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Ann Thorac Surg 1999;67:672-675
© 1999 The Society of Thoracic Surgeons

Original Articles

Comparative study of retrograde and selective cerebral perfusion with transcranial Doppler

Yoshihisa Tanoue, MDa, Ryuji Tominaga, MDa, Yoshie Ochiai, MDa, Kouji Fukae, MDa, Shigeki Morita, MDa, Yoshito Kawachi, MDa, Hisataka Yasui, MDa

a Department of Cardiovascular Surgery, Faculty of Medicine, Kyushu University, Fukuoka, Japan

Accepted for publication August 10, 1998.

Address reprint requests to Dr Tanoue, Department of Cardiovascular Surgery, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan
e-mail: tanoue{at}heart.med.kyushu-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Retrograde cerebral perfusion (RCP) is a simple technique and is expected to provide cerebral protection. However, its optimum management and limitations remain unclear. Transcranial Doppler has been used to monitor cerebral perfusion. Using this Doppler technique, we compared cerebral blood flow for RCP with that for selective cerebral perfusion.

Methods. Thirty-two consecutive patients underwent elective surgical repair of an aortic aneurysm involving the aortic arch at Kyushu University Hospital. Retrograde cerebral perfusion was used in 15 patients and selective cerebral perfusion, in 17 patients. Continuous measurement of middle cerebral artery blood flow velocities was performed by transcranial Doppler technique.

Results. Retrograde middle cerebral artery blood flow velocities during RCP could be measured in only 3 patients, whereas middle cerebral artery blood flow velocities during selective cerebral perfusion could be measured in all but 1 woman. The increase in middle cerebral artery blood flow velocities after RCP was significantly greater than that after selective cerebral perfusion.

Conclusions. The measurement of middle cerebral artery blood flow velocities with transcranial Doppler technique is practicable during selective cerebral perfusion but difficult during RCP. The increase in middle cerebral artery blood flow velocities after RCP indicates reactive hyperemia and reflects the critical decrease in cerebral blood flow during this type of perfusion.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Surgical repair of aortic aneurysms involving the aortic arch is often associated with great technical difficulty. Brain damage accounts for the high perioperative mortality and morbidity despite the developments in surgical techniques. Retrograde cerebral perfusion (RCP) through the superior vena cava was clinically introduced as an added technique of circulatory arrest to protect the brain during operations on the aortic arch, and there are a number of studies involving this method of perfusion [1–7]. Although the clinical results reported with RCP are good, the correct conditions, that is, the proper pressure and flow of RCP, are still unknown. Thus, selective cerebral perfusion (SCP) and hypothermic circulatory arrest (HCA) are widely used as adjuncts for cerebral protection.

The transcranial Doppler (TCD) technique has been used in various clinical settings to monitor cerebral perfusion [8]. It makes possible the noninvasive continuous monitoring of cerebral blood flow for long periods. The TCD technique is also useful for cerebral blood flow monitoring during cardiac operations [9, 10]. The purpose of this study was to compare the middle cerebral artery (MCA) blood flow velocities for RCP and SCP using the TCD technique during aortic arch surgical procedures.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
From April 1993 to January 1997, 32 consecutive patients electively underwent resection and graft replacement of ascending aortic, transverse aortic arch, or descending thoracic aortic aneurysms at Kyushu University Hospital. Retrograde cerebral perfusion was used in 15 patients (RCP group) and SCP, in 17 patients (SCP group) for cerebral protection during the reconstruction of the aortic arch. This was a randomized, prospective study, and informed consent was obtained from all patients. Profiles of the two patient groups are shown in Table 1.


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  		Table 1. Profiles of the Two Patient Groups

 
Operative technique
The patients were usually placed in a right semidecubitus position. Anesthesia was accomplished using a standard intravenous technique with fentanyl, midazolam hydrochloride, and pancuronium bromide for muscle relaxation. Cardiopulmonary bypass (CPB) was instituted with a heart-lung machine consisted of a rotating pump (Pemco Inc, Cleveland, OH) and a membrane oxygenator (Compactflo D703; Dideco, Mirandola, Italy). Cannulation for CPB was undertaken with separate superior and inferior venae cavae cannulas, returning the oxygenated blood to the ascending aorta or the left femoral artery. A left ventricular venting tube was inserted into the right upper pulmonary vein. All patients were cooled to a rectal temperature of 18°C during the reconstruction of the aortic arch. Arch vessels were reconstructed individually. The descending aorta was clamped during the reconstruction of arch vessels, and the blood flow of the lower body was maintained, if possible. Open technique was used on the anastomosis of the graft and the descending aorta under circulatory arrest of the lower body. Coronary artery bypass grafting was performed in 2 patients in the RCP group and 3 in the SCP group. The Bentall procedure was performed in 2 patients in the RCP group. Myocardial preservation was achieved by cold crystalloid cardioplegic solution [11] and ice slush. Tympanic temperature was measured during the procedure.

