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Contralateral hyperacute intracerebral hemorrhageafter carotid artery stenting with contralateralinternal carotid artery occlusionHirokazu Takami, MD,a Kazuo Hanakawa, MD,a Hiroaki Sato, MD,b Kyouske Tsutsumi, MD,a

Masahiko Murao, MD,a and Takafumi Ide, MD,a Tokyo, Japan

An 87-year-old man sustained an intracerebral hemorrhage in the watershed area of the contralateral frontal lobeimmediately after carotid artery stenting (CAS) for severe cervical internal carotid artery (ICA) stenosis. The contralateralcervical ICA was occluded. CAS resulted in increased cross-flow through the anterior communicating artery and increasedflow in the contralateral middle cerebral artery. This case demonstrates that CAS in patients with contralateral ICAocclusion and insufficient collateral flow can cause dramatically increased collateral flow through the circle of Willis andresult in contralateral hyperperfusion. In patients with severely compromised cerebral perfusion, measures should betaken to prevent hyperperfusion-related complications. (J Vasc Surg 2014;59:821-4.)

Revascularization of carotid artery stenosis results inhyperperfusion syndrome in rare cases. This is a potentiallydevastating complication characterized by seizures, head-ache, and cerebral hemorrhage.1,2 Pathophysiologically,hyperperfusion syndrome is caused by a rapid increase incerebral blood flow that exceeds the metabolic demands.Bilateral carotid artery stenosis or occlusion is a hemody-namically critical state, and revascularization of one carotidartery may dramatically change the flow dynamics throughthe circle of Willis, thereby affecting contralateral cerebralperfusion.

CASE REPORT

An 87-year-old right-handed man presented after loss ofconsciousness for w15 minutes and right-sided limb weaknessand aphasia for w1 hour, suggesting a transient ischemic attack.He had a history of hypertension, diabetes mellitus, interstitiallung disease, and chronic heart failure. He was taking two antipla-telet drugs: aspirin (81 mg daily) and clopidogrel (75 mg daily).His coagulation parameters and platelet count were within normallimits.

Angiography showed right cervical internal carotid artery(ICA) occlusion (Fig 1, A) and severe left cervical ICA stenosis(Fig 1, B). Collateral blood flow was detected from the rightexternal carotid artery through both ophthalmic and middlemeningeal arteries to the intracranial ICA (Fig 1, C). There was

the Department of Neurosurgery, Tokyo Metropolitan Bokutohospitala; and the Department of Neuroendovascular Therapy, Tokyoetropolitan Police Hospital.b

or conflict of interest: none.rint requests: Hirokazu Takami, MD, Department of Neurosurgery,kyo Metropolitan Bokutoh Hospital, 4-23-15, Koutoubashi, Sumida-ku,

okyo 130-8575, Japan (e-mail: takami-tky@umin.ac.jp).editors and reviewers of this article have no relevant financial relationshipsdisclose per the JVS policy that requires reviewers to decline review of anyanuscript for which they may have a conflict of interest.-5214/$36.00yright � 2014 by the Society for Vascular Surgery.://dx.doi.org/10.1016/j.jvs.2013.04.051

cross-flow through the anterior communicating artery from theleft ICA to the right anterior cerebral artery (Fig 1, D). By criteriafrom the North American Symptomatic Carotid EndarterectomyTrial, the left ICA stenosis was 78%.

During the month before treatment, the patient experiencedtwo transient ischemic attacks. Because he had many risk factorsfor carotid endarterectomy, as defined in the Stenting and Angio-plasty with Protection in Patients at High-Risk for Endarterectomytrial, including cardiac and respiratory disease and contralateralICA occlusion, carotid artery stenting (CAS) was considered themost appropriate treatment.

CAS was performed under local anesthesia with mild sedation.Heparin (4000 IU) was administered preoperatively, resulting inan increase in the activated clotting time from 140 to 313 seconds.

The left ICA lesion was approached through the left femoralartery using a 90-cm 8F Brite Tip guiding catheter (Cordis John-son & Johnson Inc, Miami, Fla) and a 125-cm 6F JB2 CX catheter(Katex Inc, Tokyo, Japan). The stenosis was crossed with a 190-cmEZ Filter Wire (Stryker Inc, Kalamazoo, Mich). Predilatation wasperformed with a 3.0- � 20-mm Sterling balloon (Stryker). A 10-� 31-mm carotid Wallstent Monorail stent (Stryker) was placed,followed by dilatation using a 4.0- � 30-mm Rx Genity balloon(Kaneka Inc, Tokyo, Japan).

Angiography after stent placement demonstrated nearly totalresolution of the stenosis (Fig 1, F). Cross-flow through the ante-rior communicating artery increased dramatically, and flow wasobserved in the right middle cerebral artery, which was absentpreoperatively (Fig 1, G).

The patient’s systolic blood pressure (SBP) was 165 to 185mm Hg before CAS. After stent deployment, a nicardipine infu-sion was started with the aim of keeping SBP <140 mm Hg,but there was a delay before the drug began to take effect. Fig 2shows the BP during and after the procedure.

