Studies of leptomeningeal collateral circulation in Macacus rhesus

Abstract

In previous experiments on dogs (Symon, 1960), it was shown that, within a few minutes of occlusion of a major cerebral vessel, free flow of blood occurred within the area of supply of the occluded vessel, borne via leptomeningeal anastomoses from the vascular fields of adjacent vessels. Since it has been established anatomically (Vander Eecken, 1959) that the number and size of collateral vessels within the pial circulation decreases with increasing convolution of the cortex in higher animals, it became of interest to find out whether such prompt collateral flow could be demonstrated in these animals as well. Similar experiments were therefore carried out in the primate Macacus rhesus. METHODSEighteen macaque monkeys weighing between 3 and 5 kg were used. They were anaesthetized with intravenous thiopentone sodium in an initial dose of 25 mg/kg, supplemented at intervals by intravenous doses of 25 mg as required. An endotracheal tube was passed to facilitate maintenance of a clear airway throughout. The blood pressure was continuously recorded from the cannulated femoral artery.Dissection of the carotid sinus. The area of the right carotid sinus was exposed, and the carotid-sinus nerve divided. No ligations of vessels were necessary, since in the macaque, unlike the dog, the main route for blood from the area of the carotid sinus to the cerebral cortex is via the internal carotid artery, and anastomoses between intra-and extra-cranial vessels are small and functionally unimportant.A polythene cannula with dead space 0 1 ml. was introduced into the lingual artery and threaded for a few millimetres down the external carotid artery, so that its tip lay in the carotid sinus, care being taken not to occlude the origin of the internal carotid artery. Injections of 0-5 ml. of labelled erythrocyte suspension were made through this cannula from a tuberculin syringe. These injections were made as rapidly as possible. After each injection the cannula was flushed out and filled with a solution of heparin (500 u./ml.). In some experiments this dissection was performed on both sides.Exposure and occlusion of the vertebral arteries in the neck. A curved transverse incision was made half an inch (12 mm) above the sternoclavicular joints, extending for 2-5 cm on either side of the mid line. Both sternomastoid muscles were divided and the carotid sheaths gently retracted medially. The origin of scalenus anterior was defined, behind the carotid sheath, arising from the transverse processes of the cervical vertebrae. The vertebral artery was found in the interval between the longus cervicis muscle on the vertebral bodies and

Haemodynamics of the circle of Willis and the leptomeningeal anastomoses: an electromagnetic flowmeter study of intracranial arterial occlusion in the monkey

“…The data do not agree with the result of a previous study (Symon, 1961) using radioactive isotopes, in which the main collateral was thought to be from the contralateral anterior cerebral artery. This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment.…”

“…This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment. Spasm in basal vessels in the monkey following mechanical stimulation has been reported by Harvey and Rasmussen (1951), Lende (1960), and Symon (1961). In the present study, slight spasm was observed in two animals.…”

Haemodynamics of the circle of Willis and the leptomeningeal anastomoses: an electromagnetic flowmeter study of intracranial arterial occlusion in the monkey

“…The data do not agree with the result of a previous study (Symon, 1961) using radioactive isotopes, in which the main collateral was thought to be from the contralateral anterior cerebral artery. This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment.…”

“…This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment. Spasm in basal vessels in the monkey following mechanical stimulation has been reported by Harvey and Rasmussen (1951), Lende (1960), and Symon (1961). In the present study, slight spasm was observed in two animals.…”

Effect of Oxygen Affinity of Liposome-Encapsulated Hemoglobin on Cerebral Ischemia and Reperfusion as Detected by Positron Emission Tomography in Nonhuman Primates

“…Although the evaluation timing after the onset of ischemia (6 h) was shorter than in rodent models (24 h), the preferential protection in the cortex rather than basal ganglia was similar to those in rodent studies as well as in primate models . This may result from similarity in the cerebral perfusion and experimental models—focal ischemia of the MCA territory with leptomeningeal collaterals followed by reperfusion, which is similar to clinical brain ischemia, suggesting utility in a clinical setting. Significant preservation of CMRO 2 and morphological context in the cortex suggests that LEH, regardless of O 2 affinity, is useful in the protection of the penumbral cortex from cerebral I/R injury.…”

“…In particular, in the brain I/R, it does not seem to be as simple as O 2 working to maintain aerobic metabolism favoring efficient energy synthesis, since benefits occur late after reperfusion with preferential protection of the cortex rather than basal ganglia. There was a clear contrast between the damaged basal ganglia with heavy LEH deposition and the intact cortex without a trace of LEH , suggesting that the cortex might have been protected by circulating LEH via collateral flow through the leptomeningeal system . Its existence had been recognized by the substantial blood flow starting immediately after MCA occlusion mainly from the anterior communicating artery .…”

The concepts of thresholds of ischaemia in relation to brain structure and function.

