Journal http://jcn.sagepub.com/ of Child Neurology

Acute Ischemic Stroke in a 12-Year-Old Successfully Treated With Mechanical Thrombectomy Susana Sainz de la Maza, Alicia De Felipe, Maria Consuelo Matute, Eduardo Fandiño, José Carlos Méndez, Pablo Morillo and Jaime Masjuan J Child Neurol published online 21 November 2013 DOI: 10.1177/0883073813509889 The online version of this article can be found at: http://jcn.sagepub.com/content/early/2013/11/21/0883073813509889

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Brief Communication

Acute Ischemic Stroke in a 12-Year-Old Successfully Treated With Mechanical Thrombectomy

Journal of Child Neurology 201X, Vol XX(X) 1–5 ª The Author(s) 2013 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0883073813509889 jcn.sagepub.com

Susana Sainz de la Maza, MD1, Alicia De Felipe, MD1, Maria Consuelo Matute, MD1, Eduardo Fandin˜o, MD2, Jose´ Carlos Me´ndez, MD, PhD2, Pablo Morillo, MD3, and Jaime Masjuan, MD, PhD1

Abstract We report the case of a healthy 12-year-old girl with an acute ischemic stroke successfully treated with mechanical thrombectomy. The child was referred to our hospital 6 hours after sudden onset of severe headache and left hemiparesis. Cerebral angiography findings were consistent with right distal internal carotid artery occlusion in addition to ipsilateral middle cerebral artery occlusion. Subsequent mechanical thrombectomy with Solitaire AB device resulted in complete vessel recanalization. The patient experienced progressive neurologic improvement with good clinical recovery at the 3-month follow-up. To our knowledge, only 3 cases of primary mechanical thrombectomy in children have been previously reported in the literature. Safety and efficacy data for endovascular therapies in pediatric acute ischemic stroke are lacking. We propose mechanical thrombectomy as an option in children with significant neurologic deficits and proven arterial occlusion, especially when the therapeutic window for intravenous thrombolysis has been exceeded. Keywords pediatric stroke, endovascular treatment, transient cerebral arteriopathy Received August 07, 2013. Received revised August 19, 2013; September 21, 2013. Accepted for publication September 24, 2013.

Although pediatric stroke is uncommon, when it does arise, it is associated with significant morbidity and mortality. Stroke recurs in 25% of all cases and has a 3% to 6% mortality rate, whereas up to 70% survive with long-term neurologic deficits.1 Causes of ischemic stroke in children differ from those in adults; intracranial arteriopathies are the most common underlying condition in pediatric cases. The recently published etiologic classification of childhood arterial ischemic stroke describes unilateral focal cerebral arteriopathies as a separate entity.2 Included among these is transient cerebral arteriopathy—a unilateral arterial wall disease that affects the distal internal carotid and its proximal branches, leading to a predominantly lenticulostriate infarction in previously healthy children.3 There is a lack of evidence-based data concerning pediatric acute ischemic stroke treatment because of the routine exclusion of patients under 18 years old from clinical trials; therefore, recommendations in pediatric clinical practice guidelines4,5 are not as strong as those in adult clinical practice guidelines. An ongoing trial—Thrombolysis in Pediatric Stroke—will be the first to assess safety and feasibility of systemic and intraarterial thrombolytic therapy in pediatric population.6 However,

experience with endovascular mechanical treatment remains limited to sporadic case reports. Here, we report the case of a healthy girl with an acute ischemic stroke who was successfully treated with mechanical thrombectomy.

