Is stagnating flow in former feeding arteries an indication of cerebral hypoperfusion after resection of arteriovenous malformations?

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1 See the Letter to the Editor and the Response in this issue in Neurosurgical Forum, pp J Neurosurg 95:36 43, 2001 Is stagnating flow in former feeding arteries an indication of cerebral hypoperfusion after resection of arteriovenous malformations? BERNHARD MEYER, M.D., HORST URBACH, M.D., CARLO SCHALLER, M.D., AND JOHANNES SCHRAMM, M.D. Departments of Neurosurgery and Radiology, University of Bonn, Germany Object. The authors goal in this study was to challenge the proposed mechanism of the occlusive hyperemia theory, in which it is asserted that stagnating flow in the former feeding arteries of cerebral arteriovenous malformations (AVMs) leads to parenchymal hypoperfusion or ischemia, from which postoperative edema and hemorrhage originate. Methods. Cortical oxygen saturation (SaO 2 ) was measured in 52 patients by using microspectrophotometry in areas adjacent to AVMs before and after resection. The appearance of the former feeding arteries was categorized as normal (Group A); moderately stagnating (Group B); and excessively stagnating (Group C) on postoperative angiographic fastfilm series. Patients and SaO 2 values were pooled accordingly and compared using analysis of variance and Duncan tests (p 0.05). Angiographic stagnation times in former feeding arteries were correlated in a linear regression/correlation analysis with SaO 2 data (p 0.05). All values are given as the mean standard deviation. The average median postoperative SaO 2 in Group C (15 patients) was significantly higher than in Groups B (17 patients) and A (20 patients) (Group C, ; Group B, ; Group A, %SaO 2 ), as was the average postoperative increase in SaO 2 (Group C, ; Group B, ; Group A, %SaO 2 ). Angiographically confirmed stagnation times were also significantly longer in Group C than in Group B (Group C, ; Group B, seconds). A significant correlation/regression analysis showed a clear trend toward higher postoperative SaO 2 levels with increasing stagnation time. Conclusions. Stagnating flow in former feeding arteries does not cause cortical ischemia, but its presence on angiographic studies is usually indicative of hyperperfusion in the surrounding brain tissue after AVM resection. In the context of the pathophysiology of AVMs extrapolations made from angiographically visible shunt flow to blood flow in the surrounding brain tissue must be regarded with caution. KEY WORDS cerebral arteriovenous malformation stagnating flow cerebrovascular circulation cerebral oxygen saturation T HE term stagnating artery was coined by Hassler, et al., 10 in 1983 to describe a phenomenon observed on angiograms obtained in patients who had undergone removal of cerebral AVMs. It describes the slow washout of contrast material from the former feeding arteries, which thereby remain visible in the venous phase of the angiogram. This stagnant arterial flow can be visualized immediately after surgical or interventional obliteration of the AVM nidus and may last for more than 1 month after treatment. 11,17,18,26,31 It is known to occur in large AVMs in particular, because the sudden interruption of these high-flow shunt systems causes an immediate decrease in blood flow and an increase in pressure in the markedly dilated feeding arteries. 17,24,26,33 These arteries Abbreviations used in this paper: AVM = arteriovenous malformation; CBF = cerebral blood flow; DS = digital subtraction; MABP = mean arterial blood pressure; SaO 2 = arterial saturation of oxygen; SD = standard deviation. 36 mostly retain their larger than normal diameter in the postoperative period, for which structural abnormalities induced by persistent hemodynamic stress 30 and hitherto unknown factors 21 are thought to be responsible. The resultant very low blood flow velocity in these vessels, as evidenced by intraoperative Doppler ultrasonography, 11,24 is the pathophysiological correlate of the sluggish washout of contrast material. Stagnating arteries have always been seen in a somewhat loose context, with the occurrence of postoperative edema formation and hemorrhage (for example, normal perfusion pressure breakthrough) 29 by several authors. 10,11, 13,18,26,28,31 In 1993, however, a widely acknowledged study was published by Al-Rodhan, et al., 1 in which they proposed an alternative theory ( occlusive hyperemia theory) to explain postoperative edema and hemorrhage. Based on their retrospective review of routine postoperative imaging studies, they identified two possible causative pathophysiological mechanisms. According to them,

