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Intracranial arterial occlusion in the conscious neurologically intact dog
Intracranlal Arterial Occlusion in the Conscious Neurologically Intact Dog An Experimental Technique g'iLLIAM S. OWEN, M.D.,
New York
llospital
The effects of experimental occlusion of intracranial vessels have been tested by a number of investigators working with various laboratory animals; detailed studies of occlusion of cerebral arteries in the dog have been made by Rasmussen. 1'4"'t However, in all the reports the arterial occlusions occurred while the animal was under general anesthesia. Efforts to treat clinical vascular occlusion with anticoagulants, hypothermia, sympathetic block and other agents and methods have led to considerable controversy concerning the efficacy of each. Without reliable experimental controls it is difficult to evaluate the merit, or lack of merit, of the various methods; general anesthesia adds many variables to an already complex problem, z, s Although a healthy dog with normal cerebral vessels is not comparable to the human patient with cerebrovascular disease, if the occlusion is made to occur in the fully conscious, neurologically intact animal, the experimental situation somewhat parallels the human pathologic state of the cerebrovascular occlusion due to thrombosis or embolism, s There are numerous objections to general anesthesia during experimental cerebrovascular occlusion. It introduces variations in blood pressure, pulse, pulmonary ventilation, cerebral blood flow, cerebral o x y g e n consumption, vasomotor tone, temperature, and pCO z and pOz which can produce variations in the metabolism of the cerebral tissues being studied. These variables are not constant, but vary according to techniques, equipment and anesthetic agents used. From the Department of S u r g e r y (Neurosurgery), The New York tlospital-Cornell Medical Center, New York, New York.
Submitted for publication June 20, 1962. JSR -
Vol. II!, No. 3 - M a y ,
1963
--
Cornell Medical Center
The following report describes a device and the method of its application which accomplishes the occlusion of the middle cerebral a r t e r y in the c o n s c i o u s , neurologically intact dog.
DEVICE The basic materials are: (1) an Abbott Venotube, (2) a rubber band ] inch long, (3) a 3-0 black silk suture 12 inches long, (4) a 2-0 braided stainless steel wire 12 inches long, (5) a straight sewing needle and (6) polyethylene tubing (PE-190/$36) 4 inches long. These materials are easily modified and assembled to produce the device (Fig. l, A ) a n d permit its snare-like action (Fig. 1, B). Approximately 4 ram. of the loop for the snare should
.
' ~. " [ [[ [
" [~ [. " " _
~j//
Fig. 7. A, The de+ice is tully assembled with the silk snare around a blood vessel. B, The blood vessel is occluded by the snare after the rubber band is released by removing the "firing pin."
171
172
OWEN
JSR
- -
Vo/. II!, No. 3 -
May, 196.3
protrude from the polyethylene shaft after the rubber band has been stretched and held in place by the modified sewing needle ("firing pin"). The snare retracts into the polyethylene tubing after the pin is extracted by the stainless steel pull-wire. The p',astic portions of this device are sterilized by soaking in 1:1000 aqueous benzalkonium solution. The r e m a i n i n g parts are autoclaved. __
Anchor
~ . -
OPERATION A right temporal craniectomy is performed under sterile conditions. Intravenous sodium pentobarbital (25 mg./kg.) is the anesthetic agent used. Moderate hyperventilation is accomplished by a mechanical device controlling respiration which delivers 100 per cent oxygen to the tracheobronchial tree by means of an endotracheal tube. Intravenous 5 per cent sodium chloride solution (7cc./kg.) is used to shrink the brain (urea would serve a similar purpose). An oblique linear skin incision is made from below the right zygoma to a point 1 cm. to the left of the midline and carried through the galea. A V-shaped incision is made in the temporalis fascia and muscle. The muscle is reflected anteriorly and a burr hole made in the superior portion of the temporal bone. The bony defect is enlarged and the dura incised. The brain is gently retracted, the proximal portion of the middle cerebral artery isolated, and a 3-0 black silk ligature placed around the artery as close =
i t
Fig. 3.
