Periorbital Ultrasound Hemodynamics
Findings
in Patients With Cerebral Vascular Disease
Jonathan B. Towne, MD; Sergio Salles-Cunha, MSc; Victor M. Bernhard, MD
\s=b\ The direction of supraorbital and frontal artery flow and its response to compression of the superficial temporal, facial, and angular arteries were measured in 250 carotid arteries in 114 patients. All patients had arch and/or selective carotid arteriography. The carotid arteries were placed into the following three groups: hemodynamically normal, greater than 60% occlusion of the internal carotid artery, and total occlusion of the internal carotid artery. The test's accuracy was 94.5% in the hemodynamically normal group, 68.8% in the totally occluded group, and only 51.4% in the group with hemodynamically significant stenosis. Although the carotid Doppler examination is not reliable in detecting hemodynamically significant lesions of the internal carotid artery, it is valuable in assessing the adequacy of collateral cerebral circulation.
(Arch Surg 114:158-160, 1979) of the
arteries gives information in internal carotid artery occlusive disease and establishes the adequa¬ cy of collateral cerebral circulation. The periorbital anasto¬ moses between the branches of the external carotid artery and the ophthalmic branch of the distal internal carotid artery have been described.1 ·· Normally in the absence of a hemodynamically significant internal carotid artery steno¬ sis there is antegrade flow from within the orbit outward to the face that increases or augments when branches of the external carotid artery are compressed. With internal carotid artery stenosis, the direction of flow is reversed as these vessels supply collateral flow to the distal internal carotid system. This prospective study assessed the value
examination periorbital Doppler important hemodynamic
Accepted for publication July 12, 1978. From the Department of Surgery, Medical College of Wisconsin, Milwaukee County Medical Complex. Reprint requests to Department of Surgery, Milwaukee County Medical Complex, 8700 W Wisconsin Ave, Milwaukee, WI 53226 (Dr Towne).
of the supraorbital Doppler examination in determining the adequacy of collateral cerebral circulation in patients with totally occluded or hemodynamically significant stenosis of the internal carotid artery by comparing roent¬ genographic anatomic findings with clinical symptoms. MATERIALS AND METHODS We performed carotid Doppler examinations on all patients undergoing aortic arch and selective carotid artery arteriography
for the evaluation of extracranial carotid occlusive disease between November 1975 and March 1978. This group included patients with neurologic symptoms as well as patients with asymptomatic carotid bruits. We performed the Doppler test as described by Brockenbrough1 with the compression maneuvers described by Barnes et al." The patient was examined while in a supine position with his head on a small pillow. A directional Doppler was used to determine the direction of flow of the frontal and supraorbital arteries. While continuing to listen over these arteries, the ipsilateral and contralateral superficial temporal artery, facial artery, and angular artery were sequentially compressed. The effect of the compression maneuvers on the direction and velocity of periorbital flow was noted. The superficial temporal artery was compressed anterior and superior to the external auditory meatus, the facial artery was compressed just anterior to the angle of the mandible and the angular artery at the inferior medial aspect of the orbit. When two people performed these tests, both superficial tempo¬ ral arteries and both facial arteries were simultaneously compressed to prevent movement of the head. If a positive response was noted, each artery was compressed individually to determine the source of the collateral flow. Normal response was antegrade flow of blood from within the orbit outward to the face that was either augmented or unaffected by the compression maneuvers. A hemodynamically significant stenosis caused retro¬ grade flow in the frontal and supraorbital vessels, which was diminished or obliterated by the compression maneuvers. In addition, retrograde flow reverting to antegrade flow with
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
compression as well as antegrade flow diminishing with compres¬ sion were positive responses. All studies that demonstrated abnor¬ mal direction of flow but were unaffected by compression of the ipsilateral and contralateral external carotid branches were repeated to eliminate the possibility of inaccurate probe place¬ ment. Common carotid artery compression was not used. All patients had aortic arch and selective carotid arteriography with standard biplane films of the carotid bifurcation most often performed through right femoral artery catheterization. A few patients with diffuse aortoiliac occlusive disease were studied by the transaxillary approach. Occasionally, spot films were obtained to further delineate the pathologic anatomy. The amount of stenosis was measured by comparing the diameter of the narrow¬ est portion of the internal carotid artery to the diameter of the normal lumen distal to the stenosis. The arteriograms were evaluated without knowing the results of the Doppler evaluation, and the arteries were placed in the following three groups: (1) totally occluded, (2) greater than 60% stenosis, and (3) hemody¬ namically normal vessels. This later category included all patients with less than 60% stenosis as well as all normal vessels. A 60%-stenosis represents an 84% decrease in the cross-sectional area and is hemodynamically important. Two hundred and fifty carotid arteries were evaluated in 114 patients. Several patients had multiple Doppler examinations to determine the reproducibility of the test.
