Arterial blood samples were obtained from an indwelling radial or umbilical artery line. Nasopharyngeal and rectal temperatures, arterial carbon dioxide tension, and mean arterial pressure were recorded throughout the operative procedure. Once CPB was established, we also recorded pump flow rate and cooling time. Jugular venous and arterial blood samples were obtained simultaneously and evaluated by cooximetry after appropriate institutional temperature measurements suitable for initiating circulatory arrest were reached. In group A, sampling was at a TNp and T R less than or equal to 15 C. In group B, sampling occurred when the TNp was 18 C or lower and the T R was 20 C or lower. Patients undergoing circulatory arrest were cooled for a minimum of 20 minutes before pump flow was discontinued. Data Analysis Temperature, oxygen saturation, and demographic data were compared for differences between groups A and B using unpaired Student's t test. Statistical significance was declared at p -< Results The patient demographic characteristics are listed in Table 1. Jugular venous saturations were not obtainable in 2 of the patients in group B, and these patients were not included in the analysis. Table 2 compares the results between the cooling technique used for group A patients

1200 KERN ET AL Ann Thorac Surg BRAIN COOLING DURING CPB IN INFANTS 1995;60:1198-202 Table 1.

3 1200 KERN ET AL Ann Thorac Surg BRAIN COOLING DURING CPB IN INFANTS 1995;60: Table 1. Demographic Data Jugular Age Weight Venous Diagnosis Operation (d) (kg) Saturation Group A HLHS ASD/VSD IAA TGA/VSD TGA/VSD HLHS Truncus TGA/WS Group B PS/VSD IAA DORV VSD TGA/WS VSD VSD/coarctation Cor triatriatum Truncus VSD/coarctation A-P window Arterial switch Arterial switch Arterial switch repair Stage I palliation ASD/VSD closure End to end repair Arterial switch Arterial switch Arterial switch repair Arterial switch Arterial switch Stage I palliation Truncus repair repair Arterial switch Primary repair Arterial switch Arterial switch Rastelli repair End to end repair Repair Repair Repair Patch closure Arterial switch Patch closure Repair Patch closure/ repair Repair Truncus repair Primary repair Patch closure/ repair repair Primary repair Arterial switch Primary repair A-P - aortopulmonary; ASD - atrial septal defect; = common atrioventricular canal; DORV = double-outlet right ventricle; HLHS = hypoplastic left heart syndrome; IAA interruption of aortic arch; IVS = interventricular septum; PS = pulmonary stenosis; = total anomalous pulmonary venous return; TGA = transposition of great arteries; = tetralogy of Fallot; VSD = ventricular septal defect. and the cooling technique used for group B patients. In group A, the mean cooling time required to reach TNp and T R of 15 C or lower was 15.0 ± 0.45 minutes (mean value ± SD). The mean jugular venous saturation was 98.0%, and the arterial venous saturation difference across the brain was 0.3% ± 0.5%. In group B, the cooling time required to reach TNp temperatures of 18 C or less and T R of 20 C or less was minutes. Group B demonstrated a lower mean jugular venous saturation of 86.2% ± 12% and an arterial venous saturation difference of 10.8% %. The arterial carbon dioxide tension, pump flow rate, and mean arterial pressure were not statistically different between the groups (Table 2). Comment The use of DHCA is associated with neuropsychologic dysfunction in newborns and infants requiring surgical procedures for congenital cardiac defects [5]. Although deep hypothermia is used to protect the brain from the arrest period, evidence suggests that this protection may be incomplete and results in a measurable incidence of postoperative neuropsychologic dysfunction [3, 7-10]. The technical approach used to cool the brain is not standardized and differs widely among institutions [11, 12]. Therefore, differences in the reported incidence of neuropsychologic outcome may, in part, be due to differences in cooling. We chose to investigate two different cooling practices designed to maximize cerebral cooling before the initiation of DHCA. We observed that different cooling techniques produced different cerebral cooling efficiency. Specifically, we demonstrated a significant difference in measured jugular venous saturations between two cooling strategies. One strategy (group A) achieved lower core temperatures before DHCA institution, did not maintain a narrow cooling gradient between the water bath temperature of the heat exchanger and the arterial blood, and used a more aggressive approach to surface cooling. The other strategy (group B) accepted slightly higher TNI P and T R before DHCA was started, maintained a narrow cooling gradient between the water bath temperature of the heat exchanger and the arterial blood, and did not begin aggressive surface cooling until after CPB was initiated. Although the total cooling time before sampling jugular venous blood was on average 2.5 Table 2. Comparison of Group A and Group B at Complete Cooling ~ Characteristic Group A Group B JVsA T (%) % /0 b SaO2-JVsA T Diff (%) c TNp ( C) 14.3 _ ~ c TRT ( C) c Age (too) _+ 1.5 PaCO 2 (ram Hg) Pump flow (ml kg i. min 1) MAP (mm Hg) _+ 11 Cooling time (rain) 15.0 _ _+ 1.1 a Data are reported as mean -+ standard deviation, group A. c p < 0.05 versus group A. b p K 0.01 versus JvsA T - jugular venous oxygen saturation; MAP = mean arterial pressure; PaCO 2 = arterial carbon dioxide tension; SaO 2 = arterial oxygen saturation; TNp -- nasopharyngeal temperature; TRT rectal temperature.

