Ultrasound Findings in Spontaneous Carotid Artery Dissection The Value of
Duplex Sonography
Matthias Sturzenegger, MD
\s=b\ Extracranial and transcranial Doppler and duplex sonographic findings in six patients with internal carotid artery dissection proven by angiography is reported. Extracranial Doppler analysis showed occlusion without a recordable signal from the internal carotid artery at any level or stenosis with accelerated flow in the high cervical segment. Transcranial Doppler findings demonstrated the hemodynamic consequences of the internal carotid artery occlusion or stenosis with collateral flow across the circle of Willis and also showed the dampened pulse wave of the middle cerebral artery ipsilateral to the dissection. In duplex sonography, the indirect signs indicating internal carotid artery dissection were a patent carotid bifurcation and proximal internal carotid artery segment but with no or only a short systolic flow signal. Atherosclerotic wall changes were absent, an important finding that suggests
rp
he cervical part ofthe internal carotid artery (ICA) is by far the most frequent site of spontaneous wall dis¬ section,13 but any brain-supplying ar¬ tery may be affected.4 The exact fre¬ quency is unknown, but it may be quite underestimated. With less rigid indica¬ tions for cerebral angiography5"7 in the last few years, an increasing number of patients with spontaneous dissection of the ICA (ICD) have been identified." From this experience, we have learned that the clinical presentation of ICD may be extremely variable, ranging Accepted for publication March 12,1991. From the Department of Neurology, University
of Bern, Switzerland.
Reprint requests to Department of Neurology, University of Bern, Inselspital, CH-3010 Bern, Switzerland (Dr Sturzenegger).
nonatherosclerotic stenosis or occlusion. Direct signs making the diagnosis likely were a tapering of the internal carotid artery lumen distal to the bulb, an irregular membrane crossing the vessel lumen, and the demonstration of a true lumen with flow and a false one without flow. While cerebral angiography is still considered the gold standard, ultrasound may become the primary modality for early diagnosis. Doppler and duplex examinations help to indicate angiography and are the methods of choice for follow-up investigations. They clearly demonstrate spontaneous recanalization with normalization of carotid circulation or, in case of persistent occlusion, improvement of collateral blood supply. Sequential examinations may prove helpful to determine the duration of
anticoagulant treatment. (Arch Neurol. 1991 ;48:1057-1063)
from the patient with unspecific head¬ ache or even no clinical symptoms and signs to the patient with severe stroke and rapidly ensuing death. These clini¬ cal extremes usually do not give rise to further investigations, and the real cause, ICD, goes unrecognized.
Younger patients
are
preferentially
affected: Hart and Miller9 found two cases (2%) among 100 patients with stroke under the age of 40 years, and Bogousslavsky and Regli1" found nine cases (22%) among 41 patients with stroke under the age of 30 years. Mean age at presentation in a group of 146 cases2 was 45 years; 70% were between 35 and 50 years old. The younger age at presentation is suggestive of ICD rath¬ er than atherosclerotic carotid dis¬ ease.24 Considering all patients with stroke, ICD is a rare cause of stroke:
among a series of 1200 consecutive pa¬ tients with stroke," 30 (2.5%) had ICD. In another series of 4531 patients exam¬ ined with cerebral angiography because of acute cerebrovascular symptoms,12
extracranial carotid artery dissection diagnosed in 11 (0.24%). When the characteristic triad of facial or neck pain, ipsilateral oculosympathetic paresis, and hemispheric ischemie symptoms is present, diagnosis may be strongly suspected on clinical grounds.2,4,13"16 For definite diagnosis, angiography is required, which can show characteristic but also variable signs.3,4,17'21 The findings, except double lumen, are nonspecific. Differential di¬ agnosis includes arterial compression or invasion by tumor or pharyngeal inflam¬ mation, congenital hypoplasia, vasculi¬ tis, radiation-induced arteriopathy, and was
vasospasm. In general,
prognosis
is
spontaneous recanalization more
good,
than 80% of patients.2,4
and in
occurs
However,
persisting disability can result,21,22 ow¬ ing to ensuing stroke. Considering pa¬ tients with ICD and stroke,11 prognosis is clearly worse: recanalization occurs in only 60% and death in 23%, and 48% of the patients remain severely disabled. Stroke is,
known from angiogra¬ due to embolism from local thrombosis at the site of dissection. Rarely, insufficient collateral blood sup¬ ply causes hemodynamic infarction. Because of the danger of embolism, early anticoagulation is considered the treatment of choice. However, its effec¬ tiveness has not been proved yet by a randomized controlled study. On the other hand, to my knowledge there is no case of ICD reported in the literature in which symptoms worsened with anticoas
phy,18,23 mostly
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Table 1.—Clinical
Vascular Risk Factors
Patient No./
Symptoms Recurrent TIA (L hemiparesis), pain R eye and temple R hemiparesis, aphasia, occipital
Age, y/Sex 1/49/M
2/42/F
headache Recurrent R amaurosis fugax, recurrent TIA
3/41 /M
Signs None
R
4/41/M
R
R temple and cheek hemiparesis, aphasia, frontal
headache Recurrent TIA
5/40/M
Heparin sodium,
Migraine, hypertension
Heparin, coumarin
None
Aspirin
coumarin Partial recanalization with
stenosis after 15 wk Resolution on both sides
persisting slight after 2
hemiparesis, transient aphasia,
mo
bruit R carotid R
None
hemiparesis
Heparin,
Persisting occlusion
coumarin
after 2
mo, better intracranial
collateral flow Partial HS
(L
Evolution Resolution after 12 d
Treatment
Migraine, hypertension, smoking, cholesterol
R
hemiparesis), gait disturbance, pain R
eye and
hemiparesis
Loss of consciousness,
(R hemiparesis), pain
_
Findings*
on
R,
hemianopia to L, L hemiparesis, L sensory neglect,
temple
Symmetric BFV
Heparin, coumarin
Migraine, hypertension
in both
MCAs after 5 d, complete recanalization after 6 wk
CT: infarction 6/41/M
Partial HS,
Recurrent TIA
(asphasia), pain
none on
L
Resolution after 10 wk
Heparin, coumarin
L
eye and forehead
*TIA indicates
transient ischemie attack; HS, Horner's
agulant therapy. If anticoagulation is beneficial, early diagnosis is essential for the treatment of patients with ICD, a goal that can be achieved with com¬ bined ultrasonographic examination (CUE) using conventional extracranial direct and indirect Doppler sono¬ graphy, transcranial Doppler sono¬ graphy (TCD), and duplex scanning. I report my experience using CUE in six patients with ICD in the extracranial segment verified by angiography.
syndrome; CT, computed tomography; BFV,
blood flow
for all TCD ultrasound examinations (TC264, Eden Medizinische Elektronic GmbH, Ueberlingen, Germany). The middle cere¬ bral artery (MCA), anterior cerebral artery, posterior cerebral artery, and ICA bifurca¬ tion were analyzed at different depths by a transtemporal approach and the intracranial vertebral and basilar arteries were analyzed through the occipital foramen. Systolic, dia¬ stolic, and mean blood flow velocity (BFV) were measured in each vessel. Pulsatility index (PI) was calculated according to the following formula: PI (svstolic BFV dias¬ tolic BFWmean BFV. The values of 52 normal controls served as reference. The MCA-BFV and PI values of the six patients were compared with those ofthe controls. =
-
PATIENTS AND METHODS Duplex Examination
A high-resolution, real-time, duplex ultra¬ sound system (Diasonics SPA 1000, Sonotron
Holding AG, Zug, Switzerland)
used that consisted of
a
was
10-MHz echoto-
mography imaging probe and a 4.5-MHz pulsed-wave Doppler probe with real-time gray-scale Fast-Fourier transform Doppler spectrum analysis. Common carotid artery (CCA), bulb, ICA, external carotid artery (ECA), and vertebral arteries were imaged on
both sides.