The pull-wire is secured beneath tile skin sutures.
as possible to its origin from the internal carotid artery. The ligature forms the snare for the device, which is attached (Fig. 2) and anchored beneath the temporalis fascia. The pull-wire is brought out through the skin and the head of the "firing p i n " lies free between the edges of the temporalis fascia, which is closed over the device with interrupted silk suture. The dura is not closed b u t merely laid over the exposed cerebral cortex. The gatea and skin are closed as separate layers with interrupted silk sutures and the pull-wire secured beneath the skin sutures (Fig. 3). Collodion is applied to the wound as the only dressing. Diphenylhydantoin (3 m g . / k g . / d a y ) is given the day prior to operation and continued for two weeks. Postoperative antibiotics are not used.
OCCLUSION h.
t t..'.
Fig. 2.
The device is attached to the ligature around the middle cerebral artery.
On the second postoperative day the animal is examined and, if neurologically intact, the pull-wire is extracted to r e l e a s e the "firing p i n . " The snare is thus tightened, occluding the middle cerebral artery immediately. Tile animal is reexamined at intervals thereafter to observe any neurologic changes. Skin sutures are removed on the seventh postoperative day. The animal is sacrificed on the twenty-first postoperative day and prior to its removal the brain is perfused with normal saline, followed by 10 per cent formalin. A small amount of
JSR -
Vol, !11, No. 3 - M a y ,
1963
methylene blue dye is injected into the right carotid artery near the end of the perfusion to demonstrate the o c c I u s i o n of the middle cerebral artery.
i/ESULTS Five mongrel dogs weighing 12 to 16 kg. have had occlusion of the middle cerebral artery with this technique. Complete occlusion of the middle cerebral artery was demonstrated in all animals. There were no hemorrhages due to the u s e of the device and no wound infections. Gross examination of the s e c t i o n e d brains revealed obvious areas of i n f a r c t i o n in all s p e c i m e n s , the internal capsule region being involved most consistently. All the dogs exhibited varying degrees of contralateral hemiparesis and one had a cont,.alateral h o m o n y m o u s hemianopsia. The neurologic deficits were greatest during the first several days following the occlusion and were minimal by the twenty-first day,
CON CLUSION The method d e s c r i b e d for occluding the middle cerebral artery in dogs avoids the variables introduced by general a n e s t h e s i a . After brief experience with a control s e r i e s one may study the effect of cerebrovascular occlusion under different conditions and with various therapeutic m e a s u r e s . The device described need not be restricted in its u s e to the cerebrovascular circulation, but with some refinement can be applied to other surgically approachable blood v e s s e l s .
INTRACRANIAL ARTERIAL OCCLUSION 173 Thus, by a relatively simple device the middle cerebral artery has been occluded in a neurologically intact dog; other intracranial v e s s e l s could be similarly occluded. The method has particular advantage in that the lesion is produced without the variables that accompany general a n e s t h e s i a . In addition, the method provides a means of studying experimentally the influence of various agents that may enhance or detract from the effects of occluding intracranial blood v e s s e l s .
REFERENCES 1. llarvey, J., and Rasmussen, T.: Occlusion of the middle cerebral artery. An experimental study. A.M.A. Arch. Neurolog. & Psychiat., 66: 20-29, 1951. 2. ltimwich, W. A., llamburger, E., Maresca, R.,and llimwieh, It. E.: Brain metabolisnl in m~n: unanesthetized and in Pentothal narcosis. Am..]. Psyehiat., 103: 689-690, 1947. 3. Kety, S. S.: Circulation and metabolism of the human brain in health and disease. Am. J. Med., 8: 205-217, 1950. 4. Meyer, j. S.: Circulatory changes following occlusion of the middle cerebral artery and their relation to function. J.Neurosurg., 15: 653-673, 1958. 5. Ralston, B., Rasmussen, T., and Kennedy, T.: Occlusion of the middle cerebral artery under normotension, and anemically induced and clinically induced hypotension. J. Neurosurg., 12: 26-33, 1955. 6. Rasmussen, T. B.: Experimental ligation of the cerebral arteries of the dog. Thesis, University of Minnesota, 1938. 7. Thompson, ll. K., and Smith, G. W.: Experimental occlusion of the middle cerebral artery during arterial hypotension. Tr. Am. Neurolog. Assn., 203-206, 1951. 8. Wechslcr, I1. 1.... l)ripps, R. D., and Kety, S. S.: Blood flow and oxygen consumption of the human brain during anesthesia produce,t by thiopentat. Anesthesiol., 12: 308-314, 1951.
