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Ann Thorac Surg 2001;71:673-677
© 2001 The Society of Thoracic Surgeons


Original article: cardiovascular

Clinical implication of orbital ultrasound monitoring during selective cerebral perfusion

Kazumasa Orihashi, MDa, Yuichiro Matsuura, MDa, Taijiro Sueda, MDa, Hiroo Shikata, MDa, Masanobu Watari, MDa, Kenji Okada, MDa

a First Department of Surgery, Hiroshima University School of Medicine, Hiroshima, Japan

Accepted for publication May 12, 2000.

Address reprint requests to Dr Orihashi, First Department of Surgery, Hiroshima University School of Medicine, Kasumi 1-2-3, Minami-ku, Hiroshima 734-8551, Japan
e-mail: ka-ori{at}mcai.med.hiroshima-u.ac.jp


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. We evaluated clinical relevance of orbital ultrasound (OUS) monitoring to neurological events in aortic surgery associated with selective cerebral perfusion (SCP).

Methods. In 24 consecutive cases, blood flow was monitored at central retinal artery (CRA) and retrobulbar vessels. The threshold perfusion pressure for detecting CRA flow in the color Doppler mode (BPt) was determined in individual eyes.

Results. The BPt ranged from 25 to 71 mm Hg. Events (infarction, anisocoria, delirium) occurred in 8 cases. Infarction occurred in all 3 cases when retrobulbar flow was severely impaired for 40 minutes or longer, while none of the remaining 21 cases had infarction (p = 0.0005). Among the latter cases, perfusion pressure was below BPt for longer than 100 minutes in all 5 cases with events, and in 5 of 16 cases without events (p = 0.0124). No significant difference was found in age, duration of cardiopulmonary bypass, SCP, and circulatory arrest, and duration of blood pressure below 50 mm Hg.

Conclusions. Sustained hypoperfusion detected with OUS monitoring is related to an occurrence of neurological events.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Total flow rate and perfusion pressure have been most commonly regulated for managing cerebral perfusion in selective cerebral perfusion (SCP). However, these are extracranial parameters and do not necessarily reflect the intracranial perfusion. In particular, the patients who are indicated for aortic surgery with SCP are likely to have, either manifest or concealed, diseased cerebral vessels. There can be some discrepancy between the extracranial data and actual cerebral perfusion, resulting in an unexpected occurrence of neurological sequelae.

Although transcranial Doppler (TCD) has been used for assessing the intracranial blood flow [1], it is often difficult to obtain signal of reliable quality during SCP [2], and a question often arises whether it is due to a technical problem or to a reduced blood flow. Thus, we previously examined the blood flow velocity in the central retinal artery (CRA) and found that: 1) maximal velocity is linearly correlated to perfusion pressure and "critical closing pressure (BP0)" of CRA where blood flow velocity becomes zero can be determined as the intercept of the linear regression line; 2) BP0 varies among individual patients; and 3) the blood flow can be detected in the retrobulbar vessels at a pressure lower than BP0 [3]. At a perfusion pressure below BP0, the CRA-dependent region can be in de facto circulatory arrest. However, clinical implication of this method was not clear in the previous study. In this study, we examined the clinical relevance of the findings of orbital ultrasound (OUS) to the occurrence of neurological events.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The consecutive 24 cases who underwent aortic surgery with SCP were examined. Two cases in this period were excluded from the study because a sonographer was not available. The included cases comprised of 16 men and 8 women with ages ranging from 52 to 79 (66.6 ± 8.3) years old. The preoperative diagnosis was aortic arch aneurysm, chronic aortic dissection, and acute aortic dissection in 16, 4, and 4 cases, respectively. Operative procedures were total arch replacement in 18 cases, hemiarch replacement in 2 cases, transaortic endovascular stent-grafting in 3 cases, and replacement of ascending aorta in 1 case. The study was approved by the institutional review board and informed consent was obtained from every patient. The surgeon and perfusionist were consistent throughout the study, as was the method of anesthesia.

