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Carotid Angiography; Its Value In Premalignant Intracranial Conditions
CAROTID ANGIOGRAPHY; ITS VALUE IN PREMALIGNANT INTRACRANIAL CONDITIONS
ARTHUR A. MORRIS, M.D. * AND O. HUGH FULCHER, M.D., F.A.C.S. t THE detection of any disease in the early stage is desirable and may frequently determine the success of therapy. Early diagnosis is essential if one is able to assay the gravity of the illness and to mobilize all efforts toward combating it: otherwise his efforts toward treatment will end in frustration. Nowhere is this concept more mandatory than in premalignant lesions. Every intracranial lesion of expanding nature is potentially malignant. This does not relate to the cellular content but to the fact that all of these lesions will eventually cause death by occupying space and by producing pressure on the brain. Whether or not an intracranial lesion will metastasize does not demand first consideration. Of greater importance is the consideration of the cerebral vascular tree. At the present time far more people are dying from pathological conditions created by cerebral blood vessels than are dying from brain tumors. Therefore as related to craniocerebral surgery the problem of premalignant conditions will assume a significance that is not related simply to changes in cellular growth. . The authors would like to suggest that the term "premalignant conditions," when used in reference to the intracranial contents, should include all lesionsthat are likely to end fatally. Thus a small aneurysm of one of the cerebral arteries may represent a premalignant condition so far as life is concerned. An arteriovenous fistula, intracranial varicosity, hemangioma, intracerebral hematoma, subdural or epidural hematoma, brain abscess, or any lesion of expanding proportions is a potential cause of death and therefore, regardless of its cellular structure, may under this concept be considered premalignant. The intracranial contents are enclosed in a rigid nonflexible, nonexpanding bony box of aconstant volume for each individual. This bony box, the cranial cavity, surrounds its contents which consist of the meninges, the spinal fluid, the brain and the blood vessels. If expanding lesions develop within the cranial cavity, additional room is made by From the Department of Neurological Surgery, Georgetown University Medical Center, Washington, D. C. * Instructor in Neurosurgery, Junior Attending Neurosurgeon, Georgetown University Hospital, Gallinger Municipal Hospital (Georgetown Division). t Professor of Neurosurgery, Georgetown University Medical Center; Chief of Neurosurgical Service, Georgetown University Hospital, Gallinger Municipal Hospital (Georgetown Division) and Providence Hospital. 1783
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sacrificing the normal volume of one of its contents. Finally the expansion will so destroy the functions of essential structures that death ensues. Blood outside of the cranial vessels will occupy space and will cause increased intracranial pressure. Thus an impending disruption of the walls of a blood vessel, in our concept, represents a premalignant state. Although the carotid arteries and the vertebral arteries have several right angle bends to dissipate the impact of the heart beat, under certain abnormal conditions the flexibility of the walls may make dissipation of the heart impact less and less effective until a condition of impending disruption exists. This situation should be diagnosed early and certainly it should be recognized so that appropriate therapy may be instituted. Furthermore, it is recalled that the reinforcement of vascular walls is almost nil within the brain. CEREBRAL ANGIOGRAPHY
Since the intracranial contents cannot be inspected, one has to make a diagnosis by utilizing certain physiological responses throughout the entire body and by employing certain objective procedures. The introduction of the spinal puncture in 1890 and the discovery of roentgen rays in 1895 provided the fundamental basis for objective demonstrations of intracranial lesions. A monumental advance was made in 1918 when Dandy discovered that air could be safely injected into the ventricles. By this means the positions and the states of many of the intracranial structures may be accurately determined. Another great advance was made by Moniz in 1927 when he introduced cerebral angiography. This procedure was slow in acceptance in this country because it was considered hazardous, but during the last few years it has become increasingly popular because of recent technical improvements in the required x-ray equipment, the development of the percutaneons method of puncturing the carotid and vertebral arteries, and the discovery of a contrast medium which has proved to be relatively harmless. Angiography consists merely of the roentgenologic visualization of vessels secured by placing an opaque solution in the arterial blood so that, as it is swept along, it will outline its path of travel. By studying the vascular pattern by angiography much has been learned about the anatomy of the cerebral vessels, and it has contributed materially to the diagnosis of intracranial aneurysms, tumors and other space-occupying conditions that might produce a deviation of blood vessels. It has also afforded a method for estimating the circulation time and has aided in the preoperative pathological diagnosis in tumors. The arterial supply of the brain is furnished by the carotid and the vertebral systems. The carotid system is by far the more important from the standpoint of angiography. It supplies about 75 per cent of the brain
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which includes the frontal, parietal, and superior temporal lobes. One has to employ the. vertebral system to obtain the vascular pattern of the occipital lobes, the posterior fossa, the pons and the basilar artery. The vertebral vessels can be injected by a percutaneous. method quite satisfactorily. The method of Sugar, Holden and Powell has been the most successful in our hands. Obtaining a good arteriogram is a relatively simple procedure after the neurosurgical and roentgenological teams have been developed. There will be some failures during the amateur era but these should not be too discouraging. TECHNIC OF CAROTIJ;l ANGIOGRAPHY
This discussion will be limited to carotidangiography. This procedure is simple and can be fairly well performed with a minimum of x-ray equipment. The patient is instructed to take nothing by mouth for six to eight hours prior to the contemplated injection. Nembutal 0.1 gm. (I! grains) is administered two hours before his appearance in the x-ray department. Injections are done on an outpatient or in-hospital basis. After the radiologic equipment has been set up and the injection tray has been prepared, the patient is placed in the horizontal position with the side upright which has been selected for injection (Fig. 530, a). The corresponding shoulder is elevated by the use of a large sandbag so that there will be no overrotation of the neck or compression of the opposite carotid artery. The head is placed in the true lateral position. The common carotid artery is then palpated and the site of the puncture is selected directly over it about 3 t04 cm. above the clavicle. Preparation for the puncture is most essential. It is recommended that one take ample time to palpate the artery, obtain good hyperextension of the neck in the lateral position, and gain as much relaxation of the sternomastoid muscle as possible. A 16-gauge needle 6 cm. long which has a long beveled sharp point is used for the injection; it is attached to a 10 cc. Luer-Lock syringe. Intravenous sodium pentothal (2.5 per cent) is administered to the patient for anesthesia. The puncture is always made from the right side of the patient (Fig. 530, b). The bevel of the needle is placed upright so that the numbers on it and the syringe correspond. The position of the needle and syringe should parallel the course of the common carotid artery, and the angle between the skin and the needle need not exceed 15 degrees. The skin puncture is made and the point of the needle is allowed to rest on the common carotid artery (Fig. 530, c). With a single short thrust the artery is entered; the syringe is then quickly lowered as close as possible to the skin and the needle is threaded into the common carotid artery
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for about 2 cm. The bevel of the needle is rotated laterally so that the contrast medium can follow the lateral stream and most of it will flow into the internal carotid artery (Fig. 530, d). The injection is made as rapidly as possible, utilizing only 8 cc. of 35 per cent diodrast. After 6 cc. has been injected the initial film is taken. A seriograph is used which will make six exposures in four seconds
Fig. 530. a, Correct position of patient for injection of the right common carotid artery. Anesthesia consists of 2.5% solution of sodium pentothal given intravenously. b, The site of skin puncture is directly over the palpated carotid artery about 4 cm. above the clavicle. c, The skin puncture has been made and the point of the needle is resting on the common carotid artery. d, A puncture of the common carotid is made and the artery cannulalized for 3 cm. The needle is in correct position for injection of 35 per cent solution of diodrast. To obtain the A-P projection the face is simply placed upward. The rapid casette changer seriograph is set in motion when about 6 cc. of the diodrast has been injected.