2 Stagnating flow and cerebral oxygen saturation in AVMs edema and hemorrhage are due to 1) obstruction of the venous outflow system of brain adjacent to the AVM, with subsequent passive hyperemia and engorgement; and 2) stagnant arterial flow in former AVM feeders and their parenchymal branches, with subsequent worsening of the existing hypoperfusion, ischemia,... It is primarily the latter hypothesis that we dispute, because we believe it to be an erroneous conclusion based on the misconception that visualization of former shunt flow on routine DS angiography allows valid assumptions to be made about CBF in the surrounding brain tissue. We therefore analyzed intraoperative cortical capillary SaO 2 data in conjunction with postoperative DS angiography findings that were derived from a prospective study of AVM pathophysiological features to provide evidence for our point of view. Clinical Material and Methods This study was approved by the local ethics review committee. All patients gave written consent for the experiments at least 24 hours before the operation. Measurements of Intracapillary SaO 2 Values of intracapillary SaO 2 were measured with a spectrophotometer (Erlangen Microlightguide [model EMPHO II]; Bodenseewerk Gerätetechnik GmbH, Überlingen, Germany), which was introduced in and has previously been described in the context of AVM pathophysiological studies. 15 It was designed for fast, diffuse remission spectrophotometry by using flexible microlightguides in small tissue volumes of moving organs in situ. Light in the visible domain illuminates tissue via the illuminating fiber, and backscattered light is transmitted via six detecting fibers ([Ø 70 m] arranged in a hexagonal pattern around the illuminating fiber) to a rotating bandpass interference filter disc. This serves as a monochromating unit in the spectral range of 502 to 628 nm in 2-nm steps. The spectra of 64 wavelengths per rotation are transmitted to a photomultiplier, an analog digital converter, and finally to a computer, in which one SaO 2 value per spectrum is calculated. The SaO 2 values obtained reliably indicate O 2 transport to tissue 9,16 and, indirectly, nutritive capillary flow. 22 The high temporal (100 spectra/second) and spatial ( m) resolution permit easy scanning of superficial cortical capillaries by moving the lightguide above the brain surface. Study Groups and Protocol Fifty-two patients (23 female and 29 male, mean age 34 years, range 5 66 years) harboring cerebral AVMs with Spetzler Martin 27 grades of I (nine patients), II (19 patients), III (18 patients), and IV (six patients) were included in the study. All patients underwent elective microsurgery for complete resection of the AVMs. As described previously, 15 SaO 2 distributions were measured in small (approximately 5-mm 2 ) areas (approximately SaO 2 values per area and measurement) of the surrounding cortex of the AVM before and after the resection at distances of 2 to 4 cm from the nidus. All areas were numbered and photographically documented at the highest magnification of the operating microscope for exact postoperative relocation and allocation to angioarchitecture. Areas in which surgical trauma was suspected as a result of microscopic inspection or for other reasons (for example, too close to resection margin) were excluded from postoperative measurements. Postoperative fast-film DS angiography series were evaluated by the neuroradiologist, who was blinded to SaO 2 data. The angiographic appearance of former feeding arteries was categorized in one of three groups: A) normal; B) stagnating into the capillary/early venous phase; or C) stagnating into the late venous phase. Patients were accordingly subdivided into these three groups. Circulation times of all stagnating arteries were documented in Groups B and C. To correct for interindividual differences in global circulation times and contrast-injection velocity, the length of stagnation was calculated as the time of disappearance of the stagnating artery (in seconds) minus the time of disappearance of normal arteries (in seconds) on individual angiograms. This calculated value was defined as the stagnation time. For all operations general anesthesia was induced intravenously with 1.5 mg/kg propofol (maintained with 5 10 mg/kg/hr), 15 g/kg alfentanil (maintained with mg/kg/hr), and 0.1 mg/kg vecuronium (maintained with g/kg/hr), with patients receiving 40% O 2 and 60% N 2. The MABP and heart rate were continuously monitored via a radial arterial line. Arterial blood samples (PaO 2, PaCO 2, and ph) and venous blood samples (hematocrit) were taken at times of SaO 2 measurements. Data Analysis The SaO 