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Ann Thorac Surg 1997;63:167-174
© 1997 The Society of Thoracic Surgeons
Departments of Cardiac Surgical Research and Cardiothoracic Surgery, The Rayne Institute, St. Thomas' Hospital, London, United Kingdom
Accepted for publication September 20, 1996.
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Abstract |
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 TopFootnotes Abstract IntroductionMaterial and MethodsResultsCommentReferences |
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Methods. We compared the changes in CBF using xenon-133 clearance with changes in middle cerebral artery velocity by transcranial Doppler sonography (VMCA) using pH-stat and alpha-stat acid-base management during cardiopulmonary bypass. Measurements were taken (1) before bypass, (2) at 28°C on bypass, (3) at 37°C on bypass, and (4) after bypass. Relative changes in CBF and VMCA, calculated as the percent change from the prebypass baseline value normalized to 100%, were used in this analysis.
Results. During the hypothermic phase of cardiopulmonary bypass, CBF and VMCA increased by 45.9% and 51.8%, respectively (p < 0.001), during pH-stat acid-base management but decreased by only 26.4% and 22.4%, respectively (p < 0.0001), during alpha-stat acid-base management. Linear regression analysis of the absolute changes in CBF (mL•100 g-1•min-1) and VMCA (cm/s) showed a significant correlation (r = 0.60; r2 = 0.36; p < 0.0001), but a better correlation was obtained when relative changes in CBF and VMCA were compared (r = 0.89; r2 = 0.79; p < 0.0001).
Conclusions. Measurements of VMCA, expressed as relative changes of a pre-cardiopulmonary bypass level (using the noninvasive transcranial Doppler sonographic technique), can be used to examine CBF changes during cardiopulmonary bypass.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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The gold standard techniques for measuring CBF are Kety-Schmidt and xenon-133 (133Xe) clearance techniques. However, these measurement techniques for CBF during CPB are cumbersome, expensive, and invasive. In addition, there is debate as to which technique is more accurate [6], although Young and colleagues [7] argued in an editorial in this journal that "absolute values in ...CBF is a secondary issue, especially if the question is how CBF changes under the variable physiologic conditions of CPB." Although use of 133Xe clearance has become commonplace during cardiac operations, it has a number of limitations. Stable bypass conditions over a 10- to 15-minute period are required, and this is not always possible during cardiac operations, where several variable factors that influence CBF, such as temperature, perfusion pressure, and arterial carbon dioxide tension (PaCO2), change frequently. In addition, 133Xe is expensive and has a relatively long half-life, which limits the number of repeat measurements that can be safely made in an individual patient.
Since the first report of the application of the Doppler principle for measuring blood flow velocity [8, 9] there have been considerable improvements in the instrumentation to allow analysis of the pulsatile hemodynamics of blood flow. Transcranial Doppler (TCD) evaluation of blood flow velocity in the cerebral basal arteries was introduced in clinical practice by Aaslid and associates [10] in 1982. This technique is noninvasive and inexpensive, and it has the advantage of offering continuous monitoring for long periods [11]. A number of studies have used TCD sonography for measurement of blood flow velocity in the middle cerebral artery (MCA) to monitor changes in cerebral perfusion [12–14]. Using the TCD technique will not provide absolute values in CBF as the diameter of the MCA is unknown in any individual. Assuming that the MCA diameter remains unchanged, any changes in velocity would reflect changes in flow, and it is often this change in CBF rather than the absolute CBF that is of interest.
During CPB, acid-base management influences CBF. In the pH-stat protocol, blood pH is maintained close to pH 7.4 and PaCO2 is maintained at 40 mm Hg regardless of temperature changes (temperature-corrected) by addition of CO2 during CPB. It is well known that CO2 has a profound influence on CBF [15], with increasing CO2 resulting in an increase in CBF. In contrast, the alpha-stat protocol maintains neutrality of blood pH and PaCO2 is not adjusted (temperature-uncorrected) during hypothermic CPB [16, 17]. In recent studies, we [18, 19] have demonstrated that, during alpha-stat acid-base regulation, cerebral blood flow velocity (measured by TCD sonography) was less pressure passive than during pH-stat regulation. In addition, there was better matching of cerebral metabolism to cerebral blood flow velocity (ie, flow-metabolism coupling) with alpha-stat regulation. Generally, interest is in changes in flow-metabolism relationships rather than absolute changes in CBF or metabolism during hypothermic CPB; thus, a reliable technique that allows continuous and noninvasive measurement of relative changes in CBF during CPB would be ideal.