thus making possible a study of the unilateral carotid arterial and venous systems.' After the injection and the exposures have been completed, the needle is quickly removed from the carotid artery and point pressure is applied without occluding the artery. The patient soon regains consciousness and is taken to his room, or he is permitted to remain in the x-ray department for an hour or two after which he may be taken home. Seventyfour percutaneous arteriograms have been carried out in this manner without any complications other than a slight soreness in the neck which persisted for two to three days. This pain may be relieved by the ap-
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plication of ice packs. Twenty-five bilateral arteriograms have been made without complications. Provided a successful unilateral carotid arteriogram has been obtained we think that there is no additional risk in bilateral carotid arteriography. Bilateral carotid arteriograms in the lateral and anteroposterior projections and percutaneous bilateral vertebral arteriograms have been made on one female patient, using a total of 90 cc. of 35 per cent solution of diodrast without deleterious effects. The use of such large quantities of the medium is rarely necessary and is not recommended as a routine procedure. Complications can usually be avoided by a skillful technic of injection, the selection of 35 per cent solution of diodrast, and the use of only 8 cc. of the contrast medium. Reactions to diodrast have occurred on three occasions, which consisted of a widespread allergic rash associated with severe itching. These symptoms were quickly relieved by the intravenous administration of benadryl. Occasionally it may be desirable to use local anesthesia only. In this instance, about 0.3 gm. (4! grains) of oral nembutal is administered two hours prior to the procedure. The stellate ganglion is injected bilaterally with 2 per cent procaine solution and a very slight amount of the local anesthesia is infiltered into the skin just over the common carotid artery. The rest of the procedure is exactly as described above. When carotid angiography is done under local anesthesia the injection of the stellate ganglia appears to diminish the vasospasms caused by the diodrast. Pneumoencephalography and percutaneous carotid arteriography have been combined in thirteen cases without harmful effects. If the pneumoencephalogram should prove inconclusive and arteriography appear desirable one may proceed before the intravenous anesthesia is discontinued and while the patient is still on the x-ray table. This procedure avoids a second anesthesia, a second trip to the x-ray department, and may add considerably to. the accuracy of the diagnosis. THE CONTRAST MEDIUM
Moniz used 60 per cent strontium bromide during his early experience which produced a 2.6 per cent mortality and. there were also a number of patients who experienced temporary hemiplegia. It was quite evident that this solution represented a real hazard. Subsequently, he used 25 per cent sodium iodide which likewise caused too many complications. In 1931 he introduced a colloidal solution of thorotrast, which was radioactive. Furthermore, the radioactive substance was taken up quite selectively by the reticulo-endothelial system. Consequently, large quantities of the radioactive material were concentrated in the liver and spleen. It was thought at first that the radioactivity was of such low magnitude that no harmful results would ensue. More recently there
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have been cases reported of malignancy developing in the liver. Furthermore, mechanical damage through occlusions of small cerebral vessels frequently ensued. Thorotrast also provoked thrombopenia that sometimes gave rise to postoperative hematomas. This material is still used in a great many European clinics and its advocates believe that if the amount is limited to 30 cc. or less no harmful effects will follow. Furthermore, they think that better visualization is obtained, especially of the smaller cerebral arteries, than with other media. Many American physicians have hesitated to use the colloidal solution of thorotrast. In 1939 Gross published his results with the use of 35 per cent solution of diodrast, which has the advantage of being soluble in water and readily excreted from the body. We have used both the 35 per cent and the 50 per cent solutions, and it has been our experience that the 35 per cent solution is far preferable. It does not cause as much vasospasm and appears to give adequate contrast. It would appear that the radiologic technic is of far more importance in determining good visualization of the vessels than is the 15 per cent difference in opacity between the solutions. In this respect it is often wise to obtain a preliminary plain x-ray film of the skull to aid in selecting the x-ray exposure that will give optimal visualization. We have injected 5 to 10 cc. of 35 per cent diodrast solution into the pericarotid spaces inadvertently on seven occasions with only minor undesirable effects. In each instance there was an increase in soreness for several days. No permanent induration developed. On the other hand, we have recently examined two patients who had experienced the same misfortune elsewhere when the colloidal solution of thorotrast was used. Both of these patients had disabling muscular contractions, obvious deformity, and complained of local tenderness and discomfort. Thirty-five per cent diodrast solution is not the perfect medium, however. It sometimes causes vasospasm and produces a sensation of vertigo if the injection is made under local anesthesia. There have been instances of transient hemiplegias resulting from the diodrast solution reported in the literature. This complication we believe can be avoided if small quantities are used. IMPROVEMENTS IN RADIOLOGIC EQUIPMENT
Roentgenologists have worked diligently to develop a technic that will produce good visualization of the contrast medium. In our clinic we formerly used no additional x-ray equipment. The cassettes were placed in position manually and could be changed at about two-second intervals by. an experienced team. In this way good pictures of the arterial phase could frequently be obtained. In 1931 Moniz began to use the anteroposterior position also. With the manual method one picture only could