General anesthesia was induced with fentanyl and midazolam, and was maintained with additional fentanyl and continuous infusion of propofol. A small amount of prostaglandin E1 (0.005 to 0.01 µg/kg/min) was continuously given in this period to improve visceral circulation. When perfusion pressure was as low as below 30 mm Hg, the dose was reduced. An arterial cannula was placed at the ascending aorta, whenever feasible, and otherwise at the femoral artery. Cardiopulmonary bypass (CPB) was established with a roller pump and a membranous oxygenator by using a circuit primed with crystalloid solution and incorporated with an arterial filter. Hematocrit was maintained above 20% by means of hemoconcentration or transfusion, if needed. SCP was established with the cannulae inserted in the branch arteries under deep hypothermic circulatory arrest (CA) (20° to 22°C at the rectal temperature). The left subclavian artery was cannulated unless it was technically difficult, decided by the surgeon who was blinded to the OUS findings. During SCP, pH was maintained by means of the alpha-stat protocol. Perfusion pressure was monitored at the radial artery on the right side and at the tip of cannula placed in the left common carotid artery on the left side. When the right perfusion pressure was unusually lower than the left (the difference larger than 20 mm Hg), the cannula tip pressure was monitored on the right side to rule out vasospasm of radial artery. The total flow rate was basically set at 10 mL/kg/min. When the perfusion pressure was unusually low (lower than 30 mm Hg) or when the blood flow at the orbital vessels was undetectable with unusually low perfusion pressure bilaterally, the flow rate was gradually increased. However, we refrained from increasing the flow rate over 1,000 mL/min in order to avoid neurological complication due to excessive cerebral perfusion, since the clinical implication of OUS monitoring had not been determined yet. The patient was rewarmed at the rate of 5° to 7°C per hour toward 37°C at the rectal temperature. SCP was terminated just prior to the last anastomosis of branch arteries.

The observation was performed by a single echographer, the author, as reported before [3]. After the eyes were covered with adhesive patches (Me-PatchTM Clear L, Nichiban Co Inc, Tokyo, Japan), they were scanned horizontally in color Doppler mode by means of a conventional 7.5 MHz echocardiographic system (EUP-S33, EUB-555, Hitachi Medical Co Inc, Tokyo, Japan) with ultrasonic power set to the lowest level. The CRA was visualized with its course as parallel to the ultrasonic beam as possible, and the blood flow was depicted with a pulse repetition rate of 500 Hz.

The CRA flow was monitored intermittently in order to minimize the hazard on the eye, basically every 10 to 20 minutes during SCP but more frequently (every 2 to 3 minutes) when the pressure dropped by 5 to 10 mm Hg or flow was hardly detectable. Duration of each observation was 5 to 20 seconds and the total duration of observation was approximately 5 minutes, varying among individual cases and eyes.

The lowest perfusion pressure with the CRA flow detectable in color Doppler imaging (threshold pressure: BPt) was determined for the individual eyes. In the later analysis, the duration of perfusion pressure lower than BPt or 50 mm Hg (T-BPt, T-50) was counted in the anesthetic chart and pump chart, which was recorded every 5 minutes. Blood flow in the retrobulbar vessels was normally continuous forward flow but became undetectable at a perfusion pressure further below BPt (approximately 20 mm Hg). Duration of absent flow at retrobulbar vessels was counted (T-RB0).

Intra- and postoperative neurological events were classified into two categories: 1) permanent damage, that is, cerebral infarction; and 2) transient neurological events including anisocoria over 1 mm or delirium that necessitated a use of sedatives for safety in management. Infarction was diagnosed by a consulted neurologist based on the findings of brain computed tomography (CT), which was indicated when any neurological abnormality newly developed and was sustained. The pupil size was monitored by the anesthesiologist and a use of sedatives was decided by the presiding doctor, both of whom were blinded to the OUS data. When the patient had neurological sequelae, he or she was followed up by the presiding surgeon with consulted neurologist.

All results were expressed as the mean ± standard deviation. Difference of values of various parameters between two groups was examined by means of Student’s t test. The coincidence between the OUS findings and occurrence of neurological events was examined by means of a chi-square test. When the number in any category was smaller than 5, Fisher’s exact probability test was used. Statistical significance was determined when the p value was less than 0.05. When the OUS parameters were examined, a larger value in two eyes was assigned as the value of the case.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The OUS monitoring was carried out without complication such as visual disturbance or dermal damage due to the adhesive patch or exposure to ultrasound. The operative parameters, OUS data, and neurological events are listed in the Table 1.


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Table 1. Results of Operative Parameters, Orbital Ultrasound Data, and Neurological Events

 
Duration of CPB, SCP, and CA ranged from 157 to 363 (252.8 ± 49.6) minutes, from 26 to 255 (123.3 ± 48.6) minutes, and from 35 to 80 (55.8 ± 13.7) minutes, respectively. The BPt ranged from 25 to 71 (41.3 ± 9.8) mm Hg. T-BPt and T-50 ranged from 0 to 210 (87.1 ± 58.1) minutes and from 25 to 240 (134.5 ± 48.8) minutes, respectively. The blood flow at the retrobulbar vessels was abnormal for 40 minutes or longer in 3 cases and for 25 minutes in case 7.