In the present study we have used these two extremes of acid-base management, pH-stat and alpha-stat, to evaluate the ability of the TCD technique to estimate changes in CBF during cardiac operations. This was performed by comparing the mean velocity of blood flow in the MCA (VMCA) with simultaneous 133Xe clearance-estimated hemispheric CBF. Two groups of patients were studied with CPB conducted under either alpha-stat or pH-stat acid-base management. This would provide a wide range of PaCO2 over which the CBF would vary and act as a means to validate any relationship between 133Xe-measured CBF and VMCA.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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). Patients with evidence of cerebrovascular disease, untreated hypertension, diabetes mellitus, or a history of neurologic or psychiatric disease were excluded.
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Cardiopulmonary Bypass
A nonpulsatile roller pump with a membrane oxygenator (HF-5701; William Harvey, CR Bard Inc, Billerica, MA) was used, and the circuit was primed with 2.0 L compound sodium lactate (Hartmann's solution; Baxter Healthcare, Irvine, CA) solution. The operation was performed with core cooling to 28°C (nasopharyngeal temperature). Systemic pump flow of 2.4 L•min-1•m-2 was maintained at normothermia and reduced to 1.75 L•min-1•m-2 during hypothermia. Myocardial protection was achieved with intermittent antegrade crystalloid cardioplegia (St. Thomas' Hospital solution No. 1), augmented by topical saline slush. Distal coronary anastomoses were performed during a single period of cardiac arrest. The proximal anastomoses were constructed after removal of the aortic cross-clamp and partial occlusion of the aorta. The pump flow was maintained at 2.4 L•min-1•m-2. Rewarming was continued until the nasopharyngeal temperature reached 37°C.
During CPB cerebral perfusion pressure was maintained greater than 50 mm Hg. This was achieved pharmacologically with alpha-agonist (metaraminol) and antagonist (phentolamine), and was controlled by the anesthetist.
Acid-Base Management
End-tidal carbon dioxide was monitored by a capnograph (Hewlett Packard 472COA, Andover, MA) and the minute volume of the ventilator adjusted to maintain the PaCO2 at 40 mm Hg before and after CPB. During CPB continuous in-line arterial blood monitoring for PaCO2, pH, oxygen, bicarbonate, and base excess was performed using an in-line monitor (Cardiomet 4000; Shiley, Irvine, CA) attached to the arterial line. This allowed rapid correction, by the perfusionist, of any deviation from the desired values that occurred during CPB. Radial arterial samples were used to validate the in-line arterial blood gas analyzer on each occasion.
Measurement of Cerebral Blood Flow
All CBF measurements were made using a Novocerebrograph 10a (Novo Diagnostic Systems, Bagsvaerd, Denmark) fitted with two scintillation probes (model SD 2020.C1) with a 17-mm-long collimator and 19-mm aperture. After correction for the background count, 2 to 4 mCu of radioactive 133Xe (Amersham International, Slough, UK) was injected as a bolus directly into the left common carotid artery for prebypass and postbypass measurements, and the resulting uptake and washout of 133Xe from the cerebral tissues were measured by the biparietal collimated scintillation detectors to produce a washout curve. During bypass, 10 mCu of 133Xe was injected into the arterial limb of the perfusion circuit to produce the washout curve. The 133Xe tissue partition coefficient was corrected for differences in temperature and hematocrit [20], and CBF was determined by stochastic analysis (height-over-area) for clearance curves over 15 minutes.
Measurements of CBF were assessed during the four phases of operation concurrently with VMCA recordings: (1) after induction of anesthesia, (2) on CPB at 28°C, (3) on bypass at 37°C, and (4) 15 minutes after the termination of CPB.
Measurements of Velocity of Blood Flow in the Middle Cerebral Artery
A pulsed gated Doppler ultrasound velocimeter (EME TCD-2-64, Überlingen, Germany) was used to measure VMCA. After positioning of the patient on the operating table, acoustic gel was applied to the temporal region of the head. A detailed search for the ultrasound window of the left MCA was made using a 2-MHz ultrasound transducer with range gate set at 5 cm. The ultrasound window was located just above the zygomatic process and 1 to 3 cm in front of the ear. The optimum insonation point for the MCA was located by altering the depth setting in increments of 5 mm to achieve a maximum Doppler signal output. Thereafter, the transducer remained in this exact position throughout the study period. The position of the probe was fixed in two planes with a specifically designed holder, and care was taken not to dislodge the probe. The instrument and details of examination procedures have been described previously [10].