Ann Thorac Surg KERN ET AL 1201 1995;60:1198-202 BRAIN COOLING DURING CPB IN INFANTS minutes longer for group B, the group A cooling strategy resulted in more complete cerebral cooling as assessed by

4 Ann Thorac Surg KERN ET AL ;60: BRAIN COOLING DURING CPB IN INFANTS minutes longer for group B, the group A cooling strategy resulted in more complete cerebral cooling as assessed by a higher jugular venous saturation. Inefficient cerebral cooling has been reported to increase the likelihood of neuropsychologic dysfunction after circulatory arrest [2, 3, 8-10]. In most institutions, direct cerebral cooling is inferred from TNp and T R. When these temperatures are reduced to 15 to 20 C, conventional management strategies assume that temperature gradients throughout the body are minimal and that brain cooling is uniform and effective [13]. Based on jugular venous saturation monitoring, our study suggests that conventional estimates of brain temperature using TNp and T R may not accurately reflect brain temperature. This has been suggested in previous experimental and clinical studies [2, 7, 9, 14-16]. We speculate that metabolic monitoring or a simplified correlate such as jugular venous saturation monitoring may be important in judging the effectiveness of cerebral cooling in individual patients before institution of DHCA. Because variability in institutional cooling strategies and patient cooling efficiency exist, more precise clinical monitoring of cerebral hypothermia seems warranted. Although neuropsychologic outcome data were not evaluated in this study, previous evidence suggests that inadequate cerebral cooling is a contributing factor to neuropsychologic dysfunction [2, 3, 7, 8]. Although we cannot demonstrate an improvement in neuropsychologic outcome from this study, it seems prudent to believe that the first step in attempting to reduce the incidence of neuropsychologic dysfunction after DHCA may be to ensure thorough cerebral cooling before instituting DHCA or, if cooling remains incomplete, to substitute low flow CPB if possible. Based on these data, our approach to cooling has been modified to include earlier institution of surface cooling, more aggressive cooling during CPB, monitoring of jugular venous saturations, and extension of the cooling period before initiating circulatory arrest to 25 minutes when jugular venous saturations remain low. Alternative approaches include a more aggressive cooling technique, as described in this report. Allowing wider temperature gradients during the cooling and rewarming phase of CPB has been questioned. The main concern with larger temperature gradients is gaseous microbubbles coming out of solution when blood is warmed too rapidly. This is potentially problematic during rewarming, when air is more likely to be present in the heart and therefore may enter the systemic circulation. Hypothermia is protective in that it reduces the size of gaseous microbubbles, allowing them to pass through the arterial and capillary system and resulting in fewer microinfarcts and eventual clearance by the lungs. Limitations of our study include several inferences from jugular bulb monitoring. We recognize that the blood obtained from the jugular bulb is the effluent from many regions of the brain. Consequently, the oxygen content and saturation of jugular venous bulb blood is a global average and may not reflect areas of regional cerebral hypoperfusion. Therefore, a normal or elevated jugular venous saturation does not necessarily ensure complete cerebral cooling, but a low saturation suggests elevations in cerebral metabolism and incomplete cerebral cooling. A second limitation of this study includes cannula placement. Alterations in arterial and venous cannula placement may affect the distribution of blood flow to the brain and therefore cerebral cooling efficiency. The influence of cannula location was not addressed in this study. The most effective method for ensuring thorough cerebral cooling remains to be determined. Our study suggests that earlier institution of surface cooling measures (ice packs on the head), lower cooling blanket temperatures, and a lower water bath temperature of the heat exchanger during cooling may improve cerebral cooling when total cooling time is restricted to approximately 20 minutes. Other factors, such as the duration of cooling before instituting DHCA, use of higher perfusion flow rates during cooling, or the addition of carbon dioxide or other cerebrovasodilating agent during active cooling, were not addressed by this study, but may potentiate cerebral cooling efficiency and possibly reduce the incidence of neuropsychologic dysfunction after DHCA. References 1. Castaneda AR, Mayer JE Jr, Jonas RA, Lock JE, Wessel DL, Hickey PR. The neonate with critical congenital heart disease: repair--a surgical challenge. J Thorac Cardiovasc Surg 1989;98: Bellinger PC, Wernovsky G, Rappaport LA, et al. Rapid cooling of infants on cardiopulrnonary bypass adversely affects later cognitive function. Circulation 1988;78(Suppl 2): Greeley WJ, Kern FH, Ungerleider RM, et al. The effect of hypothermic cardiopulmonary bypass and total circulatory arrest on cerebral metabolism in neonates, infants and children. J Thorac Cardiovasc Surg 1991;101: Newburger JW, Jonas RA, Wernovsky G, 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: Ferry PC. Neurologic sequelae of open-heart surgery in children. Am J Dis Child 1990;144: Glauser TA, Rorke LB, Weinberg PM, et al. Acquired neuropathologic lesions associated with the hypoplastic left heart syndrome. Pediatrics 1990;85: Kern FH, Jonas RA, Mayer JE, et al. Temperature monitoring during infant CPB: does it predict efficient brain cooling? Ann Thorac Surg 1992;54: Jonas RA, Bellinger DC, Rappaport LA, et al. Relationship of ph strategy and developmental outcome after hypothermic circulatory arrest. J Thorac Cardiovasc Surg 1993;106: Hindman BJ, Dexter F, Cutkomp J, et al. Brain blood flow and metabolism do not decrease at stable brain temperature during cardiopulmonary bypass in rabbits. Anesthesiology 1992;77: Hindman BJ. Cerebral physiology of hypothermia during bypass. Cardiol Young 1993;3: Elliott M, Rao PV, Hampton M. Current paediatric perfusion practice in the UK. Perfusion 1993;8: Hill AG, Groom RC, Aki BF, et al. Current paediatric perfusion practice in North America. Perfusion 1993;8: Blackwood MJ, Haka-Ikse K, Steward DJ. Developmental