Immediately after the procedure, the patient had no neurologicdeficits or clinical symptoms, and the activated clotting time was328 seconds. Routine postoperative computed tomography (CT)at 50 minutes after stent placement showed a small hemorrhagiclesion in the right frontal lobe (Fig 3, A). Protamine was infused,and the SBP was carefully maintained at <140 mm Hg.

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Fig 1. Preoperative and intraoperative angiography and magnetic resonance imaging findings. A, Angiography image(lateral view) of the right carotid artery bifurcation shows occlusion of the right cervical internal carotid artery (ICA).B,Angiography image (lateral view) of the left carotid artery bifurcation shows severe stenosis of the ICA. This was a 78%stenosis according to the criteria of the North American Symptomatic Carotid Endarterectomy Trial. C, Digitalsubtraction image (lateral view) of the intracranial circulation during right common carotid artery injection shows bloodflow from the external carotid artery to the cavernous portion of the right ICA through the right middle meningeal arteryand the right ophthalmic artery.D,Digital subtraction image (anteroposterior view) of the intracranial circulation duringleft common carotid artery injection shows cross-flow through the anterior communicating artery to the right hemisphereand perfusion of part of the territory of the right anterior cerebral artery. E, Magnetic resonance angiography image(inferior view) shows poor flow in the right middle cerebral artery, despite visualization of the posterior communicatingartery. F,Angiography image (lateral view) of the left carotid artery bifurcation after stent placement and dilatation showsnearly total resolution of the stenosis. G, Digital subtraction image (anteroposterior view) of the intracranial circulationduring left common carotid artery injection shows increased cross-flow through the anterior communicating artery andincreased flow in the right middle cerebral artery.

JOURNAL OF VASCULAR SURGERY822 Takami et al March 2014

After admission to the intensive care unit, the patient’s level ofconsciousness gradually deteriorated, and he developed left hemipa-resis. A head CT at 3 hours after the previous examination showedmassive expansion of the hematoma (Fig 3,B).He underwent emer-gency craniotomy for drainage, and almost all of the hematoma wasevacuated (Fig 3, C). The patient’s level of consciousness graduallyincreased, and his left hemiparesis improved. His National Institutesof Health Stroke Scale score was 22 just before the craniotomy,improved to 11 over a few days, and was 2 after 4 months.

DISCUSSION

Hyperperfusion syndrome is defined as a major increasein ipsilateral cerebral blood flow beyond the metabolicdemands of the brain tissue after revascularization. Ogasa-wara et al3 performed a meta-analysis of 4494 patients whounderwent CAS or carotid endarterectomy and found that1.1% developed hyperperfusion, including 0.7% who

developed intracerebral hemorrhage after CAS. Intracere-bral hemorrhage caused by hyperperfusion occurredat a mean of 1.7 6 2.1 days postoperatively, with mostoccurring #12 hours. The risk factors for hyperperfusionsyndrome included hypertension, poor collateral circula-tion, and severe ICA stenosis.4,5

Kablak-Ziembicka et al6 studied flow changes usingtranscranial Doppler ultrasound imaging. They foundthat patients with bilateral ICA stenosis and unilateralCAS had increased cross-flow through the anteriorcommunicating artery, resulting in normalization of flowin the contralateral middle cerebral artery. Reinhard et al7

reported that cerebral autoregulation and vasodilatoryreserve were impaired in patients with bilateral criticalcarotid artery stenosis or occlusion.

In the current patient, the right cervical ICA wasoccluded. The right hemisphere was perfused by the right

Fig 2. Graph shows systolic and diastolic blood pressure (BP) during and after the stenting procedure. CT, Computedtomography; ICU, intensive care unit.

Fig 3. A, Axial computed tomography (CT) image at 50 minutes after stent deployment shows a small amount ofhemorrhage in the right frontal lobe near the cortex. B, Axial CT image at 3 hours after the previous examination showsextension of the hematoma to a maximum diameter of 61 mm. C, Axial CT image after craniotomy shows almost all ofthe hematoma was evacuated.

JOURNAL OF VASCULAR SURGERYVolume 59, Number 3 Takami et al 823

external carotid artery through the middle meningeal andophthalmic artery collaterals, cross-flow through theanterior communicating artery from the stenotic left ICA,and the right posterior communicating artery from theposterior circulation (Fig 1, C-E). Considering the poorvisualization of the vessels of the anterior circulation onmagnetic resonance angiography and the collateral flowthrough the external carotid artery observed on angiog-raphy, we speculate that right hemisphere perfusion wasinadequate despite the collateral flow through the anteriorand posterior communicating arteries. The absence ofsufficient perfusion would have critically impaired thecerebral autoregulation and vasodilatory reserve of theright hemisphere.

The hemorrhagic area was at the watershed betweenthe perfusion territories of the anterior and middle cerebralarteries. After revascularization of the left ICA, this areawith poor perfusion might have been the most vulnerableto an abrupt increase in blood flow.