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be obtained in the anteroposterior projection. Recently' many devices have been invented for changing the cassettes mechanically and rapidly. It is believed that shortly a simple economical device will be developed. For the past years we have been using the seriograph, which has been satisfactory but has the objection of being rather expensive and consequently not always practical. We have had no experience with the cinefluorograph but we believe that such a mechanism has great possibilities. Since the percutaneous method of puncturing the carotid artery has been developed to the point where it is considered almost as simple as doing a venipuncture in the forearm, it is believed that the use of angiography will become a great deal more widespread as soon as some cheap mechanical device is developed for the mechanical changing of the cassettes. We consider it no longer necessary to submit a patient to an operative exposure of the carotid artery unless the percutaneous method has failed. ANATOMY OF THE CEREBRAL CIRCULATION
Generally speaking, the external carotid arteries supply the skull, the soft parts of the head, the neck and the dura. The internal carotid arteries supply the supratentoral part of the brain (Fig. 2). The vertebral arteries supply the cerebral contents of the posterior fossa and in addition they contribute to the posterior cerebral arteries. In about 20 per cent of instances the posterior cerebral arteries received their blood supply almost entirely from the carotid system through the posterior communicating arteries. The internal carotid artery has no branches in the neck. It enters .the carotid canal and as it passes through the temporal bone it makes two sharp turns (Fig. 531). The first bend 'is forward and medially and the second bend is upward. The vessel then passes through the outer layer of the dura and enters the cavernous sinus where it makes a right angle bend and proceeds forward and upward medially just lateral to the sphenoid body. At the border of the anterior clinoid process the artery turns medially and penetrates the inner layer of the dura. It then leaves the cavernous sinus, making another bend forward at which point the posterior communicating artery is given off. It continues forward to the anterior perforated substance to the most medial portion of the lateral cerebral fissure where it breaks off into the anterior cerebral and middle cerebral arteries. The middle cerebral artery courses almost straight laterally beneath the anterior perforated substance lying in the lateral cerebral fissure. It is very short and its terminal branches begin so close to the carotid syphon that they form a vascular bundle. The vascular bundle consists of three
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branches which are of special interest in studying the arteriogramthe posterior temporal, the artery of the angular gyrus, and the posterior parietal. These vessels which lie in the lateral cerebral fissure are of great importance in the interpretation of the x-ray picture. They may be displaced by an expanding lesion. They also represent a frequent site of aneurysms. It is well to keep in mind, however, that variations of these vessels can occur in the normal individual and that often a combination
Fig. 531. Diagram showing the larger intracranial arteries demonstrable by carotid anteriography. A, Internal carotid; B, ophthalmic; C, posterior communicating; D, anterior choroidal; E. anterior cerebral; F, frontopolar; G, callosomarginal; H, pericallosal; I, middle cerebral; J, ascending frontal; K, posterior parietal; L, angular artery, M, posterior temporal.
analysis of several vessels will be necessary to effect a correct interpretation. Woringer and Gernez stated that the posterior cerebral artery is visible in about one-half the cases as a minute filament arising from the syphon. The anterior choroidal artery will sometimes arise from the middle cerebral rather than from the internal carotid artery. The anterior cerebral artery courses above the optic nerve in a medial direction and then forward where it communicates with the anterior cerebral artery on the opposite side by the way of the anterior communicating artery. At this point the vessel makes a sharp upward bend
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and divides into its terminal branches, the peri callosal and the callosomarginal arteries which run parallel to each other. The final branches supply the paracentral lobule. In the anteroposterior projection the anteriorcerebral artery runs in the midline. The anterior communicating artery is almost never visible because of the bony shadow. The frontopolar branches of the anterior cerebral arteries are visible in about three patients out of four.
Fig. 532. Diagram showing the cerebral venous system as outlined by angiography. A, Superior longitudinal sinus; B, inferior longitudinal sinus; C, transverse sinus; D, inferior longitudinal sinus; C, transverse sinus; D, straight sinus; E, great vein of Galen; F, internal cerebral vein; G, basal vein of Rosenthal; H, frontal ascending vein; D, Rolandic vein of Trolord; J, parietal ascending vein; K, communicating temporal vein of Labbe; L, descending temporal-occipital vein.
The venous system begins to fill approximately two to four seconds after the injection (Fig. 532). Initially the small superficial vessels appear filled and radiate toward the cerebral convexity. Next the larger superficial vessels fill and display considerable tortuosity. Several large veins soon appear and radiate in the direction of the insula. One of these is the anastomotic vein of Labbe which courses in a posterior direction to enter the transverse sinus. Another is the anastomotic vein of Trollard which courses upward and enters the superior sagittal sinus, and a third is a large vein which mainly follows the sylvian fissure. This brief description of the arterial and venous pattern will provide
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the fundamental knowledge necessary to interpret normal angiograms. It does not require much experience before one is able to identify the normal pattern. When an apparent abnormal pattern is encountered one must attempt to analyze just what .is unusual. Occasionally the contrast medium will produce sufficient vasospasm to cause a certain part of the pattern to appear rather avascular. Sometimes there will be filling on the contralateral sides due to pressure on the opposite common carotid artery during the injection. Abnormal anastomoses, abnormal and unusual sizes of vessels, and outpouchings will immediately be evident.
