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J Thorac Cardiovasc Surg 1994;107:1228-1236
© 1994 Mosby, Inc.

CARDIOPULMONARY BYPASS, MYOCARDIAL MANAGEMENT, AND SUPPORT TECHNIQUES

Comparative experimental study between retrograde cerebral perfusion and circulatory arrest

Nagoya and Gifu, Japan

Supported in part by a grant-in-aid for scientific research and a Japan Heart Foundation research grant for 1990.

Received for publication Oct. 5, 1992. Accepted for publication Oct. 1, 1993. Address for reprints: Akihiko Usui, MD, 2-903 Umegaoka, Tenpaku-ku, Nagoya, Japan 468.

Abstract

To evaluate the efficacy of retrograde cerebral perfusion in protecting the brain, we comparatively studied retrograde cerebral perfusion and total circulatory arrest in 18 hypothermic (20° C) mongrel dogs (retrograde cerebral perfusion, n = 10; total circulatory arrest, n = 8). Retrograde cerebral perfusion was performed, maintaining an external jugular venous pressure of 25 mm Hg for 60 minutes. Retrograde cerebral perfusion provided half the cerebral blood flow and a third of the oxygen that was supplied during hypothermic cardiopulmonary bypass, which had a flow rate of 100 ml/min per kilogram. Oxygen consumption and carbon dioxide exudation did not increase on resuming cardiopulmonary bypass after retrograde cerebral perfusion, whereas they increased after total circulatory arrest (oxygen consumption 10.7 ± 5.3 versus 19.1 ± 8.6 ml/min, p < 0.05; carbon dioxide exudation, 0.92 ± 0.54 versus 1.64 ± 0.78 mmol/min, p < 0.05). Therefore, oxygen debt during retrograde cerebral perfusion was smaller than during total circulatory arrest. Retrograde cerebral perfusion also cooled the brain better than did total circulatory arrest (20.4° ± 1.5° C versus 22.7° ± 0.7° C, p < 0.01). Cerebral tissue oxygen tension decreased slightly (27.5 ± 7.7 versus 12.3 ± 3.0 mm Hg, p < 0.01), and cerebral tissue carbon dioxide tension increased slowly during retrograde cerebral perfusion (95 ± 34 versus 147 ± 44 mm Hg, p < 0.05). These changes were smaller than those seen in total circulatory arrest. Tissue concentrations of adenosine triphosphate in the brain remained relatively high during retrograde cerebral perfusion but decreased rapidly during total circulatory arrest (0.49 ± 0.16 versus 0.21 ± 0.05 mmol/gm, p < 0.01, just before resuming cardiopulmonary bypass). Retrograde cerebral perfusion cannot maintain aerobic metabolism but may reduce ischemic damage of the brain and may safely extend the cerebral circulation interruption time. (J THORACCARDIOVASCSURG1994;107:1228-36)

Retrograde cerebral perfusion (RCP) via a superior vena caval cannula is a new and simple technique for protecting the brain during interruption of the circulation. RCP can provide blood flow and oxygen to the brain and may reduce ischemic damage. ^1,2 Clinically, there is evidence in the literature and in our own experience that RCP has good cerebral protection. ^3,4 However, the efficacy of RCP has not been evaluated in an experimental model. We performed a comparative study between RCP and circulatory arrest in hypothermic mongrel dogs.

MATERIALS AND METHODS

All animals received humane care in compliance with the "Principles of Laboratory Animal Care," formulated by the National Society for Medical Research, and the "Guide for the Care and Use of Laboratory Animals," prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH Publication No. 86-23, revised 1985).