2 values were pooled according to groups and displayed as frequency histograms. The medians (%SaO 2 ) for every patient before and after excision of the AVM, as well as their differences, were calculated. Stagnation times, SaO 2 data, and nidus size (defined as the largest diameter on preoperative magnetic resonance images) were compared among groups. The occurrence of hyperemic complications (that is, breakthrough) was documented. Identification of breakthrough was performed according to clinical and radiological criteria by the senior author (J.S.) and neuroradiologist (H.U.), both of whom were blinded to SaO 2 data. The analysis of variance and Duncan tests for correction of multiple comparisons were used for statistical analysis, with the level of significance set at p Linear regression/correlation analyses (p 0.05) of SaO 2 data on stagnation times were performed for Groups B and C. All values are expressed as the mean SD. Results Physiological variables showed no significant differences among groups and times of measurements (Table 1). In 20 patients no abnormalities were demonstrated on postoperative DS angiography in terms of former feeding arteries (Group A), whereas stagnating arterial flow was documented in 32 cases. The washout of contrast material took place 17 times in the capillary/early venous phase of the angiogram (Group B), and on 15 angiographic studies stagnating arteries remained visible in the late venous phase (Group C). The total time stagnating arteries re- 37

3 B. Meyer, et al. TABLE 1 Data from arterial blood gas analyses, venous hematocrits, and MABPs obtained during measurements of cortical SaO 2 * Group A Group B Group C Variable Pre Post Pre Post Pre Post no. of patients hematocrit (vol%) PaCO 2 (mm Hg) ph PaO 2 (mm Hg) MABP (mm Hg) * Measurements were obtained before (pre) and after (post) resection of AVMs. Values are given as the means SD. See Study Groups and Protocol for explanation of the group classifications. Abbreviations: PaCO 2 = partial pressure of carbon dioxide; PaO 2 = partial pressure of O 2. mained visible on DS angiography (stagnating artery circulation time) was second in Group B and seconds in Group C (p 0.05). Circulation times in arteries that formerly had not participated in AVM shunt flow (arterial circulation time) did not differ significantly (Group B, seconds; Group C, seconds). Stagnating arteries were thus observed for a significantly longer time on postoperative DS angiography (stagnation time seconds compared with 1.3 TABLE 2 Mean values of calculated parameters for pooled SaO 2 data in cortex adjacent to AVM, stagnation times of former feeding arteries on postoperative angiography, and preoperative nidus size* Group Variable A B C no. of patients total SaO 2 values (no.) preop postop median (%SaO 2 ) preop postop postop increase (%SaO 2 ) arterial circulation time NA (secs) stagnating artery circula- NA tion time (secs) stagnation time (secs) NA nidus size preop (cm) * Medians for every patient were calculated before (preop) and after (postop) resection of AVMs; the postoperative increase in SaO 2 describes their difference. Arterial circulation time denotes the time in which unaffected arteries are observed for the last time on postoperative angiograms, and stagnating artery circulation the time in which former feeding arteries are observed for the last time. Stagnation time is thus equivalent to the time in which former feeding arteries are visualized longer than normal arteries on postoperative angiograms. Nidus size is defined as the largest diameter on preoperative magnetic resonance images. Significantly different (p 0.05) compared with Groups A and B. Values are given as the mean SD. Significantly different compared with Group B. Values are given as the mean SD. 0.6 seconds) in Group C than in Group B (Table 2 and Fig. 1). Comparisons of pooled cortical capillary SaO 2 data as histograms and individual medians before and after resection of AVMs showed no significant differences between patients with normal appearance of former feeding arteries (Group A, median pretreatment %SaO 2 ; median posttreatment %SaO 2 ) and those with moderately stagnant arterial flow (Group B, median pretreatment %SaO 2 ; median posttreatment %SaO 2 ). Postoperative values in Group C differed significantly from both groups (median pretreatment %SaO 2 ; median posttreatment %SaO 2 ). The relative increase of oxygenation in the brain tissue irrigated by branches of extensively stagnating arteries (Group C, %SaO 2 ) was significantly greater than in brain tissue irrigated by branches of moderately stagnating arteries (Group B, %SaO 2 ) or of angiographically normal former