Extracranial
Doppler Examination
The technique for extracranial direct and indirect Doppler sonographic examination 4 has been described in detail previously. I used the same device as for TCD recordings, which is described below. The CCA, ECA, ICA, subclavian artery, and vertebral artery at the atlas were examined by continuous insonnation on both sides. Supratrochlear and ophthalmic arteries (OpAs), as well as carotid siphons, were measured by a transor¬ bital approach. TCD Examination The technique for TCD recordings has been described in detail previously.25" A mi¬ croprocessor-controlled directional pulsed Doppler device operating at 2 MHz was used
Cerebral Angiography
Selective CCA angiograms were obtained in all patients. Catheterizations were per¬ formed by the percutaneous femoral ap¬ proach. In one case (case 3), direct CCA puncture was performed. Six French poly¬ ethylene catheters and a nonionic, low-osmolar contrast agent were used. Statistical analysis was performed using simple regression analysis and the unpaired and paired t test. RESULTS
velocity; and MCA, middle cerebral artery.
patients and additional stenosis on the other side in case 3. Four patients had collateral blood supply from the ipsilat¬ eral ECA to ICA territory and patient 3 had collateral supply across both OpAs with retrograde flow. Transcranial Doppler sonography
showed reduced MCA-BFV and PI on the side of dissection in five patients compared with the contralateral side (P=.001 for BFV, P=.002 for PI) as well as compared with the controls .0001 for PI). (P=.0001 for BFV, An additional patient had symmetric MCA velocities but reduced PI on the side of the lesion (case 2). All had collat¬ eral blood supply across the anterior communicating artery from the contralateral ICA. Mean BFV and PI with the side differences of patients and controls are given in Table 2. In controls, there was a correlation between right and left MCA-BFV F 516.2, (r=.955, .0001) and PI (r=.768, = 71.8, .0001) and there was no side differ¬ ence (P=.83 for both). In patients, there was no correlation between MCABFV (r=.692, F 3.7, P=.13) and PI (r=.242, F 0.25, P .64) ipsilateral and contralateral to the dissection side, and the side differences were obvious (P= .001 for BFV and P .002 for PI). =
=
=
=
=
=
Six patients (five men and one woman with a mean age of 42.5 years [range, 40 to 49 years]) admitted within a year with angiographically proved ICD were analyzed. Five had unilateral dissection and one (case 3) had bilateral dissection. The clinical findings are summarized in Table 1. Lower cranial nerve palsy did not
occur.
A
computed tomographic
normal in five patients and showed MCA infarction in one (case 5). There was no preceding trauma. Extracranial Doppler sonography showed ICA occlusion on one side in all scan was
=
=
Duplex Examination No patient changes. All
had atherosclerotic wall the proximal ICA seg¬ ments were patent on the "occluded" side, two with a residual "stump flow" and four without recordable flow signal. There was a "membrane" visible cross¬ ing the ICA lumen in four arteries, pro¬ ducing the picture of double lumen not compressible by the probe (Fig 1).
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Table 2.—Transcranial L or
Ipsilateral MCA
BFV
Group
Doppler Findings*
R or Contralateral MCA
Mean Difference
BFV
PI
BFV
Controls Mean ± SD
64.5 ± 10.5
0.76 ± 0.15
0.46 ± 3.6
0.01 ± 0.1
0.48-1.24
64.1 ± 11.6 41-90
0.75 ± 0.15
45-90
0.51-1.37
17
0.55
43.2 ± 9.5 33-55
0.46 ± 0.08
51.2 ± 11.4
0.65 ± 0.08
18 ± 8.4
0.33-0.57
48-82
0.52-0.75
0.2 ± 0.1 0.26
Range Patients Mean ± SD
Range
*MCA MCAs in
indicates middle cerebral artery; BFV, blood flow velocity; and PI, pulsatility Index. Left and right MCAs In cases with bilateral dissection, the ipsilateral side indicates the side more occluded.
were
examined in controls,
ipsilateral and contralateral
patients.
nal. In case 1, stenosis started immedi¬ ately distal to a carotid kinking. There was a tapering occlusion start¬ ing 2 cm distal to the bifurcation with a flame-shaped stump in one artery (case 2). Collateral blood supply across the anterior part ofthe circle of Willis (ante¬ rior communicating artery) was con¬ firmed in all five cases with bilateral carotid angiograms. No patient showed pseudoaneurysm formation or signs indicative of fibro¬ muscular dysplasia. None had athero¬ sclerotic wall lesions (Fig 2). The results of ultrasound findings and angiography are summarized in Table 3. REPORT OF A CASE
Fig 1. —Results of initial Duplex scanning (case 3): a, open left carotid bifurcation and identification of external carotid artery (ECA); b, only short systolic flow signal in the most proximal left internal carotid artery (ICA; stump flow); c, membrane (arrow) crossing lumen of left ICA in a more distal segment; d, preserved flow signal in proximal right ICA; e, high blood flow velocity indicating stenosis in more distal segment of right ICA, membrane crossing vessel lumen; and f, membrane crossing vessel lumen of right ICA (arrow). CCA indicates common carotid artery.
Angiography Five patients (cases 1, 2, 3, 5, and 6) had bilateral, and one (case 4) had uni¬ lateral, carotid angiography. One pa¬ tient (case 3) had bilateral dissection; consequently, seven dissected ICAs could be analyzed. In all of them, the carotid bifurcation and at least the most proximal 2 cm of the ICA were normal. Four showed smoothly tapering stenoses (cases 3 [left], 4,5, and 6) starting 3 to 4 cm distal
to the
bifurcation, in all extending up to the base of the skull (in case 5 probably to the siphon segment). In three, the stenoses were high grade with a filiform residual lumen resulting in a "string sign" (cases 4,5 and 6). Abrupt return to normal caliber was noted in all at the entrance of the carotid canal. Two showed irregular segmental stenosis (cases 1 and 3 [rightl), in both cases of the prepetrosal segment and with abrupt reconstitution of a normal lumen width at the entrance of the carotid ca-
A 41-year-old technician had no vascular risk factors. Three weeks before his hospital¬ ization, he felt increasing pain in his right temple and cheek. Plain roentgenograms showed an opacified maxillary sinus, and polyposis was considered as the likely cause of his pain. The patient was admitted for sinuscopy. Soon after premedication with intra¬ muscular atropine sulfate (0.5 mg) and mor¬ phine chloride (5 mg), he fainted. When he regained consciousness after several min¬ utes, there was right-sided hemiplegia and asphasia clearing within 2 hours. Physical examination revealed a bruit over the right carotid artery. Results of routine blood lab¬ oratory tests, electrocardiogram, and com¬ puted tomography were normal. Now, on detailed questioning, he reported several at¬ tacks of blurred vision or transient blindness of his right eye, lasting 1 or 2 minutes, in the days before admission. In addition, he had had three episodes of feeling cold and heavi¬ ness or loss of motor control of his right arm and hand. Doppler analysis (Fig 3) showed reduced diastolic flow and increased PI in the left CCA. The left ICA could not be identified. The left ECA showed high diastolic flow re¬ sembling an intracranial vessel. The BFVs in the right CCA, the ECA, and the proximal part of the ICA were normal. However, in the high cervical segment of the right ICA, there was increased BFV over a long seg¬ ment up to the base of the skull. Both OpAs showed reversed flow direction toward the intracranial region. The TCD analysis (Fig 3) revealed reduced BFV and reduced PI in the left MCA. The left anterior cerebral artery showed reversal of flow direction. High BFVs in the left pos-
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terior cerebral artery indicated collateral flow from the posterior circulation.