In each patient, VMCA was recorded during the four phases of operation: (1) after induction of anesthesia, (2) on CPB at 28°C, (3) on bypass at 37°C, and (4) 15 minutes after the termination of CPB. At each phase, VMCA was recorded every minute over a 15-minute period and then averaged from this period. The VMCA recordings were made at the same time as the CBF measurements by 133Xe isotope clearance technique were carried out during these four phases of operation. Core temperature, cerebral perfusion pressure, systemic pump flows, and arterial blood gas profilewere maintained constant during the period of measurements to minimize errors of measurement in both CBF and VMCA.
Normalization
The individual patient variation in the cross-sectional diameter of the MCA results in a wide range of VMCA for any given absolute CBF. This limitation was overcome by comparing changes in the VMCA relative to the baseline value before CPB (phase 1). To facilitate comparisons between the two methods, VMCA and CBF were normalized by relating all values to the prebypass level. Thus, pre-CPB VMCA in the MCA of each patient was normalized (100%) and the VMCA during 28°C bypass, during 37°C bypass, and after CPB were expressed as a percentage of their pre-CPB value. A similar normalization was performed for the CBF as calculated using 133Xe clearance.
Statistics
Data were analyzed using Statview 4.1 (Abacus Concepts, Inc, Berkeley, CA) on an Apple Macintosh PowerPC computer. Differences between the two groups of acid-base management were compared using repeated-measures analysis of variance for changes in CBF (133Xe) and VMCA during CPB. Comparison of the relative changes in CBF (133Xe) and VMCA between the alpha-stat and pH-stat groups was done using the Mann-Whitney test. Simple linear regression analysis, using the method of ordinary least squares, was used to compare changes in CBF measured by 133Xe clearance and changes in VMCA measured by TCD sonography. The correlation coefficient (r) and the coefficient of determination (r2) were determined for each regression.
Data are expressed as means ± standard error of the mean. A p value of less than 0.05 was considered to be significant.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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. Significant differences in PaCO2 occurred during the hypothermic phase of CPB in the alpha-stat group. The use of a crystalloid prime and pre-CPB removal of 500 mL of blood for post-CPB use caused an initial significant decrease in the hematocrit in both the groups; this remained unchanged throughout the rest of the study period in both groups. Mean arterial pressure was significantly less during bypass in both the groups, but there were no differences between the groups at any phase of the operation.
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and Table 3 show the absolute values of CBF (measured by 133Xe) and VMCA (measured by TCD sonography) at the four phases of operation. The pattern of change between CBF and VMCA is very similar; there is a significant increase in both CBF and VMCA during hypothermic (28°C) bypass, which remains elevated during normothermic (37°C) bypass and during the postbypass period. Relative changes are shown in Figure 2A and Table 4. The increase in CBF and VMCA during 28°C bypass is 45.9% and 51.8%, respectively, reflecting the increased CO2 required to maintain pH-stat regulation at this temperature.
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and Table 3. As for the pH-stat patients, the pattern of change between CBF and VMCA is very similar; however, in the alpha-stat patients there is a significant decrease in both CBF and VMCA during hypothermic (28°C) bypass, and the difference between the two groups of patients (pH-stat and alpha-stat) during this phase is highly significant (p = 0.0001).
The relative changes are shown in Figure 2B and Table 4; CBF and VMCA decrease during 28°C bypass by 26.4% and 22.4%, respectively. This is associated with the significant reduction in PaCO2 in this group of patients during hypothermic (28°C) bypass (see Table 2). During normothermic (37°C) bypass CBF and VMCA increased significantly to values that were not different from those seen in the pH-stat group of patients, and these levels were maintained during the post-CPB phase. The PaCO2 increased from a mean of 25.8 mm Hg (temperature-corrected value) at hypothermic (28°C) bypass to 40.2 mm Hg at normothermia; as a result, CBF increased by 5.6%/mm Hg and VMCA increased by 4.2%/mm Hg.
