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Epicerebral Angiography by Fluorescein during Craniotomy*
471
Epicerebral Angiography by Fluorescein durin g Craniotomy * WILLIAM FEINDEL, CHARLES P. HODGE AND Y. LUCAS YAMAMOTO Cone Laboratory for Neurosurgical Research, Montreal Neurological Institute and McGill University, Montreal (Canada)
In previous reports we have described the use of radio-activeisotopes and Coomassie Blue dye injected by internal carotid catheter for analysis of the regional blood flow in the epicerebral circulation (the pial arteries and veins and the cortical capillary bed) during craniotomyl. This method allows for the comparison of quantitative radioisotopic blood flow curves directly with the anatomical pattern of the normal and abnormal vasculature on the surgically exposed brain. This approach has provided information on changes in blood flow in angiomas and adjacent cortex before and after obliteration of arterial feeders, or after arterial manipulation during clipping of aneurysms, and on abnormal flow rates in tumours with arterio-venous shunts2. With Coomassie Blue, a highly coloured non-toxic dye (sodium anazolene) and rapid serial stroboscopic colour photography the anatomical patterns of flow in pial arteries and veins and in the cortical capillary bed can be displayed and analysed. It should be emphasized that this direct comparison of the anatomy and rheology of the cerebral circulation directly from the surface of the brain offers many advantages over the technique of external monitoring by radio-isotopes of cerebral blood flow, where the details of the cerebral microcirculation have not been available. We now wish to describe the technique of fluorescein angiography as an additional means of examining the surface of the brain during operation. Details of the method were developed during a study of experimental cerebral ischaemia in cat and monkey brains3.4. In the operating room 2 ml of 1 % sodium fluorescein are rapidly injected into an internal carotid catheter. The passage of the dye through the vasculature of the exposed brain is recorded on serial photographs taken at intervals of 0.40 sec by a Nikon camera with motor-driven film changer. The shutter is synchronized with the discharge of a rapid re-charging stroboscopic light. A Wratten 47 colour filter was used over the light and a Wratten 58 over the camera lens for Tri-X film to obtain black and white photographs. Using high-speed Ektachrome film (daylight), the camera filter was changed to Wratten 29 with a 2-B ultra-violet absorbing filter and the film processed as Ektacolor to give an enhanced contrast and a speed of ASA 1200. The timing of the interval between photographs was measured to within 0.02 sec
* This work was supported by thecone Memorial Fund and the Medical Research Council of Canada. References p . 477
472
w. F E I N D E L et al.
by recording from a cadmium photo-cell placed near the strobe light. Thus the velocity of flow in individual vessels could be calculated from the serial photographs. The most important feature of fluorescence angiography is the display of the small pial arteries and veins and the cortical capillary bed, all of which appear in high contrast and in great detail. These are vessels of a size which are not visible on standard X-ray angiography, and the additional vasculature seen on the fluorescence photographs and on direct observation of the brain is often remarkable. The arterial and venous vessels stand out distinctly during their separate phases. Because of the dense filling of the capillary bed of the cortex the “water-shed’’ of the major arterial territories is clearly defined. The dynamics of central and mural laminar flow appear in detail, particularly in larger veins. In cerebral tumours, the fine blood vessels in the tumour bed show up earlier than the normal vascular bed and remain filled later than the normal venous phase, so that the tumour stands out with considerable prominence from the surrounding normal tissue. Shunting of the fluorescein from arteries to veins is readily seen in some tumours, and the velocity of flow in different draining veins can be distinguished.Areas of ischaemia are well demarcated by absence of fluorescence, while areas of damage may retain the dye beyond the normal circulation time. Such areas may escape detection on X-ray angiography. Two examples of fluorescein epicerebral angiograms in brain tumours taken from our series will serve to illustrate some of these points.
Fig. la. X-ray angiogram,arterialphaseshowingslight tumour blushintheparietalregion. Patient J. J.
EPICEREBRAL ANGIOGRAPHY
473
Fig. lb. Fluorescein angiogram, arterial phase from exposed brain. Note intensity ofturnourblushand filling of small arterial vessels. Patient J. J.