feeding arteries (Group A, %SaO 2 ) (Table 2 and Fig. 2). A significant linear regression and correlation was calculated for postoperative median SaO 2 and increases in oxygenation on stagnation times for patients in Groups B and C. We demonstrated a clear tendency for higher rates of postoperative cortical oxygenation with increasing stagnation time. The strength of the correlation is moderate, with coefficients of correlation given as r = 0.63 and r = 0.51, respectively (Fig. 3). Of five hyperemic complications (breakthrough), four occurred in patients in Group C and one in a patient in Group B. The nidus size in Group C ( cm) differed significantly from Groups A and B (3 0.8 cm and cm, respectively; Table 2). Discussion An extensive discussion of potential methodological drawbacks of the applied microspectrophotometric technique, as well as the possibilities and limitations of drawing conclusions from the acquired SaO 2 data on nutritive capillary flow, has been published previously. 15,22 Cerebral O 2 metabolism was assumed to be constant during these experiments, with changes in SaO 2 reflecting primarily changes in regional CBF. 38

4 Stagnating flow and cerebral oxygen saturation in AVMs FIG. 1. Angiograms obtained before (upper left) and after (upper right, lower left, and lower right) resection of a Spetzler Martin Grade IV left parietal AVM. On the postoperative films, stagnation of the two former main feeding arteries from the anterior and middle cerebral artery can be observed. Both feeding vessels remain dilated and prominent in the early arterial phase of the angiogram (upper right). They are still visible in the late arterial phase (lower left), which is the last time (4.2 seconds in this case) normal arteries are seen (arterial circulation time). Complete washout of contrast material does not occur before the late venous phase (lower right). This timespan (14.1 seconds in this case) was named stagnating artery circulation time, and the patient was classified in Group C. The interval between those times was referred to as stagnation time; it is 9.9 seconds in this example. A so-called perinidal hypervascular network 31 can also be appreciated in the late venous phase (see Discussion). Stagnating Arteries and Breakthrough Our results confirm several points with regard to stagnating arteries after AVM removal. Stagnation of flow in former feeding arteries is a common phenomenon; 17,34 in 61% of our patients a prolonged transit time for contrast material was demonstrated in former AVM feeding vessels, and in 29% of all cases the washout occurred in the late venous phase, which is the equivalent of the original definition for stagnating arteries. 10 For the latter group, we were able to confirm the notion that stagnant arterial flow tends to occur in large AVMs, 10,11,17,19,28,34 because patients in this group harbored significantly larger AVMs than the rest. Four (27%) of 15 patients in Group C, one (6%) of 17 in Group B, and none of 20 in Group A suffered a postoperative breakthrough. This seems to corroborate the impression that stagnating arteries are somehow associated with otherwise unexplained formation of postoperative edema and hemorrhage. 10,11,13,17,18,31 The simultaneous occurrence of breakthrough and stagnating arteries may be only coincidental, however, simply because the frequency of both is higher in large AVMs. We do not agree with the assumption that stagnating arteries are a causative pathophysiological mechanism for postoperative edema and hemorrhage, 1 for reasons that we will enumerate. 39

5 B. Meyer, et al. FIG. 2. Frequency histograms showing a comparison of SaO 2 (%SO2) distributions in the surrounding cortex after AVM resection. An insignificant rightward shift of the SaO 2 distribution in the cortex of patients with normal-appearing former feeding arteries on postoperative DS angiography (Group A, 20 patients) can be seen, compared with the distribution in patients with moderately stagnating arterial flow in those vessels (Group B, 17 patients). The histogram of SaO 2 values obtained in patients with extensive stagnation of flow in former feeding arteries (Group C, 15 patients), however, reveals a significantly higher level of postoperative cortical oxygenation. Stagnant Arterial Flow and Cerebral Perfusion The hypothesis that stagnant arterial flow in former AVM feeders and their parenchymal branches..., as visualized on routine postoperative DS angiography, leads to hypoperfusion and ischemia in the surrounding brain tissue contains some misconceptions. First, stagnating flow is primarily visualized in former feeding arteries but not in their small branches. The opposite seems to be true for the small branches, which is described in detail by Takemae, et al., 31 or Solomon, et al., 25 and is illustrated by our example in Fig. 1. On early postoperative DS angiography a cluster of small vessels can often be observed next to stagnating arteries, which is interpreted as perinidal hyperemia 25 and a state of vascular overload. 