Original Article
The Anatomy of the Posterior Communicating Artery as a Risk Factor for Ischemic Cerebral Infarction
N Engl J Med 1994; 330:1565-1570June 2, 1994
- Abstract
Background
After the occlusion of an internal carotid artery the principal source of collateral flow is through the arteries of the circle of Willis, but the size and patency of these arteries are quite variable. Study of the anatomy of the collateral pathways in patients with internal-carotid-artery occlusion with or without infarction in the watershed area of the deep white matter may identify patterns that afford protection from ischemic infarction.
Methods
Using conventional magnetic resonance imaging and three-dimensional phase-contrast magnetic resonance angiography, we evaluated 29 consecutive patients (32 hemispheres at risk) with angiographically proved occlusion of the internal carotid artery. Four collateral pathways to the occluded vessel were evaluated: the proximal segment of the anterior cerebral artery, the posterior communicating artery, the ophthalmic artery, and leptomeningeal collateral vessels from the posterior cerebral artery.
Results
Only features of the ipsilateral posterior communicating artery were related to the risk of watershed infarction. The presence of posterior communicating arteries measuring at least 1 mm in diameter was associated with the absence of watershed infarction (13 hemispheres, no infarcts; P<0.001). Conversely, there were 4 watershed infarcts in the 6 hemispheres with posterior communicating arteries measuring less than 1 mm in diameter and 10 infarcts in the 13 hemispheres with no detectable flow in the ipsilateral posterior communicating artery.
Conclusions
A small (<1 mm in diameter) or absent ipsilateral posterior communicating artery is a risk factor for ischemic cerebral infarction in patients with internal-carotid-artery occlusion.
Media in This Article
Figure 1
Vessels Forming the Circle of Willis.Figure 2
Typical Findings in a Patient with Occlusion of the Right Internal Carotid Artery, a Large Right Posterior Communicating Artery (White Arrow), and No Watershed Infarct.Article Activity
- Article
The risk of cerebral infarction is multifactorial and includes genetic, anatomical, and environmental considerations. If a major vessel such as a carotid artery is occluded, flow may still be possible through primary or secondary collateral vessels. Primary collateral vessels are those that can respond quickly to low perfusion pressure with simple reversal of flow. Secondary collateral vessels require time for recruitment and are acquired in response to the stress of chronic hypoperfusion. Collateral pathways can protect perfusion in the event of severe stenosis or occlusion of a carotid artery. Therefore, the size and patency of primary collateral pathways may be risk factors for cerebral infarction in patients with severe stenosis or occlusion of a carotid artery.
To test this hypothesis, we studied subjects with occlusion of the internal carotid artery to assess their individual patterns of collateral pathways. Since these patients are dependent on collateral flow for cerebral perfusion, this population is a good one in which to evaluate cerebrovascular reserve from collateral flow. We correlated patterns of primary and secondary collateral flow with the presence and radiologic character of cerebral infarctions to ascertain the importance of individual collateral pathways in the perfusion of the cerebral hemisphere.
Methods
Twenty-nine consecutive patients presenting to Stanford University Hospital with 32 hemispheres at risk due to occlusion of the internal carotid artery were enrolled in the study. Two of the patients had both internal carotid arteries occluded. Another patient, followed with serial examinations, was treated for a giant aneurysm with intraluminal occlusion of an internal carotid artery, followed several weeks later by surgical alteration of the circle of Willis. All patients had angiographically proved occlusion of the internal carotid artery.
Twenty-four patients had progressive stenosis leading to chronic occlusion of the internal carotid artery; the cause was atherosclerotic disease in 23 and radiation therapy for a head and neck tumor in 1. Five patients had acute occlusion of the internal carotid artery: three from therapeutic balloon occlusion to reduce pressure in cerebral aneurysms and two from acute dissection (one traumatic and one due to fibromuscular dysplasia).