RESULTS The Doppler evaluation was normal in 171 of 181 hemo¬ dynamically normal vessels for an accuracy of 94.5% (Table). There were ten false-positive results (5.5%). Of the
37 internal carotid arteries with greater than 60% stenosis, the test was positive in 19 (51.4%) and negative in 18 (48.6%). In 32 totally occluded vessels, the test was positive in 22 (68.8%) and negative in ten (31.2%). We evaluated the examinations in which both frontal and supraorbital flow were antegrade and did not change with compression maneuvers. This group contained 44 of the 250 arteries (17.6%), only nine of which had hemody¬ namically significant occlusive disease of the internal ca¬ rotid artery for an incidence of 20%. Therefore, an evalua¬ tion with antegrade flow without augmentation has an 80% chance of being normal. There were 28 false-negative examinations in this series. This group's responses to the compression maneuvers were as follows: of the ten totally occluded arteries, three had antegrade flow without augmentation and seven had antegrade flow with augmentation, and of the 18 arteries with greater than 60% occlusion, six had antegrade flow without augmentation and 12 had antegrade flow with augmenta¬ tion. Five of the nine arteries that had antegrade flow without augmentation were in neurologically asymptomat¬ ic patients. Four other patients had the following neuro¬ logic symptoms: vague arm weakness (one), vertebral basilar symptoms (one), transient ischemie attack (one), Results of
Supraorbital Doppler Evaluation Accuracy, %
Normal > 60% stenosis Total occlusion
False
False-
Negative, %
Positive, %
94.5
5.5
51.4
48.6
68.8
31.2
...
and amaurosis fugax (one). There were 19 arteries with antegrade flow and augmentation of periorbital flow on compression of branches of the external carotid artery. Thirteen patients were asymptomatic and six had the following neurologic symptoms: amaurosis fugax (two), nonspecific neurologic symptoms (two), cerebrovascular accident (one), and decreased memory (one). COMMENT The accuracy of the supraorbital Doppler examination in the detection of hemodynamically significant internal carotid artery stenosis has been quite variable in the several published series ranging from 58% to 98%.r"s There are several causes of false-negative examinations. The test' is technically difficult to perform because the periorbital vessels are small, approximately 1 to 2 mm in diameter, whereas the probe is 7.5 mm in diameter. The signal is altered by the slightest movement of the probe or by a slight increase in the pressure applied by the probe over the artery, which may decrease the flow in the artery. However, we have not noted an increase in the diagnostic accuracy during the 2% years we have been using this test. The number of ambiguous tests that had to be repeated has decreased in this interval, but the number of false-negative examinations in the totally occluded and stenotic internal carotid artery group has not changed substantially. Barnes et al4 recommended common carotid artery compression to detect those patients whose collateral flow is primarily through the circle of Willis. In his experience, 7% of the patients with hemodynamically significant stenosis will have collateral flow through the circle of Willis, which is not detected by the compression maneuvers of both the ipsilateral and contralateral branches of the external carotid artery. We do not feel this small increase in accuracy justifies even the slight risk of inducing a neurologic deficit by dislodging atheromatous debris by common carotid artery compression. Lye et al"1 reported concomitant stenosis of the ipsilater¬ al external carotid artery as a cause of false-negative examinations. This was present in four of our 28 falsenegative tests. However, the contralateral compression of the superficial temporal, facial, and angular arteries should detect the collateral except in those patients with bilateral external carotid artery stenosis. Despite this lack of accuracy, supraorbital Doppler examination is a valuable tool to determine the physiologic importance of occlusive disease of the carotid