Duplex scanning (Fig 1) showed a widely patent left proximal ICA, but only minimal systolic intraluminal flow signal (stump flow). In its more distal part, a membranelike structure traversing the vessel lumen could be visualized. The right proximal ICA was also patent, and flow was normal. Still more
distally, there was a membranelike structure in the vessel lumen, and at this site high BFVs were present, indicating stenosis. A diagnosis of left ICA occlusion and right ICA stenosis distal to their origin from the
bulb was made, with collateral flow to the left carotid territory across the anterior and pos¬ terior communicating arteries. The patent proximal ICA segments and the membranes traversing the vessel lumen suggested bilat¬ eral ICDs. Cerebral four-vessel angiography (Fig 2) showed a normal proximal ICA on both sides. In the higher cervical part, the left one showed progressive narrowing to a stringlike lumen with abrupt luminal recon¬ stitution at the entry to the petrosal canal. There was moderate stenosis of the right ICA in the higher cervical part, again with abrupt reconstitution of the vessel lumen at the base ofthe skull. Intracranially, flow was from the right ICA to the left across the anterior communicating artery. Because of the smooth boundaries of luminal narrowings, bilateral carotid hypoplasia was diag¬ nosed by the radiologist (which did not ex¬ plain the sudden neurologic symptoms). Doppler control 10 days later showed nor¬ malized BFV in both CCAs. Both IC As could be identified with normal BFV in their proxi¬ mal parts but with high BFV in their upper cervical segments due to stenosis. The MCABFV was symmetric. The anterior cerebral artery and OpA flows were antegrade on both sides. Duplex scanning showed flow in both ICAs, but there were still stenoses due to membranelike structures. This flow reconstitution clearly made hypoplasia unlike¬ ly and a diagnosis of dissection more favor¬ able. Doppler reexamination 2 months later showed normal results proving spontaneous recanalization and yielded the diagnosis of spontaneous bilateral ICD. The patient has remained asymptomatic taking aspirin. COMMENT
Fig 2. —Left common carotid arteriogram in case 3 (a, anteroposterior projection; b, lateral view) demonstrates common carotid narrowing (arrowheads in a) resulting from subintimai injection following direct artery puncture. Carotid bifurcation and proximal 3 cm of internal carotid artery (ICA) are normal. Then, smoothly tapering stenosis of left cervical ICA (arrows in a and b) with severe slowing of flow is noted, extending up to the skull base, where abrupt return to normal caliber is seen at entrance of carotid canal (open arrows in a and b). There is no filling of left anterior cerebral artery. Right common carotid arteriogram (c, anteroposterior projection; d, lateral view) again shows normal carotid bifurcation and proximal right ICA. Irregular segmental moderate stenosis of the high cervical prepetrosal ICA segment (arrows in c and d) is demonstrated with abrupt reconstitution of normal lumen width at the entrance of the carotid canal (open arrows in c and d). There is collateral flow from right to left carotid territory across anterior circle of Willis (arrowheads in c).
Because the clinical presentation of ICD may be extremely variable,2 the diagnosis cannot be made on clinical grounds alone. Carotid angiography is at present still the method of choice for definite diagnosis. Though it has be¬ come much less risky owing to technical achievements,5'' it remains an invasive procedure that should not be performed when there is only weak clinical suspi¬ cion of ICD. In these situations, an easi¬ ly available, noninvasive method is de¬ sirable that can confirm the suspicion and allow the selective use of carotid
angiography.
Conventional direct and indirect
(pulsed- or continuous-wave) Doppler sonography of the extracranial carotid arteries and their branches24
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can
reveal
Table
3.—Summary of Results*
Patient No./
Age, y/Sex 1/49/M
Arteriography Segmental stenosis of high cervical R ICA; collateral circle of Willis, L to R Tapering occlusion of L ICA; collateral fiow across circle of Willis, RtoL L ICA: string sign, reconstitution at skull base; R ICA: high cervical segmental stenosis, reconstitution at skull base; collateral flow across circle of Willis, R to L flow
2/42/F
3/41/M
4/41/M
L ICA:
R ICA:
retrograde
R MCA BFV i; collateral flow across AComA, LtoR
OpA
across
string sign, string sign up
cavernous
L ICA occlusion,
orthograde
OpA
L MCA PI
both
across
to
segment;
i;
collateral flow to L
AComA, R
i;
Duplex Sonography proximal R ICA with stump flow
Patent
Patent proximal L ICA, no intraluminal flow; membrane with double lumen Patent proximal L ICA without flow; membrane L ICA (distal); membrane R ICA (distal and stenosis); double lumen
L ICA occlusion, R ICA stenosis (high cervical segment), OpAs both
L MCA BFV
occlusion, L OpA retrograde
L MCA BFV
Patent proximal L ICA with stump flow
occlusion, R OpA retrograde
R MCA BFV 1; collateral flow across AComA, L to R; R MCA, no reactivity
Patent proximal R ICA without flow
flow
across
collateral
AComA,
R to L and from vertebrobasilar system
retrograde (bilateral dissection)
i; collateral flow across AComA, RtoL
L ICA
reconstitution at skull base 5/40/M
TCD
ECD R ICA occlusion, R
R ICA
collateral flow across on C02 breathing circle of Willis, L to R L MCA BFV |; collateral Patent proximal L ICA L ICA occlusion, L OpA 6/41/M L ICA: string sign, flow across AComA, without flow; membrane reconstitution at skull retrograde RtoL with double lumen not base; collateral flow across circle of Willis, compressible RtoL ECD indicates extracranial Doppler sonography; TCD, transcranial Doppler sonography; ICA, internal carotid artery; OpA, ophthalmic artery; MCA, middle cerebral artery; BFV, blood flow velocity; AComA, anterior communicating artery; and PI, pulsatility index. Occlusion on ECD indicates no signal from ICA at origin from bulb and at skull base.
48(70/31) MCA, (67/39) PCA, 37(51/28) ACA, 48
OpA, 37 (59/30)
retro
ACA, 25 (36/20) retro
MCA, 34 (44/28) PCA, 53 (73/42)
OpA.
50
(69/37)
retro
ICA, d, 109(118/90) ICA, p, 25(45/19) CCA, 25(70/17)
Fig 3. —Results of initial extracranial and transcranial Doppler analysis in case 3 (see text for details). ACA indicates anterior cerebral artery; retro, retrograde; MCA, middle cerebral artery; PCA, posterior cerebral artery; OpA, ophthalmic artery; ICA, internal carotid artery (d and indicating distal and proximal); and CCA, common carotid artery. The numbers represent the values of blood flow velocities in each vessel: mean (systolic/diastolic). The pathological values are underlined.
occlusion or stenosis if it exceeds 50% of lumen diameter. The technique does not yield further information about origin. Only the finding of a stenosis located in the upper cervical ICA segment or ex¬ tending over a long distance may sug¬ gest dissection,22,29 but this is not a
specific sign. Transcranial Doppler son¬ ography,26"28 though detecting the ef¬
fects on intracranial circulation includ¬ ing collateral blood flow, does not help in further differentiating the origin of ste¬ nosis or occlusion. The primary goal of CUE is the differ-
entiation of ICD from occlusion or ste¬ nosis due to other causes such as athero¬ sclerosis. Atherosclerotic lesions ofthe brain-supplying arteries show a predi¬ lection for the carotid bifurcation.30 Spontaneous ICD, on the other hand, is usually localized in the middle or upper cervical segment ofthe ICA or begins at least 2 to 3 cm distal to the carotid bifur¬ cation. läi'16'17·20·23These anatomic facts and the easy accessibility of the carotid bi¬ furcation in most patients by duplex scanning make this method suitable for differentiation. When conventional Doppler sono¬ graphy indicates ICA stenosis or occlu¬ sion, the indirect findings at duplex scanning listed in Table 481"34 suggest a dissection. These are ultimately non¬ specific findings, and the diagnosis may be hampered when there is the simul¬ taneous presence of atheromatous plaques22 or when the ICD starts al¬ ready at the bifurcation.2021 Therefore, direct visualization of the dissection should be attempted. Direct and more specific signs of ICD at duplex scanning are listed in Table 4. Internal carotid artery dissection is virtually always extracranial but varies considerably in extent.21 It typically oc¬ curs distal to the extracranial bifurca¬ tion,4 often at or around the C-2 verte¬ bral level.2,21 Because this region may be beyond the range of carotid imaging by
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Table 5.—Limitations of
4.—Duplex Sonography: Findings Suggesting ICA Dissection* Table
Indirect findings
No atheromatous plaques are visible in ca¬ rotid bifurcation Bulb and proximal segment of ICA are
patent No flow signal
or high-resistance flow pat¬ (short, only systolic flow peak [stump flow] or bidi¬ rectional [reverberating] systolic flow) in
tern
proximal
ICA
Lack of wall
pulsations
Direct signs Tapering of ICA lumen starting >2 tal to bulb
cm
dis¬
Irregular "membrane" crossing ICA lumen (Fig 1)
Demonstration of true lumen with flow and false (thrombosed) lumen without flow; unlike veins, true and false lumens are
noncompressible by probe pressure; flow in false lumen resulting from more distal reentry into true lumen, as fre¬ quently found in CCA dissection associ¬ ated with dissecting aortic aneu¬
rysm,3'"3' is rare Axial sections show "membrane" as flap in lumen Findings at follow-up examinations Recovery of lumen patency Flow recovery Recovery of normal hemodynamics, when combined with TCD *
ICA indicates Internal carotid artery; CCA, com¬ carotid artery; and TCD, transcranial Doppler
mon
sonography.
ultrasound, direct visualization of the
ICD is not possible in all cases.22 Sensitivity of CUE in detecting occlu¬ sion in the case of ICD was very high in one study (95%).22 Its emergency use in cases where clinical presentation sug¬ gests dissection does help in rapid diag¬ nosis and selection of patients for
angiography. Duplex sonography has several méth¬ odologie limitations, listed in Table 5. These are the major reasons why I still consider angiography to be necessary to
assess the full extent of the vascular process and to confirm the ultrasound
findings.