All patients underwent routine spin-echo magnetic resonance imaging of the brain with conventional T1-weighted (repetition time, 800 msec; echo time, 20 msec; 1 excitation), double-echo T2-weighted (repetition time, 2500 msec; echo time, 30 and 80 msec; 1 excitation) pulse sequences and three-dimensional phase-contrast magnetic resonance angiography through the circle of Willis. The three-dimensional phase-contrast magnetic resonance angiographic evaluation of the circle of Willis was accomplished with a repetition time of 25 msec, a minimal echo time (<10 msec), a flip angle of 25 degrees, and one excitation. Flow encoding producing a 180-degree phase shift for a velocity of 40 cm per second was used to produce images sensitive to all directions of flow. A matrix of 256 by 256 was used to maximize the resolution of small vessels while not exceeding reasonable scanning times. All images were acquired on a 1.5-T magnetic resonance imaging system (Signa, GE Medical Systems, Milwaukee).
Individual collateral pathways were identified by three-dimensional phase-contrast magnetic resonance angiography1-3. Two primary and two secondary collateral pathways were analyzed: retrograde flow (toward the internal carotid artery) in the proximal segment of the anterior cerebral artery; posterior-to-anterior (retrograde) flow in the posterior communicating artery; retrograde flow in the ophthalmic artery; and flow in the leptomeningeal collateral vessels from the posterior cerebral artery, which is a potential pathway from the posterior to the anterior circulation. The proximal segment of the anterior cerebral artery is a potential collateral conduit from the contralateral internal carotid artery through the anterior communicating artery. The ophthalmic-artery collateral represents a potential conduit between the external carotid artery and the ipsilateral internal carotid artery. The vessels forming the circle of Willis represent primary collateral sources (Figure 1Figure 1
Vessels Forming the Circle of Willis.). Recruitment of flow from the ophthalmic artery and leptomeningeal collateral vessels takes longer and represents secondary collateral pathways.The magnetic resonance image of each patient's brain was evaluated for infarction by a senior neuroradiologist who was unaware of the results of angiography. All infarcts were characterized as cortical, watershed (infarction in the watershed area of the deep white matter), mixed (those containing both cortical and watershed components), or other (infarcts not falling into the first three categories). It was assumed that watershed infarcts are due to low perfusion in the distal territories of the major intracranial arteries4 and therefore indicate a hemodynamic cause of infarction. Infarcts categorized as mixed all had substantial watershed components and were included with that group for statistical analysis. Non-watershed infarcts can be related to factors such as thromboembolism and thus were not considered to be hemodynamic in origin.
The magnetic resonance angiographic images were analyzed qualitatively for the presence or absence of four specific anatomical patterns with the use of axial collapsed-projection images. Velocity encoding during the image acquisition allows the production of images sensitive to the direction of the flow. When these images are reconstructed, they may be displayed as axial composite images that show flow in three orthogonal directions: right or left, anterior or posterior, and superior or inferior. Once the presence of a specific anatomical pathway was established on the projection images, flow-sensitive images were evaluated to determine whether that anatomical pathway served as a collateral vessel to the hemisphere jeopardized by internal-carotid-artery occlusion.
Since the status of the posterior communicating artery varies, the patients in the study were divided into three groups on the basis of the size of this vessel: large, small, or not visualized by either conventional or magnetic resonance angiography. For magnetic resonance angiography the minimal threshold of resolution of small posterior communicating arteries is uncertain. Very small vessels are occasionally seen on conventional angiography but not on magnetic resonance angiography. These vessels are less than 1 mm in diameter on conventional angiograms. Therefore, for magnetic resonance angiography, a threshold of less than 1 mm was used to define the small posterior communicating arteries. All patients with posterior communicating arteries visualized by angiography but not magnetic resonance angiography and those with posterior communicating arteries just visible by magnetic resonance angiography were considered to have small posterior communicating arteries. Patients whose posterior communicating arteries were easily visualized (those ≥ 1 mm in diameter) by magnetic resonance angiography were considered to have large posterior communicating arteries. This grouping of patients according to the size of the posterior communicating arteries was done separately from the analysis of the magnetic resonance images for infarcts to avoid any potential bias.