bifurcation by evaluating the adequacy of the collateral flow. The presence of antegrade flow, which normally augments with compression maneuvers in the presence of substantial occlusive disease, indicates that collateral flow to the brain is adequate at the time of examination. Of the 19 patients with false-negative examinations who had antegrade flow with augmentation, only six had neurologic symptoms, two of which had amaurosis fugax most likely secondary to emboli and unrelated to flow. Knowledge of the physiology of periorbital blood flow is helpful in selecting for opera¬ tion those high-risk patients with asymptomatic carotid stenosis. Also, in patients with asymptomatic bruit
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
during admission for other vascular or major surgical procedure, the presence of a normal Doppler with augmentation to compression maneuvers assures adequate cerebral perfusion. These Doppler findings provide a better understanding of the dynamics of cerebral blood flow. An evaluation of the periorbital flow and response to compression of the branches of the external carotid artery can help differen¬ tiate flow related problems from embolie disease. In patients with equivocal symptoms, this test can help distinguish symptoms secondary to decrease flow from other problems not related to large vessel flow in the detected
neck. This data also suggest that the Doppler evaluation can be used to select patients for superficial temporal to intra¬ cranial artery bypass who have total occlusion of the internal carotid artery. In the absence of occlusive disease of the carotid siphon, a patient with a totally occluded
artery who has antegrade flow with augmentation would
not be
to benefit from extracranial-intracranial Further evaluation of this group of patients is in bypass. progress to evaluate this hypothesis. A positive Doppler examination is quite important and should be evaluated by arteriography if clinically indicated. In a symptomatic patient, a negative Doppler evaluation does not contraindícate angiography. In this study, the periorbital evaluation was only able to detect a hemody¬ namically significant stenosis 51% of the time. Also, an ulcerative plaque associated with a nonstenotic occlusion could shower the brain with emboli and not be detected by Doppler examination. Presently, we are following patients with asymptomatic bruits who have a negative Doppler test. The periorbital Doppler evaluation is a useful adjunct in the evaluation of patients with extracranial carotid occlusive disease and is a useful means of studying collat¬ eral cerebral circulation.
expected
References 1. LoGerfo FW, Mason GR: Directional Doppler studies of supraorbital artery flow in internal carotid stenosis and occlusion. Surgery 76:723-728, 1974. 2. Machleder HI, Barker WF: Stroke on the wrong side. Arch Surg 105:943-947, 1972. 3. Wise G, Brockenbrough EC, Marty R, et al: The detection of carotid artery obstruction: A correlation with arteriography. Stroke 2:105-113, 1971. 4. Barnes RW, Russell HE, Bone GE, et al: Doppler cerebrovascular examination: Improved results with refinement in technique. Stroke 8:468\x=req-\ 471, 1977. 5. Bone GE, Barnes RW: Clinical implications of the Doppler cerebrovascular examination: A correlation with angiography. Stroke 7:271-274, 1976.
6. Gross WS, Verta MJ Jr, Van Bellen B, et al: Comparison of noninvasive diagnostic techniques in carotid artery occlusive disease. Surgery 82:271\x=req-\
278, 1977.
7. Machleder HI, Barker WF: Noninvasive methods for evaluation of extracranial cerebrovascular disease. Arch Surg 112:944-946, 1977. 8. Moore WS, Bean B, Burton R, et al: The use of ophthalmosonometry in the diagnosis of carotid artery stenosis. Surgery 82:107-115, 1977. 9. Keller H, Meier W, Yonekawa Y, et al: Noninvasive angiography for the diagnosis of carotid artery disease using Doppler ultrasound (carotid artery Doppler). Stroke 7:354-363, 1976. 10. Lye CR, Sumner DS, Strandness DE Jr: The accuracy of the supraorbital Doppler examination in the diagnosis of hemodynamically significant carotid occlusive disease. Surgery 79:42-46, 1976.