In the first example, a patient with carcinoma of the colon who began to have dysphasia, the X-ray film in the arterial phase showed a definite though scanty tumour blush in the left parietal region (Fig. la) which persisted in the venous phase (Fig. 2a). In two frames from a 36-frame fluorescein series and on direct observation, the tumour blush of fine vessels was quite obvious. In the venous phase especially the tumour is clearly demarcated from the normal brain (Figs. l b and 2b). The arteries and the capillary bed appear pale grey or white (Fig. lb). The veins at this stage are dark, since they are not yet filled with fluorescein. During the venous phase, rather complex laminar flow patterns of alternating dark and light can be seen in the pial veins. The tumour as defined by fluorescence of its vascular bed was excised carefully but radically. The patient recovered a great deal of his speech function and a clearing o€ his confusion and was discharged home. The second example, a patient with an intrinsic brain tumour, presented clinically with a sudden onset of dysphasia. X-ray angiography showed a well defined highly vascular tumour in the posterior sylvian area with an arterio-venous shunt. Exploration was carried out. The superior detail of the fluorescein angiogram is depicted in Figs. 3a and 3b, comparing the X-ray arterial phase with the fluorescein arterial phase. Note especially the dense filling of the cortical capillary bed, the large pair of veins which were filled early with arterialized blood, and the central area of tumour References p. 477
474
w. FEINDEL et ai.
Fig. 2a. Venous phase, X-ray angiogram. Patient J. J.
Fig. 2b. Venous phase, fluorescein angiogram. Note high contrastfrom fluoresceinretainedintumour.
EPICEREBRAL A N G I O G R A P H Y
47 5
Fig. 3a. Arterial phase, X-ray angiogram. Patient L. N. Note vascular tumour, slight central shadow of lesser vascularity in centre of the tumour and the early filling veins.
Fig. 3b. Arterial phase, fluorescein angiogram. Patient L. N. Note the increased detail and contrast especially of the microvascular bed as compared to X-ray angiogram. Patient L. N. References p . 477
476
W. FEINDEL eC
al.
Fig. 4a. Venous phase, X-ray angiogram. Patient L. N.
Fig. 4b. Venous phase, fluorescein angiogram. Patient L. N. Noteretention offluoresceinin themargin of the tumour marking it out clearly from the surrounding brain.
EPICEREBRAL ANGIOGRAPHY
477
which fails to show fluorescence. In this part of the tumour, small thrombosed veins were found and this was considered to be evidence of a vascular occlusive phenomenon which went on within the neoplasm and gave an explanation for the onset of symptoms simulating a stroke. This area of avascularity was not as clear on the X-ray films in either the arterial or venous phases, being obscured by the dense subcortical vascular bed of the tumour which was on biopsy a malignant glioma (Figs. 4a and 4b). In summary, a new method of fluorescein angiography for demonstration of the epicerebral circulation during craniotomy provides for rapid sequential recording of the flow in the pial and cortical vessels. The advantages of the method include the display of the small vessels of the brain not seen on X-ray angiography so that examination of the cerebral microcirculation in vivo now becomes possible. Secondly, it allows the neurosurgeon to study the anatomical pattern of the epicerebral vesseh in man under a wide variety of abnormal conditions. Thirdly, though techniques for external measurement of cerebral blood flow by radioactive Xenon or Krypton have been of value, it has not been possible to correlate the many data from these techniques with the anatomical picture of the cerebral microcirculation. This now becomes possible with fluorescein angiography when combined withintracarotid radio-isotopic tracers5. The use of fluorescein angiography therefore, has a wide application for examination of the cerebral circulation under neurosurgical conditions. We consider that it will help to explain many of the features of local cerebral blood flow which have not so far been understandable by using only the external radio-isotopic measurement techniques.
REFERENCES 1 . FEINDEL, W., GARRETSON, H., YAMAMOTO, Y. L., PEROT,P. AND RUMIN, N. (1965) Blood flow patterns in the cerebralvessels and cortex in man studied by intracarotid injection of radioisotopes and Coornassie Blue dye. J . Neurosurg., 23,12-22. 2. FEINDEL, W. (1963) Scandinavian symposium on cerebral circulation. Canad. Med. Ass. J., 88,951-952. 3. FEINDEL, W., YAMAMOTO, Y. L. AND HODGE, C. P. (1967) The human microcirculation studied by intra-arterial radio-active tracers, Coomassie Blue and fluorescein dyes. Proc. 4th European Conference on Microcirculation, Cambridge, England, June, 1966. Bibl. Anat., fasc. 9, 220-224. 4. FEINDEL, W., YAMAMOTO, Y. L. AND HODGE, C. P. (1967) Intracarotid fluorescein angiography: A new method for examination of the epicerebral circulation in man. Canad. Med. Ass. J., 96, 1-7. 5. FEINDEL, W. AND YAMAMOTO, Y. L. (1967); Luxury-Perfusion Syndrome. Lancet, i, 48-49.