“…The distribution of the middle cerebral artery in the experimental primate Perfusion studies following acute experimental occlusion of the middle cerebral artery (Symon, 1961) and pathological studies of the brain inanimalswhich have survived up to three years following middle cerebral occlusion (Brierley and Symon, 1977) have shown that the average perfusion of the middle cerebral artery in the monkey is very similar to the description of Shellshear (1921) and Abbie (1934) in man. Thus Symon (1961) showed by a technique of carmine-gelatine perfusion that the intensity of perfusion after middle cerebral artery occlusion was reduced in the parietal and temporal lobes, particularly the opercular and insular areas.…”

Haemodynamics of the circle of Willis and the leptomeningeal anastomoses: an electromagnetic flowmeter study of intracranial arterial occlusion in the monkey

“…The data do not agree with the result of a previous study (Symon, 1961) using radioactive isotopes, in which the main collateral was thought to be from the contralateral anterior cerebral artery. This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment.…”

“…This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment. Spasm in basal vessels in the monkey following mechanical stimulation has been reported by Harvey and Rasmussen (1951), Lende (1960), and Symon (1961). In the present study, slight spasm was observed in two animals.…”

Effect of Oxygen Affinity of Liposome-Encapsulated Hemoglobin on Cerebral Ischemia and Reperfusion as Detected by Positron Emission Tomography in Nonhuman Primates

“…Although the evaluation timing after the onset of ischemia (6 h) was shorter than in rodent models (24 h), the preferential protection in the cortex rather than basal ganglia was similar to those in rodent studies as well as in primate models . This may result from similarity in the cerebral perfusion and experimental models—focal ischemia of the MCA territory with leptomeningeal collaterals followed by reperfusion, which is similar to clinical brain ischemia, suggesting utility in a clinical setting. Significant preservation of CMRO 2 and morphological context in the cortex suggests that LEH, regardless of O 2 affinity, is useful in the protection of the penumbral cortex from cerebral I/R injury.…”

“…In particular, in the brain I/R, it does not seem to be as simple as O 2 working to maintain aerobic metabolism favoring efficient energy synthesis, since benefits occur late after reperfusion with preferential protection of the cortex rather than basal ganglia. There was a clear contrast between the damaged basal ganglia with heavy LEH deposition and the intact cortex without a trace of LEH , suggesting that the cortex might have been protected by circulating LEH via collateral flow through the leptomeningeal system . Its existence had been recognized by the substantial blood flow starting immediately after MCA occlusion mainly from the anterior communicating artery .…”

The concepts of thresholds of ischaemia in relation to brain structure and function.

“…The distribution of the middle cerebral artery in the experimental primate Perfusion studies following acute experimental occlusion of the middle cerebral artery (Symon, 1961) and pathological studies of the brain inanimalswhich have survived up to three years following middle cerebral occlusion (Brierley and Symon, 1977) have shown that the average perfusion of the middle cerebral artery in the monkey is very similar to the description of Shellshear (1921) and Abbie (1934) in man. Thus Symon (1961) showed by a technique of carmine-gelatine perfusion that the intensity of perfusion after middle cerebral artery occlusion was reduced in the parietal and temporal lobes, particularly the opercular and insular areas.…”

Haemodynamics of the circle of Willis and the leptomeningeal anastomoses: an electromagnetic flowmeter study of intracranial arterial occlusion in the monkey

“…The data do not agree with the result of a previous study (Symon, 1961) using radioactive isotopes, in which the main collateral was thought to be from the contralateral anterior cerebral artery. This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment.…”

“…This discrepancy, however, is probably due to the absence of any recognizable spasm in the ipsilateral anterior cerebral artery following M1 occlusion in the present experiment. Spasm in basal vessels in the monkey following mechanical stimulation has been reported by Harvey and Rasmussen (1951), Lende (1960), and Symon (1961). In the present study, slight spasm was observed in two animals.…”

Effect of Oxygen Affinity of Liposome-Encapsulated Hemoglobin on Cerebral Ischemia and Reperfusion as Detected by Positron Emission Tomography in Nonhuman Primates

“…Although the evaluation timing after the onset of ischemia (6 h) was shorter than in rodent models (24 h), the preferential protection in the cortex rather than basal ganglia was similar to those in rodent studies as well as in primate models . This may result from similarity in the cerebral perfusion and experimental models—focal ischemia of the MCA territory with leptomeningeal collaterals followed by reperfusion, which is similar to clinical brain ischemia, suggesting utility in a clinical setting. Significant preservation of CMRO 2 and morphological context in the cortex suggests that LEH, regardless of O 2 affinity, is useful in the protection of the penumbral cortex from cerebral I/R injury.…”

“…In particular, in the brain I/R, it does not seem to be as simple as O 2 working to maintain aerobic metabolism favoring efficient energy synthesis, since benefits occur late after reperfusion with preferential protection of the cortex rather than basal ganglia. There was a clear contrast between the damaged basal ganglia with heavy LEH deposition and the intact cortex without a trace of LEH , suggesting that the cortex might have been protected by circulating LEH via collateral flow through the leptomeningeal system . Its existence had been recognized by the substantial blood flow starting immediately after MCA occlusion mainly from the anterior communicating artery .…”

The concepts of thresholds of ischaemia in relation to brain structure and function.

“…The distribution of the middle cerebral artery in the experimental primate Perfusion studies following acute experimental occlusion of the middle cerebral artery (Symon, 1961) and pathological studies of the brain inanimalswhich have survived up to three years following middle cerebral occlusion (Brierley and Symon, 1977) have shown that the average perfusion of the middle cerebral artery in the monkey is very similar to the description of Shellshear (1921) and Abbie (1934) in man. Thus Symon (1961) showed by a technique of carmine-gelatine perfusion that the intensity of perfusion after middle cerebral artery occlusion was reduced in the parietal and temporal lobes, particularly the opercular and insular areas.…”