RCP technique
An arterial line of the heart-lung machine was connected to the superior vena cava cannula (thin-walled angled metal venous cannula [Pacifico venous cannula; Medtronic DLP, Grand Rapids, MI]), which was snared by an umbilical tape. Retrograde cerebral perfusion was then commenced with oxygenated blood flowing through the superior vena cava to the internal jugular vein with a rotating pump (Mera blood pump HCP-100 or HCP-5000; Senko Medical Instrument, Tokyo, Japan). The superior vena cava pressure was monitored and maintained between 15 and 25 mm Hg by adjusting RCP flow. The temperature of circulating blood was kept at 15°C by a heat exchanger (Mera hot & cool unit; Senko Medical Instrument).

SCP technique
An arterial line of the heart-lung machine was connected to three balloon infusion cannulas (Sumitomo Bakelite Co, Ltd, Tokyo, Japan), which were inserted into the three arch vessels, respectively. Selective cerebral perfusion was started with oxygenated blood, and the flow rate was fixed at 500 mL/min with a rotating pump. Perfusion pressure of SCP was monitored at the left superficial temporal artery. The temperature of the circulating blood was kept at 15°C by a heat exchanger.

TCD technique
A TCD unit (Neuroguard, Medasonics, Fremont, CA) with a 2-MHz probe attachment was used to continuously measure the MCA flow velocities. The transducer was positioned on the left temporal region with a fixation device. There were six monitoring times: before CPB; 5 minutes after the start of CPB; at a rectal temperature of 20°C during the cooling period; during cerebral perfusion (RCP or SCP); at a rectal temperature of 30°C during the rewarming period; and 30 minutes after weaning from CPB. A high-pass filter was used to prevent the detection of low-frequency artifacts. The filter of choice in this study was the 150-Hz high-pass filter except during RCP, when the 75-Hz high-pass filter was used because retrograde signals were so small as to be eliminated by the 150-Hz high-pass filter.

Statistical analysis
Results are presented as the mean ± the standard deviation. The Student t test was used to analyze differences between groups. A p value of less than 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
The two groups were similar with respect to operation time (RCP group, 636 ± 183 minutes; SCP group, 656 ± 254 minutes), CPB time (RCP group, 281 ± 87 minutes; SCP group, 271 ± 93 minutes), aortic cross-clamp time (RCP group, 64.4 ± 44.9 minutes; SCP group, 78.4 ± 32.4 minutes), and circulatory arrest time of the lower body (RCP group, 33.4 ± 20.7 minutes; SCP group, 33.8 ± 17.5 minutes). Data on cerebral perfusion are shown in Table 2. The duration of RCP was significantly shorter than that of SCP (38.3 ± 14.6 minutes versus 71.9 ± 40.4 minutes; p = 0.0047).


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  		Table 2. Cerebral Perfusion Dataa

 
Three patients died (operative mortality rate, 9.4%), and a total of 5 patients had cerebral complications. Two patients in the RCP group sustained a cerebral infarction, diagnosed with computed tomography, did not regain consciousness, and died 12 days and 15 days after operation; and 1 patient in the SCP group died of uncontrollable bleeding after operation. Three patients in the SCP group had a stroke, most probably due to embolic phenomena. One of them has severe mental confusion, and 2 have partial paralysis.