New York
llospital
The effects of experimental occlusion of intracranial vessels have been tested by a number of investigators working with various laboratory animals; detailed studies of occlusion of cerebral arteries in the dog have been made by Rasmussen. 1'4"'t However, in all the reports the arterial occlusions occurred while the animal was under general anesthesia. Efforts to treat clinical vascular occlusion with anticoagulants, hypothermia, sympathetic block and other agents and methods have led to considerable controversy concerning the efficacy of each. Without reliable experimental controls it is difficult to evaluate the merit, or lack of merit, of the various methods; general anesthesia adds many variables to an already complex problem, z, s Although a healthy dog with normal cerebral vessels is not comparable to the human patient with cerebrovascular disease, if the occlusion is made to occur in the fully conscious, neurologically intact animal, the experimental situation somewhat parallels the human pathologic state of the cerebrovascular occlusion due to thrombosis or embolism, s There are numerous objections to general anesthesia during experimental cerebrovascular occlusion. It introduces variations in blood pressure, pulse, pulmonary ventilation, cerebral blood flow, cerebral o x y g e n consumption, vasomotor tone, temperature, and pCO z and pOz which can produce variations in the metabolism of the cerebral tissues being studied. These variables are not constant, but vary according to techniques, equipment and anesthetic agents used. From the Department of S u r g e r y (Neurosurgery), The New York tlospital-Cornell Medical Center, New York, New York.
Submitted for publication June 20, 1962. JSR -
Vol. II!, No. 3 - M a y ,
1963
--
Cornell Medical Center
The following report describes a device and the method of its application which accomplishes the occlusion of the middle cerebral a r t e r y in the c o n s c i o u s , neurologically intact dog.
DEVICE The basic materials are: (1) an Abbott Venotube, (2) a rubber band ] inch long, (3) a 3-0 black silk suture 12 inches long, (4) a 2-0 braided stainless steel wire 12 inches long, (5) a straight sewing needle and (6) polyethylene tubing (PE-190/$36) 4 inches long. These materials are easily modified and assembled to produce the device (Fig. l, A ) a n d permit its snare-like action (Fig. 1, B). Approximately 4 ram. of the loop for the snare should
.
' ~. " [ [[ [
" [~ [. " " _
~j//
Fig. 7. A, The de+ice is tully assembled with the silk snare around a blood vessel. B, The blood vessel is occluded by the snare after the rubber band is released by removing the "firing pin."
171
172
OWEN
JSR
- -
Vo/. II!, No. 3 -
May, 196.3
protrude from the polyethylene shaft after the rubber band has been stretched and held in place by the modified sewing needle ("firing pin"). The snare retracts into the polyethylene tubing after the pin is extracted by the stainless steel pull-wire. The p',astic portions of this device are sterilized by soaking in 1:1000 aqueous benzalkonium solution. The r e m a i n i n g parts are autoclaved. __
Anchor
~ . -
OPERATION A right temporal craniectomy is performed under sterile conditions. Intravenous sodium pentobarbital (25 mg./kg.) is the anesthetic agent used. Moderate hyperventilation is accomplished by a mechanical device controlling respiration which delivers 100 per cent oxygen to the tracheobronchial tree by means of an endotracheal tube. Intravenous 5 per cent sodium chloride solution (7cc./kg.) is used to shrink the brain (urea would serve a similar purpose). An oblique linear skin incision is made from below the right zygoma to a point 1 cm. to the left of the midline and carried through the galea. A V-shaped incision is made in the temporalis fascia and muscle. The muscle is reflected anteriorly and a burr hole made in the superior portion of the temporal bone. The bony defect is enlarged and the dura incised. The brain is gently retracted, the proximal portion of the middle cerebral artery isolated, and a 3-0 black silk ligature placed around the artery as close =
i t
Fig. 3.
