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Ann Thorac Surg 1996;61:1348-1354
© 1996 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Comparative Experimental Study of Cerebral Protection During Aortic Arch Reconstruction

Department of Thoracic and Cardiovascular Surgery, Sapporo Medical University School of Medicine, Sapporo, Japan

Accepted for publication December 12, 1995.

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The optimal adjunctive method for cerebral protection during aortic arch repair remains controversial.

Methods. Retrograde cerebral perfusion, selective cerebral perfusion, and hypothermic circulatory arrest were compared in terms of their effect on cerebral function of mongrel dogs using somatosensory evoked potentials. Brain temperatures were held at 20°C for 90 minutes during cerebral perfusion or circulatory arrest and then rewarmed gradually to normal temperature.

Results. Somatosensory evoked potentials completely disappeared as soon as retrograde cerebral perfusion or hypothermic circulatory arrest started and did not recover completely. In the selective cerebral perfusion group, it recovered in all cases. Only 2% of cerebral blood flow and about 3% of the cerebral metabolic rate for oxygen were obtained during retrograde cerebral perfusion compared with the preoperative value. The analysis of adenosine triphosphate and water content of the brain supported these results.

Conclusions. Retrograde cerebral perfusion had some advantage for cerebral protection compared with hypothermic circulatory arrest, but could not supply sufficient cerebral blood flow to maintain brain function. Selective cerebral perfusion was the safest method for arch reconstruction that requires cerebral protection for 90 minutes.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 1354.

Because the operative treatment of aneurysms of the aortic arch requires clamping of arch vessels, cerebral protection is a vital prognostic factor. So far, hypothermic circulatory arrest (HCA) [1–3] and selective cerebral perfusion (SCP) [4–6] have been used primarily, and good results have been obtained. Clinical applications of retrograde cerebral perfusion (RCP) through the superior vena cava are recent developments, with reports of favorable results [7–9]. However, the related cerebral function and pathophysiologic processes remain unclear in many points, and experimental studies have not been performed adequately. Moreover, there are few reports of cerebral function during RCP in comparison with SCP and HCA. To establish safer cerebral protection during aortic arch repair, we investigated and compared RCP, SCP, and HCA, which were performed at a brain temperature of 20°C for 90 minutes, respectively, in terms of their effects on cerebral function as evaluated by somatosensory evoked potentials (SEP).

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Animal Preparation
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 85-23, revised 1985).

In this study, 19 mongrel dogs (body weight 10.0 to 14.5 kg) were used. After intramuscular injection of ketamine hydrochloride (15 mg/kg), fentanyl (30 µg/kg) and pancuronium bromide (2 mg/kg) were given intravenously, and endotracheal intubation was performed to control respiration. The respiratory variables were adjusted to maintain a stable pH (7.35 to 7.45) and carbon dioxide (35 to 45 mm Hg) and oxygen (200 mm Hg) tensions, with monitoring done by intermittent blood gas measurement. Pancuronium bromide (1 mg) was given intravenously every hour to prevent myoelectric invasion during SEP monitoring. Anesthesia during the experiment was maintained by continuous intravenous drip infusion of fentanyl (3 µg•kg^-1•h^-1).

After preparation of SEP and cerebral tissue blood flow (CBF) monitoring, we inserted an indwelling needle into the superior sagittal sinus (SSS) to collect blood samples and to monitor blood pressure. A thermistor probe was inserted and placed on the dura of the left parietal lobe. Similar thermistor probes were placed in the rectum and esophagus.

The blood samples were analyzed at 37°C to determine the pH, oxygen and carbon dioxide tensions, hematocrit, and oxygen saturation using a GEM-STAT machine (Senkoika, Tokyo, Japan).

Somatosensory Evoked Potentials and Cerebral Tissue Blood Flow Monitoring
With the dog in the prone position, the temporoparietal area of the left skull bone was removed, and a silver-ball electrode for recording SEP was placed directly on the dura mater over the sensory cortex. Reference electrodes were placed on the ear, and stimulating needle electrodes were inserted percutaneously over the median nerve of the right foreleg. A CA5200A system (Serucomu, Fukuoka, Japan) was used for SEP recordings. The median nerve was stimulated by square-wave electric pulses (0.2 milliseconds at a frequency of 2/s), and about 100 sweeps were averaged. Stimulation was performed with an intensity of about 5 to 8 mA.

Using the same technique, we removed the temporoparietal area of the right skull bone and fixed a laser probe onto the cortical surface of the right parietal lobe. The CBF was monitored continuously using a Laser Flo (BPM403A; Primetech, Japan) [10].