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
Findings
in Patients With Cerebral Vascular Disease
Jonathan B. Towne, MD; Sergio Salles-Cunha, MSc; Victor M. Bernhard, MD
\s=b\ The direction of supraorbital and frontal artery flow and its response to compression of the superficial temporal, facial, and angular arteries were measured in 250 carotid arteries in 114 patients. All patients had arch and/or selective carotid arteriography. The carotid arteries were placed into the following three groups: hemodynamically normal, greater than 60% occlusion of the internal carotid artery, and total occlusion of the internal carotid artery. The test's accuracy was 94.5% in the hemodynamically normal group, 68.8% in the totally occluded group, and only 51.4% in the group with hemodynamically significant stenosis. Although the carotid Doppler examination is not reliable in detecting hemodynamically significant lesions of the internal carotid artery, it is valuable in assessing the adequacy of collateral cerebral circulation.
(Arch Surg 114:158-160, 1979) of the
arteries gives information in internal carotid artery occlusive disease and establishes the adequa¬ cy of collateral cerebral circulation. The periorbital anasto¬ moses between the branches of the external carotid artery and the ophthalmic branch of the distal internal carotid artery have been described.1 ·· Normally in the absence of a hemodynamically significant internal carotid artery steno¬ sis there is antegrade flow from within the orbit outward to the face that increases or augments when branches of the external carotid artery are compressed. With internal carotid artery stenosis, the direction of flow is reversed as these vessels supply collateral flow to the distal internal carotid system. This prospective study assessed the value
examination periorbital Doppler important hemodynamic
Accepted for publication July 12, 1978. From the Department of Surgery, Medical College of Wisconsin, Milwaukee County Medical Complex. Reprint requests to Department of Surgery, Milwaukee County Medical Complex, 8700 W Wisconsin Ave, Milwaukee, WI 53226 (Dr Towne).
of the supraorbital Doppler examination in determining the adequacy of collateral cerebral circulation in patients with totally occluded or hemodynamically significant stenosis of the internal carotid artery by comparing roent¬ genographic anatomic findings with clinical symptoms. MATERIALS AND METHODS We performed carotid Doppler examinations on all patients undergoing aortic arch and selective carotid artery arteriography
for the evaluation of extracranial carotid occlusive disease between November 1975 and March 1978. This group included patients with neurologic symptoms as well as patients with asymptomatic carotid bruits. We performed the Doppler test as described by Brockenbrough1 with the compression maneuvers described by Barnes et al." The patient was examined while in a supine position with his head on a small pillow. A directional Doppler was used to determine the direction of flow of the frontal and supraorbital arteries. While continuing to listen over these arteries, the ipsilateral and contralateral superficial temporal artery, facial artery, and angular artery were sequentially compressed. The effect of the compression maneuvers on the direction and velocity of periorbital flow was noted. The superficial temporal artery was compressed anterior and superior to the external auditory meatus, the facial artery was compressed just anterior to the angle of the mandible and the angular artery at the inferior medial aspect of the orbit. When two people performed these tests, both superficial tempo¬ ral arteries and both facial arteries were simultaneously compressed to prevent movement of the head. If a positive response was noted, each artery was compressed individually to determine the source of the collateral flow. Normal response was antegrade flow of blood from within the orbit outward to the face that was either augmented or unaffected by the compression maneuvers. A hemodynamically significant stenosis caused retro¬ grade flow in the frontal and supraorbital vessels, which was diminished or obliterated by the compression maneuvers. In addition, retrograde flow reverting to antegrade flow with
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
compression as well as antegrade flow diminishing with compres¬ sion were positive responses. All studies that demonstrated abnor¬ mal direction of flow but were unaffected by compression of the ipsilateral and contralateral external carotid branches were repeated to eliminate the possibility of inaccurate probe place¬ ment. Common carotid artery compression was not used. All patients had aortic arch and selective carotid arteriography with standard biplane films of the carotid bifurcation most often performed through right femoral artery catheterization. A few patients with diffuse aortoiliac occlusive disease were studied by the transaxillary approach. Occasionally, spot films were obtained to further delineate the pathologic anatomy. The amount of stenosis was measured by comparing the diameter of the narrow¬ est portion of the internal carotid artery to the diameter of the normal lumen distal to the stenosis. The arteriograms were evaluated without knowing the results of the Doppler evaluation, and the arteries were placed in the following three groups: (1) totally occluded, (2) greater than 60% stenosis, and (3) hemody¬ namically normal vessels. This later category included all patients with less than 60% stenosis as well as all normal vessels. A 60%-stenosis represents an 84% decrease in the cross-sectional area and is hemodynamically important. Two hundred and fifty carotid arteries were evaluated in 114 patients. Several patients had multiple Doppler examinations to determine the reproducibility of the test.