Although contralateral intracerebral hemorrhage afterCAS is unpredictable, the patients at highest risk can be

identified and preventive measures adopted. The resultsof previous studies suggest that patients with preoperativehemodynamic impairment are at risk of developing hyper-perfusion.2,8,9 Preoperative single-photon emission CTwith acetazolamide loading shows the hemodynamicfeatures based on cerebral blood flow, blood volume, andvascular reserve capacity, making it possible to screenfor high-risk patients with severely impaired cerebral autor-egulation.10-12

Strict control of BP in the postoperative period canprevent cerebral hemorrhage after carotid revasculariza-tion, and currently, there are few other effective treat-ments.2,3,13,14 The SBP was lower in our patient afterstent placement than before because of the nicardipineinfusion, but control of SBP during and after the proceduremight not have been sufficient to protect the cerebrum,which had been severely underperfused. In patients athigh risk of postoperative hyperperfusion, rigorous BPcontrol during and immediately after the procedure is ofutmost importance to decrease the likelihood of thiscomplication.

JOURNAL OF VASCULAR SURGERY824 Takami et al March 2014

CONCLUSIONS

Hyperperfusion syndrome with intracerebral hemor-rhage after carotid revascularization is a rare but seriouscomplication. Severe ICA stenosis in the setting of contra-lateral ICA occlusion critically impairs cerebral blood flowand autoregulation. Most importantly, strict control ofBP should be instituted during and after revascularizationto minimize the effects of a sudden increase in bloodflow, which might exceed the compensatory capacity ofthe cerebral microcirculation.

REFERENCES

1. Bernstein M, Fleming JF, Deck JH. Cerebral hyperperfusion aftercarotid endarterectomy: a cause of cerebral hemorrhage. Neurosurgery1984;15:50-6.

2. Piepgras DG, Morgan MK, Sundt TM Jr, Yanagihara T, Mussman LM.Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg1988;68:532-6.

3. Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K,et al. Intracranial hemorrhage associated with cerebral hyperperfusionsyndrome following carotid endarterectomy and carotid artery stenting:retrospective review of 4494 patients. J Neurosurg 2007;107:1130-6.

4. Ouriel K, Shortell CK, Illig KA, Greenberg RK, Green RM. Intrace-rebral hemorrhage after carotid endarterectomy: incidence, contribu-tion to neurologic morbidity, and predictive factors. J Vasc Surg1999;29:82-7; discussion: 87-9.

5. Abou-Chebl A, Yadav JS, Reginelli JP, Bajzer C, Bhatt D, Krieger DW.Intracranial hemorrhage and hyperperfusion syndrome followingcarotid artery stenting: risk factors, prevention, and treatment. J AmColl Cardiol 2004;43:1596-601.

6. Kablak-Ziembicka A, Przewlocki T, Pieniazek P, Musialek P, Motyl R,Moczulski Z, et al. Assessment of flow changes in the circle of Willisafter stenting for severe internal carotid artery stenosis. J EndovascTher 2006;13:205-13.

7. Reinhard M, Muller T, Roth M, Guschlbauer B, Timmer J, Hetzel A.Bilateral severe carotid artery stenosis or occlusiondcerebral autor-egulation dynamics and collateral flow patterns. Acta Neurochir (Wien)2003;145:1053-9; discussion: 1059-60.

8. Schroeder T, Sillesen H, Sorensen O, Engell HC. Cerebral hyper-perfusion following carotid endarterectomy. J Neurosurg 1987;66:824-9.

9. Reigel MM, Hollier LH, Sundt TM Jr, Piepgras DG, Sharbrough FW,Cherry KJ. Cerebral hyperperfusion syndrome: a cause of neurologicdysfunction after carotid endarterectomy. J Vasc Surg 1987;5:628-34.

10. Kaku Y, Yoshimura S, Kokuzawa J. Factors predictive of cerebralhyperperfusion after carotid angioplasty and stent placement. AJNRAm J Neuroradiol 2004;25:1403-8.

11. Hosoda K, Kawaguchi T, Shibata Y, Kamei M, Kidoguchi K, Koyama J,et al. Cerebral vasoreactivity and internal carotid artery flow help toidentify patients at risk for hyperperfusion after carotid endarterectomy.Stroke 2001;32:1567-73.

12. Ogasawara K, Yukawa H, Kobayashi M, Mikami C, Konno H,Terasaki K, et al. Prediction and monitoring of cerebral hyperperfusionafter carotid endarterectomy by using single-photon emissioncomputerized tomography scanning. J Neurosurg 2003;99:504-10.

13. van Mook WN, Rennenberg RJ, Schurink GW, van Oostenbrugge RJ,Mess WH, Hofman PA, et al. Cerebral hyperperfusion syndrome.Lancet Neurol 2005;4:877-88.

14. Moulakakis KG, Mylonas SN, Sfyroeras GS, Andrikopoulos V.Hyperperfusion syndrome after carotid revascularization. J Vasc Surg2009;49:1060-8.

Submitted Sep 11, 2012; accepted Apr 20, 2013.