Cardiopulmonary Bypass
After the median sternotomy was done, the azygos vein was ligated and then 2 mg/kg of heparin was given intravenously. A cannula was inserted in the right femoral artery, and blood removal cannulas were inserted in both vena cavae. An indwelling needle was inserted in the common carotid artery for collection of blood and blood pressure monitoring during SCP. In SCP, a cerebral perfusion cannula was inserted in the aortic arch, and in RCP, 9F perfusion cannulas were inserted in the bilateral maxillary veins.

The perfusion system, consisting of a roller pump and a membrane oxygenator (D-705 Midiflo, Dideco, Italy) with a cardiotomy reservoir, was primed with homologous heparinized blood, lactated Ringer's solution, 20% mannitol (7 mL/kg), and sodium bicarbonate (40 mL). The hematocrit was maintained at 20% to 25% during cardiopulmonary bypass. Alpha stat management was used in this experiment.

Experimental Protocol
Complete extracorporeal circulation was instituted at a flow rate of about 100 mL•kg^-1•min^-1, and 90 minutes of cerebral perfusion or circulatory arrest was initiated when the brain temperature reached 20°C by cooling. The dogs were divided into three groups and subjected to RCP (n = 8), SCP (n = 6), and HCA (n = 5), respectively. In the SCP group, a cerebral perfusion cannula was inserted in the aortic arch. After the proximal and distal sites of the aortic arch and the right and left subclavian arteries were clamped, SCP was performed. Blood was drained from the superior vena cava (Fig 1). The perfusion flow rate was 50% of the physiologic cerebral perfusion flow [11], which is the total blood flow of the brachiocephalic trunk and the proximal left subclavian artery, determined by an electromagnetic flowmeter (MVF-3200; Nippon Koden, Tokyo, Japan) in the condition of clamped right and left subclavian arteries before the initiation of cardiopulmonary bypass. In the RCP group, 9F cannulas for cerebral perfusion were inserted in the bilateral maxillary veins, and both vena cavae were clamped. Blood was returned through the incised ascending aorta to a reservoir by a suction circuit (see Fig 1). Cerebral perfusion pressure during RCP was monitored by measuring the SSS pressure. The perfusion volume was controlled to maintain the mean SSS pressure at 25 mm Hg. During RCP, SCP, and HCA, the systemic circulation was arrested. After the completion of each perfusion, extracorporeal circulation was performed for rewarming to the preoperative brain temperature.

View larger version (33K): [in this window] [in a new window]   Fig 1. . The system of cardiopulmonary bypass during cerebral perfusion. (H.E. = heat exchanger; Oxg. = oxygenator; RCP = retrograde cerebral perfusion; Res. = reservoir; SCP = selective cerebral perfusion.)

Analysis of Somatosensory Evoked Potential Waveforms
In the SEP, the latency of the first negative potential (N1) and the amplitude between peaks of P1 and N1 were analyzed. Each latency and amplitude was expressed as a percentage rate against the preoperative value as a control (100%).

Analysis of Cerebral Metabolic Rate for Oxygen
The cerebral metabolic rate for oxygen (CMRO₂) was calculated from the collection of blood and CBF during extracorporeal circulation for comparison of SCP and RCP. The equation was: CMRO₂ = (CaO₂ - CvO₂) x CBF/100 (mL•100 g^-1•min^-1), where CaO₂ = arterial oxygen content and CvO₂ = venous oxygen content. Blood was collected from the aortic arch perfusion route and SSS during SCP, in the cooling and rewarming period, and from the maxillary vein perfusion line and left common carotid artery during RCP.

Analysis of Cerebral Tissue Adenosine Triphosphate and Water Content
In the blood samples, ATP content was analyzed quantitatively by high-performance liquid chromatography (Jasco 800 series; Nippon Bunko, Japan).

Cerebral tissue water content was calculated from the equation: cerebral tissue water content = (wet brain weight - dry brain weight)/wet brain weight x 100.

Analysis of Cerebral Lactate Uptake Ratio and Lactate/Pyruvate Ratio
The lactate and pyruvate concentrations of arterial and venous blood were measured by enzymatic methods and calculated using the following equations: Lactate uptake ratio = (La - Lv)/La and lactate/pyruvate ratio = Lv/Pv; where La = arterial lactate content; Lv = venous lactate content; and Pv = venous pyruvate content. Blood was collected from the aortic arch perfusion route and SSS during SCP, in the cooling and rewarming period, and from the maxillary vein perfusion line and left common carotid artery during RCP.