RESULTS The Doppler evaluation was normal in 171 of 181 hemo¬ dynamically normal vessels for an accuracy of 94.5% (Table). There were ten false-positive results (5.5%). Of the
37 internal carotid arteries with greater than 60% stenosis, the test was positive in 19 (51.4%) and negative in 18 (48.6%). In 32 totally occluded vessels, the test was positive in 22 (68.8%) and negative in ten (31.2%). We evaluated the examinations in which both frontal and supraorbital flow were antegrade and did not change with compression maneuvers. This group contained 44 of the 250 arteries (17.6%), only nine of which had hemody¬ namically significant occlusive disease of the internal ca¬ rotid artery for an incidence of 20%. Therefore, an evalua¬ tion with antegrade flow without augmentation has an 80% chance of being normal. There were 28 false-negative examinations in this series. This group's responses to the compression maneuvers were as follows: of the ten totally occluded arteries, three had antegrade flow without augmentation and seven had antegrade flow with augmentation, and of the 18 arteries with greater than 60% occlusion, six had antegrade flow without augmentation and 12 had antegrade flow with augmenta¬ tion. Five of the nine arteries that had antegrade flow without augmentation were in neurologically asymptomat¬ ic patients. Four other patients had the following neuro¬ logic symptoms: vague arm weakness (one), vertebral basilar symptoms (one), transient ischemie attack (one), Results of
Supraorbital Doppler Evaluation Accuracy, %
Normal > 60% stenosis Total occlusion
False
False-
Negative, %
Positive, %
94.5
5.5
51.4
48.6
68.8
31.2
...
and amaurosis fugax (one). There were 19 arteries with antegrade flow and augmentation of periorbital flow on compression of branches of the external carotid artery. Thirteen patients were asymptomatic and six had the following neurologic symptoms: amaurosis fugax (two), nonspecific neurologic symptoms (two), cerebrovascular accident (one), and decreased memory (one). COMMENT The accuracy of the supraorbital Doppler examination in the detection of hemodynamically significant internal carotid artery stenosis has been quite variable in the several published series ranging from 58% to 98%.r"s There are several causes of false-negative examinations. The test' is technically difficult to perform because the periorbital vessels are small, approximately 1 to 2 mm in diameter, whereas the probe is 7.5 mm in diameter. The signal is altered by the slightest movement of the probe or by a slight increase in the pressure applied by the probe over the artery, which may decrease the flow in the artery. However, we have not noted an increase in the diagnostic accuracy during the 2% years we have been using this test. The number of ambiguous tests that had to be repeated has decreased in this interval, but the number of false-negative examinations in the totally occluded and stenotic internal carotid artery group has not changed substantially. Barnes et al4 recommended common carotid artery compression to detect those patients whose collateral flow is primarily through the circle of Willis. In his experience, 7% of the patients with hemodynamically significant stenosis will have collateral flow through the circle of Willis, which is not detected by the compression maneuvers of both the ipsilateral and contralateral branches of the external carotid artery. We do not feel this small increase in accuracy justifies even the slight risk of inducing a neurologic deficit by dislodging atheromatous debris by common carotid artery compression. Lye et al"1 reported concomitant stenosis of the ipsilater¬ al external carotid artery as a cause of false-negative examinations. This was present in four of our 28 falsenegative tests. However, the contralateral compression of the superficial temporal, facial, and angular arteries should detect the collateral except in those patients with bilateral external carotid artery stenosis. Despite this lack of accuracy, supraorbital Doppler examination is a valuable tool to determine the physiologic importance of occlusive disease of the carotid bifurcation by evaluating the adequacy of the