MCA flow velocities
The MCA blood flow velocities of 1 woman in the SCP group could not be measured because of the absence of a temporal ultrasonic window as a result of osteoporosis, and hence the MCA flow velocity data are for 31 patients. The changes in MCA flow velocity measured by TCD are shown in Table 3 (raw data) and Figure 1 (percent changes). Retrograde MCA flow velocities during RCP could be measured in only 3 patients and were 6%, 20%, and 21% of MCA flow velocities before CPB. In the other 12 patients in the RCP group, retrograde MCA flow velocities during cerebral perfusion could not be detected. Middle cerebral artery flow velocities were measured in 16 patients in the SCP group, and the average velocity was 43.8% ± 35.8% of MCA flow velocity before CPB. The MCA flow velocity during RCP decreased significantly compared with that during the cooling period (3.2% ± 7.3% versus 68.2% ± 20.6%; p < 0.0001). During SCP, the MCA flow velocity also decreased significantly as compared with that during the cooling period (43.8% ± 35.8% versus 67.3% ± 36.9%; p = 0.0370). The MCA flow velocity during RCP was significantly decreased compared with that during SCP (3.2% ± 7.3% versus 43.8% ± 35.8%; p = 0.0002), and the MCA flow velocity after RCP was significantly increased compared with that after SCP (on rectal temperature of 30°C during rewarming period, 154.1% ± 67.3% versus 88.4% ± 43.4%; p = 0.0029; 30 minutes after weaning from CPB, 152.8% ± 53.9% versus 108.1% ± 40.5%; p = 0.0138).


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  		Table 3. Changes in Middle Cerebral Artery Blood Flow Velocities Measured by Transcranial Dopplera

 


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  		Fig 1. Percent changes in middle cerebral artery blood flow velocities measured by transcranial Doppler technique. The flow velocities could not be measured in 1 patient in the selective cerebral perfusion (SCP) group because there was no temporal ultrasonic window as a result of osteoporosis. Retrograde middle cerebral artery flow velocities during retrograde cerebral perfusion (RCP) could be measured in only 3 patients. Middle cerebral artery flow velocities after RCP were significantly increased compared with those after SCP. Data are shown as the mean ± the standard deviation (SD). (Cooling = at a rectal temperature of 20°C during cooling period; CP = during cerebral perfusion, either RCP or SCP; CPB OFF = 30 minutes after weaning from cardiopulmonary bypass; CPB ON = 5 minutes after start of cardiopulmonary bypass; Pre CPB = before cardiopulmonary bypass; Rewarming = at a rectal temperature of 30°C during rewarming period.)

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Strategies for protecting the brain during operations for aortic aneurysms involving the aortic arch have evolved into three major categories: HCA, SCP, and RCP. Hypothermic circulatory arrest is the simplest and provides a good operative field but has the disadvantage of a time limit in terms of safety [12]. Selective cerebral perfusion is a useful adjunct when reconstruction of the aortic arch and arch vessels is likely to take a long time. However, SCP requires complicated techniques for cannulation and increases the clutter in the operative field. Further, SCP increases the risk of particulate embolization associated with cannulation, which may be related to the dislodgment of atheromatous debris [13]. Retrograde cerebral perfusion is a simple technique and may provide cerebral protection superior to that of HCA, although less effective than that of SCP. The operative field is unencumbered by additional cannulas or clamps, and there is no requirement of invasion of the cerebral vessels, which provides a better operative field, avoids possible arterial damage, and mitigates the risk of particulate embolization [4, 14]. We chose RCP or SCP for cerebral protection and did not perform operation under HCA alone mainly because reconstruction of the aortic arch and arch vessels can take on occasion longer than 40 minutes, which is the safe period for HCA [12].

The TCD technique has attractive features, such as noninvasiveness and a high temporal resolution. It makes possible continuous monitoring of cerebral blood flow for long periods. However, its quality is inherently dependent on the skill of the technician. Retrograde signals during RCP were detected in only 3 of 15 patients in this study, whereas Ganzel and colleagues [10] reported retrograde signals in 16 of 18 patients. This discrepancy was due to the difference in perfusion pressure, that is, superior vena cava pressure, during RCP. The average superior vena cava pressure in our study was 23 mm Hg (range, 15 to 25 mm Hg), whereas 40 mm Hg (range, 30 to 49 mm Hg) was necessary to establish TCD–verified RCP in the study of Ganzel and associates [10]. We maintained superior vena cava pressure between 15 and 25 mm Hg, because Usui and coworkers [6] reported that the risk of brain complications increased significantly when superior vena cava pressure exceeded 35 mm Hg and recommended that superior vena cava pressure be maintained between 15 and 24 mm Hg whenever possible. We believe that RCP is an excellent addition to HCA, although the acceptable period of RCP is limited. To avoid brain edema, we did not make superior vena cava pressure during RCP greater than 25 mm Hg [15].