Statistics
All measured values were expressed as mean plusmn; standard deviation. Data obtained at each stage of the experiment were analyzed with the Wilcoxon signed rank test, and data from the same stage were compared with the Mann-Whitney U test. A p value of less than 0.05 was considered to indicate significance.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Changes in Somatosensory Evoked Potentials
No significant difference was observed among the groups during cooling. The latency was gradually prolonged as the brain was cooled, but in the SCP group, the potentials could be measured without disappearance during cerebral perfusion. The latency increased by 259.3% plusmn; 61.0% at maximum, and finally recovered up to 113.3% plusmn; 7.9%. In the RCP and HCA groups, the potentials in all cases disappeared within 5 minutes after cerebral perfusion or circulatory arrest was started. In the RCP group, it recovered in 5 dogs but showed no recovery in the remaining 3 dogs. In the HCA group, the potentials never recovered except in 1 case.

The amplitude in 5 dogs whose potentials recovered in RCP was 20% to 50% of the preoperative value. In the SCP group, the SEP recovered in all cases, and its amplitude was 73.0% plusmn; 4.7% of the preoperative value (Figs 2, 3).

View larger version (38K): [in this window] [in a new window]   Fig 2. . Changes in somatosensory evoked potential (SEP) latency. At final measurement, no abnormal levels of SEP latency were found in the SCP group, but 3 dogs in the RCP group and all dogs except 1 in the HCA group showed disappearance of SEP. (HCA = hypothermic circulatory arrest; RCP = retrograde cerebral perfusion; SCP = selective cerebral perfusion.)

View larger version (39K): [in this window] [in a new window]   Fig 3. . Changes in somatosensory evoked potential (SEP) amplitude. At final measurement, no abnormal levels of SEP amplitude were found in the SCP group, but 3 dogs in the RCP group and all dogs except 1 in the HCA group showed disappearance of SEP. (Abbreviations as in Fig 2.)

View larger version (27K): [in this window] [in a new window]   Fig 4. . Changes in cerebral tissue blood flow (CBF). There were no differences among the three groups during the cooling and warming periods. Sufficient CBF could not be obtained during RCP. (Abbreviations as in Fig 2.)

View larger version (25K): [in this window] [in a new window]   Fig 5. . Changes in cerebral metabolic rate for oxygen (CMRO2). There were no significant differences among the three groups during the cooling and warming periods. (Abbreviations as in Fig 2.)

View larger version (20K): [in this window] [in a new window]   Fig 6. . Cerebral tissue content of water and adenosine triphosphate (ATP). There were significant differences between RCP and SCP in water content, but no statistical difference was observed in ATP content. (Abbreviations as in Fig 2.)

Lactate Uptake Ratio and Lactate/Pyruvate Ratio
Ninety minutes after the initiation of cerebral perfusion, the lactate uptake ratio and the ratio of lactate to pyruvate in the RCP group were -0.01 plusmn; 0.57 and 26.0 plusmn; 9.3, respectively, and showed anaerobic metabolism as compared with the SCP groups. In contrast, SCP and RCP significantly maintained aerobic metabolism as compared with the HCA group (Fig 7).

View larger version (26K): [in this window] [in a new window]   Fig 7. . Lactate uptake ratio and lactate/pyruvate ratio during cerebral perfusion or circulatory arrest. At 90-minute measurement, there were statistical differences between RCP and SCP in the lactate uptake ratio. (Abbreviations as in Fig 2.)

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Retrograde cerebral perfusion infused through the superior vena cava was initially performed as treatment of massive air embolism during extracorporeal circulation by Mills and Ochsner [12], and developed into intermittent RCP by Lemole and associates [13] and continuous RCP by Ueda and colleagues [7]. At present, RCP has been applied clinically as a method of cerebral protection during operative treatment of aneurysms of the aortic arch.

Previously, we conducted a comparative study of 90 minutes of RCP at moderate hypothermia of 25°C in a manner similar to the present study and concluded that RCP did not show a protective effect on the brain [14]. Clinically, RCP was performed at hypothermia of less than 20°C in most institutions, so that in this study, the experiment was performed at 20°C to evaluate the protective effect of RCP on the brain. In the experimental model of the mongrel dog, blood was perfused through the bilateral maxillary veins so as to avoid the competent value in the jugular veins and transmit blood directly to the basilar venous plexus during RCP. The perfusion flow rate was adjusted to maintain the SSS pressure at 25 mm Hg. Although Usui and colleagues [15] measured the extrajugular venous pressure in their study, we used the SSS during RCP because we considered it preferable as a measure of the intracranial cerebral perfusion pressure. Midulla and associates [16] also established RCP based on sagittal sinus pressure in their comparison of RCP with SCP and HCA in a porcine model.