5 1202 KERN ET AL Ann Thorac Surg BRAIN COOLING DURING CPB IN INFANTS 1995;60: outcome in children undergoing surgery with profound hypothermia. Anesthesiology 1986;65: Busto R, Dietrich WD, Globus MY, et al. Small differences in the intra-ischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab 1987;7: Busto R, Mordecai Y-T, Dietrich D, et al. Effects of mild hypothermia on brain ischemia. Stroke 1989;20: Okada Y, Tanimoto M, Yoneda K. The protective effect of hypothermia on reversibility in the neuronal function of the hippocampal slice during long lasting anoxia. Neurosci Lett 1988;84: INVITED COMMENTARY In the past, it was believed that the management of cardiopulmonary bypass in infants and small children should be based on the preferences (prejudices?) and practice of the institution. The feeling was that the "package" that worked well in the institution's practice should not be changed. This view should now be challenged. With the improving survival after heart operations in infants, the need to look at quality of life and in particular neurologic quality has become increasingly important. Several centers are now studying this, and slowly a picture is emerging of what is "best practice." This study is a valuable contribution to this end. In this study, ph management during cooling followed alpha stat principles. Recent evidence suggests that ph stat management is superior, perhaps through enhanced brain cooling. A repeat of this study using ph star acid-base management may define "best practice" more clearly. Michael Scallan, FRCA Christopher Lincoln, FRCS Department of Cardiac Surgery Royal Brompton National Heart and Lung Hospital Sydney St London SW3 6NP, England

Acid-base management during hypothermic CPB alpha-stat and ph-stat models of blood gas interpretation

Acid-base management during hypothermic CPB alpha-stat and ph-stat models of blood gas interpretation Michael Kremke Department of Anaesthesiology and Intensive Care Aarhus University Hospital, Denmark