Case Summary A previously healthy right-handed 12-year-old girl was admitted to the emergency department of another hospital 1 hour after acute onset of severe headache while doing exercise. 1

Department of Neurology, Comprehensive Stroke Center, Hospital Universitario Ramo´n y Cajal, Madrid, Spain 2 Department of Neuroradiology, Hospital Universitario Ramo´n y Cajal, Madrid, Spain 3 Department of Pediatrics, Hospital Universitario Ramo´n y Cajal, Madrid, Spain Corresponding Author: Susana Sainz de la Maza, MD, Department of Neurology, Comprehensive Stroke Center, Hospital Universitario Ramo´n y Cajal, Ctra. de Colmenar Viejo Km. 9,100. 28034, Madrid, Spain. Email: [email protected]

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Journal of Child Neurology XX(X)

Figure 1. (A) Cranial computed tomography showing early signs of cerebral infarction: attenuation of the caudate nucleus, sulci effacement, and loss of gray-white matter differentiation. (B) Complete occlusion of the right internal carotid artery on cerebral angiogram. (C) Postprocedure angiogram demonstrating recanalization of the occluded artery. (D) Diffusion-weighted magnetic resonance imaging (MRI) illustrating restricted diffusion in the right middle cerebral artery territory. (E) Minimal petechiae within basal ganglia on T1-weighted MRI. (F) Magnetic resonance angiography showing irregular stenosis of right distal internal carotid artery and M1 segment of the ipsilateral middle cerebral artery.

There was no history of head injury or neck stretching. Initial assessment revealed mild left hemiparesis but the first cranial computed tomography (CT) was unremarkable. Over the next 4 hours, she suffered rapid deterioration with left hemiplegia, right oculocephalic deviation, and impaired consciousness. Her Pediatric National Institute of Health Stroke Scale score was 18. Moreover, she became agitated and aggressive, requiring sedation with propofol and orotracheal intubation. An acute ischemic stroke was suspected and she was subsequently referred to our Comprehensive Stroke Centre, which had a neurointerventional team available. Cranial CT with angiography and perfusion sequences was performed on arrival, 6 hours after onset. The cranial CT showed early signs of right middle cerebral artery infarction (Figure. 1A). CT angiography revealed a tapered luminal narrowing of the upper right internal carotid artery with a more distal occlusion of the supraclinoid segment and the ipsilateral middle cerebral artery. Perfusion CT revealed a mismatch area

greater than two-thirds of right middle cerebral artery vascular territory, suggesting a large area of penumbra. At the time of arrival at our hospital, the patient was beyond the time window for intravenous thrombolysis. Therefore, taking into account both the severity of her symptoms and the radiologic evidence of large vessel occlusion, mechanical thrombectomy was regarded as the best treatment option. Diagnostic angiography confirmed the presence of an occlusive thrombus in the right distal internal carotid artery (Figure 1B) with evidence of extensive leptomeningeal collateral circulation. A Solitaire AB device 4  20 mm (ev3 Inc, Plymouth, MN) was deployed through the Merci Balloon Guide Catheter 8F (Concentric Medical Inc, Mountain View, CA), maneuvered up to the carotid artery, and then placed just beyond the embolus. Capture and removal of the clot was successfully achieved after 2 attempts with the retriever device, 8 hours after symptom onset. Intra-arterial thrombolytics were not administered. Posttreatment angiogram demonstrated complete recanalization of

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Sainz de la Maza et al

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the right middle cerebral artery (Figure 1C) and occlusion of some M3 pre-Rolandic and Rolandic sulcal arteries, which were supplied by leptomeningeal collaterals irrigated by anterior and posterior cerebral arteries. The patient was transferred to the pediatric intensive care unit. She was extubated the next day, at which time the Pediatric National Institute of Health Stroke Scale score was 11. Brain magnetic resonance imaging (MRI) with diffusionweighted sequences showed acute cortical infarction of right middle cerebral artery territory with minimal petechiae within the basal ganglia (Figure 1D and E). Magnetic resonance angiography revealed irregular stenosis of the M1 and M2 segments of the middle cerebral artery, suggesting unilateral intracranial arteriopathy (Figure 1F). An extensive evaluation to determine stroke etiology was carried out. Transesophageal echocardiogram revealed no cardiac thrombus or tumor; laboratory findings including screening for hypercoagulable states and autoinmune disorders were normal, and investigations for an underlying infectious disease were all negative. During the following days, the patient progressively improved and, at discharge, neurologic examination revealed a Pediatric National Institute of Health Stroke Scale score of 2. At 3-month follow-up, the Pediatric National Institute of Health Stroke Scale score had fallen to 1 (mild facial palsy) and she is currently functionally independent—obtaining a modified Rankin Scale score of 1—and is attending school, where she is participating in normal activities, including sports. To evaluate the course of arteriopathy, a follow-up magnetic resonance angiography was performed 6 months after stroke, showing no changes in long segmental stenosis involving the distal right internal carotid and M1 and M2 segments of middle cerebral artery.