Epicerebral Angiography by Fluorescein durin g Craniotomy * WILLIAM FEINDEL, CHARLES P. HODGE AND Y. LUCAS YAMAMOTO Cone Laboratory for Neurosurgical Research, Montreal Neurological Institute and McGill University, Montreal (Canada)
In previous reports we have described the use of radio-activeisotopes and Coomassie Blue dye injected by internal carotid catheter for analysis of the regional blood flow in the epicerebral circulation (the pial arteries and veins and the cortical capillary bed) during craniotomyl. This method allows for the comparison of quantitative radioisotopic blood flow curves directly with the anatomical pattern of the normal and abnormal vasculature on the surgically exposed brain. This approach has provided information on changes in blood flow in angiomas and adjacent cortex before and after obliteration of arterial feeders, or after arterial manipulation during clipping of aneurysms, and on abnormal flow rates in tumours with arterio-venous shunts2. With Coomassie Blue, a highly coloured non-toxic dye (sodium anazolene) and rapid serial stroboscopic colour photography the anatomical patterns of flow in pial arteries and veins and in the cortical capillary bed can be displayed and analysed. It should be emphasized that this direct comparison of the anatomy and rheology of the cerebral circulation directly from the surface of the brain offers many advantages over the technique of external monitoring by radio-isotopes of cerebral blood flow, where the details of the cerebral microcirculation have not been available. We now wish to describe the technique of fluorescein angiography as an additional means of examining the surface of the brain during operation. Details of the method were developed during a study of experimental cerebral ischaemia in cat and monkey brains3.4. In the operating room 2 ml of 1 % sodium fluorescein are rapidly injected into an internal carotid catheter. The passage of the dye through the vasculature of the exposed brain is recorded on serial photographs taken at intervals of 0.40 sec by a Nikon camera with motor-driven film changer. The shutter is synchronized with the discharge of a rapid re-charging stroboscopic light. A Wratten 47 colour filter was used over the light and a Wratten 58 over the camera lens for Tri-X film to obtain black and white photographs. Using high-speed Ektachrome film (daylight), the camera filter was changed to Wratten 29 with a 2-B ultra-violet absorbing filter and the film processed as Ektacolor to give an enhanced contrast and a speed of ASA 1200. The timing of the interval between photographs was measured to within 0.02 sec
* This work was supported by thecone Memorial Fund and the Medical Research Council of Canada. References p . 477
472
w. F E I N D E L et al.
by recording from a cadmium photo-cell placed near the strobe light. Thus the velocity of flow in individual vessels could be calculated from the serial photographs. The most important feature of fluorescence angiography is the display of the small pial arteries and veins and the cortical capillary bed, all of which appear in high contrast and in great detail. These are vessels of a size which are not visible on standard X-ray angiography, and the additional vasculature seen on the fluorescence photographs and on direct observation of the brain is often remarkable. The arterial and venous vessels stand out distinctly during their separate phases. Because of the dense filling of the capillary bed of the cortex the “water-shed’’ of the major arterial territories is clearly defined. The dynamics of central and mural laminar flow appear in detail, particularly in larger veins. In cerebral tumours, the fine blood vessels in the tumour bed show up earlier than the normal vascular bed and remain filled later than the normal venous phase, so that the tumour stands out with considerable prominence from the surrounding normal tissue. Shunting of the fluorescein from arteries to veins is readily seen in some tumours, and the velocity of flow in different draining veins can be distinguished.Areas of ischaemia are well demarcated by absence of fluorescence, while areas of damage may retain the dye beyond the normal circulation time. Such areas may escape detection on X-ray angiography. Two examples of fluorescein epicerebral angiograms in brain tumours taken from our series will serve to illustrate some of these points.
Fig. la. X-ray angiogram,arterialphaseshowingslight tumour blushintheparietalregion. Patient J. J.
EPICEREBRAL ANGIOGRAPHY
473
Fig. lb. Fluorescein angiogram, arterial phase from exposed brain. Note intensity ofturnourblushand filling of small arterial vessels. Patient J. J.