Two of the six patients assigned to the group with small posterior communicating arteries had posterior communicating arteries that were visualized with conventional angiography but were too small to be seen on magnetic resonance angiography. Thus, the direction of the flow could not be determined in these two patients; retrograde flow was assumed to exist in these small vessels for the purpose of statistical analysis. This assumption is conservative, since anterograde flow (away from the occluded internal carotid artery) in these tiny posterior communicating arteries is hemodynamically unlikely. Furthermore, if anterograde flow was present, it would essentially exclude this vessel as a collateral source for the occluded internal carotid artery. One patient had a posterior communicating artery originating directly from the occluded internal artery (also known as fetal origin), with no communication to the basilar artery. This patient was classified as having an absent posterior communicating artery for the purposes of statistical analysis, since the two conditions are hemodynamically equivalent.
Each patient was assigned to a group on the basis of his or her collateral-flow pattern. Fisher's exact test was used to establish whether the presence of an infarct was related to the collateral-flow pattern. Confidence intervals for odds ratios were calculated with the use of asymptotic methods based on the logistic model. When no infarcts were observed for a given two-by-two classification, a value of 0.5 was added to each count for the calculation of odds ratios and confidence intervals in order to avoid dividing these values by zero. Calculations were done with SAS version 6.07,5 which uses the algorithm of Mehta and Patel6 to perform Fisher's exact test for contingency tables larger than two by two.
Results
Twenty-nine patients with 32 hemispheres at risk due to occlusion of the internal carotid artery were evaluated. Twenty-one infarcts were observed in this series of patients; 14 were of the watershed type. The severity of symptoms in the watershed-infarct group ranged from no apparent symptoms in one patient to dense hemiplegia and global aphasia in another. Most patients with watershed infarcts were left with mild-to-moderate motor or speech deficits. Posterior communicating arteries were visualized in 19 of 32 hemispheres (59 percent); 13 (41 percent) were large and 6 (19 percent) were small. Twenty (62 percent) had retrograde flow in the proximal segment of the anterior cerebral artery. Twenty-seven (84 percent) had evidence of secondary collateral development: 12 (37 percent) had reversed flow in the ophthalmic artery, and 15 (47 percent) leptomeningeal collateral flow.
Despite the range in the prevalence of collateral pathways, only the presence and size of the posterior communicating arteries correlated (either positively or negatively) with watershed infarction (Table 1Table 1
Relation of Infarct Prevalence to the Anatomy of the Posterior Communicating Artery. and Table 2Table 2
Odds of Infarction According to the Status of the Posterior Communicating Artery.). Table 1 shows infarct-prevalence data according to the status of the posterior communicating artery. Large ( ≥ 1 mm) posterior communicating arteries were seen in 13 hemispheres at risk, none of which had watershed infarcts. Figure 2Figure 2Typical Findings in a Patient with Occlusion of the Right Internal Carotid Artery, a Large Right Posterior Communicating Artery (White Arrow), and No Watershed Infarct. shows the typical findings in a patient with a large posterior communicating artery and no evidence of a watershed infarction despite occlusion of the internal carotid artery. Four non-watershed infarcts (31 percent) were observed in this group.Six hemispheres at risk had small (<1 mm) posterior communicating arteries, four (67 percent) of which had watershed infarcts. Two of the watershed infarcts were large, and two were small (Table 1). The other two infarcts in this group were large cortical infarcts.
The remaining 13 hemispheres at risk had no radiologically demonstrable posterior-communicating-artery collateral flow. Ten hemispheres at risk (77 percent) in this group had watershed infarctions. Seven had large watershed infarcts, and one had a small watershed infarct. Two patients had mixed infarcts with large watershed components. Figure 3Figure 3
Typical Findings in a Patient with Occlusion of the Right Internal Carotid Artery, No Radiologically Discernible Posterior Communicating Artery, and a Large Watershed Infarct. shows the typical findings in a patient with an occluded right internal carotid artery, no radiologically discernible right posterior communicating artery, and a large watershed infarct.Only two patients without collateral flow in the posterior communicating artery did not have watershed infarctions. Both had large ophthalmic arteries with retrograde flow. One had bilateral internal-carotid-artery occlusion and reverse flow in both ophthalmic arteries. This patient had a large posterior communicating artery supplying one hemisphere at risk but no posterior communicating artery supplying the other hemisphere. The patient was blind ipsilateral to the absent posterior communicating artery. Vision was described as only mildly impaired ipsilateral to the large posterior communicating artery.
