INJURED MOUSE PIAL ARTERIOLES/Rosenblum and El-Sabban 39

The free radical pathology and the microcirculation in the ma­jor central nervous system disorders. Acta Physiol Scand Suppl 492, pp 91-120, 1980

7. Meyer JS, Fukuuchi Y, Shimazu K, Ohuchi T, Ericsson AD: Effect of intravenous infusion of glycerol on hemispheric blood flow and metabolism in patients with acute cerebral infarction. Stroke 3: 168-180, 1972

8. Meyer JS, Charney JZ, Rivera VM, Mathew NT: Treatment with glycerol of cerebral edema due to acute cerebral infarc­tion. Lancet 2: 993-997, 1971

9. Rosenblum WI, El-Sabban F: Platelet aggregation in the cerebral microcirculation. Effect of aspirin and other agents. Circ Res 40: 320-328, 1977

10. Rosenblum WI, El-Sabban F, Ellis EF: Aspirin and indo-methacin enhance platelet aggregation in mouse mesenteric arterioles. Am J Physiol 239: H220-H226, 1980

11. Rosenblum WI: Fluorescence induced in platelet aggregates as a guide to luminal contours in the presence of platelet aggrega­tion. Microvasc Res 15: 103-106, 1978

12. Wayland H, Johnson PC: Erythrocyte velocity measurement in microvessels by a two slit photometric method. J Appl Physiol 22: 333-337, 1967

13. Baker M, Wayland H: On-line volumetric flow rate and velocity profile measurement for blood in microvessels. Microvasc Res 7: 131-143, 1974

14. Tompkins WR, Monti R, Intaglietta M: Velocity measure­ments by self tracking correlator. Res Sci Inst 45: 647-649, 1974

15. Lipowsky H, Zweifach BW: Application of the "two-slit" photometric technique to measurement of microvascular volumetric flow rates. Microvasc Res 15: 93-101, 1978

16. Rosenblum WI, El-Sabban F: Enhancement of platelet aggregation by tranylcypromine in mouse cerebral micro-

KNOWLEDGE of the pathogenesis of occlusions of the intracranial arteries would be important to ther­apy. Despite several studies of this problem it cannot be decided whether a particular occlusion has its ori­gin in a local thrombus or in an embolus. Recently the theory of the embolic origin of intracranial vascular occlusions has been favored.1'2 However, primary evi­dence for it is still lacking.

There are considerable, regular differences in the incidence of occlusions among the individual intra­cranial arteries. These differences are regarded by

From the Department of Neurosurgery, University of Pecs Medical School, Ifjusag-utja 31, 7624 Pecs, Hungary.

Mailing of Proofs and Reprint Requests to F.T. Merei, M.D. Supported by the Scientific Research Council, Ministry of

Health, Hungary (3-21-0301-04-0/M)

vessels. Circ Res 43: 238-241, 1978 17. Ashwood-Smith MJ: Current concepts concerning radio­

protective and cryoprotective properties of dimethyl sulfoxide in cellular systems. Ann NY Acad Sci 243: 246-256, 1975

18. Kovacs IB, Tigyi-Sebes A, Trombitas K, Gorog P: Evans blue, an ideal energy absorbing material to produce intravascular microinjury by He-Ne gas laser. Microvasc Res 10: 107-124, 1975

19. Kontos HA, Wei EP, Povlishock JT, Dietrich WD, Magiera CJ, Ellis EF: Cerebral arteriolar damage by arachidonic acid and prostaglandin G2, Science 209: 1242-1245, 1980

20. Kontos HA, Wei EP, Dietrich WD, Navari RM, Povlishock JT, Ghatak NR, Ellis EF, Patterson JL Jr: Mechanism of cerebral arteriolar abnormalities after acute hypertension. Am J Physiol 240: H511-H527, 1981

21. Rosenblum WI, El-Sabban F: Use of AHR-5850 and 6293 to distinguish the effect of anti-platelet aggregating drug proper­ties from the effect of anti-inflammatory properties, on an in vivo model of platelet aggregation. Microvasc Res 17:309-313, 1979