Discussion We present a case of pediatric acute ischemic stroke primary treated with mechanical thrombectomy, with successful recanalization of occlusion of the internal carotid and middle cerebral arteries, resulting in complete functional recovery despite a prolonged period of time from symptom onset to treatment. In children, the incidence of pediatric acute ischemic stroke is low and is difficult to differentiate from other causes of acute neurologic symptoms. These 2 factors often lead to a delay in diagnosis beyond the 4.5-hour window, which has proven to be safe and efficacious for intravenous recombinant tissue plasminogen activator in adults. Adult patients with significant neurologic deficits and dominant cerebral artery occlusion beyond this therapeutic window might benefit from endovascular techniques up to 8 hours after onset. However, to date there is no conclusive evidence showing that late mechanical treatment is better or safer. It is recommended that only children with both significant neurologic deficits (Pediatric National Institute of Health Stroke Scale score  10) and occlusion of a dominant cerebral artery should be considered for endovascular therapies.1 In our case, we made the decision to proceed with mechanical

thrombectomy based on the presence of hemiplegia and altered level of consciousness, with a Pediatric National Institute of Health Stroke Scale score of 18, as well as the angiographic confirmation of a large vessel occlusive thrombus. Ellis et al1 have recently summarized the reported use of endovascular therapies in pediatric acute ischemic stroke, including intra-arterial pharmacologic thrombolytics and mechanical approaches. They found a hemorrhage rate of 7/ 23 (30.4%) for cases treated with intra-arterial thrombolytic, whereas for those treated mechanically, the hemorrhage rate was 1/11 (9.1%) and it should be noted that, in this single case, intra-arterial tissue plasminogen activator had also been administered. As a result, they recommended caution when using intra-arterial tissue plasminogen activator and advocate the use of mechanical approaches alone whenever a neurointerventional team is available. Table 1 shows a summary of all reported cases of pediatric acute ischemic stroke treated with mechanical endovascular therapies, including clot retrieval/aspiration devices and balloon angioplasty.7-16 Twelve cases have been reported, including 8 males and 4 females, ranging from 5 to 16 years old (mean 11.25). Four patients presented with an anterior circulation artery occlusion and just 1 had occlusion of both the internal carotid and the middle cerebral arteries as was the case with our patient. In most cases, including ours, the reason to proceed with endovascular treatment was the prolonged period of time since the onset of symptoms, with a mean time of 17.6 hours; these data reflect the previously mentioned delay in pediatric acute ischemic stroke diagnosis. The functional outcome according to the modified Rankin Scale score was excellent in almost all patients, and only 1 case of moderate lifelong disability has been described. However, drawing conclusions from these outcomes requires caution, as there can be additional unpublished cases of pediatric acute ischemic stroke with unsuccessful recanalization, severe complications, and/or a poor clinical outcome. Regarding the etiology in our case, the first magnetic resonance angiography revealed unilateral arterial wall disease with distal internal carotid artery and proximal middle cerebral artery involvement that remained stabilized at follow-up magnetic resonance angiography, fulfilling diagnostic criteria for transient cerebral arteriopathy.17 A monophasic inflammatory mechanism underlying transient cerebral arteriopathy has been suggested, because up to 44% of the cases are preceded by varicella zoster virus infection, and clinical nonabrupt onset of symptoms as well as angiographic appearance of irregular stenosis are consistent with an inflammatory process. It is possible to distinguish transient cerebral arteriopathy from primary angiitis of the central nervous system, based on clinical and radiological features, as primary angiitis more frequently has a progressive course, often with bilateral and distal arterial lesions, and a clinical syndrome characterized by diffuse neurologic deficits.2 In some cases of transient cerebral arteriopathy, initial vascular imaging can show radiologic findings suggesting an intracranial arterial dissection.2 Indeed, both conditions are not mutually exclusive, and it is argued that