Cerebral infarction occurred in 3 cases (11.5%). Anisocoria appeared during SCP in 3 cases (11.5%) and improved after surgery except in case 24. Postoperatively, six cases (26.1%) showed delirium that necessitated use of sedatives.

In case 12, a right axillo-femoral bypass had been placed 7 years before for ischemic limb due to acute aortic dissection. With an SCP flow rate of 600 mL/min and systemic perfusion through the femoral artery at 410 mL/min, the perfusion pressure was 18 mm Hg and 30 mm Hg on the right and left side, respectively. Blood flow was undetectable both at CRA and retrobulbar vessels on both sides until the systemic perfusion rate was increased to 3,000 mL/min and the SCP rate to 700 mL/min (pressure rose to 52 and 50 mm Hg). Although the CRA flow recovered after bypass, broad infarction was found in the right hemisphere postoperatively.

In case 24, blood flow was undetectable except in a tiny retrobulbar vessel of the right eye for 142 minutes. He had anisocoria during SCP that remained postoperatively. The consciousness did not recover. The brain CT on the third postoperative day showed multiple infarct at the supratentorial and left frontal region associated with marked edema in the posterior cranial fossa.

In case 4, the retrobulbar vessels showed blood flow of a to-and-fro pattern for about 40 minutes (Fig 1). He developed delirium, involuntary movement of arms, and left homonymous hemianopsia with infarcts at the bilateral occipital lobes revealed with CT.



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Fig 1. An echogram showing a to-and-fro pattern of blood flow at the retrobulbar vessel in case 4, suggesting a no-flow state. Flow could not be detected at the central retinal artery.

 
In case 7, the right retrobulbar vein was markedly dilated with a spontaneous contrast echo (Fig 2). The perfusion pressure gradually rose to 60 to 70 mm Hg with the SCP flow unchanged. An accidental obstruction of the venous cannula proved to be responsible. As the obstruction was released, the venous dilatation disappeared, perfusion pressure dropped to 50 mm Hg, and the retrobulbar blood flow became detectable.



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Fig 2. An echogram showing a dilated vein in case 7, by an accidental occlusion of venous cannula. Spontaneous echo contrast is seen in the lumen. This disappeared when the occlusion was released.

 
Cerebral infarction occurred in all 3 cases in which the retrobulbar flow was severely impaired for 40 minutes or longer, while none of the remaining 21 cases had infarction (p = 0.0005). The 21 cases without cerebral infarction were divided into 2 groups: cases with transient neurological events (n = 5) and cases without those (n = 16). In the former group, the BPt was significantly higher and the T-BPt was significantly longer than the latter, while no significant difference was found in age, CPB time, SCP time, CA time, and T-50 (Table 2). The T-BPt was 100 minutes or longer in all 5 cases in the former, while in only 5 of 16 cases in the latter (p = 0.0124).


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Table 2. Difference in Parameters Between Cases With and Without Transient Neurological Eventsa

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
This study distinctly demonstrated the clinical relevance of OUS monitoring, that is, sustained absence of detectable blood flow in the CRA and retrobulbar vessels is closely related to occurrence of transient and permanent neurological events, respectively. Cerebral infarction occurred in cases with an absent flow at the retrobulbar vessels for 40 minutes or longer. This reminds us of the report by Svensson and coworkers that neurological damage increased when CA time exceeded 40 minutes [4]. An absent flow at the retrobulbar vessels appears to be equivalent to the CA. Fish and colleagues [5] examined the cases undergoing coronary revascularization and reported that inadequate perfusion of the brain during surgery appeared to be partially responsible for an occurrence of delirium in the intensive care unit. Our results demonstrated that an absent flow at the CRA for longer than 100 minutes was related to an occurrence of transient neurological events. When blood flow is detectable at the retrobulbar vessels but not at the CRA, regional ischemia may occur at the peripheral tissue. If it occurs diffusely in the brain, reversible ischemic damage of brain without infarction may result. Thus, severity of inadequate cerebral perfusion can be graded into three categories: Grade 0, blood flow detectable at CRA; Grade 1, blood flow undetectable at CRA but detectable at retrobulbar vessels; and Grade 2, blood flow undetectable at retrobulbar vessels.

The retrobulbar vessels appear to be equivalent to the middle cerebral artery or ophthalmic artery in the TCD examination. When a cut-off value is assigned as 40 minutes in Grade 2, this criterion was highly predictive to an occurrence of cerebral infarction. Malperfusion of Grade 1 for longer than 100 minutes was correlated to an occurrence of transient neurological events.