22. Smith JB: The prostanoids in hemostasis and thrombosis. A review. Am J Path 99: 743-804, 1980

23. Cook HW, Lands WEM: Mechanism for suppression of cellular biosynthesis of prostaglandins. Nature 260: 632, 1976

24. Cook HW, Lands WEM: Evidence for an activating factor formed during prostaglandin biosynthesis. Biochem Biophys Res Comm 65: 464-471, 1975

25. Rosenblum WI, El-Sabban F, Ellis EF: Aspirin and indo-methacin, nonsteroidal antiinflammatory agents alter the responses to microvascular injury in brain and mesentery. Microvasc Res 20: 374-378, 1980

26. Larsson O, Marinovich N, Barber K: Double blind trial of glycerol therapy in early stroke. Lancet 1: 832-834, 1976

several workers as a proof of local thromboses because emboli might be expected to have an irregular distribution.3 Others consider possible a certain regu­larity in the distribution of occlusions even in the case of emboli, because of the laminar blood flow in the cerebral arteries.1,4 Our balloon catheterizations seem to be suitable for checking the probable course of em­boli in the main human intracranial arteries.

Materials and Methods A total of 960 angiographies performed in patients

having had ischemic events in the carotid territory were analyzed in order to determine the frequency of occlusions of intracranial arteries. One hundred and forty-two of the 960 patients had TIAs, while the others had strokes of varying severity.

In 221 of the 960 angiograms we found intracranial

Balloon Catheter as a Model of Cerebral Emboli in Humans GY. GACS, M.D., F. T. MSREI, M.D. AND M. BODOSI, M.D.

SUMMARY A striking similarity has been found between the distribution of occlusions in various cerebral arteries and the statistical regularity of the pathways of balloon catheters drifting freely in the blood stream. Based on the assumption that the course of a balloon is determined by the same hydrodynamic laws as that of an embolus of similar size, it is concluded that the majority of occlusions of the cerebral arteries are of em­bolic origin. Emboli, then, might also be an explanation for most of the TIAs.

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40 STROKE VOL 13, No 1, JANUARY-FEBRUARY 1982

occlusions. The indication for angiography was TIA in 49 patients and stroke in 172.

The balloon catheterization was performed as de­scribed in detail previously by Gacs.5 The most impor­tant features of this technique are as follows: A thin soft polyethylene catheter /0.45 mm in outside diam­eter/ having a latex balloon /0.6-0.8 mm in outside diameter/ with a calibrated leak in its tip is intro­duced into the carotid artery. The length of the balloon is between 4-5 mm. The slightly inflated balloon /0.05-0.2 ml in volume/ is carried along by the blood flow, pulling the catheter after it. When the catheter is allowed to move freely, the balloon can be regarded as an embolus of the same size. Conse­quently, its most preferred pathway if there is any, will presumably be similar to that of an embolus.

The spontaneous pathway of the balloon was fol­lowed in 42 cases. The site where the "balloon em­bolus" stopped was checked by injecting a radio-opaque dye through the calibrated leak in the balloon: superselective angiography (fig. 1).

All 42 patients who were selected for balloon cath-

TABLE 1 Distribution of Intracranial Artery Occlusions

Site of occlusion

Anterior cerebral artery

Middle cerebral artery

Main trunk

Main branches just beyond trifurcation

Orbitofrontal artery

Operculofrontal artery

Rolandic artery

Parietal arteries

Angular artery

Temporal arteries

Total

Number of pat ients

64

38

2

10

13

29

39

11

15

206

221

% 6.8

93.2

29.0

17.2

0.9

4.5

6.0

13.1

17.6

5.0

eterization had cerebrovascular disease and sub­sequently underwent an EC/IC bypass operation. During the operation fluorescein angiography was used to localize the ischemic area and to study the

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FIGURE 1. Superselective angiogram of a trapped balloon embolus. The radio-opaque dye was injected through a calibrated leak in the balloon. The balloon is situated in a branch of the anterior cerebral artery fa and b), and in branches of the middle cerebral artery (c and d).