In addition to its use in initial diagno¬
sis, duplex scanning is an excellent non-
Duplex
Sonography Anatomic Short and / or fat neck, high cervical carotid bifurcation, goiter, calcification of ath¬ erosclerotic lesions (sound shadow) Individual Restless, agitated, continuously swallow¬ ing patients, air emphysema; direct ex¬ amination may be impossible Methodic Occlusion cannot always be demonstrated directly because of its high cervical location Usually, whole longitudinal extension of wall dissection and especially involve¬ ment of intracranial ICA segments (oc¬ curring in up to 20%39·40) cannot be de¬ tected Detection of aneurysms is usually not possible29 Identification of fibromuscular dysplasia as underlying cause1639 is hardly ever pos¬ sible
invasive
modality
for serial
follow-up
examination.29,35,36 The signs indicating
are listed in Table 4. Sponta¬ resolution or reduction of stenosis may occur at variable intervals, ranging from a few days to several months.19,22,29 Sequential follow-up studies have shown that this process generally oc¬ curs within a few days and only occa¬ sionally over weeks or months.3,29,30,37"39 Most authors agree that ischemie in¬ farction is due in most cases to distal embolism from local thrombosis at the stenotic segment. The role of embolism is evident from the occurrence of isch¬ emie symptoms when a stenosis is hemodynamically insignificant, from arte¬ riography that shows distal emboli, and from intraluminal thrombus seen arteriographically and at surgery. Embolie stroke may develop in the first few days of dissection,* and its frequency is esti¬ mated to be at least 15%3 to 24%.21 More¬ over, stenosis may progress to occlu¬ sion,17,18,40 resulting in a critical hemodynamic situation and preventing recanalization. These potential compii-
recovery neous
*References 3, 4, 17, 18, 20,
23, 37, 40, and 41.
cations are the reason why anticoagu¬ lant therapy, first with heparin, is rec¬ ommended by several authors2,42 with the idea to prevent thrombosis and em¬ bolism. It is logical that treatment should be started as early as possible, implicating early diagnosis, facilitated by application of CUE. As controlled studies are lacking, the efficacy of such therapy remains unproved, regardless ofthe nature and degree ofthe anatomic disease present. To date, no harmful effect of anticoagulant therapy, includ¬ ing cases with extracranial aneurysms, has been reported,2,8,11,17,22,42 and only the simultaneous presence of an intracrani¬ al aneurysm is considered a contraindi¬ cation.2 Several uncontrolled studies suggest beneficial effects of anticoagu¬ lation.21,22,43 On the other hand, it seems pointless to continue anticoagulant therapy once vascular patency has been restored. The CUE offers the possibili¬ ty of noninvasive follow-up to detect the moment of recanalization. As spontane¬ ous recanalization is the rule,2"4,17,22,37,44"46 surgical interventions remain excep¬ tional2"4,8,37,47,48 and are reserved for pa¬ tients with recurrent or progressive ischemie symptoms despite anticoagu¬ lant therapy. If these ischemie symp¬ toms are due to insufficient collateral blood supply, it may be detected by TCD (case 5). Therefore, TCD may help in selecting patients for revasculariza¬ tion procedures. In conclusion, CUE with special em¬ phasis on duplex scanning is particular¬ ly useful to select patients with suspect¬ ed ICD for arteriography and thus provides a tool for early diagnosis by its emergency use. It is the method of choice for follow-up examinations to de¬ termine duration of anticoagulation and may help to assess the real frequency of ICD when also used in patients in whom angiography would not be considered. I wish to thank Peter Huber, director of the
Department of Neuroradiology, University of Bern, Switzerland, for performing the neuroradio¬ logie examinations.
References 1. Hart
RG, Easton JD. Dissection of cervical and cerebral arteries. Neurol Clin. 1983;1:155-182. 2. Houser WO, Mokri B, Sundt TM, Baker HL, Reese DF. Spontaneous cervical cephalic arterial dissection and its residuum: angiographic spectrum. AJNR. 1984;5:27-34. 3. Gauthier G, Rohr J, Wildi E, Megret M. L'h\l=e'\matome diss\l=e'\quantspontan\l=e'\de l'art\l=e`\recarotide interne. Arch Suisses Neurol Psychiatr. 1985; 136:53-74. 4. Hart RG, Easton JD. Dissection and trauma of cervico-cerebral arteries. In: Barnett HJM, ed. Stroke, Pathophysiology, Diagnosis and Management. New York, NY: Churchill Livingstone Inc; 1986:775-788. 5. Smoker WRK, Biller J, Hingtgen WL, Adams HP, Toffol GJ. Angiography of nonhemorrhagic
cerebral infarction in young adults.
Stroke.
1987;18:708-711. 6. Earnest F, Forbes G, Sandok PA, et al. Complications of cerebral angiography: prospective assessment of risk. AJR Am J Roentgenol. 1985; 142:247-253. 7. Patterson RH, Goodell H, Dunning HS. Complications of carotid angiography. Arch Neurol.
1964;10:513-520. 8. Mokri B, Sundt TM, Houser OW, Piepgras DG. Spontaneous dissection of the cervical internal carotid artery. Ann Neurol. 1986;19:126-138. 9. Hart RG, Miller VT. Cerebral infarction in young adults: a practical approach. Stroke. 1983;
14:110-114. 10. Bogousslavsky J, Regli F. Ischemie stroke in adults younger than 30 years of age. Arch Neurol.
1987;44:479-482. 11. Bogousslavsky J, Despland PA, Regli F. Spontaneous carotid dissection with acute stroke. Arch Neurol. 1987;44:137-140. 12. Biller J, Hingtgen WL, Adams HP, Smoker WRK, Godersky JC, Toffol GJ. Cervicocephalic arterial dissections: a ten-year experience. Arch Neurol. 1986;43:1234-1238. 13. Francis KR, Williams DP, Troost BT. Facial numbness and dysesthesia, new features of carotid artery dissection. Arch Neurol. 1987;44:345-346. 14. Goldberg HI, Grossmann RI, Gomory JM, Ashbury AK, Bilaniuk LT, Zimmermann RA. Cervical internal carotid artery dissecting hemorrhage: diagnosis using MRI. Radiology. 1986; 158:157-161. 15. Maitland
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CH, Black J, Smith
W. Abducens
palsy due to spontaneous dissection of the internal carotid artery. Arch Neurol. 1983;40:448\x=req-\ 449. 16. Bradac GB, Kaernbach A, Bolk-Weischedel D, Finck GA. Spontaneous dissecting aneurysm of cervical cerebral arteries. Neuroradiology. 1981; 21:149-154. 17. Fisher CM, Ojemann RG, Roberson GH. Spontaneous dissection of cervico-cerebral arteries. Can J Neurol Sci. 1978;5:9-19. 18. Ehrenfeld WK, Wylie EJ. Spontaneous dissection of the internal carotid artery. Arch Surg. nerve
1976;111:1294-1301. 19. Quisling RG, Friedman WA, Rhoton AL. High cervical carotid artery dissection: spontaneous resolution. AJNR. 1980;1:463-468. 20. O'Dwyer JA, Moscow N, Trevor R, Ehrenfeld WK, Newton TH. Spontaneous dissection of the carotid artery. Radiology. 1980;137:379-385. 21. Sellier N, Chiras J, Benhamou M, Bories J. Dissections spontan\l=e'\esde la carotide interne: aspects cliniques, radiologiques et \l=e'\volutifs:a propos de 46 cas. J Neuroradiol. 1983;10:243-259. 22. De Bray JM, Dubas F, Joseph PA, Causeret H, Pasquier JP, Emile E. Etude ultrasonique de
22
dissections
carotidiennes.
Rev
Neurol.
1989;145:702-709. 23. Petro GR, Witwer GA, Cacayorin ED, et al.