Fig. 533. Arteriogram revealing an aneurysm of the middle cerebral artery.
THE CLINICAL VALUE OF CAROTID ANGIOGRAPHY
The outstanding value of-carotid angiography is in the diagnosis and the management of intracranial aneurysms, arteriovenous fistulas and hemangiomas. There is no other method by which the existence of these conditions can be objectively demonstrated except by the use of a contrast medium intra-arterially. The exact relationship and location of an arterial aneurysm can be demonstrated (Figs. 533 to 535) by the use of the lateral and anteroposterior positions. Thus, the surgical approach can be carefully planned and adequate precaution can usually be executed because the pitfalls can be visualized beforehand. The size of
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the aneurysm can be estimated. When one has the knowledge of the size and the location of the aneurysm he can obtain some idea as to whether or not immediate surgical therapy is imperative. If the aneurysm has previously ruptured one may frequently determine whether or not there exists a localized hematoma. In the case illustrated (Figs, 534 and 535) a large intracerebral hematoma was present. The grave condition of the patient responded favorably when
Fig. 534. Carotid percutaneous arteriogram showing a large saccular aneurysm of the internal carotid artery (intracranial portion). The arrow shows the uppermost border of the aneurysm. The anterior cerebral artery is elevated at the anterior bend by a large associated intracerebral clot. Compare with Figure 535.
the blood clot was evacuated. We are convinced that this patient's life was preserved because the demonstration of the presence and location of this hematoma by carotid angiography enabled us to institute appropriate and accurate surgical therapy. Hence, a premalignant condition was successfully eradicated. Angiography can frequently be employed in conjunction with ventriculography or pneumoencephalography (Fig. 536). Often it is desirable to visualize the vascular pattern of an intracranial lesion. One patient revealed a small defect of the right anterior horn of the lateral ventricle
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upon pneumoencephalography. The arteriogram demonstrated a small capillary hemangioma in the corresponding area which responded to x-ray therapy. Thus a craniotomy was avoided. In another patient the encephalogram showed a protrusion into the temporal horn of the left
Fig. 535. Arteriogram of same patient as shown in Figure 534. Note the marked displacement of the anterior cerebral artery to the opposite side. A large intracerebral clot produced this displacement, was responsible for the comatose condition of the patient, and was successfully evacuated without the use of ventriculography.
lateral ventricle. An immediate left carotid angiogram revealed the mass to consist of capillary malformations which were interpreted as the cause of the recurrent seizures with an aura of dizziness, microscopia and tinnitus. Occasionally the vascular pattern as seen in the angiogram will afford a basis for making a tentative pathological diagnosis. In this manner the
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tentative preoperative diagnosis of glioblastoma multiforme has been made in several patients and this has been of some value in planning the surgical therapy and in predicting the prognosis. With six patients we have made -tp.e preoperative diagnosis of hemangioma by angiography. Since hemangioma may be successfully treated by' x-ray we have thus been able to avoid craniotomy.
Fig. 536. This arteriogram was made shortly after the pneumoencephalogram was completed, utilizing the same anesthesia. The combination use of pneumoencephalography and arteriography has enhanced the accuracy of the preoperative diagnosis.
Angiography on a patient suffering with an intracranial lesion does not aggravate his symptoms or condition. The necessity for immediate operation is thus avoided whereas when ventriculography is employed immediate craniotomy is often imperative. Occasionally the angiographic or the pneumographic evidence of an expanding lesion is inadequate alone to permit a definite conclusion but in combination they may be adequate for localization. Very occasionally it is necessary not only to have arteriographic and pneumographic evidence but also to have electroencephalographic tracings in order to
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reach a conclusion. All three of these methods have been used in the diagnosis of focal epileptogenic lesions of the cerebral cortex. It is believed that the practical use of angiography constitutes an additional effort to make more accurate preoperative or ante-mortem diagnoses. The more frequent use of angiography has demonstrated that anatomical variations of the vascular patterns exist in normal individuals which may make interpretations difficult. The accuracy of the interpretations in these patients may be increased by the use of bilateral carotid arteriograms. The diagnosis of cerebral arteriosclerosis, endarteritis obliterans, small cortical venous or arterial thromboses, cerebral scars and cortical atrophy has not proved accurate in our hands except in rare instances. It is accepted that the most complete filling obtainable by clinical angiography does not demonstrate all of the cerebral vessels. CONCLUSIONS
Carotid angiography is a relatively simple procedure. It can be performed unilaterally, bilaterally and immediately upon completion of pneumoencephalography. If it is used with wisdom, it aids considerably in the diagnosis of intracranial lesions previously not demonstrable. It may provide an excellent guide in the surgical removal of tumors and occasionally it affords adequate information for a tentative preoperative diagnosis of the type of lesion. Angiography is the only method that will demonstrate objectively the presence of intracranial aneurysms, arteriovenous fistulas, arteriovenous malformations, and hemangiomas prior to exploration. REFERENCES 1. Dandy,W. E.: Ann. Surge 68:5,1918. 2. Moniz, Egas P.: Handbuch der neurologic Ergans. Ser. 2. Berlin, Springer, 1940. 3. Sugar, 0., Holden, L. B. and Powell, C. B.: Am. J. Roentgenol. 61:166-182 (Feb.) 1949. 4. Ingraham, Franc D. and Cobb, Culley A., Jr.: J. Neurosurg. 4:5, 422-433 (Sept.) 1947. 5. Gross, S. W.: J. Indiana M. A.: 37:109, 1944. 6. Holm, 0.: Acta radiol. 25:163, 1944. 7. Woringer, E. and Gernez, A.: Presse med. 56:8881-82 (Dec. 18) 1948. 8. Domnick, 0.: Zentralbl..f. Neurochir. 4:184, 1940. 9. Wolff, H. and Schaltenbrand, G.: Zentralbl. f. Neurochir.: 4: 233,1939. 10. Turnbull, F.: An. J. Roentgenol.: 41:116, 1939. 11. Lindgren, E.: Brit. J. Radiol. 20:236,1947.