Preparation of animals and RCP methods
Eighteen mongrel dogs were used in this study. Ten dogs (RCP group) with a mean weight of 13.4 ± 0.7 (range 12 to 15 kg) underwent 60 minutes of RCP under hypothermic conditions (20° C). The other eight dogs (total circulatory arrest [TCA] group) with a mean weight of 13.2 ± 0.7 (range 12 to 14.5 kg) underwent 60 minutes of total circulatory arrest under similar hypothermic conditions (20° C). Anesthesia was induced with ketamine hydrochloride, 10 mg/kg, given intramuscularly, and thiopental sodium, 5 mg/kg, given intravenously. After endotracheal intubation, the animals' lungs were ventilated mechanically with 100% oxygen. The ventilatory rate and tidal volume were adjusted to maintain the arterial carbon dioxide tension at approximately 35 mm Hg. Anesthesia was maintained with intravenous ketamine hydrochloride, 2 mg/kg per hour. Catheters were placed in the right external jugular vein, right femoral vein, and the brachiocephalic artery to measure blood pressures. Cerebral tissue blood flow was measured by the hydrogen clearance method. A hydrogen electrode was inserted into the left parietal lobe cortex through a burr hole in the skull. Tissue oxygen tension (PO₂), carbon dioxide tension (PCO₂), pH, and temperature in the cerebrum were also measured. Electrodes for the measurement of PO₂, PCO₂, pH and temperature were also inserted into the left parietal lobe cortex. A temperature probe was also placed in the nasopharynx. A perfusion cannula (8F) for RCP was placed in both internal maxillary veins. A thoracotomy was performed through the right fourth intercostal space. Heparin, 300 U/kg, was given intravenously. The ascending aorta and the right atrium were cannulated with two separate venous cannulas (28F), and vena caval tapes were applied with clamping of the azygos vein. Cardiopulmonary bypass (CPB) was established at a flow rate of 100 ml/min per kilogram and remained normothermic for 10 minutes for stabilization. After then, the animal was cooled to the cerebral temperature of 20° C, with core cooling maintaining the difference of blood temperature between the inflow and outflow within 5° C while oxygenating with pure oxygen at 0.5 L/min. Mechanical ventilation was then discontinued. After cerebral temperature reached 20° C, hypothermic CPB was continued for 10 minutes and a crossclamp was applied to the ascending aorta. The heart was arrested and intermittent cold crystalloid cardioplegic solution was applied. In the RCP group, RCP was established by perfusing blood through both internal maxillary vein cannula with separate pumps. The aortic cannula was opened and directed by gravity to the cardiotomy reservoir while clamping the caval cannula bilaterally (Fig. 1). External jugular venous pressure was maintained at approximately 25 mm Hg during RCP. In the TCA group, after applying a crossclamp, perfusion was discontinued. The pump circuit consisted of a membranous oxygenator (D705 Midiflo; Dideco, Italy) with a cardiotomy reservoir (3L Cardf plus; Shiley, Inc., Irvine, Calif.) primed with an electrolyte solution and 500 ml of blood obtained from another dog. No intervention was made to control blood pressure during this study.

View larger version (30K): [in this window] [in a new window]   Fig. 1. Perfusion and drainage in RCP through a superior vena cava cannula. Only the aortic cannula (AO) was opened and directed by gravity to the cardiotomy reservoir while bilaterally clamping the caval cannula (SVC,IVC). Returned blood (dark gray) was perfused through an oxygenator into both the internal maxillary venous cannula with a separate pump (bright gray).

Analysis
The blood samples were drawn into heparinized syringes, placed immediately in ice, and analyzed at 37° C for pH, PO₂, PCO₂, oxygen saturation, oxygen content, total carbon dioxide, and hemoglobin with a blood-gas analyzer (ABL-300, Radiometer, Copenhagen, Denmark). Plasma lactate and pyruvate were also measured. Cerebral tissue blood flow was measured with an RBF-2 (Biomedical Science, Inc., Kanazawa, Japan) by the hydrogen clearance method. ^5,6 The biopsy specimen was placed in liquid nitrogen immediately and was stored at –80° C until analysis. Adenosine triphosphate was measured by the ultraviolet absorption spectrum method, and lactate and pyruvate were measured by the enzyme method.