Spontaneous dissection of the cervical internal carotid artery: correlation of arteriography, CT and Pathology. AJNR. 1986;7:1053-1058. 24. von Reutern GM, B\l=u"\dingenHJ. Ultraschalldiagnostik der hirnversorgenden Arterien. Stuttgart, Germany: Georg Thieme Verlag; 1989. 25. Aaslid R. Transcranial Doppler Sonography. New York, NY: Springer-Verlag NY Inc; 1986. 26. Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982;57:769-774. 27. Lindegaard KF, Bakke SJ, Grolimund P,
Aaslid R, Huber P, Nornes H. Assessment of intracranial hemodynamics in carotid artery disease by transcranial Doppler ultrasound. J Neurosurg.
ies. J Neurosurg. 1982;56:857-860. 38. Cusick JF, Daniels D. Spontaneous reversal of internal carotid artery occlusion. J Neurosurg.
Reutern GM. Transcranial Doppler sonography: examination technique and normal reference values. Ultrasound Med Biol.
neous
1985;63:890-898. 28. Arnolds BJ,
von
1986;12:115-123.
29. Hennerici M, Steinke W, Rautenberg W. High-resistance Doppler flow pattern in extracra-
nial carotid dissection. Arch Neurol. 1989;46:670\x=req-\ 672. 30. Hass WK, Fields WS, North RR, Kricheff II, Chase NE, Bauer RB. Joint study of extracranial occlusion, II: arteriography, techniques, sites and complications. JAMA. 1968;203:962-968. 31. Zirkle PK, Wheeler JR, Gregory RT, Snyder SO, Gayle RG, Sorrell K. Carotid involvement in aortic dissection diagnosed by duplex scanning. J Vasc Surg. 1984;1:700-703. 32. Hirst AE, Johns VJ, Kime SW. Dissecting aneurysms of the aorta: a review of 505 cases. Medicine. 1958;37:217-279. 33. Bashour TT, Crew JP, Dean M, Hanna ES. Ultrasonic imaging of common carotid artery dissection. J Clin Ultrasound. 1985;13:210-211. 34. Zurbr\l=u"\ggHR, Leupi F, Sch\l=u"\pbachP, Althaus U. Duplex scanner study of carotid artery dissection following surgical treatment of aortic dissection type A. Stroke. 1988;19:970-976. 35. Rothrock JF, Lym V, Press G, Gosink B. Serial magnetic resonance and carotid duplex examinations in the management of carotid dissection. Neurology. 1989;39:686-692. 36. Benrabah R, Bousser RG, Cabanis EA, Lopez A, Moreau J. Syndrome de Claude-Bernard\x=req-\ Horner douloureux revelateur d'une dissection spontan\l=e'\ede l'art\l=e'\recarotide interne: interet du bilan ultrasonique cervical: a propos de deux observations. Bull Soc Ophtalmol Fr. 1988;88:763-768. 37. Pozzati E, Gaist G, Poppi M. Resolution of occlusion in spontaneously dissected carotid arter-
1981;54:811-813. 39. Gee W, Kaupp HA, McDonald KM. Sponta-
dissection of internal carotid arteries: sponby serial ocularpneumoplethysmography and angiography. Arch taneous resolution documented
Surg. 1980;115:944-949. 40. Friedman WA, Day AL, Quisling RG, Sypert GW, Rhoton AL. Cervical carotid dissecting aneurysms. Neurosurgery. 1980;7:207-214. 41. Stringer WL, Kelly DL. Traumatic dissection of the extracranial internal carotid
artery. Neurosurgery. 1980;6:123-130. 42. McNeill DH, Dreisbach J, Marsden RJ. Spontaneous dissection of the internal carotid artery: its conservative management with heparin
sodium. Arch Neurol. 1980;37:54-55. 43. Marx A, Messing B, Storch B, Busse O. Spontane Dissektion hirnversorgender Arterien. Nervenarzt. 1987;58:8-18. 44. Cusmano F, Piazza P, De Donatis M, Montanari E, Saginario A, Bassi P. Dissecazione dell' arteria carotide interna. Radiol Med. 1988;76:262\x=req-\ 273. 45. Parenti G, Marconi F, Canapicchi R, Puglioli M, Giradli C. Spontaneous recanalization of carotid artery occlusion following non traumatic dissection. Ital J Neurol Sci. 1989;10:361-367. 46. Markwalder TM, Starrett RW, Mumenthaler M. Spontaneous bilateral recanalization in bilateral internal carotid artery occlusion. Stroke.
1980;11:95-97.
47. Landre E, Roux FX, Cioloca C. Dissection spontan\l=e'\ede la carotide interne exocranienne: aspects th\l=e'\rapeutiques.Presse Med. 1987;16:1273\x=req-\
1276. 48. Hart RG, Easton JD. Dissections. Stroke.
1985;16:925-927.
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Duplex Sonography
Matthias Sturzenegger, MD
\s=b\ Extracranial and transcranial Doppler and duplex sonographic findings in six patients with internal carotid artery dissection proven by angiography is reported. Extracranial Doppler analysis showed occlusion without a recordable signal from the internal carotid artery at any level or stenosis with accelerated flow in the high cervical segment. Transcranial Doppler findings demonstrated the hemodynamic consequences of the internal carotid artery occlusion or stenosis with collateral flow across the circle of Willis and also showed the dampened pulse wave of the middle cerebral artery ipsilateral to the dissection. In duplex sonography, the indirect signs indicating internal carotid artery dissection were a patent carotid bifurcation and proximal internal carotid artery segment but with no or only a short systolic flow signal. Atherosclerotic wall changes were absent, an important finding that suggests
rp
he cervical part ofthe internal carotid artery (ICA) is by far the most frequent site of spontaneous wall dis¬ section,13 but any brain-supplying ar¬ tery may be affected.4 The exact fre¬ quency is unknown, but it may be quite underestimated. With less rigid indica¬ tions for cerebral angiography5"7 in the last few years, an increasing number of patients with spontaneous dissection of the ICA (ICD) have been identified." From this experience, we have learned that the clinical presentation of ICD may be extremely variable, ranging Accepted for publication March 12,1991. From the Department of Neurology, University
of Bern, Switzerland.
Reprint requests to Department of Neurology, University of Bern, Inselspital, CH-3010 Bern, Switzerland (Dr Sturzenegger).
nonatherosclerotic stenosis or occlusion. Direct signs making the diagnosis likely were a tapering of the internal carotid artery lumen distal to the bulb, an irregular membrane crossing the vessel lumen, and the demonstration of a true lumen with flow and a false one without flow. While cerebral angiography is still considered the gold standard, ultrasound may become the primary modality for early diagnosis. Doppler and duplex examinations help to indicate angiography and are the methods of choice for follow-up investigations. They clearly demonstrate spontaneous recanalization with normalization of carotid circulation or, in case of persistent occlusion, improvement of collateral blood supply. Sequential examinations may prove helpful to determine the duration of
anticoagulant treatment. (Arch Neurol. 1991 ;48:1057-1063)
from the patient with unspecific head¬ ache or even no clinical symptoms and signs to the patient with severe stroke and rapidly ensuing death. These clini¬ cal extremes usually do not give rise to further investigations, and the real cause, ICD, goes unrecognized.