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BALLOON CATHETER/Gacy et al. 41

blood flow from the direction of the intact to the ische­mic hemisphere via the anterior communicating artery. To achieve this the balloon catheter was intro­duced into the internal carotid artery opposite to the stenotic or occluded side. No angiographically visible alteration of these vessels was found.

Drifting of the balloon with the blood flow is influ­enced only by the degree of its inflation and not by the curves in the vessels or the catheter, presuming that it can freely be carried along by the balloon. The latter was carefully observed on the X-ray image intensifier in all patients. Thus the results discussed in the pres­ent paper should be regarded as byproducts of these procedures.

Results The distribution of the 221 occlusions among the in­

tracranial arteries is shown in table 1. A 1/14 ratio was found between the occlusions of

the anterior and the middle cerebral arteries. The most frequently affected cortical branches are the angular and the parietal branches of the middle cere­bral artery.

The distribution of the "balloon emboli" in the in­tracranial arteries is shown in table 2. The balloons drifting freely in the blood flow "chose" the middle cerebral artery in 39 out of the 42 cases, but got trapped in the anterior cerebral artery in only 3 of them. Thus, the ratio between "balloon-embolism" of the anterior and that of the middle cerebral arteries

TABLE 2 Distribution of the Spontaneous Pathway of the Balloon

Localization of the "balloon-embolus" Number of

Anterior cerebral artery Middle cerebral artery

Main trunk Main branches just

beyond trifurcation Orbitofrontal artery Operculofrontal artery Rolandic artery Parietal arteries Angular artery Posterior temporal artery

Total

3

39

11

2 3 5 9 1

7.1 92.9 19.0

26.2

4.8 7.1

11.9 21.4 2.4

42

was also 1/14. The more distal landing points of the balloons in the middle cerebral artery were in its main trunk (8), the suprasylvian trunk (30), and the tem­poral arteries (1).

Discussion We have long known that occlusions of the small in­

tracranial arteries play a much more important role in the genesis of cerebral infarction than previously pre­sumed.7, "•9 Angiograms made shortly after the onset

FIGURE 2. Schematic presentation of the dis­tribution of the spontaneous occlusions and the "balloon emboli." Lower numbers:percentage distribution of the spontaneous occlusions; up­per numbers: percentage of the balloon-emboli. The small differences in distribution between the sites of lodgement of the balloon and those of the emboli can be explained by the fact that while the size of the balloon was rather con­stant, those of the emboli were not. Major em­boli were lodged in the main trunk, whereas smaller bits reached more distal branches of the middle cerebral artery. OBFA = orbitofrontal artery; OPFA = operculofrontal artery; CSA = central sulcus artery; PAA = parietal arter­ies; ANGA = angular artery; TAA = tem­poral arteries.

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42 S T R O K E V O L 13, N o 1, JANUARY-FEBRUARY 1982

of the symptoms revealed cortical branch occlusions also in a considerable number of TIA patients.10

Pathological and angiographical studies seldom permit definite distinction between thrombi and em­boli. Old, organized emboli and thrombi are indis­tinguishable under the microscope, and the angio­graphic appearance of occlusions seldom offers data for a decision. The frequency of embolism used to be underestimated, although Chiari11 drew attention to the importance of mural internal carotid thrombosis in cerebral embolism as early as 1905. After Fisher,12

Gunning,13 et al., it was McBrien et al.14 and others who stressed the view that primary thrombotic occlu­sion of the intracranial arteries represents a rarity.16,16

At the same time other workers17 found a much greater frequency for local thrombi than for emboli.

The question of relative frequency could be studied by comparing the incidence of spontaneous intra­cranial vascular occlusions with that of "balloon occlusions" of the same arteries. Our findings (table 2) indicate that there is a predictable regularity in the distribution of the paths taken by the balloon, probably owing to the laminar nature of blood flow. Consequently, other particles, i.e. emboli of the same size, will drift into the various cerebral arteries with the same predictability. There is a similarity between the incidence of spontaneous vascular occlusions and that of balloon emboli (fig. 2). Bearing these observa­tions in mind, one may conclude that the majority of intracranial vascular occlusions are of embolic origin.