Calculation
Vascular resistance (R) was calculated using the formula: R = 79920 (Pj – Ps)/Q (dynes · sec · cm ^-5), where Pj is the external jugular venous pressure, Ps is the subclavian arterial pressure, and Q is the returned blood flow (in milliliters per minute). Oxygen consumption (CMO₂) was calculated from the equation: CMO₂ = (O₂CTf - O₂CTr) Q/ 100 (ml/min) where O₂CTf is the oxygen content of perfused blood, O₂CTr is the oxygen content of returned blood, and Q is return blood flow. Exudation of carbon dioxide (EXCO₂) was calculated using the formula: ExCO₂ = (tCO₂r – tCO₂f) Q/ 1000 (in millimoles per minute), where tCO₂f is the carbon dioxide content of perfused blood, tCO₂r is the carbon dioxide content of returned blood, and Q is the return blood flow (in milliliters per minute). Lactate exudation (ExL) was calculated from the equation: ExL = (Lf - Lr) Q/100 (in milligrams per minute), where Lf is the plasma lactate concentration of perfused blood, Lr is the lactate in returned blood, and Q is return blood flow. Results were expressed as the mean ± standard deviation and statistical significance was determined with the nonpaired t test.

RESULTS

Cerebral tissue blood flow
Average cerebral tissue blood flow in the left parietal lobe cortex was about 40 ml/min per 100 gm during hypothermic CPB. When perfusion was switched to RCP, it decreased by 50% to about 20 ml/min per 100 gm. However, RCP provided blood flow to the cerebrum, whereas TCA did not (Fig. 2).

View larger version (65K): [in this window] [in a new window]   Fig. 2. Cerebral tissue blood flow in the RCP group or the TCA group. Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. CPB is with 100 ml/min per kilogram of flow rate. Bars indicate a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

View larger version (75K): [in this window] [in a new window]   Fig. 3. Oxygen consumption in the RCP group or the TCA group. CPB is 100 ml/min per kilogram of flow rate. Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA:*p < 0.05;**p < 0.01.

Cerebral tissue temperature and cerebral tissue pH
Cerebral tissue temperature did not increase during RCP, although it increased gradually, showing a significantly higher value, during TCA (20.4° ± 1.4° versus 22.7° ± 0.7° C at 60 minutes after applying RCP or TCA) (Fig. 4). Nasopharyngeal temperature was also significantly different between groups during RCP or TCA. Cerebral tissue pH in the left parietal lobe decreased slightly during RCP, whereas it decreased significantly during TCA. There was a significant difference between groups (6.86 ± 0.34 versus 6.50 ± 0.32, p < 0.05, 60 minutes after RCP or TCA).

View larger version (78K): [in this window] [in a new window]   Fig. 4. Cerebral tissue temperature and nasopharyngeal temperature in the RCP group or the TCA group. Circles show cerebral tissue temperature, and squares show nasopharyngeal temperature. CPB is with 100 ml/min per kilogram of flow rate. Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

View larger version (74K): [in this window] [in a new window]   Fig. 5. Cerebral tissue oxygen tension in the RCP group or the TCA group. CPB means cardiopulmonary bypass with 100 ml/min per kilogram of flow rate. X axis indicates time since applying RCP or TCA and since resuming CPB. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

View larger version (67K): [in this window] [in a new window]   Fig. 6. Cerebral tissue carbon dioxide tension in the RCP group or the TCA group. CPB is with 100 ml/min per kilogram of flow rate. X axis indicates Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

View larger version (77K): [in this window] [in a new window]   Fig. 7. Cerebral tissue concentrations of adenosine triphosphate (ATP) in the RCP group or the TCA group. CPB is with 100 ml/min per kilogram of flow rate. Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

View larger version (75K): [in this window] [in a new window]   Fig. 8. Cerebral tissue lactate/pyruvate ratio in the RCP group or the TCA group. CPB is with 100 ml/min per kilogram of flow rate. Time since applying RCP or TCA and since resuming CPB is indicated on the x axis. Bar indicates a standard deviation. Shaded area shows RCP or TCA time period. Asterisks show significant difference between RCP and TCA: *p < 0.05; **p < 0.01.