ARTHUR A. MORRIS, M.D. * AND O. HUGH FULCHER, M.D., F.A.C.S. t THE detection of any disease in the early stage is desirable and may frequently determine the success of therapy. Early diagnosis is essential if one is able to assay the gravity of the illness and to mobilize all efforts toward combating it: otherwise his efforts toward treatment will end in frustration. Nowhere is this concept more mandatory than in premalignant lesions. Every intracranial lesion of expanding nature is potentially malignant. This does not relate to the cellular content but to the fact that all of these lesions will eventually cause death by occupying space and by producing pressure on the brain. Whether or not an intracranial lesion will metastasize does not demand first consideration. Of greater importance is the consideration of the cerebral vascular tree. At the present time far more people are dying from pathological conditions created by cerebral blood vessels than are dying from brain tumors. Therefore as related to craniocerebral surgery the problem of premalignant conditions will assume a significance that is not related simply to changes in cellular growth. . The authors would like to suggest that the term "premalignant conditions," when used in reference to the intracranial contents, should include all lesionsthat are likely to end fatally. Thus a small aneurysm of one of the cerebral arteries may represent a premalignant condition so far as life is concerned. An arteriovenous fistula, intracranial varicosity, hemangioma, intracerebral hematoma, subdural or epidural hematoma, brain abscess, or any lesion of expanding proportions is a potential cause of death and therefore, regardless of its cellular structure, may under this concept be considered premalignant. The intracranial contents are enclosed in a rigid nonflexible, nonexpanding bony box of aconstant volume for each individual. This bony box, the cranial cavity, surrounds its contents which consist of the meninges, the spinal fluid, the brain and the blood vessels. If expanding lesions develop within the cranial cavity, additional room is made by From the Department of Neurological Surgery, Georgetown University Medical Center, Washington, D. C. * Instructor in Neurosurgery, Junior Attending Neurosurgeon, Georgetown University Hospital, Gallinger Municipal Hospital (Georgetown Division). t Professor of Neurosurgery, Georgetown University Medical Center; Chief of Neurosurgical Service, Georgetown University Hospital, Gallinger Municipal Hospital (Georgetown Division) and Providence Hospital. 1783
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sacrificing the normal volume of one of its contents. Finally the expansion will so destroy the functions of essential structures that death ensues. Blood outside of the cranial vessels will occupy space and will cause increased intracranial pressure. Thus an impending disruption of the walls of a blood vessel, in our concept, represents a premalignant state. Although the carotid arteries and the vertebral arteries have several right angle bends to dissipate the impact of the heart beat, under certain abnormal conditions the flexibility of the walls may make dissipation of the heart impact less and less effective until a condition of impending disruption exists. This situation should be diagnosed early and certainly it should be recognized so that appropriate therapy may be instituted. Furthermore, it is recalled that the reinforcement of vascular walls is almost nil within the brain. CEREBRAL ANGIOGRAPHY
Since the intracranial contents cannot be inspected, one has to make a diagnosis by utilizing certain physiological responses throughout the entire body and by employing certain objective procedures. The introduction of the spinal puncture in 1890 and the discovery of roentgen rays in 1895 provided the fundamental basis for objective demonstrations of intracranial lesions. A monumental advance was made in 1918 when Dandy discovered that air could be safely injected into the ventricles. By this means the positions and the states of many of the intracranial structures may be accurately determined. Another great advance was made by Moniz in 1927 when he introduced cerebral angiography. This procedure was slow in acceptance in this country because it was considered hazardous, but during the last few years it has become increasingly popular because of recent technical improvements in the required x-ray equipment, the development of the percutaneons method of puncturing the carotid and vertebral arteries, and the discovery of a contrast medium which has proved to be relatively harmless. Angiography consists merely of the roentgenologic visualization of vessels secured by placing an opaque solution in the arterial blood so that, as it is swept along, it will outline its path of travel. By studying the vascular pattern by angiography much has been learned about the anatomy of the cerebral vessels, and it has contributed materially to the diagnosis of intracranial aneurysms, tumors and other space-occupying conditions that might produce a deviation of blood vessels. It has also afforded a method for estimating the circulation time and has aided in the preoperative pathological diagnosis in tumors. The arterial supply of the brain is furnished by the carotid and the vertebral systems. The carotid system is by far the more important from the standpoint of angiography. It supplies about 75 per cent of the brain
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which includes the frontal, parietal, and superior temporal lobes. One has to employ the. vertebral system to obtain the vascular pattern of the occipital lobes, the posterior fossa, the pons and the basilar artery. The vertebral vessels can be injected by a percutaneous. method quite satisfactorily. The method of Sugar, Holden and Powell has been the most successful in our hands. Obtaining a good arteriogram is a relatively simple procedure after the neurosurgical and roentgenological teams have been developed. There will be some failures during the amateur era but these should not be too discouraging. TECHNIC OF CAROTIJ;l ANGIOGRAPHY
This discussion will be limited to carotidangiography. This procedure is simple and can be fairly well performed with a minimum of x-ray equipment. The patient is instructed to take nothing by mouth for six to eight hours prior to the contemplated injection. Nembutal 0.1 gm. (I! grains) is administered two hours before his appearance in the x-ray department. Injections are done on an outpatient or in-hospital basis. After the radiologic equipment has been set up and the injection tray has been prepared, the patient is placed in the horizontal position with the side upright which has been selected for injection (Fig. 530, a). The corresponding shoulder is elevated by the use of a large sandbag so that there will be no overrotation of the neck or compression of the opposite carotid artery. The head is placed in the true lateral position. The common carotid artery is then palpated and the site of the puncture is selected directly over it about 3 t04 cm. above the clavicle. Preparation for the puncture is most essential. It is recommended that one take ample time to palpate the artery, obtain good hyperextension of the neck in the lateral position, and gain as much relaxation of the sternomastoid muscle as possible. A 16-gauge needle 6 cm. long which has a long beveled sharp point is used for the injection; it is attached to a 10 cc. Luer-Lock syringe. Intravenous sodium pentothal (2.5 per cent) is administered to the patient for anesthesia. The puncture is always made from the right side of the patient (Fig. 530, b). The bevel of the needle is placed upright so that the numbers on it and the syringe correspond. The position of the needle and syringe should parallel the course of the common carotid artery, and the angle between the skin and the needle need not exceed 15 degrees. The skin puncture is made and the point of the needle is allowed to rest on the common carotid artery (Fig. 530, c). With a single short thrust the artery is entered; the syringe is then quickly lowered as close as possible to the skin and the needle is threaded into the common carotid artery
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for about 2 cm. The bevel of the needle is rotated laterally so that the contrast medium can follow the lateral stream and most of it will flow into the internal carotid artery (Fig. 530, d). The injection is made as rapidly as possible, utilizing only 8 cc. of 35 per cent diodrast. After 6 cc. has been injected the initial film is taken. A seriograph is used which will make six exposures in four seconds
Fig. 530. a, Correct position of patient for injection of the right common carotid artery. Anesthesia consists of 2.5% solution of sodium pentothal given intravenously. b, The site of skin puncture is directly over the palpated carotid artery about 4 cm. above the clavicle. c, The skin puncture has been made and the point of the needle is resting on the common carotid artery. d, A puncture of the common carotid is made and the artery cannulalized for 3 cm. The needle is in correct position for injection of 35 per cent solution of diodrast. To obtain the A-P projection the face is simply placed upward. The rapid casette changer seriograph is set in motion when about 6 cc. of the diodrast has been injected.