Younger patients
are
preferentially
affected: Hart and Miller9 found two cases (2%) among 100 patients with stroke under the age of 40 years, and Bogousslavsky and Regli1" found nine cases (22%) among 41 patients with stroke under the age of 30 years. Mean age at presentation in a group of 146 cases2 was 45 years; 70% were between 35 and 50 years old. The younger age at presentation is suggestive of ICD rath¬ er than atherosclerotic carotid dis¬ ease.24 Considering all patients with stroke, ICD is a rare cause of stroke:
among a series of 1200 consecutive pa¬ tients with stroke," 30 (2.5%) had ICD. In another series of 4531 patients exam¬ ined with cerebral angiography because of acute cerebrovascular symptoms,12
extracranial carotid artery dissection diagnosed in 11 (0.24%). When the characteristic triad of facial or neck pain, ipsilateral oculosympathetic paresis, and hemispheric ischemie symptoms is present, diagnosis may be strongly suspected on clinical grounds.2,4,13"16 For definite diagnosis, angiography is required, which can show characteristic but also variable signs.3,4,17'21 The findings, except double lumen, are nonspecific. Differential di¬ agnosis includes arterial compression or invasion by tumor or pharyngeal inflam¬ mation, congenital hypoplasia, vasculi¬ tis, radiation-induced arteriopathy, and was
vasospasm. In general,
prognosis
is
spontaneous recanalization more
good,
than 80% of patients.2,4
and in
occurs
However,
persisting disability can result,21,22 ow¬ ing to ensuing stroke. Considering pa¬ tients with ICD and stroke,11 prognosis is clearly worse: recanalization occurs in only 60% and death in 23%, and 48% of the patients remain severely disabled. Stroke is,
known from angiogra¬ due to embolism from local thrombosis at the site of dissection. Rarely, insufficient collateral blood sup¬ ply causes hemodynamic infarction. Because of the danger of embolism, early anticoagulation is considered the treatment of choice. However, its effec¬ tiveness has not been proved yet by a randomized controlled study. On the other hand, to my knowledge there is no case of ICD reported in the literature in which symptoms worsened with anticoas
phy,18,23 mostly
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Table 1.—Clinical
Vascular Risk Factors
Patient No./
Symptoms Recurrent TIA (L hemiparesis), pain R eye and temple R hemiparesis, aphasia, occipital
Age, y/Sex 1/49/M
2/42/F
headache Recurrent R amaurosis fugax, recurrent TIA
3/41 /M
Signs None
R
4/41/M
R
R temple and cheek hemiparesis, aphasia, frontal
headache Recurrent TIA
5/40/M
Heparin sodium,
Migraine, hypertension
Heparin, coumarin
None
Aspirin
coumarin Partial recanalization with
stenosis after 15 wk Resolution on both sides
persisting slight after 2
hemiparesis, transient aphasia,
mo
bruit R carotid R
None
hemiparesis
Heparin,
Persisting occlusion
coumarin
after 2
mo, better intracranial
collateral flow Partial HS
(L
Evolution Resolution after 12 d
Treatment
Migraine, hypertension, smoking, cholesterol
R
hemiparesis), gait disturbance, pain R
eye and
hemiparesis
Loss of consciousness,
(R hemiparesis), pain
_
Findings*
on
R,
hemianopia to L, L hemiparesis, L sensory neglect,
temple
Symmetric BFV
Heparin, coumarin
Migraine, hypertension
in both
MCAs after 5 d, complete recanalization after 6 wk
CT: infarction 6/41/M
Partial HS,
Recurrent TIA
(asphasia), pain
none on
L
Resolution after 10 wk
Heparin, coumarin
L
eye and forehead
*TIA indicates
transient ischemie attack; HS, Horner's
agulant therapy. If anticoagulation is beneficial, early diagnosis is essential for the treatment of patients with ICD, a goal that can be achieved with com¬ bined ultrasonographic examination (CUE) using conventional extracranial direct and indirect Doppler sono¬ graphy, transcranial Doppler sono¬ graphy (TCD), and duplex scanning. I report my experience using CUE in six patients with ICD in the extracranial segment verified by angiography.
syndrome; CT, computed tomography; BFV,
blood flow
for all TCD ultrasound examinations (TC264, Eden Medizinische Elektronic GmbH, Ueberlingen, Germany). The middle cere¬ bral artery (MCA), anterior cerebral artery, posterior cerebral artery, and ICA bifurca¬ tion were analyzed at different depths by a transtemporal approach and the intracranial vertebral and basilar arteries were analyzed through the occipital foramen. Systolic, dia¬ stolic, and mean blood flow velocity (BFV) were measured in each vessel. Pulsatility index (PI) was calculated according to the following formula: PI (svstolic BFV dias¬ tolic BFWmean BFV. The values of 52 normal controls served as reference. The MCA-BFV and PI values of the six patients were compared with those ofthe controls. =
-
PATIENTS AND METHODS Duplex Examination
A high-resolution, real-time, duplex ultra¬ sound system (Diasonics SPA 1000, Sonotron
Holding AG, Zug, Switzerland)
used that consisted of
a
was
10-MHz echoto-
mography imaging probe and a 4.5-MHz pulsed-wave Doppler probe with real-time gray-scale Fast-Fourier transform Doppler spectrum analysis. Common carotid artery (CCA), bulb, ICA, external carotid artery (ECA), and vertebral arteries were imaged on
both sides.
Extracranial
Doppler Examination
The technique for extracranial direct and indirect Doppler sonographic examination 4 has been described in detail previously. I used the same device as for TCD recordings, which is described below. The CCA, ECA, ICA, subclavian artery, and vertebral artery at the atlas were examined by continuous insonnation on both sides. Supratrochlear and ophthalmic arteries (OpAs), as well as carotid siphons, were measured by a transor¬ bital approach. TCD Examination The technique for TCD recordings has been described in detail previously.25" A mi¬ croprocessor-controlled directional pulsed Doppler device operating at 2 MHz was used
Cerebral Angiography
Selective CCA angiograms were obtained in all patients. Catheterizations were per¬ formed by the percutaneous femoral ap¬ proach. In one case (case 3), direct CCA puncture was performed. Six French poly¬ ethylene catheters and a nonionic, low-osmolar contrast agent were used. Statistical analysis was performed using simple regression analysis and the unpaired and paired t test. RESULTS
velocity; and MCA, middle cerebral artery.
patients and additional stenosis on the other side in case 3. Four patients had collateral blood supply from the ipsilat¬ eral ECA to ICA territory and patient 3 had collateral supply across both OpAs with retrograde flow. Transcranial Doppler sonography
showed reduced MCA-BFV and PI on the side of dissection in five patients compared with the contralateral side (P=.001 for BFV, P=.002 for PI) as well as compared with the controls .0001 for PI). (P=.0001 for BFV, An additional patient had symmetric MCA velocities but reduced PI on the side of the lesion (case 2). All had collat¬ eral blood supply across the anterior communicating artery from the contralateral ICA. Mean BFV and PI with the side differences of patients and controls are given in Table 2. In controls, there was a correlation between right and left MCA-BFV F 516.2, (r=.955, .0001) and PI (r=.768, = 71.8, .0001) and there was no side differ¬ ence (P=.83 for both). In patients, there was no correlation between MCABFV (r=.692, F 3.7, P=.13) and PI (r=.242, F 0.25, P .64) ipsilateral and contralateral to the dissection side, and the side differences were obvious (P= .001 for BFV and P .002 for PI). =
=
=
=
=
=
Six patients (five men and one woman with a mean age of 42.5 years [range, 40 to 49 years]) admitted within a year with angiographically proved ICD were analyzed. Five had unilateral dissection and one (case 3) had bilateral dissection. The clinical findings are summarized in Table 1. Lower cranial nerve palsy did not
occur.
A
computed tomographic
normal in five patients and showed MCA infarction in one (case 5). There was no preceding trauma. Extracranial Doppler sonography showed ICA occlusion on one side in all scan was
=
=
Duplex Examination No patient changes. All
had atherosclerotic wall the proximal ICA seg¬ ments were patent on the "occluded" side, two with a residual "stump flow" and four without recordable flow signal. There was a "membrane" visible cross¬ ing the ICA lumen in four arteries, pro¬ ducing the picture of double lumen not compressible by the probe (Fig 1).
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Table 2.—Transcranial L or
Ipsilateral MCA
BFV
Group
Doppler Findings*
R or Contralateral MCA
Mean Difference
BFV
PI
BFV
Controls Mean ± SD
64.5 ± 10.5
0.76 ± 0.15
0.46 ± 3.6
0.01 ± 0.1
0.48-1.24
64.1 ± 11.6 41-90
0.75 ± 0.15
45-90
0.51-1.37
17
0.55
43.2 ± 9.5 33-55
0.46 ± 0.08
51.2 ± 11.4
0.65 ± 0.08
18 ± 8.4
0.33-0.57
48-82
0.52-0.75
0.2 ± 0.1 0.26
Range Patients Mean ± SD
Range
*MCA MCAs in
indicates middle cerebral artery; BFV, blood flow velocity; and PI, pulsatility Index. Left and right MCAs In cases with bilateral dissection, the ipsilateral side indicates the side more occluded.
were
examined in controls,
ipsilateral and contralateral
patients.
nal. In case 1, stenosis started immedi¬ ately distal to a carotid kinking. There was a tapering occlusion start¬ ing 2 cm distal to the bifurcation with a flame-shaped stump in one artery (case 2). Collateral blood supply across the anterior part ofthe circle of Willis (ante¬ rior communicating artery) was con¬ firmed in all five cases with bilateral carotid angiograms. No patient showed pseudoaneurysm formation or signs indicative of fibro¬ muscular dysplasia. None had athero¬ sclerotic wall lesions (Fig 2). The results of ultrasound findings and angiography are summarized in Table 3. REPORT OF A CASE
Fig 1. —Results of initial Duplex scanning (case 3): a, open left carotid bifurcation and identification of external carotid artery (ECA); b, only short systolic flow signal in the most proximal left internal carotid artery (ICA; stump flow); c, membrane (arrow) crossing lumen of left ICA in a more distal segment; d, preserved flow signal in proximal right ICA; e, high blood flow velocity indicating stenosis in more distal segment of right ICA, membrane crossing vessel lumen; and f, membrane crossing vessel lumen of right ICA (arrow). CCA indicates common carotid artery.