It is important in aortic arch operations to protect the brain when cerebral circulation is interrupted. RCP via a superior vena caval cannula is a new technique used to protect the brain during circulatory interruption. RCP was first used to manage massive air embolism during CPB. ⁷ As a method for protecting the brain during circulatory interruption, RCP was first used and reported by Lemole ³ and Ueda ⁴ and their associates. We have used RCP in surgical procedures of the aortic arch since January 1990. Clinically, RCP has several technical advantages in aortic arch operations. Extension of the period of circulatory interruption is a major advantage. In RCP, no vascular clamps are needed for any artery; it avoids cerebral thrombosis and embolism caused by debris or air and also any arterial injury. Absence of arterial clamps provides good anastomotic sites. Returned blood via the arteries can be managed with suckers and does not impair visibility. In the present study, RCP provided half the cerebral tissue blood flow and a third of the oxygen that was observed during controlled CPB. The tissue concentrations of adenosine triphosphate in the brain remained higher during RCP than during TCA. Oxygen consumption and carbon dioxide exudation did not increase significantly when CPB was resumed after RCP, whereas they increased significantly after TCA. Therefore, oxygen debt during RCP was smaller that than during TCA. RCP also cooled the brain better than did TCA. These findings indicate that ischemic damage during RCP may be smaller than that during TCA. However, cerebral tissue oxygen tension decreased, and cerebral tissue carbon dioxide tension increased, even during RCP. Tissue concentrations of adenosine triphosphate in the brain also decreased slightly during RCP. RCP cannot provide enough blood flow and oxygen to maintain aerobic metabolism in cerebral cells and to avoid ischemic change in the brain. RCP, however, can extend the period of time over which the cerebral circulation may be safely interrupted. However, RCP still has limitations as to the time period for which it can be applied. Oxygen demand in the whole body decreases as body temperature decreases. Profound hypothermia, therefore, can minimize ischemic damage by reducing the oxygen debt. ^8-11 Safe duration of circulatory interruption in profound hypothermia has been reported to be 45 to 60 minutes. ^12-15 RCP can supply blood flow and oxygen to the brain and minimize oxygen debt and so should minimize ischemic damage to the brain. RCP in profound hypothermia, therefore, should extend the duration over which cerebral circulation can be safely interrupted. RCP can also cool the brain homogeneously and maintain a low cerebral temperature, which is another advantage of RCP in protecting the brain. Clinically, RCP is performed by infusing blood via a superior vena caval cannula and monitoring pressure in the superior vena caval system while the inferior vena cava is clamped. Blood is returned only from an aortotomy by sucking. Pressure in superior vena cava is the driving pressure that performs the RCP. As the pressure increases, RCP provides more blood flow and oxygen. However, high venous pressure is associated with high cerebrospinal fluid pressure. ¹⁶ It has been reported that any cerebrospinal fluid pressure exceed 17.5 mm Hg or 200 cm H₂O may be associated with brain edema. Therefore, the optimum venous pressure for RCP should be the highest pressure under which massive brain edema does not result. ¹⁶ We clinically performed RCP, maintaining superior vena cava pressure under 25 mm Hg, which is the optimum for RCP. The dog has many venous valves in the superior vena cava systems, which may interfere with retrograde perfusion in a superior vena cava system. In our study, infusion was made directly into the basilar venous plexus bilaterally via the internal maxillary veins to avoid venous valves. ^17,18 The dog, which has a small internal jugular vein with many venous valves, is not a good model for RCP. Nevertheless, this experimental study suggests several advantages for using RCP in human beings. Retrograde cerebral perfusion can be performed without clamping or cannulating cervical arteries. It should reduce any chance of cerebral thrombosis and also provide a better operative field. Retrograde cerebral perfusion may reduce ischemic damage during interruption of the circulation. It should be mentioned, however, that there is a limit to this duration of circulatory interruption and that high venous pressures may cause brain edema.

Footnotes

From the Nagoya University School of Medicine, Department of Thoracic Surgery, Nagoya^a; and the Oogaki Municipal Hospital, Thoracic Surgery Division, Gifu, Japan.^b

References

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