thus making possible a study of the unilateral carotid arterial and venous systems.' After the injection and the exposures have been completed, the needle is quickly removed from the carotid artery and point pressure is applied without occluding the artery. The patient soon regains consciousness and is taken to his room, or he is permitted to remain in the x-ray department for an hour or two after which he may be taken home. Seventyfour percutaneous arteriograms have been carried out in this manner without any complications other than a slight soreness in the neck which persisted for two to three days. This pain may be relieved by the ap-
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plication of ice packs. Twenty-five bilateral arteriograms have been made without complications. Provided a successful unilateral carotid arteriogram has been obtained we think that there is no additional risk in bilateral carotid arteriography. Bilateral carotid arteriograms in the lateral and anteroposterior projections and percutaneous bilateral vertebral arteriograms have been made on one female patient, using a total of 90 cc. of 35 per cent solution of diodrast without deleterious effects. The use of such large quantities of the medium is rarely necessary and is not recommended as a routine procedure. Complications can usually be avoided by a skillful technic of injection, the selection of 35 per cent solution of diodrast, and the use of only 8 cc. of the contrast medium. Reactions to diodrast have occurred on three occasions, which consisted of a widespread allergic rash associated with severe itching. These symptoms were quickly relieved by the intravenous administration of benadryl. Occasionally it may be desirable to use local anesthesia only. In this instance, about 0.3 gm. (4! grains) of oral nembutal is administered two hours prior to the procedure. The stellate ganglion is injected bilaterally with 2 per cent procaine solution and a very slight amount of the local anesthesia is infiltered into the skin just over the common carotid artery. The rest of the procedure is exactly as described above. When carotid angiography is done under local anesthesia the injection of the stellate ganglia appears to diminish the vasospasms caused by the diodrast. Pneumoencephalography and percutaneous carotid arteriography have been combined in thirteen cases without harmful effects. If the pneumoencephalogram should prove inconclusive and arteriography appear desirable one may proceed before the intravenous anesthesia is discontinued and while the patient is still on the x-ray table. This procedure avoids a second anesthesia, a second trip to the x-ray department, and may add considerably to. the accuracy of the diagnosis. THE CONTRAST MEDIUM
Moniz used 60 per cent strontium bromide during his early experience which produced a 2.6 per cent mortality and. there were also a number of patients who experienced temporary hemiplegia. It was quite evident that this solution represented a real hazard. Subsequently, he used 25 per cent sodium iodide which likewise caused too many complications. In 1931 he introduced a colloidal solution of thorotrast, which was radioactive. Furthermore, the radioactive substance was taken up quite selectively by the reticulo-endothelial system. Consequently, large quantities of the radioactive material were concentrated in the liver and spleen. It was thought at first that the radioactivity was of such low magnitude that no harmful results would ensue. More recently there
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have been cases reported of malignancy developing in the liver. Furthermore, mechanical damage through occlusions of small cerebral vessels frequently ensued. Thorotrast also provoked thrombopenia that sometimes gave rise to postoperative hematomas. This material is still used in a great many European clinics and its advocates believe that if the amount is limited to 30 cc. or less no harmful effects will follow. Furthermore, they think that better visualization is obtained, especially of the smaller cerebral arteries, than with other media. Many American physicians have hesitated to use the colloidal solution of thorotrast. In 1939 Gross published his results with the use of 35 per cent solution of diodrast, which has the advantage of being soluble in water and readily excreted from the body. We have used both the 35 per cent and the 50 per cent solutions, and it has been our experience that the 35 per cent solution is far preferable. It does not cause as much vasospasm and appears to give adequate contrast. It would appear that the radiologic technic is of far more importance in determining good visualization of the vessels than is the 15 per cent difference in opacity between the solutions. In this respect it is often wise to obtain a preliminary plain x-ray film of the skull to aid in selecting the x-ray exposure that will give optimal visualization. We have injected 5 to 10 cc. of 35 per cent diodrast solution into the pericarotid spaces inadvertently on seven occasions with only minor undesirable effects. In each instance there was an increase in soreness for several days. No permanent induration developed. On the other hand, we have recently examined two patients who had experienced the same misfortune elsewhere when the colloidal solution of thorotrast was used. Both of these patients had disabling muscular contractions, obvious deformity, and complained of local tenderness and discomfort. Thirty-five per cent diodrast solution is not the perfect medium, however. It sometimes causes vasospasm and produces a sensation of vertigo if the injection is made under local anesthesia. There have been instances of transient hemiplegias resulting from the diodrast solution reported in the literature. This complication we believe can be avoided if small quantities are used. IMPROVEMENTS IN RADIOLOGIC EQUIPMENT
Roentgenologists have worked diligently to develop a technic that will produce good visualization of the contrast medium. In our clinic we formerly used no additional x-ray equipment. The cassettes were placed in position manually and could be changed at about two-second intervals by. an experienced team. In this way good pictures of the arterial phase could frequently be obtained. In 1931 Moniz began to use the anteroposterior position also. With the manual method one picture only could