collateral flow. The presence of antegrade flow, which normally augments with compression maneuvers in the presence of substantial occlusive disease, indicates that collateral flow to the brain is adequate at the time of examination. Of the 19 patients with false-negative examinations who had antegrade flow with augmentation, only six had neurologic symptoms, two of which had amaurosis fugax most likely secondary to emboli and unrelated to flow. Knowledge of the physiology of periorbital blood flow is helpful in selecting for opera¬ tion those high-risk patients with asymptomatic carotid stenosis. Also, in patients with asymptomatic bruit
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
during admission for other vascular or major surgical procedure, the presence of a normal Doppler with augmentation to compression maneuvers assures adequate cerebral perfusion. These Doppler findings provide a better understanding of the dynamics of cerebral blood flow. An evaluation of the periorbital flow and response to compression of the branches of the external carotid artery can help differen¬ tiate flow related problems from embolie disease. In patients with equivocal symptoms, this test can help distinguish symptoms secondary to decrease flow from other problems not related to large vessel flow in the detected
neck. This data also suggest that the Doppler evaluation can be used to select patients for superficial temporal to intra¬ cranial artery bypass who have total occlusion of the internal carotid artery. In the absence of occlusive disease of the carotid siphon, a patient with a totally occluded
artery who has antegrade flow with augmentation would
not be
to benefit from extracranial-intracranial Further evaluation of this group of patients is in bypass. progress to evaluate this hypothesis. A positive Doppler examination is quite important and should be evaluated by arteriography if clinically indicated. In a symptomatic patient, a negative Doppler evaluation does not contraindícate angiography. In this study, the periorbital evaluation was only able to detect a hemody¬ namically significant stenosis 51% of the time. Also, an ulcerative plaque associated with a nonstenotic occlusion could shower the brain with emboli and not be detected by Doppler examination. Presently, we are following patients with asymptomatic bruits who have a negative Doppler test. The periorbital Doppler evaluation is a useful adjunct in the evaluation of patients with extracranial carotid occlusive disease and is a useful means of studying collat¬ eral cerebral circulation.
expected
References 1. LoGerfo FW, Mason GR: Directional Doppler studies of supraorbital artery flow in internal carotid stenosis and occlusion. Surgery 76:723-728, 1974. 2. Machleder HI, Barker WF: Stroke on the wrong side. Arch Surg 105:943-947, 1972. 3. Wise G, Brockenbrough EC, Marty R, et al: The detection of carotid artery obstruction: A correlation with arteriography. Stroke 2:105-113, 1971. 4. Barnes RW, Russell HE, Bone GE, et al: Doppler cerebrovascular examination: Improved results with refinement in technique. Stroke 8:468\x=req-\ 471, 1977. 5. Bone GE, Barnes RW: Clinical implications of the Doppler cerebrovascular examination: A correlation with angiography. Stroke 7:271-274, 1976.
6. Gross WS, Verta MJ Jr, Van Bellen B, et al: Comparison of noninvasive diagnostic techniques in carotid artery occlusive disease. Surgery 82:271\x=req-\
278, 1977.
7. Machleder HI, Barker WF: Noninvasive methods for evaluation of extracranial cerebrovascular disease. Arch Surg 112:944-946, 1977. 8. Moore WS, Bean B, Burton R, et al: The use of ophthalmosonometry in the diagnosis of carotid artery stenosis. Surgery 82:107-115, 1977. 9. Keller H, Meier W, Yonekawa Y, et al: Noninvasive angiography for the diagnosis of carotid artery disease using Doppler ultrasound (carotid artery Doppler). Stroke 7:354-363, 1976. 10. Lye CR, Sumner DS, Strandness DE Jr: The accuracy of the supraorbital Doppler examination in the diagnosis of hemodynamically significant carotid occlusive disease. Surgery 79:42-46, 1976.
Downloaded From: http://archsurg.jamanetwork.com/ by a University of Iowa User on 05/24/2015