Relationship Between Cerebral Blood Flow and Middle Cerebral Artery Velocity
Regression analysis of the absolute and relative changes in CBF and VMCA data during the different phases of operation was performed. The relationships between the absolute values of CBF and VMCA in all patients at the four phases of operation are shown in Figure 3. The two groups of patients are shown independently; the correlation coefficient (r) and the coefficient of determination (r2) for the pH-stat patients are 0.59 and 0.35; for the alpha-stat patients, 0.59 and 0.34; and for all patients, 0.60 and 0.36. These correlation coefficients are statistically significant (p < 0.0001).
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; again, the two groups of patients are shown independently and as a whole group. The correlation coefficient (r) and the coefficient of determination (r2) for pH-stat patients are 0.84 and 0.70; for the alpha-stat patients, 0.90 and 0.80; and for the whole group, is 0.89 and 0.79. These values are again statistically significantly (p < 0.0001).
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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Cerebral blood flow values obtained using either the Kety-Schmidt or the 133Xe clearance technique, which remain the "gold standard" methods for measuring CBF, are relatively imprecise, and this variation is reflected in the literature. Govier and colleagues [26], using a relative pH-stat acid-base protocol (PaCO2 varying between 33 and 45 mm Hg), reported CBF values measured by 133Xe clearance of 20.4 ± 6.5, 10.1 ± 3.2, 17.2 ± 6.5, and 26.3 ± 9.4 mL•100 g-1•min-1 before CPB, during 26° to 29°C bypass, during 37°C bypass, and after CPB, respectively. Consequently, they demonstrated the opposite effect on CBF of our data, with CBF being reduced during hypothermic bypass for pH-stat regulation. In fact, their data are similar to our alpha-stat data, which suggests that their acid-base regulation may not have been strictly regulated (the PaCO2 values ranged from 28.6 to 37.2 mm Hg during CPB). In contrast to the results of Govier and colleagues, Stephan and colleagues [27] obtained CBF values measured by Kety-Schmidt technique (using argon wash-in) from patients subjected to either pH-stat or alpha-stat management that were not dissimilar to values obtained in the present study. Thus, in their pH-stat group of patients the CBF values were 33 ± 4, 96 ± 39, and 44 ± 8 mL•100 g-1•min-1 for pre-CPB, 26°C bypass, and post-CPB periods, respectively; in the alpha-stat patients, these values were 34 ± 8, 28 ± 5, and 43 ± 9 mL•100 g-1•min-1, respectively. In a study by Croughwell and colleagues [28], in which CBF was measured by 133Xe clearance in patients undergoing alpha-stat acid-base management during CPB, the CBF values at 27°C bypass and 37°C bypass were 21.0 ± 6.8 and 35.0 ± 9.0 mL•100 g-1•min-1, respectively. These values were very similar to the data obtained in our present study during the bypass period.
Values for VMCA in previous studies are also similar to those obtained in the present study. Lundar and co-workers [13] studied CO2 reactivity in 5 patients subjected to pH-stat acid-base regulation; values for VMCA before CPB varied between 37 and 53 cm/s and increased to values of 70 to 95 cm/s during 28° to 32°C bypass. In contrast, patients undergoing CPB using an alpha-stat protocol in a study by van der Linden and colleagues [29] demonstrated VMCA values in awake patients of 45.1 ± 3.3 cm/s, which decreased to about 80% of this value (36 cm/s) after sternotomy, decreased again to about 50% (23 cm/s) during 20°C bypass, and increased to 100% before weaning from bypass, remaining at this level after bypass.
Current techniques for measuring changes in CBF (133Xe clearance or the Kety-Schmidt methods) do not provide a continuous measurement. Changes in CBF have to be measured at discrete intervals with constraints of time and ability to carry out repeated measurements. In contrast, TCD sonography is able to continuously monitor changes in blood flow velocity. Due to the variation in the MCA diameter, absolute values of VMCA do not correspond to absolute values in CBF between individuals. By using relative changes in VMCA it is possible to compare changes in CBF between different individuals or groups. The MCA has the highest volume flow from the circle of Willis, carrying 80% of the blood from the internal carotid to the ipsilateral hemisphere [30]. Any changes in flow in this vessel, therefore, should reflect changes in the cerebral perfusion. From this it had been assumed that changes in VMCA per se can be used to measure changes in CBF. This concept has been supported by clinical studies performed in normal subjects and in patients at normothermia. Risberg and Smith [31] found significant correlations (r = 0.66 to 0.88) between 133Xe-estimated CBF and carotid artery velocity measurements. Bishop and co-workers [32] found a correlation coefficient of 0.85 between changes in VMCA and 133Xe isotope washout measurement of CBF. Lindegaard and co-workers [33] observed a correlation coefficient of 0.95 between changes in VMCA and electromagnetically measured flow in the ipsilateral internal carotid artery. A significant correlation of 0.7 was reported in the study by van der Linden and colleagues [29] between synchronously measured VMCA and CBF estimated by the thermodilution technique during cardiac operations.