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be obtained in the anteroposterior projection. Recently' many devices have been invented for changing the cassettes mechanically and rapidly. It is believed that shortly a simple economical device will be developed. For the past years we have been using the seriograph, which has been satisfactory but has the objection of being rather expensive and consequently not always practical. We have had no experience with the cinefluorograph but we believe that such a mechanism has great possibilities. Since the percutaneous method of puncturing the carotid artery has been developed to the point where it is considered almost as simple as doing a venipuncture in the forearm, it is believed that the use of angiography will become a great deal more widespread as soon as some cheap mechanical device is developed for the mechanical changing of the cassettes. We consider it no longer necessary to submit a patient to an operative exposure of the carotid artery unless the percutaneous method has failed. ANATOMY OF THE CEREBRAL CIRCULATION
Generally speaking, the external carotid arteries supply the skull, the soft parts of the head, the neck and the dura. The internal carotid arteries supply the supratentoral part of the brain (Fig. 2). The vertebral arteries supply the cerebral contents of the posterior fossa and in addition they contribute to the posterior cerebral arteries. In about 20 per cent of instances the posterior cerebral arteries received their blood supply almost entirely from the carotid system through the posterior communicating arteries. The internal carotid artery has no branches in the neck. It enters .the carotid canal and as it passes through the temporal bone it makes two sharp turns (Fig. 531). The first bend 'is forward and medially and the second bend is upward. The vessel then passes through the outer layer of the dura and enters the cavernous sinus where it makes a right angle bend and proceeds forward and upward medially just lateral to the sphenoid body. At the border of the anterior clinoid process the artery turns medially and penetrates the inner layer of the dura. It then leaves the cavernous sinus, making another bend forward at which point the posterior communicating artery is given off. It continues forward to the anterior perforated substance to the most medial portion of the lateral cerebral fissure where it breaks off into the anterior cerebral and middle cerebral arteries. The middle cerebral artery courses almost straight laterally beneath the anterior perforated substance lying in the lateral cerebral fissure. It is very short and its terminal branches begin so close to the carotid syphon that they form a vascular bundle. The vascular bundle consists of three
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branches which are of special interest in studying the arteriogramthe posterior temporal, the artery of the angular gyrus, and the posterior parietal. These vessels which lie in the lateral cerebral fissure are of great importance in the interpretation of the x-ray picture. They may be displaced by an expanding lesion. They also represent a frequent site of aneurysms. It is well to keep in mind, however, that variations of these vessels can occur in the normal individual and that often a combination
Fig. 531. Diagram showing the larger intracranial arteries demonstrable by carotid anteriography. A, Internal carotid; B, ophthalmic; C, posterior communicating; D, anterior choroidal; E. anterior cerebral; F, frontopolar; G, callosomarginal; H, pericallosal; I, middle cerebral; J, ascending frontal; K, posterior parietal; L, angular artery, M, posterior temporal.
analysis of several vessels will be necessary to effect a correct interpretation. Woringer and Gernez stated that the posterior cerebral artery is visible in about one-half the cases as a minute filament arising from the syphon. The anterior choroidal artery will sometimes arise from the middle cerebral rather than from the internal carotid artery. The anterior cerebral artery courses above the optic nerve in a medial direction and then forward where it communicates with the anterior cerebral artery on the opposite side by the way of the anterior communicating artery. At this point the vessel makes a sharp upward bend
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and divides into its terminal branches, the peri callosal and the callosomarginal arteries which run parallel to each other. The final branches supply the paracentral lobule. In the anteroposterior projection the anteriorcerebral artery runs in the midline. The anterior communicating artery is almost never visible because of the bony shadow. The frontopolar branches of the anterior cerebral arteries are visible in about three patients out of four.
Fig. 532. Diagram showing the cerebral venous system as outlined by angiography. A, Superior longitudinal sinus; B, inferior longitudinal sinus; C, transverse sinus; D, inferior longitudinal sinus; C, transverse sinus; D, straight sinus; E, great vein of Galen; F, internal cerebral vein; G, basal vein of Rosenthal; H, frontal ascending vein; D, Rolandic vein of Trolord; J, parietal ascending vein; K, communicating temporal vein of Labbe; L, descending temporal-occipital vein.
The venous system begins to fill approximately two to four seconds after the injection (Fig. 532). Initially the small superficial vessels appear filled and radiate toward the cerebral convexity. Next the larger superficial vessels fill and display considerable tortuosity. Several large veins soon appear and radiate in the direction of the insula. One of these is the anastomotic vein of Labbe which courses in a posterior direction to enter the transverse sinus. Another is the anastomotic vein of Trollard which courses upward and enters the superior sagittal sinus, and a third is a large vein which mainly follows the sylvian fissure. This brief description of the arterial and venous pattern will provide
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the fundamental knowledge necessary to interpret normal angiograms. It does not require much experience before one is able to identify the normal pattern. When an apparent abnormal pattern is encountered one must attempt to analyze just what .is unusual. Occasionally the contrast medium will produce sufficient vasospasm to cause a certain part of the pattern to appear rather avascular. Sometimes there will be filling on the contralateral sides due to pressure on the opposite common carotid artery during the injection. Abnormal anastomoses, abnormal and unusual sizes of vessels, and outpouchings will immediately be evident.
Fig. 533. Arteriogram revealing an aneurysm of the middle cerebral artery.