Our experience with balloon catheters offers a good explanation both for the relatively low rate of anterior cerebral artery occlusions and for the differences in the incidence of cortical branch occlusions of the mid­dle cerebral artery. Furthermore, the laminar flow of emboli explains the puzzling uniformity of con­secutive ischemic events.3 Finally, while some work­ers regard the rarity of transient symptoms of the anterior cerebral and temporal regions (e.g., jargon aphasia) as a strong argument against embolism,3 this fact appears to have its explanation in the relative "safety" of these regions from the balloons and em­boli.

Although the primary goal of our investigations was to draw a comparison between balloon emboli and

angiographically proved occlusions of embolic origin, some conclusions can be drawn from them which suggest transient ischemic attacks might be regarded as of embolic origin.

References 1. Russel RWR: Transient cerebral ischemia. In: Cerebral

Arterial Disease. Edit. R.W.R. Russel. Churchill and Living­ston, Edinburgh-London-New York, 1976. pp 125-145.

2. Barnett HJM: Pathogenesis of transient ischemic attacks. In: Cerebrovascular Diseases. Edit. P. Scheinberg. Raven Press, New York, 1976. pp 1-21

3. Fisher CM: Discussion at the Tenth Princeton Conference. In Cerebrovascular Diseases, P. Scheinberg (ed), Raven Press, New York, 1976, pp 43-57

4. Malcolm AD, Roach MR: Flow disturbances at the apex and lateral angles of a variety of bifurcation models and their role in development and manifestations of arterial disease. Stroke 10: 335-343, 1979

5. Gacs Gy: Catheterization and superselective angiography of the cerebral vessels. Neuroradiol 12: 237-241, 1977

6. Merei FT, Bodosi M, Gacs Gy: Fluorescein angiography in the surgical treatment of cerebral ischemic lesions. Surgical Neurol 11: 269-276, 1979

7. Winter WJ, Gyori E: Pathogenesis of small cerebral infacts. Arch Path 69: 224-234, 1960

8. Ring BA: Middle cerebral artery: anatomical and radiographic study. Acta Radiol 57: 289-300, 1962

9. Ring BA: Diagnosis of embolic occlusions of smaller branches of the intracerebral arteries. Am J Roentgenol 97: 575-582, 1966

10. Giles Gy, Rihmer A, Bodosi M: Occlusions of the leptomenin-geal branches of the middle cerebral artery. Ideggydgy Szemle 29: 108-118, 1976 (Hung)

11. Chiari H: Ober das Verhalten des Teilungswinkels der Carotis communis be: der Endarteritis chronica deformans. Zbl allg Path Anat 16: 326-330, 1906

12. Fisher CM: Observation of the fundus oculi in transient monocular blindness. Neurology (Minneap) 9: 333-347, 1959

13. Gunning AJ, Pickering GW, Robb-Smith AHT, Russel RWR: Mural thrombosis of the internal carotid artery and subsequent embolism. Quart J Med 33: 155-195, 1964

14. McBrien DJ, Bradley RD, Ashton N: The nature of retinal em-bo li in stenosis of the internal carotid artery. Lancet 1:697-699, 1963

15. Crawford R, Crompton MR: The pathology of strokes. In The Management of Cerebrovascular Disease. Marshall J (ed), Churchill-Livingston, London, 1968, pp 34-60

16. Lhermitte F, Gautier JC, Desousne C: Nature of occlusion of the middle cerebral artery. Neurology (Minneap) 20: 82-88, 1970

17. Moossy J: Cerebral infarction and intracranial arterial throm­bosis. Transact of the Am Neurol Assoc 90: 113-115, 1965

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G Gács, F T Mérei and M BodosiBalloon catheter as a model of cerebral emboli in humans.

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 1982 American Heart Association, Inc. All rights reserved.

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