Angiography Five patients (cases 1, 2, 3, 5, and 6) had bilateral, and one (case 4) had uni¬ lateral, carotid angiography. One pa¬ tient (case 3) had bilateral dissection; consequently, seven dissected ICAs could be analyzed. In all of them, the carotid bifurcation and at least the most proximal 2 cm of the ICA were normal. Four showed smoothly tapering stenoses (cases 3 [left], 4,5, and 6) starting 3 to 4 cm distal
to the
bifurcation, in all extending up to the base of the skull (in case 5 probably to the siphon segment). In three, the stenoses were high grade with a filiform residual lumen resulting in a "string sign" (cases 4,5 and 6). Abrupt return to normal caliber was noted in all at the entrance of the carotid canal. Two showed irregular segmental stenosis (cases 1 and 3 [rightl), in both cases of the prepetrosal segment and with abrupt reconstitution of a normal lumen width at the entrance of the carotid ca-
A 41-year-old technician had no vascular risk factors. Three weeks before his hospital¬ ization, he felt increasing pain in his right temple and cheek. Plain roentgenograms showed an opacified maxillary sinus, and polyposis was considered as the likely cause of his pain. The patient was admitted for sinuscopy. Soon after premedication with intra¬ muscular atropine sulfate (0.5 mg) and mor¬ phine chloride (5 mg), he fainted. When he regained consciousness after several min¬ utes, there was right-sided hemiplegia and asphasia clearing within 2 hours. Physical examination revealed a bruit over the right carotid artery. Results of routine blood lab¬ oratory tests, electrocardiogram, and com¬ puted tomography were normal. Now, on detailed questioning, he reported several at¬ tacks of blurred vision or transient blindness of his right eye, lasting 1 or 2 minutes, in the days before admission. In addition, he had had three episodes of feeling cold and heavi¬ ness or loss of motor control of his right arm and hand. Doppler analysis (Fig 3) showed reduced diastolic flow and increased PI in the left CCA. The left ICA could not be identified. The left ECA showed high diastolic flow re¬ sembling an intracranial vessel. The BFVs in the right CCA, the ECA, and the proximal part of the ICA were normal. However, in the high cervical segment of the right ICA, there was increased BFV over a long seg¬ ment up to the base of the skull. Both OpAs showed reversed flow direction toward the intracranial region. The TCD analysis (Fig 3) revealed reduced BFV and reduced PI in the left MCA. The left anterior cerebral artery showed reversal of flow direction. High BFVs in the left pos-
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terior cerebral artery indicated collateral flow from the posterior circulation.
Duplex scanning (Fig 1) showed a widely patent left proximal ICA, but only minimal systolic intraluminal flow signal (stump flow). In its more distal part, a membranelike structure traversing the vessel lumen could be visualized. The right proximal ICA was also patent, and flow was normal. Still more
distally, there was a membranelike structure in the vessel lumen, and at this site high BFVs were present, indicating stenosis. A diagnosis of left ICA occlusion and right ICA stenosis distal to their origin from the
bulb was made, with collateral flow to the left carotid territory across the anterior and pos¬ terior communicating arteries. The patent proximal ICA segments and the membranes traversing the vessel lumen suggested bilat¬ eral ICDs. Cerebral four-vessel angiography (Fig 2) showed a normal proximal ICA on both sides. In the higher cervical part, the left one showed progressive narrowing to a stringlike lumen with abrupt luminal recon¬ stitution at the entry to the petrosal canal. There was moderate stenosis of the right ICA in the higher cervical part, again with abrupt reconstitution of the vessel lumen at the base ofthe skull. Intracranially, flow was from the right ICA to the left across the anterior communicating artery. Because of the smooth boundaries of luminal narrowings, bilateral carotid hypoplasia was diag¬ nosed by the radiologist (which did not ex¬ plain the sudden neurologic symptoms). Doppler control 10 days later showed nor¬ malized BFV in both CCAs. Both IC As could be identified with normal BFV in their proxi¬ mal parts but with high BFV in their upper cervical segments due to stenosis. The MCABFV was symmetric. The anterior cerebral artery and OpA flows were antegrade on both sides. Duplex scanning showed flow in both ICAs, but there were still stenoses due to membranelike structures. This flow reconstitution clearly made hypoplasia unlike¬ ly and a diagnosis of dissection more favor¬ able. Doppler reexamination 2 months later showed normal results proving spontaneous recanalization and yielded the diagnosis of spontaneous bilateral ICD. The patient has remained asymptomatic taking aspirin. COMMENT
Fig 2. —Left common carotid arteriogram in case 3 (a, anteroposterior projection; b, lateral view) demonstrates common carotid narrowing (arrowheads in a) resulting from subintimai injection following direct artery puncture. Carotid bifurcation and proximal 3 cm of internal carotid artery (ICA) are normal. Then, smoothly tapering stenosis of left cervical ICA (arrows in a and b) with severe slowing of flow is noted, extending up to the skull base, where abrupt return to normal caliber is seen at entrance of carotid canal (open arrows in a and b). There is no filling of left anterior cerebral artery. Right common carotid arteriogram (c, anteroposterior projection; d, lateral view) again shows normal carotid bifurcation and proximal right ICA. Irregular segmental moderate stenosis of the high cervical prepetrosal ICA segment (arrows in c and d) is demonstrated with abrupt reconstitution of normal lumen width at the entrance of the carotid canal (open arrows in c and d). There is collateral flow from right to left carotid territory across anterior circle of Willis (arrowheads in c).
Because the clinical presentation of ICD may be extremely variable,2 the diagnosis cannot be made on clinical grounds alone. Carotid angiography is at present still the method of choice for definite diagnosis. Though it has be¬ come much less risky owing to technical achievements,5'' it remains an invasive procedure that should not be performed when there is only weak clinical suspi¬ cion of ICD. In these situations, an easi¬ ly available, noninvasive method is de¬ sirable that can confirm the suspicion and allow the selective use of carotid
angiography.
Conventional direct and indirect
(pulsed- or continuous-wave) Doppler sonography of the extracranial carotid arteries and their branches24
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can
reveal
Table
3.—Summary of Results*
Patient No./
Age, y/Sex 1/49/M
Arteriography Segmental stenosis of high cervical R ICA; collateral circle of Willis, L to R Tapering occlusion of L ICA; collateral fiow across circle of Willis, RtoL L ICA: string sign, reconstitution at skull base; R ICA: high cervical segmental stenosis, reconstitution at skull base; collateral flow across circle of Willis, R to L flow
2/42/F
3/41/M
4/41/M
L ICA:
R ICA:
retrograde
R MCA BFV i; collateral flow across AComA, LtoR
OpA
across
string sign, string sign up
cavernous
L ICA occlusion,
orthograde
OpA
L MCA PI
both
across
to
segment;
i;
collateral flow to L
AComA, R
i;
Duplex Sonography proximal R ICA with stump flow
Patent
Patent proximal L ICA, no intraluminal flow; membrane with double lumen Patent proximal L ICA without flow; membrane L ICA (distal); membrane R ICA (distal and stenosis); double lumen
L ICA occlusion, R ICA stenosis (high cervical segment), OpAs both
L MCA BFV
occlusion, L OpA retrograde
L MCA BFV
Patent proximal L ICA with stump flow
occlusion, R OpA retrograde
R MCA BFV 1; collateral flow across AComA, L to R; R MCA, no reactivity
Patent proximal R ICA without flow
flow
across
collateral
AComA,
R to L and from vertebrobasilar system
retrograde (bilateral dissection)
i; collateral flow across AComA, RtoL
L ICA
reconstitution at skull base 5/40/M
TCD
ECD R ICA occlusion, R
R ICA
collateral flow across on C02 breathing circle of Willis, L to R L MCA BFV |; collateral Patent proximal L ICA L ICA occlusion, L OpA 6/41/M L ICA: string sign, flow across AComA, without flow; membrane reconstitution at skull retrograde RtoL with double lumen not base; collateral flow across circle of Willis, compressible RtoL ECD indicates extracranial Doppler sonography; TCD, transcranial Doppler sonography; ICA, internal carotid artery; OpA, ophthalmic artery; MCA, middle cerebral artery; BFV, blood flow velocity; AComA, anterior communicating artery; and PI, pulsatility index. Occlusion on ECD indicates no signal from ICA at origin from bulb and at skull base.