The pull-wire is secured beneath tile skin sutures.
as possible to its origin from the internal carotid artery. The ligature forms the snare for the device, which is attached (Fig. 2) and anchored beneath the temporalis fascia. The pull-wire is brought out through the skin and the head of the "firing p i n " lies free between the edges of the temporalis fascia, which is closed over the device with interrupted silk suture. The dura is not closed b u t merely laid over the exposed cerebral cortex. The gatea and skin are closed as separate layers with interrupted silk sutures and the pull-wire secured beneath the skin sutures (Fig. 3). Collodion is applied to the wound as the only dressing. Diphenylhydantoin (3 m g . / k g . / d a y ) is given the day prior to operation and continued for two weeks. Postoperative antibiotics are not used.
OCCLUSION h.
t t..'.
Fig. 2.
The device is attached to the ligature around the middle cerebral artery.
On the second postoperative day the animal is examined and, if neurologically intact, the pull-wire is extracted to r e l e a s e the "firing p i n . " The snare is thus tightened, occluding the middle cerebral artery immediately. Tile animal is reexamined at intervals thereafter to observe any neurologic changes. Skin sutures are removed on the seventh postoperative day. The animal is sacrificed on the twenty-first postoperative day and prior to its removal the brain is perfused with normal saline, followed by 10 per cent formalin. A small amount of
JSR -
Vol, !11, No. 3 - M a y ,
1963
methylene blue dye is injected into the right carotid artery near the end of the perfusion to demonstrate the o c c I u s i o n of the middle cerebral artery.
i/ESULTS Five mongrel dogs weighing 12 to 16 kg. have had occlusion of the middle cerebral artery with this technique. Complete occlusion of the middle cerebral artery was demonstrated in all animals. There were no hemorrhages due to the u s e of the device and no wound infections. Gross examination of the s e c t i o n e d brains revealed obvious areas of i n f a r c t i o n in all s p e c i m e n s , the internal capsule region being involved most consistently. All the dogs exhibited varying degrees of contralateral hemiparesis and one had a cont,.alateral h o m o n y m o u s hemianopsia. The neurologic deficits were greatest during the first several days following the occlusion and were minimal by the twenty-first day,
CON CLUSION The method d e s c r i b e d for occluding the middle cerebral artery in dogs avoids the variables introduced by general a n e s t h e s i a . After brief experience with a control s e r i e s one may study the effect of cerebrovascular occlusion under different conditions and with various therapeutic m e a s u r e s . The device described need not be restricted in its u s e to the cerebrovascular circulation, but with some refinement can be applied to other surgically approachable blood v e s s e l s .
INTRACRANIAL ARTERIAL OCCLUSION 173 Thus, by a relatively simple device the middle cerebral artery has been occluded in a neurologically intact dog; other intracranial v e s s e l s could be similarly occluded. The method has particular advantage in that the lesion is produced without the variables that accompany general a n e s t h e s i a . In addition, the method provides a means of studying experimentally the influence of various agents that may enhance or detract from the effects of occluding intracranial blood v e s s e l s .
REFERENCES 1. llarvey, J., and Rasmussen, T.: Occlusion of the middle cerebral artery. An experimental study. A.M.A. Arch. Neurolog. & Psychiat., 66: 20-29, 1951. 2. ltimwich, W. A., llamburger, E., Maresca, R.,and llimwieh, It. E.: Brain metabolisnl in m~n: unanesthetized and in Pentothal narcosis. Am..]. Psyehiat., 103: 689-690, 1947. 3. Kety, S. S.: Circulation and metabolism of the human brain in health and disease. Am. J. Med., 8: 205-217, 1950. 4. Meyer, j. S.: Circulatory changes following occlusion of the middle cerebral artery and their relation to function. J.Neurosurg., 15: 653-673, 1958. 5. Ralston, B., Rasmussen, T., and Kennedy, T.: Occlusion of the middle cerebral artery under normotension, and anemically induced and clinically induced hypotension. J. Neurosurg., 12: 26-33, 1955. 6. Rasmussen, T. B.: Experimental ligation of the cerebral arteries of the dog. Thesis, University of Minnesota, 1938. 7. Thompson, ll. K., and Smith, G. W.: Experimental occlusion of the middle cerebral artery during arterial hypotension. Tr. Am. Neurolog. Assn., 203-206, 1951. 8. Wechslcr, I1. 1.... l)ripps, R. D., and Kety, S. S.: Blood flow and oxygen consumption of the human brain during anesthesia produce,t by thiopentat. Anesthesiol., 12: 308-314, 1951.