Many groups [2–7] have reported good clinical results with RCP. However, limitations of its effectiveness have been noted in many experiments. Our group [16] previously demonstrated maldistribution of the cerebral blood flow during RCP in mongrel dogs. Using a laser Doppler flowmeter and the hydrogen clearance method. Yoshimura and colleagues [17] reported that the supply of oxygen or glucose with RCP was not enough to maintain sufficient cerebral metabolism, and this caused brain edema in mongrel dogs. Boeckxstaens and Flameng [18] found that RCP did not perfuse the brain in baboons because of venovenous shunting. In a comparative experimental study of SCP and RCP in which they used phosphorus 31–magnetic resonance spectroscopy to monitor brain metabolites in pigs, Filgueiras and associates [19] reported that intracellular pH and high-energy phosphates in the brain decreased during RCP. Sakurada and colleagues [20] reported that somatosensory evoked potentials completely disappeared during RCP in mongrel dogs. In clinical studies, Usui and associates [6] recommended that the period of RCP should not exceed 60 minutes, and Takamoto [7] suggested a time limit for RCP of 80 minutes.

For further investigation of the effectiveness of RCP, MCA flow velocities were measured using the TCD technique. It failed to detect MCA flow velocities during RCP in a range of perfusion pressures from 15 to 25 mm Hg, which were thought to be safe. It is unknown whether flow was absent or whether TCD was unable technologically to detect it. However, clinically it is worthwhile to have detected reactive hyperemia after a relatively short period of RCP (mean time, 38 minutes; range, 25 to 80 minutes), as reactive hyperemia is indicative of a critical decrease in cerebral blood flow.

In conclusion, the measurement of MCA flow velocity with TCD technique is practicable during SCP but was difficult during RCP when the perfusion pressure was 15 to 25 mm Hg. The increase in MCA flow velocities after RCP indicates reactive hyperemia and reflects the critical decrease in cerebral blood flow during RCP.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported in part by the Research Grant of Cardiovascular Disease (6C-3) from the Ministry of Health and Welfare, Japan.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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  5. Bavaria J.E., Woo Y.J., Hall R.A., Carpenter J.P., Gardner T.J. Retrograde cerebral and distal aortic perfusion during ascending and thoracoabdominal aortic operations. Ann Thorac Surg 1995;60:345-353.[Abstract/Free Full Text]
  6. Usui A., Abe T., Murase M. Early clinical results of retrograde cerebral perfusion for aortic arch operations in Japan. Ann Thorac Surg 1996;62:94-104.[Abstract/Free Full Text]
  7. Takamoto S. Recent progress in adjunctive methods during surgery of aortic dissection. Nippon Geka Gakkai Zasshi 1996;97:894-899.[Medline]
  8. DeWitt L.D., Wechsler L.R. Transcranial Doppler. Stroke 1988;19:915-921.[Abstract/Free Full Text]
  9. Trivedi U.H., Patel R.L., Turtle M.R.J., Venn G.E., Chambers D.J. Relative changes in cerebral blood flow during cardiac operations using xenon-133 clearance versus transcranial Doppler sonography. Ann Thorac Surg 1997;63:167-174.[Abstract/Free Full Text]
  10. Ganzel B.L., Edmonds H.L., Jr, Pank J.R., Goldsmith L.J. Neurophysiologic monitoring to assure delivery of retrograde cerebral perfusion. J Thorac Cardiovasc Surg 1997;113:748-757.[Abstract/Free Full Text]
  11. Kinoshita K., Oe M., Tokunaga K. Superior protective effect of low-calcium, magnesium-free potassium cardioplegic solution on ischemic myocardium. Clinical study in comparison with St. Thomas’ Hospital solution. J Thorac Cardiovasc Surg 1991;101:695-702.[Abstract]
  12. Svensson L.G., Crawford E.S., Hess K.R., et al. Deep hypothermia with circulatory arrest. Determinants of stroke and early mortality in 656 patients. J Thorac Cardiovasc Surg 1993;106:19-31.[Abstract]
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  16. Fukae K., Nakashima A., Hisahara M., Kawachi Y., Masuda M., Yasui H. Maldistribution of the cerebral blood flow in retrograde cerebral perfusion. Eur J Cardiothorac Surg 1995;9:496-501.[Abstract/Free Full Text]
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