48(70/31) MCA, (67/39) PCA, 37(51/28) ACA, 48
OpA, 37 (59/30)
retro
ACA, 25 (36/20) retro
MCA, 34 (44/28) PCA, 53 (73/42)
OpA.
50
(69/37)
retro
ICA, d, 109(118/90) ICA, p, 25(45/19) CCA, 25(70/17)
Fig 3. —Results of initial extracranial and transcranial Doppler analysis in case 3 (see text for details). ACA indicates anterior cerebral artery; retro, retrograde; MCA, middle cerebral artery; PCA, posterior cerebral artery; OpA, ophthalmic artery; ICA, internal carotid artery (d and indicating distal and proximal); and CCA, common carotid artery. The numbers represent the values of blood flow velocities in each vessel: mean (systolic/diastolic). The pathological values are underlined.
occlusion or stenosis if it exceeds 50% of lumen diameter. The technique does not yield further information about origin. Only the finding of a stenosis located in the upper cervical ICA segment or ex¬ tending over a long distance may sug¬ gest dissection,22,29 but this is not a
specific sign. Transcranial Doppler son¬ ography,26"28 though detecting the ef¬
fects on intracranial circulation includ¬ ing collateral blood flow, does not help in further differentiating the origin of ste¬ nosis or occlusion. The primary goal of CUE is the differ-
entiation of ICD from occlusion or ste¬ nosis due to other causes such as athero¬ sclerosis. Atherosclerotic lesions ofthe brain-supplying arteries show a predi¬ lection for the carotid bifurcation.30 Spontaneous ICD, on the other hand, is usually localized in the middle or upper cervical segment ofthe ICA or begins at least 2 to 3 cm distal to the carotid bifur¬ cation. läi'16'17·20·23These anatomic facts and the easy accessibility of the carotid bi¬ furcation in most patients by duplex scanning make this method suitable for differentiation. When conventional Doppler sono¬ graphy indicates ICA stenosis or occlu¬ sion, the indirect findings at duplex scanning listed in Table 481"34 suggest a dissection. These are ultimately non¬ specific findings, and the diagnosis may be hampered when there is the simul¬ taneous presence of atheromatous plaques22 or when the ICD starts al¬ ready at the bifurcation.2021 Therefore, direct visualization of the dissection should be attempted. Direct and more specific signs of ICD at duplex scanning are listed in Table 4. Internal carotid artery dissection is virtually always extracranial but varies considerably in extent.21 It typically oc¬ curs distal to the extracranial bifurca¬ tion,4 often at or around the C-2 verte¬ bral level.2,21 Because this region may be beyond the range of carotid imaging by
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Table 5.—Limitations of
4.—Duplex Sonography: Findings Suggesting ICA Dissection* Table
Indirect findings
No atheromatous plaques are visible in ca¬ rotid bifurcation Bulb and proximal segment of ICA are
patent No flow signal
or high-resistance flow pat¬ (short, only systolic flow peak [stump flow] or bidi¬ rectional [reverberating] systolic flow) in
tern
proximal
ICA
Lack of wall
pulsations
Direct signs Tapering of ICA lumen starting >2 tal to bulb
cm
dis¬
Irregular "membrane" crossing ICA lumen (Fig 1)
Demonstration of true lumen with flow and false (thrombosed) lumen without flow; unlike veins, true and false lumens are
noncompressible by probe pressure; flow in false lumen resulting from more distal reentry into true lumen, as fre¬ quently found in CCA dissection associ¬ ated with dissecting aortic aneu¬
rysm,3'"3' is rare Axial sections show "membrane" as flap in lumen Findings at follow-up examinations Recovery of lumen patency Flow recovery Recovery of normal hemodynamics, when combined with TCD *
ICA indicates Internal carotid artery; CCA, com¬ carotid artery; and TCD, transcranial Doppler
mon
sonography.
ultrasound, direct visualization of the
ICD is not possible in all cases.22 Sensitivity of CUE in detecting occlu¬ sion in the case of ICD was very high in one study (95%).22 Its emergency use in cases where clinical presentation sug¬ gests dissection does help in rapid diag¬ nosis and selection of patients for
angiography. Duplex sonography has several méth¬ odologie limitations, listed in Table 5. These are the major reasons why I still consider angiography to be necessary to
assess the full extent of the vascular process and to confirm the ultrasound
findings.
In addition to its use in initial diagno¬
sis, duplex scanning is an excellent non-
Duplex
Sonography Anatomic Short and / or fat neck, high cervical carotid bifurcation, goiter, calcification of ath¬ erosclerotic lesions (sound shadow) Individual Restless, agitated, continuously swallow¬ ing patients, air emphysema; direct ex¬ amination may be impossible Methodic Occlusion cannot always be demonstrated directly because of its high cervical location Usually, whole longitudinal extension of wall dissection and especially involve¬ ment of intracranial ICA segments (oc¬ curring in up to 20%39·40) cannot be de¬ tected Detection of aneurysms is usually not possible29 Identification of fibromuscular dysplasia as underlying cause1639 is hardly ever pos¬ sible
invasive
modality
for serial
follow-up
examination.29,35,36 The signs indicating
are listed in Table 4. Sponta¬ resolution or reduction of stenosis may occur at variable intervals, ranging from a few days to several months.19,22,29 Sequential follow-up studies have shown that this process generally oc¬ curs within a few days and only occa¬ sionally over weeks or months.3,29,30,37"39 Most authors agree that ischemie in¬ farction is due in most cases to distal embolism from local thrombosis at the stenotic segment. The role of embolism is evident from the occurrence of isch¬ emie symptoms when a stenosis is hemodynamically insignificant, from arte¬ riography that shows distal emboli, and from intraluminal thrombus seen arteriographically and at surgery. Embolie stroke may develop in the first few days of dissection,* and its frequency is esti¬ mated to be at least 15%3 to 24%.21 More¬ over, stenosis may progress to occlu¬ sion,17,18,40 resulting in a critical hemodynamic situation and preventing recanalization. These potential compii-
recovery neous
*References 3, 4, 17, 18, 20,
23, 37, 40, and 41.
cations are the reason why anticoagu¬ lant therapy, first with heparin, is rec¬ ommended by several authors2,42 with the idea to prevent thrombosis and em¬ bolism. It is logical that treatment should be started as early as possible, implicating early diagnosis, facilitated by application of CUE. As controlled studies are lacking, the efficacy of such therapy remains unproved, regardless ofthe nature and degree ofthe anatomic disease present. To date, no harmful effect of anticoagulant therapy, includ¬ ing cases with extracranial aneurysms, has been reported,2,8,11,17,22,42 and only the simultaneous presence of an intracrani¬ al aneurysm is considered a contraindi¬ cation.2 Several uncontrolled studies suggest beneficial effects of anticoagu¬ lation.21,22,43 On the other hand, it seems pointless to continue anticoagulant therapy once vascular patency has been restored. The CUE offers the possibili¬ ty of noninvasive follow-up to detect the moment of recanalization. As spontane¬ ous recanalization is the rule,2"4,17,22,37,44"46 surgical interventions remain excep¬ tional2"4,8,37,47,48 and are reserved for pa¬ tients with recurrent or progressive ischemie symptoms despite anticoagu¬ lant therapy. If these ischemie symp¬ toms are due to insufficient collateral blood supply, it may be detected by TCD (case 5). Therefore, TCD may help in selecting patients for revasculariza¬ tion procedures. In conclusion, CUE with special em¬ phasis on duplex scanning is particular¬ ly useful to select patients with suspect¬ ed ICD for arteriography and thus provides a tool for early diagnosis by its emergency use. It is the method of choice for follow-up examinations to de¬ termine duration of anticoagulation and may help to assess the real frequency of ICD when also used in patients in whom angiography would not be considered. I wish to thank Peter Huber, director of the
Department of Neuroradiology, University of Bern, Switzerland, for performing the neuroradio¬ logie examinations.
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