The method of SCP and the establishment of perfusion flow were similar to those in the report of Tanaka and co-workers [11], in which cerebral function was safely maintained at above 50% of physiologic flow.

In this study, SEP were used to evaluate cerebral function. Somatosensory evoked potentials were established as effective monitoring for cerebral function, and in the field of cardiovascular surgery, SEP have been clinically applied widely as a monitor of the central nerve during open heart operations [17–19]. It is very important to evaluate the activity of cerebral nerve cells and judge their potential, not only by investigating their metabolism, and in this regard, measurement of SEP is effective. In the RCP and HCA groups, abnormalities were observed in SEP, suggesting that the brain was injured from ischemia. Thus, we suggest that the protective effects of RCP and HCA are not satisfactory under the conditions of 90 minutes of profound hypothermia at 20°C. Midulla and associates [16] used electroencephalography to monitor the cerebral function; however, they did not mention electroencephalographic potentials during 90 minutes of RCP, SCP, or HCA.

Despite perfusion flow during RCP of 89.1 plusmn; 39.1 mL/min, the CBF was 0.8 plusmn; 0.4 mL•100 g^-1•min^-1 with about 2% of the control value, indicating that RCP could not supply effective CBF, at least for the cerebral cortex of the right parietal lobe. Although retrograde blood return was obtained from the arch vessels, CBF could not be observed. This may indicate that the returned effluent was the shunt flow, which did not perfuse the brain tissue. Our figure of CBF was considerably lower than the 50% reported by Usui and colleagues [15] in the same canine experimental model. This discrepancy might be due to the different method of monitoring CBF. In the report by Midulla and associates [16], less than 5% of retrograde blood flow via the superior vena cava returned from the aortic cannula in a porcine model, but the actual cerebral tissue blood flow may be lower than that considering the intracranial shunting. Boeckxstaens and co-workers [20] indicated that RCP did not perfuse the brain in baboons as measured using the colored microsphere method. In SCP, the CBF was 19.3 plusmn; 21.2 mL•100 g^-1•min^-1, which was about 40% to 50% of the control value, with a blood flow of 96.6% plusmn; 27.6 mL/min.

During cooling, CMRO₂ decreased as the cerebral function and CBF decreased from hypothermia. Although the CBF recovered upon rewarming, CMRO₂ recovered at degrees of only 68.7% plusmn; 20.6% and 60.2% plusmn; 48.6% in the RCP and HCA groups, respectively, which were low compared with the SCP group, at 83.7% plusmn; 50.8%. Although there was no significant difference among the groups, cerebral cells might be damaged in the HCA and RCP groups compared with the SCP group.

Regarding energy metabolism, the brain usually produces ATP in aerobic conditions, but in anaerobic circumstances, pyruvate and lactate are accumulated during ischemia. The lactate uptake ratio or lactate/pyruvate ratio, which reflects excess lactate production due to anaerobic glycolysis, can be used as an indicator of cerebral ischemia, such that a negative quantity of lactate uptake ratio shows an anaerobic condition. Retrograde cerebral perfusion showed a protective effect on the brain as compared with HCA, probably because RCP flow could wash out a small amount of the anaerobic metabolites. However, we suggest that RCP could not maintain the aerobic condition for 90 minutes. In this study, the magnitude of tissue ATP content was in the order of SCP, RCP, and HCA (no significant difference). Tissue water content showed significant differences between SCP and RCP, suggesting that RCP might cause brain edema.

In conclusion, 90 minutes of SCP at 20°C was a safe method, with no abnormalities in cerebral function, if it was kept at 50% of physiologic flow. At profound hypothermia of 20°C, RCP could not supply effective CBF. Although 90 minutes of RCP and HCA at profound hypothermia of 20°C were insufficient, RCP showed a slight protective effect on the brain as compared with HCA. According to these results, SCP is the safest method for cerebral protection during arch reconstruction that requires cerebral protection for 90 minutes.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Address reprint requests to Dr Sakurada Department of Thoracic and Cardiovascular Surgery, Sapporo Medical University School of Medicine, South 1, West 16, Chuko-ku Sapporo, 060, Japan.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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