For TCD sonography to be accepted as a means of assessing changes in CBF during CPB, a comparison of conventional clearance of isotopes such as 133Xe and the flow velocities within the basal cerebral arteries had to be made. In this study the noninvasive TCD technique and the invasive 133Xe isotope clearance technique were used to estimate changes in cerebral perfusion during cardiac operations. The results showed marked similarities between changes in the VMCA and changes in mean hemispheric CBF. This supports the validity of using changes in VMCA as an estimate of changes in CBF. We believe that it is appropriate to use the 133Xe technique in this manner as it is the change in CBF that is of prime importance.
Marked alterations in temperature might be expected to influence the vessel diameter, which would, in turn, influence the TCD computation of flow measurements. This was not the case, however, as can be inferred from the present study, where the VMCA remained unchanged between 28°C and 37°C measurements in the pH-stat group. During both these periods the hematocrit and PaCO2 values were similar. The flows were also nonpulsatile during both these periods. If the diameter had changed, a close correlation between the two methods would not be expected. This close relationship between 133Xe clearance and VMCA provides further, albeit indirect, evidence that the diameter of the MCA does not change significantly during cardiac operations. Other studies have also demonstrated that the diameter of the large cerebral arteries are relatively constant, even with changes in PaCO2 and cerebral perfusion pressure. Thus, Huber and Handa [34], using an angiographic technique, have demonstrated only marginal changes in the mean diameter of intracranial basal arteries, and Aaslid [35] has also shown that flow velocity in the MCA should be representative of CBF. Stump and colleagues [36] have demonstrated good correlation between CBF velocity and CBF. Further evidence that the diameter of the MCA does not change with temperature is provided by van der Linden and colleagues [37]. In their study the MCA diameter measured using a computerized echocardiographic tracing system in children did not change during profound hypothermia.
The total cerebrovascular resistance is very sensitive to changes in arterial PaCO2. In the present study, the VMCA changed by 4.2%/mm Hg change in PaCO2 between 28°C and 37°C measurements in the alpha-stat group. These changes were not seen in the pH-stat group during these periods, because the PaCO2 was not altered. This reactivity to PaCO2 is similar to that reported by Markwalder and co-workers [38], in whose study a VMCA reactivity of 3.4 ± 0.5%/mm Hg change in end-tidal CO2 was reported. This figure comes very close to data obtained in CBF studies, and confirms the assumption that the MCA diameter remains relatively constant during changes in PaCO2, the vasomotor action being confined to resistance arteries and arterioles.
Changes in hematocrit might also be expected to change VMCA because, as blood is a non-Newtonian fluid, viscosity will also change. Flow is proportional to the perfusion pressure and inversely related to total vascular resistance, which is itself proportional to resistance components of the vessels themselves and the viscosity of the blood. Little is known about the effect of hematocrit on VMCA. Studies involving CPB, where hematocrit changes significantly on the commencement of CPB, have shown that there is a transient increase in VMCA to 111% from baseline values, which correlated with the change in hematocrit over this short phase (r = -0.62; p < 0.02) [39]. A similar feature was reported by Lundar and colleagues [12], who showed an initial increase in VMCA of 140% to 260% relative to pre-CPB values; after CPB the VMCA remained elevated by 111% to 208%.
From the results of this study we conclude that TCD sonography can be used as a technique for assessing changes in CBF during CPB. The correlation between the relative changes in CBF as measured by 133Xe clearance and TCD VMCA under two different acid-base management protocols, which alter CBF considerably in different ways, is consistent. This reinforces our belief in using TCD sonography as a noninvasive, continuous measurement technique when one is interested in changes in CBF.
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentReferences |
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