31 Second, Al-Rodhan, et al., 1 assume that the slow transit time for a vascular tracer in such vessels necessarily reflects a linear reduction of blood flow within them, to the extent that it falls below the ischemic threshold in smallcaliber branches supplying the surrounding parenchyma. Slow washout of contrast material, however, primarily reflects a reduction of flow velocity, which has been proven 11,24 and is a function of blood flow and vascular volume. 7 Naturally, flow itself within these vessels also decreases, 17,33 because the former input channel of a high flow/low resistance system for example, the nidus is transformed into one of a low flow/high resistance system 26 for example, the surrounding capillary bed with a point of stagnation at its distal end. Blood flow velocities close to zero within stagnating arteries, which are not seen in their brain-supplying branches, 11 are therefore due to reduced flow in large-diameter vessels with distal flow reversal/perturbations. Our own results provide evidence that blood flow in the surrounding brain tissue does not decrease, when stagnating arterial flow is observed on DS angiography after resection of AVMs. Actually, the opposite is indicated. We were able to show that postoperative brain tissue oxygenation levels are highest in patients with excessive angiographically confirmed stagnation of flow. We consider this increase in capillary SaO 2 to be primarily flow-related, with the assumption that the metabolism of the brain tissue examined was constant and comparable. With a uniform anesthesiological regimen and depth of the state of anesthesia, this assumption is most probably met, although the exact metabolic conditions are unknown. Increased perfusion pressure, therefore, always transmits sufficient blood flow into the surrounding capillary bed. In our opinion this reperfusion mostly exceeds the demand, which may sometimes lead to a reperfusion injury (breakthrough) if, for example, metabolic feedback is lacking. 15 We therefore agree that edema and hemorrhage after AVM resection is a hyperemic injury to the brain, but it is primarily caused by an unlimited arterial inflow into formerly hypoxic/ischemic areas of the brain, which we have shown in a previous report. 15 Preoperatively, focal areas of low-flow anoxia exist predominantly in the cor- 40

6 Stagnating flow and cerebral oxygen saturation in AVMs FIG. 3. Graphs showing linear regression analyses of the postoperative median SaO 2 (SO2) (upper) and postoperative increase in SaO 2 (lower) in relation to stagnation times in every patient in Groups B and C; a significant (p 0.05) trend toward higher postoperative oxygenation levels with increasing stagnation of flow in former feeding arteries is demonstrated. The coefficients of correlations were calculated as r = 0.63 (upper) and r = 0.51 (lower), which indicates a moderate strength of this dependency. tex of those patients who suffer from postoperative breakthrough complications. We cannot argue directly against the first part of the scenario that is, that harmful consequences are induced by spontaneous occlusion of former draining veins. Yet, as the experimental literature shows, occlusion of cortical veins leads to an increase in cerebral blood volume (that is, venous congestion) and a decrease in regional CBF and capillary SaO 2. Edema and hemorrhage may sometimes follow, but concomitant arterial ischemia seems to be a prerequisite. 6,8,22,23,32 Whether this chain of events happens at a later stage after the removal of cerebral AVMs remains speculative. We have provided evidence, however, that stagnant arterial flow in former feeding arteries does not cause cortical ischemia, which provides the basis for this pathophysiological mechanism. Retrograde thrombosis of former feeding arteries that is associated with hypoperfusion and ischemia has been described as a rare complication after AVM removal, mainly by Miyasaka, et al., 18 although we think that true thrombosis of feeding arteries is an extremely unusual event. Most of the angiographically observed thromboses il- 41