The presence of posterior-to-anterior collateral flow in large posterior communicating arteries correlated with the absence of watershed infarcts (P<0.001). Table 2 shows the odds of infarction according to the status of the posterior communicating artery. No other combinations of collateral flow showed this type of correlation.
Discussion
Our data, obtained with three-dimensional phase-contrast magnetic resonance angiography, show that one collateral pathway, a large posterior communicating artery, may protect against watershed infarction in patients with ipsilateral occlusion of the internal carotid artery. Conversely, a very small or absent ipsilateral posterior communicating artery increases the risk of a watershed infarction in these patients. Another study7 recently demonstrated the importance of the size of the posterior communicating artery to collateral perfusion. In that study, the size of the artery, measured preoperatively, was a good predictor of tolerance of ischemia after deliberate occlusion of the upper (P = 0.004) or lower (P = 0.036) basilar artery in patients with basilar-artery aneurysms.
No other pattern of collateral flow correlated with either the presence or absence of watershed infarction. However, other patterns of primary and secondary collateral flow were found too infrequently in this study population to draw any final conclusions about them.
Atheromatous disease is the single largest cause of internal-carotid-artery occlusion. A recent study8 reports progression to complete occlusion in 4.4 percent of 993 patients undergoing medical treatment for atheromatous carotid-artery disease. Twenty-three percent of these patients (10 of 44) were asymptomatic at the time of angiographic diagnosis of occlusion. Another study9 describes progression of stenosis of the internal carotid artery to occlusion in 27 asymptomatic patients. This suggests that internal-carotid-artery occlusion may be an underrecognized complication of conservative management. The question is why are some of these patients asymptomatic?
The circle of Willis provides the principal collateral pathway in the event of internal-carotid-artery occlusion. Circulation from the contralateral internal carotid artery may be provided by a patent anterior communicating artery in which there is anterograde flow in the contralateral proximal segment of the anterior cerebral artery and retrograde flow in the ipsilateral proximal segment of the anterior cerebral artery (Figure 1). Collateral flow from the vertebrobasilar system is provided by posterior-to-anterior flow in the posterior communicating artery. The circle of Willis is considered balanced if all segments are patent and of low resistance. Unfortunately, this occurs in only about 20 percent of subjects10. Therefore, the amount of protection in the form of collateral circulation provided by the circle of Willis varies. This variability may prove important, either to patients at risk for progression to internal-carotid-artery occlusion or to candidates for the surgical removal of the internal carotid artery.
When stenosis of the internal carotid artery progresses slowly to occlusion, secondary collateral pathways may be recruited. Principal among these are leptomeningeal collateral flow from the posterior-cerebral-artery circulation and retrograde flow in the ophthalmic artery from the ipsilateral external carotid artery. Other collateral pathways may be created and may prove important in specific cases. For example, Takahashi et al.11. described a patient with occlusion of the internal carotid artery whose dominant collateral pathway was from the posterior circulation by means of an enlarged anterior choroidal artery. Such pathways, however, are atypical and were not observed in our study.
Cerebral infarction represents a severe complication of internal-carotid-artery occlusion. The availability of collateral flow affects the likelihood of ischemic infarction in patients with internal-carotid-artery occlusion12-16. Therefore, the correlation of specific collateral pathways with cerebral infarction in these patients may provide data with clinical relevance for management, especially if the collateral pathways can be imaged noninvasively.
Source Information
From the Departments of Radiology (D.F.S., M.P.M., M.R.R., N.J.P., D.R.E.) and Neurosurgery (G.K.S.), Stanford University Medical Center, and the Department of Statistics, Stanford University (I.M.J., D.B.B.), Stanford, Calif.
Address reprint requests to Dr. Enzmann at the Department of Radiology, S072 Stanford University Medical Center, Stanford, CA 94305-5105.
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