In the first example, a patient with carcinoma of the colon who began to have dysphasia, the X-ray film in the arterial phase showed a definite though scanty tumour blush in the left parietal region (Fig. la) which persisted in the venous phase (Fig. 2a). In two frames from a 36-frame fluorescein series and on direct observation, the tumour blush of fine vessels was quite obvious. In the venous phase especially the tumour is clearly demarcated from the normal brain (Figs. l b and 2b). The arteries and the capillary bed appear pale grey or white (Fig. lb). The veins at this stage are dark, since they are not yet filled with fluorescein. During the venous phase, rather complex laminar flow patterns of alternating dark and light can be seen in the pial veins. The tumour as defined by fluorescence of its vascular bed was excised carefully but radically. The patient recovered a great deal of his speech function and a clearing o€ his confusion and was discharged home. The second example, a patient with an intrinsic brain tumour, presented clinically with a sudden onset of dysphasia. X-ray angiography showed a well defined highly vascular tumour in the posterior sylvian area with an arterio-venous shunt. Exploration was carried out. The superior detail of the fluorescein angiogram is depicted in Figs. 3a and 3b, comparing the X-ray arterial phase with the fluorescein arterial phase. Note especially the dense filling of the cortical capillary bed, the large pair of veins which were filled early with arterialized blood, and the central area of tumour References p. 477
474
w. FEINDEL et ai.
Fig. 2a. Venous phase, X-ray angiogram. Patient J. J.
Fig. 2b. Venous phase, fluorescein angiogram. Note high contrastfrom fluoresceinretainedintumour.
EPICEREBRAL A N G I O G R A P H Y
47 5
Fig. 3a. Arterial phase, X-ray angiogram. Patient L. N. Note vascular tumour, slight central shadow of lesser vascularity in centre of the tumour and the early filling veins.
Fig. 3b. Arterial phase, fluorescein angiogram. Patient L. N. Note the increased detail and contrast especially of the microvascular bed as compared to X-ray angiogram. Patient L. N. References p . 477
476
W. FEINDEL eC
al.
Fig. 4a. Venous phase, X-ray angiogram. Patient L. N.
Fig. 4b. Venous phase, fluorescein angiogram. Patient L. N. Noteretention offluoresceinin themargin of the tumour marking it out clearly from the surrounding brain.
EPICEREBRAL ANGIOGRAPHY
477
which fails to show fluorescence. In this part of the tumour, small thrombosed veins were found and this was considered to be evidence of a vascular occlusive phenomenon which went on within the neoplasm and gave an explanation for the onset of symptoms simulating a stroke. This area of avascularity was not as clear on the X-ray films in either the arterial or venous phases, being obscured by the dense subcortical vascular bed of the tumour which was on biopsy a malignant glioma (Figs. 4a and 4b). In summary, a new method of fluorescein angiography for demonstration of the epicerebral circulation during craniotomy provides for rapid sequential recording of the flow in the pial and cortical vessels. The advantages of the method include the display of the small vessels of the brain not seen on X-ray angiography so that examination of the cerebral microcirculation in vivo now becomes possible. Secondly, it allows the neurosurgeon to study the anatomical pattern of the epicerebral vesseh in man under a wide variety of abnormal conditions. Thirdly, though techniques for external measurement of cerebral blood flow by radioactive Xenon or Krypton have been of value, it has not been possible to correlate the many data from these techniques with the anatomical picture of the cerebral microcirculation. This now becomes possible with fluorescein angiography when combined withintracarotid radio-isotopic tracers5. The use of fluorescein angiography therefore, has a wide application for examination of the cerebral circulation under neurosurgical conditions. We consider that it will help to explain many of the features of local cerebral blood flow which have not so far been understandable by using only the external radio-isotopic measurement techniques.
REFERENCES 1 . FEINDEL, W., GARRETSON, H., YAMAMOTO, Y. L., PEROT,P. AND RUMIN, N. (1965) Blood flow patterns in the cerebralvessels and cortex in man studied by intracarotid injection of radioisotopes and Coornassie Blue dye. J . Neurosurg., 23,12-22. 2. FEINDEL, W. (1963) Scandinavian symposium on cerebral circulation. Canad. Med. Ass. J., 88,951-952. 3. FEINDEL, W., YAMAMOTO, Y. L. AND HODGE, C. P. (1967) The human microcirculation studied by intra-arterial radio-active tracers, Coomassie Blue and fluorescein dyes. Proc. 4th European Conference on Microcirculation, Cambridge, England, June, 1966. Bibl. Anat., fasc. 9, 220-224. 4. FEINDEL, W., YAMAMOTO, Y. L. AND HODGE, C. P. (1967) Intracarotid fluorescein angiography: A new method for examination of the epicerebral circulation in man. Canad. Med. Ass. J., 96, 1-7. 5. FEINDEL, W. AND YAMAMOTO, Y. L. (1967); Luxury-Perfusion Syndrome. Lancet, i, 48-49.