7 B. Meyer, et al. lustrated in their article could also be interpreted as the sausage-string phenomena, which are described later. Interpretation of Postoperative DS Angiography These results show that assumptions about CBF and/ or cerebral metabolism derived from findings on angiographic studies can be misleading and are no more useful than a clinical guideline. A similar observation has been published recently with regard to lack of correlation between angiographic findings and metabolic data in the context of occlusive carotid artery disease. 3 The reason for this has been described earlier. First, angiographic circulation time is difficult to measure even on rapid series, and second, it reflects changes in both CBF and vascular volume, as discussed earlier. 7 Without these caveats, seemingly obvious assumptions at first glance may be diametrically opposed to the real situation. The data in our study show a strong trend toward higher postoperative reperfusion with increasing stagnation time, which is the exact opposite of the conclusion reached by Al-Rodhan, et al. 1 This is most likely caused by the association of large AVMs with excessively stagnating flow in former feeding arteries. The discussion about stagnating arteries in the context of AVM resembles the one about the pathogenesis of acute hypertensive encephalopathy. It has become clear that the cerebral edema and hemorrhage 12 associated with this entity are the consequences of massive tissue hyperperfusion caused by acutely elevated cerebral perfusion pressure. 4,14 Before this determination was made it had been postulated for decades that the concomitant changes in pial artery caliber patterns of alternating constrictions and dilations (sausage-string phenomenon) constituted vasospasm, which led to tissue hypoperfusion as the starting point of edema and hemorrhage. 2 The aforementioned studies, 4,14 however, have shown that these arterial changes are indeed remnants of autoregulatory constrictions. Vasospastic, irregular segments of stagnating arteries have also been described in all reports, 17,18,20,25,31 which is in keeping with our own experience. One could therefore just as well hypothesize that after AVM removal the dissociation of flow in large and small cerebral vessels constitutes a local equivalent to the abovementioned global situation. Conclusions Visualization of stagnating flow in former feeding arteries on angiographic studies obtained after surgical resection of cerebral AVMs does not indicate hypoperfusion or ischemia in the surrounding brain tissue, but rather hyperperfusion. In the context of the pathophysiological features of AVMs, extrapolations from angiographically visible shunt flow to ascertain CBF in the surrounding brain tissue must be regarded with caution. References 1. Al-Rodhan NRF, Sundt TM Jr, Piepgras DG, et al: Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. J Neurosurg 78: , Byrom FB: Hypertensive encephalopathy: a warning. Lancet 2: 99, 1973 (Letter) 3. 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8 Stagnating flow and cerebral oxygen saturation in AVMs 24. Nornes H, Grip A: Hemodynamic aspects of cerebral arteriovenous malformations. J Neurosurg 53: , Solomon RA, Connolly ES Jr, Prestigiacomo CJ, et al: Management of residual dysplastic vessels after cerebral arteriovenous malformation resection: implications for postoperative angiography. Neurosurgery 46: , Sorimachi T, Takeuchi S, Koike T, et al: Blood pressure monitoring in feeding arteries of cerebral arteriovenous malformations during embolization: a preventive role in hemodynamic complications. Neurosurgery 37: , Spetzler RF, Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65: , Spetzler RF, Martin NA, Carter LP, et al: Surgical management of large AVM s by staged embolization and operative excision. J Neurosurg 67:17 28, Spetzler RF, Wilson CB, Weinstein P, et al: Normal perfusion pressure breakthrough theory. Clin Neurosurg 25: , Stehbens WE: Blood vessel changes in chronic experimental arteriovenous fistulas. Surg Gynecol Obstet 127: , Takemae T, Kobayashi S, Sugita K: Perinidal hypervascular network on immediate postoperative angiogram after removal of large arteriovenous malformations located distant from the arterial circle of Willis. Neurosurgery 33: , Ungersböck K, Heimann A, Kempski O: Cerebral blood flow alterations in a rat model of cerebral sinus thrombosis. Stroke 24: , Wasserman BA, Lin W, Tarr RW, et al: Cerebral arteriovenous malformations: flow quantitation by means of two-dimensional cardiac-gated phase-contrast MR imaging. Radiology 194: , Wilson CB, Hieshima G: Occlusive hyperemia: a new way to think about an old problem. J Neurosurg 78: , 1993 Manuscript received July 6, Accepted in final form January 12, Address reprint requests to: Bernhard Meyer, M.D., Department of Neurosurgery, University of Bonn, Sigmund Freud Strasse 25, Bonn, Germany. bmey@ukb.uni-bonn.de. 43