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Downloaded from jcn.sagepub.com at SYRACUSE UNIV LIBRARY on November 26, 2013

7

6

14

16

7 16

12

14 5

Tsivgoulis et al (2008)11

Felker et al (2010)12

Grunwald et al (2010)13

Grunwald et al (2010)13 Grunwald et al (2010)13

Lai et al (2010)14

Taneja et al (2011)15 Condie et al (2012)16 F M

F

M F

F

M

M

M M

M

M

Sex

BA BA, VA dissection

L paraclinoid ICA dissection L ICA, MCA

L ICA BA

BA

L MCA

R ICA

BA BA

BA

BA, L PCA

Clot localization

24 36

4

3 3.5

8

9

3.42

20 44

20

36

TTT (h)

3-  12-mm balloon expandable stent Solitaire 4-  20-mm stent t-PA Balloon disruption of the embolus on top of the BA At 7 days, 5 coils were placed in the left VA

Solstice balloon microcatheter Intra-arterial urokinase Intra-arterial t-PA Mechanical thrombus disruption using microguidewire manipulation Attracter-18 coil retriever Retriever-18 endovascular snare Sentry 3.5-  15-mm balloon IN-TIME retrieval system Intra-arterial urokinase Crossing thrombus with microsystem Semicompliant angioplasty balloon 1.5 mm  1.5 cm Intra-arterial reteplase Merci retriever 3-mm PowerSail balloon Intra-arterial t-PA Merci intra-arterial retrieval device Intra-arterial t-PA Penumbra system Penumbra system Intra-arterial t-PA. Phenox clot retriever Intra-arterial urokinase

Procedure

Complete Complete

Complete

Complete Incomplete

Complete

None

Incomplete

Incomplete Incomplete

Incomplete

Incomplete

Recanalization

0 1

0

0 0

0

3

1

0 0

0

0

Rankin Scale score

Abbreviations: BA, basilar artery; ICA, internal carotid artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; RS, Rankin Scale; SK, streptokinase; t-PA, tissue plasminogen activator; TTT, time to treatment.

16 6

15

8

Age (y)

Zaidat et al (2005)9 Grigoriadis et al (2007)10

Kirton et al (2003)8

Cognard et al (2000)

Reference

Table 1. Published Cases of Pediatric Acute Ischemic Stroke Treated with Mechanical Endovascular Therapies.

Sainz de la Maza et al

5

arterial wall disease could act as a predisposing factor for dissecting lesions. In our case, it would have been possible to interpret internal carotid artery narrowing seen on first CT angiography as being a typical feature of dissection, but subsequent vascular imaging procedures no longer supported this diagnosis. The presence of occlusive thrombus revealed by conventional angiogram, as occurred in our case, suggests a strong argument in favor of a potential role of thrombolytics in the treatment of transient cerebral arteriopathy. To our knowledge, our case is the fourth patient with pediatric acute ischemic stroke primary treated with mechanical thrombectomy described in the literature, and it agrees with the positive results that were previously reported. Although no formal conclusions can be drawn from such a small number of cases, mechanical thrombectomy seems to be a good therapeutic alternative in selected patients whenever an expert neurointerventional team is available.

Conclusion Our case, along with those reported in the literature, suggests that the use of primary endovascular treatment can be beneficial in children with dominant artery occlusion that is diagnosed outside the intravenous thrombolytic therapeutic window. Author Contributions SSdlM wrote the first draft of the manuscript and prepared the artwork and table. ADF revised the first draft of the manuscript and, along with EF and SSdlM, drafted the final version of the article. MCM, EF, JCM, and PM revised the final version of the article. SSdlM, ADF, MCM, PM, and JM took care of the patient. SSdlM and PM acquired and collected the data. EF and JCM performed the neurointerventional procedure and obtained the images. JM was the supervisor who made decisions, conceived and designed the study, and revised all versions of the manuscript.

Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The authors received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval The patient’s mother has given her consent to publish the case study in a journal.

References 1. Ellis MJ, Amlie-Lefond C, Orbach DB. Endovascular therapy in children with acute ischemic stroke: review and recommendations. Neurology. 2012;79(suppl 1):S158-S164. 2. Braun KPJ, Bulder MMM, Chabrier S, et al. The course and outcome of unilateral intracranial arteriopathy in 79 children with ischaemic stroke. Brain. 2008;132:544-557.

3. Bernard TJ, Manco-Johnson MJ, Lo W, et al. Towards a consensus-based classification of childhood arterial ischemic stroke. Stroke. 2012;43:371-377. 4. Roach ES, Golomb MR, Adams R, et al. Management of stroke in infants and children: a scientific statement from a special writing group of the American Heart Association Stroke Council and the Council on Cardiovascular Disease in the Young. Stroke. 2008; 39:2644-2691. 5. Monagle P, Chan AK, Goldenberg NA, et al. Antithrombotic therapy in neonates and children: Antithrombotic therapy and prevention of thrombosis, 9th ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2012; 141(2suppl):e737S-e801S. 6. Amlie-Lefond C, Chan AK, Kirton A, et al. Thrombolysis in acute childhood stroke: design and challenges of the thrombolysis in pediatric stroke clinical trial. Neuroepidemiology. 2009;32: 279-286. 7. Cognard C, Weill A, Lindgren S, Piotin M, Castaings L, Moret J. Basilar artery occlusion in a child: ‘‘clot angioplasty’’ followed by thrombolysis. Childs Nerv Syst. 2000;16:496-500. 8. Kirton A, Wong JH, Mah J, et al. Successful endovascular therapy for acute basilar thrombosis in an adolescent. Pediatrics. 2003; 112:e248-e251. 9. Zaidat OO, Tolbert M, Smith TP, Alexander MJ. Primary endovascular therapy with clot retrieval and balloon angioplasty for acute basilar artery occlusion. Pediatr Neurosurg. 2005;41: 323-327. 10. Grigoriadis S, Gomori JM, Grigoriadis N, Cohen JE. Clinically successful late recanalization of basilar artery occlusion in childhood: what are the odds? Case report and review of the literature. J Neurol Sci. 2007;260:256-260. 11. Tsivgoulis G, Horton JA, Ness JM, et al. Intravenous thrombolysis followed by intra-arterial thrombolysis and mechanical thrombectomy for the treatment of pediatric ischemic stroke. J Neurol Sci. 2008;275:151-153. 12. Felker MV, Zimmer JA, Golomb MR. Failure of a clot retrieval device in an adolescent stroke patient. Pediatr Neurol. 2010;43: 435-438. 13. Grunwald IQ, Walter S, Shamdeen MG, et al. New mechanical recanalization devices: the future in pediatric stroke treatment? J Invasive Cardiol. 2010;22:63-66. 14. Lai YJ, Chang FC, Lin CJ, Hsieh TC, Wang KL. Endovascular therapy in pediatric intracranial carotid artery dissection. Pediatr Neurol. 2010;42:291-294. 15. Taneja SR, Hanna I, Hodgate A, Wenderoth J, Cordato DJ. Basilar artery occlusion in a 14-year old female successfully treated with acute intravascular intervention: case report and review of the literature. J Pediatr Child Health. 2011;47:408-414. 16. Condie J, Shaibani A, Wainwright MS. Successful treatment of recurrent basilar artery occlusion with intraarterial thrombolysis and vertebral artery coiling in a child. Neurocrit Care. 2012;16: 158-162. 17. Se´bire G, Fullerton H, Riou E, deVeber G. Toward the definition of cerebral arteriopathies of childhood. Curr Opin Pediatr. 2004; 16:617-622

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