Several investigators have recommended a flow rate of 10 mL/kg/min with the perfusion pressure of 50 to 70 mm Hg in order to avoid an excessive or inadequate cerebral perfusion during SCP [6, 7]. In this series, the flow rate was adequate but the perfusion pressure was rather low in several cases. Interestingly the BPt was below 50 mm Hg in two-thirds of cases in this series. When perfusion pressure was between 50 and 70 mm Hg, they were in Grade 0 and the remaining cases in Grade 1 because BPt for retrobulbar vessels was below 50 mm Hg in this series unless venous drainage was disturbed. However, a cut-off value of 50 mm Hg was not related to an occurrence of neurological events. Tolerance to a low perfusion pressure appears to vary among individual cases. Neurological events occurred more frequently in cases with a higher BPt. It might be better to assess the BPt in each case and keep the perfusion pressure higher in this group of patients by increasing the flow rate as was often experienced in this series. Prostaglandin E1, often used in this period to improve visceral circulation, might have been responsible for unusually low perfusion pressure. When the perfusion pressure does not reach this critical pressure with a flow rate of 1,000 mL/min, the dose of vasodilator may need to be reduced or a vasoconstrictor be given.

In this study, we introduced a new parameter, BPt, instead of BP0 because the former can be obtained as soon as the blood flow becomes undetectable, while the latter is not available until the patient is exposed to a lower perfusion pressure and regression line is calculated. Thus BPt is practical in the operative theater. The criteria using BPt are simple and related to an occurrence of transient neurological events.

There are several limitations in this study. First, we could not compare the results of OUS with those of TCD because there was not enough time or space in the operating room for using both systems simultaneously. In addition, comparative study with cerebral angiograms was not available in this study. Second, OUS can be less useful for detecting inadequate perfusion in the region dependent on the vertebral arteries. Third, continued use of ultrasound on the eye may cause some damage on the orbital tissue. We avoided continuous monitoring because the ultrasonic output in our system is 200 Ispta (mW/cm2), while the Food and Drug Administration has recommended that it should be lower than 17 Ispta and may be increased up to 720 Ispta in TRACK 3 (when supervised by a physician). Consequently no complication related to the monitoring procedures was encountered. Our method is not recommended in cases with known ocular diseases such as glaucoma because safety after a prolonged exposure to the ultrasound is not proved at the moment. Fourth, our technique cannot be applied in cases with preoperative or intraoperative obstruction of the CRA and retrobulbar arteries as is rarely encountered in diabetic patients. Fifth, this technique is less useful for detecting an occurrence of embolism to another artery such as middle cerebral artery.

We conclude that OUS monitoring is useful for detecting hypoperfusion of the brain during SCP. It is recommended that the perfusion pressure be maintained high enough to keep the flow detectable with color Doppler imaging at the retrobulbar vessels and CRA to avoid an occurrence of neurological complications.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. van der Linden J., Wesslen O., Ekroth R., Tyden H., von Ahn H. Transcranial Doppler-estimated versus thermodilution-estimated cerebral blood flow during cardiac operations. J Thorac Cardiovasc Surg 1991;102:95-102.[Abstract]
  2. Nuttall G.A., Gook D.J., Fulgham J.R., Oliver W.C., Jr, Proper J.A. The relationship between cerebral blood flow and transcranial Doppler blood flow velocity during hypothermic cardiopulmonary bypass in adults. Anesth Analg 1996;82:1146-1151.[Abstract]
  3. Orihashi K., Matsuura Y., Sueda T., et al. Flow velocity of central retinal artery and retrobulbar vessels during cardio-vascular operations. J Thorac Cardiovasc Surg 1997;114:1081-1087.[Abstract/Free Full Text]
  4. 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;106:19-28.[Abstract]
  5. Fish K.J., Helms K.N., Sarnquist F.H., et al. A prospective, randomized study of the effects of prostacyclin on neuropsychologic dysfunction after coronary artery operation. J Thorac Cardiovasc Surg 1987;93:609-615.[Abstract]
  6. Kazui T., Inoue N., Yamada O., Komatsu S. Selective cerebral perfusion during operation for aneurysms of the aortic arch: a reassessment. Ann Thorac Surg 1992;53:109-114.[Abstract]
  7. Stockard J.J., Bickford R.G., Myers R.R., Aung M.H., Dilley R.B., Schauble J.F. Hypotension-induced changes in cerebral function during cardiac surgery. Stroke 1974;5:730-746.[Abstract/Free Full Text]



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