THE CLINICAL VALUE OF CAROTID ANGIOGRAPHY
The outstanding value of-carotid angiography is in the diagnosis and the management of intracranial aneurysms, arteriovenous fistulas and hemangiomas. There is no other method by which the existence of these conditions can be objectively demonstrated except by the use of a contrast medium intra-arterially. The exact relationship and location of an arterial aneurysm can be demonstrated (Figs. 533 to 535) by the use of the lateral and anteroposterior positions. Thus, the surgical approach can be carefully planned and adequate precaution can usually be executed because the pitfalls can be visualized beforehand. The size of
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the aneurysm can be estimated. When one has the knowledge of the size and the location of the aneurysm he can obtain some idea as to whether or not immediate surgical therapy is imperative. If the aneurysm has previously ruptured one may frequently determine whether or not there exists a localized hematoma. In the case illustrated (Figs, 534 and 535) a large intracerebral hematoma was present. The grave condition of the patient responded favorably when
Fig. 534. Carotid percutaneous arteriogram showing a large saccular aneurysm of the internal carotid artery (intracranial portion). The arrow shows the uppermost border of the aneurysm. The anterior cerebral artery is elevated at the anterior bend by a large associated intracerebral clot. Compare with Figure 535.
the blood clot was evacuated. We are convinced that this patient's life was preserved because the demonstration of the presence and location of this hematoma by carotid angiography enabled us to institute appropriate and accurate surgical therapy. Hence, a premalignant condition was successfully eradicated. Angiography can frequently be employed in conjunction with ventriculography or pneumoencephalography (Fig. 536). Often it is desirable to visualize the vascular pattern of an intracranial lesion. One patient revealed a small defect of the right anterior horn of the lateral ventricle
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upon pneumoencephalography. The arteriogram demonstrated a small capillary hemangioma in the corresponding area which responded to x-ray therapy. Thus a craniotomy was avoided. In another patient the encephalogram showed a protrusion into the temporal horn of the left
Fig. 535. Arteriogram of same patient as shown in Figure 534. Note the marked displacement of the anterior cerebral artery to the opposite side. A large intracerebral clot produced this displacement, was responsible for the comatose condition of the patient, and was successfully evacuated without the use of ventriculography.
lateral ventricle. An immediate left carotid angiogram revealed the mass to consist of capillary malformations which were interpreted as the cause of the recurrent seizures with an aura of dizziness, microscopia and tinnitus. Occasionally the vascular pattern as seen in the angiogram will afford a basis for making a tentative pathological diagnosis. In this manner the
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tentative preoperative diagnosis of glioblastoma multiforme has been made in several patients and this has been of some value in planning the surgical therapy and in predicting the prognosis. With six patients we have made -tp.e preoperative diagnosis of hemangioma by angiography. Since hemangioma may be successfully treated by' x-ray we have thus been able to avoid craniotomy.
Fig. 536. This arteriogram was made shortly after the pneumoencephalogram was completed, utilizing the same anesthesia. The combination use of pneumoencephalography and arteriography has enhanced the accuracy of the preoperative diagnosis.
Angiography on a patient suffering with an intracranial lesion does not aggravate his symptoms or condition. The necessity for immediate operation is thus avoided whereas when ventriculography is employed immediate craniotomy is often imperative. Occasionally the angiographic or the pneumographic evidence of an expanding lesion is inadequate alone to permit a definite conclusion but in combination they may be adequate for localization. Very occasionally it is necessary not only to have arteriographic and pneumographic evidence but also to have electroencephalographic tracings in order to
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reach a conclusion. All three of these methods have been used in the diagnosis of focal epileptogenic lesions of the cerebral cortex. It is believed that the practical use of angiography constitutes an additional effort to make more accurate preoperative or ante-mortem diagnoses. The more frequent use of angiography has demonstrated that anatomical variations of the vascular patterns exist in normal individuals which may make interpretations difficult. The accuracy of the interpretations in these patients may be increased by the use of bilateral carotid arteriograms. The diagnosis of cerebral arteriosclerosis, endarteritis obliterans, small cortical venous or arterial thromboses, cerebral scars and cortical atrophy has not proved accurate in our hands except in rare instances. It is accepted that the most complete filling obtainable by clinical angiography does not demonstrate all of the cerebral vessels. CONCLUSIONS
Carotid angiography is a relatively simple procedure. It can be performed unilaterally, bilaterally and immediately upon completion of pneumoencephalography. If it is used with wisdom, it aids considerably in the diagnosis of intracranial lesions previously not demonstrable. It may provide an excellent guide in the surgical removal of tumors and occasionally it affords adequate information for a tentative preoperative diagnosis of the type of lesion. Angiography is the only method that will demonstrate objectively the presence of intracranial aneurysms, arteriovenous fistulas, arteriovenous malformations, and hemangiomas prior to exploration. REFERENCES 1. Dandy,W. E.: Ann. Surge 68:5,1918. 2. Moniz, Egas P.: Handbuch der neurologic Ergans. Ser. 2. Berlin, Springer, 1940. 3. Sugar, 0., Holden, L. B. and Powell, C. B.: Am. J. Roentgenol. 61:166-182 (Feb.) 1949. 4. Ingraham, Franc D. and Cobb, Culley A., Jr.: J. Neurosurg. 4:5, 422-433 (Sept.) 1947. 5. Gross, S. W.: J. Indiana M. A.: 37:109, 1944. 6. Holm, 0.: Acta radiol. 25:163, 1944. 7. Woringer, E. and Gernez, A.: Presse med. 56:8881-82 (Dec. 18) 1948. 8. Domnick, 0.: Zentralbl..f. Neurochir. 4:184, 1940. 9. Wolff, H. and Schaltenbrand, G.: Zentralbl. f. Neurochir.: 4: 233,1939. 10. Turnbull, F.: An. J. Roentgenol.: 41:116, 1939. 11. Lindgren, E.: Brit. J. Radiol. 20:236,1947.