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  • Case report
  • Open Access

Protective effect of unilateral vasospasm in the setting of HHH-associated posterior reversible encephalopathy syndrome: case report, review of the literature, and treatment considerations

  • 1Email author,
  • 2,
  • 1, 3,
  • 1, 3,
  • 4 and
  • 1, 3
Chinese Neurosurgical Journal20184:34

https://doi.org/10.1186/s41016-018-0141-8

  • Received: 30 July 2018
  • Accepted: 1 October 2018
  • Published:

Abstract

Background

Hyperdynamic therapy, also called triple-H therapy, is the standard treatment and prophylaxis for aneurysmal-associated vasospasm. In patients who are able to tolerate cardiopulmonary stressors induced by this therapy, it is of benefit as a modality for prevention and treatment of delayed ischemic neurologic deficit. However, it can be a cause of significant cardiopulmonary or neurologic sequelae. In rare cases, it can be associated with posterior reversible encephalopathy syndrome (PRES), secondary to prolonged vasopressor and hypertensive therapies.

Case presentation

We present the case of a patient with right-sided aneurysmal-associated vasospasm who, after 10 days of triple-H therapy, experienced a seizure and was found to have left-sided PRES. Right-sided vasospasm served as a protective mechanism from triple-H therapy-associated PRES. It presented a treatment conundrum due to contradictory perfusion requirements. Hypertensive therapy was curtailed and in efforts to preserve local cerebral perfusion and vasodilation, local therapy with intrathecal nicardipine was initiated. We present our case, a review of the literature, and management considerations.

Conclusions

Therapies that have conventionally functioned as second line treatments for aneurysmal subarachnoid hemorrhage (intra-arterial vasodilators and intrathecal vasodilators) may be beneficial as earlier treatments in the setting of vasospasm given the systemic difficulties and complications associated with HHH therapy in patients with PRES.

Keywords

  • Subarachnoid hemorrhage
  • Hyperdynamic therapy
  • Posterior reversible encephalopathy syndrome

Background

Hyperdynamic therapy is a conventional treatment for aneurysmal subarachnoid hemorrhage-associated cerebral vasospasm. Hypertension, hypervolemia, and hemodilution are used to ensure adequate cerebral perfusion in patients with severely constricted cerebral vasculature and abnormal autoregulation. Implementation of hyperdynamic therapy however does come with risks. Pulmonary edema, myocardial ischemia, hyponatremia, indwelling venous catheter-related complications, cerebral hemorrhage, and cerebral edema are all known sequelae [1]. A less commonly associated complication of triple-H therapy includes the development of posterior reversible encephalopathy syndrome (PRES). PRES can lead to disturbance of autoregulation, development of brain edema due to endothelial damage, and cerebral ischemia [2]. The development of PRES can be clinically confounding as presenting symptoms may be identical to delayed ischemic neurologic deficit (DIND). Management presents a significant conundrum, as treatments of these two pathologies are directly conflicting. We present a case of a patient who had complications both of clinical and angiographic right-sided vasospasm and triple-H induced PRES. On imaging, FLAIR changes were localized solely to her contralateral parieto-occipital hemisphere suggesting that her vasospasm was functioning as a protective mechanism against ipsilateral PRES. These two coinciding diagnoses created a treatment dilemma. In this article, we present our case, a review of the literature of triple-H-associated PRES and attempt to summarize the management of patients with both vasospasm and PRES from the literature and our experience.

Case presentation

A 33-year-old previously healthy woman presented after a sudden loss of consciousness and reported seizure. Upon arrival to the hospital, she complained of a moderate headache with severe neck pain with a Hunt Hess Score of 2. CT imaging demonstrated subarachnoid hemorrhage (Fig. 1a) from a right posterior communicating artery aneurysm. Importantly, no vasospasm was seen in the CTA from admission (Fig. 1b). She had an external ventricular drain (EVD) placed and underwent a craniotomy for clipping on post-bleed day 1. Post operatively, she was intact and monitored in the neurointensive care unit. Post-operative angiogram showed no evidence of flow-occluding spasm (Fig. 2a, b).
Fig. 1
Fig. 1

a Non-contrast CT head demonstrating the patient’s initial presenting scan with primarily right-sided subarachnoid hemorrhage. b CTA reconstructed images demonstrating normal bilateral vessel caliber

Fig. 2
Fig. 2

a Postoperative angiogram demonstrating clip occlusion. L ICA injection demonstrated no evidence of spasm. b R MCA and ACA concerning for mild non-flow-limiting spasm. c Repeat angiogram after neurologic deterioration demonstrates progressive narrowing of right MCA and ACA vasculature

Her hospital course was complicated by severe vasospasm of the right anterior and middle cerebral artery. On post-bleed day 5, she began to experience visual auras and complain of blurry vision. Transcranial Doppler velocities were notably increased. She underwent endovascular intervention and administration of intra-arterial (IA) verapamil resulting in improved neurologic function. Triple-H therapy was initiated and her symptoms improved despite persistently elevated right transcranial doppler (TCD) velocities. On post bleed day 15, after 10 days of blood pressure augmentation to goal systolic blood pressures of 180 mmHg, she had an acute change in neurologic exam with a mixed aphasia and disorientation. Blood pressure was increased to a goal of 200 mmHg with no significant improvement. That same day, she experienced a complex partial seizure that progressed to a generalized tonic-clonic seizure. A repeat CTA demonstrated persistent right MCA spasm. An angiogram was performed (Fig. 2c), which showed vasospasm of the right ICA, MCA, and ACA, which was treated with IA verapamil. EEG did not demonstrate any subclinical seizure activity.

When her aphasia failed to resolve, an MRI of her brain was performed which showed left parieto-occipital vasogenic edema suggestive of PRES (Fig. 3). Hemodilution and hypervolemic therapy were discontinued. Her blood pressure parameters were relaxed to systolic blood pressure goals of 140–160 mmHg. Given the right-sided vasospasm and the left-sided PRES, the decision was made to administer intrathecal nicardipine through her EVD. She received 2 mg of nicardipine every 8 h for five doses. Her aphasia and confusion began to improve over the next few days. Vasopressors were discontinued and blood pressure goals relaxed. She was transferred out to the floor on day 26 and discharged to an acute rehab on day 28 with no focal neurological deficits. She followed up in the outpatient clinic after 2 months and was neurologically intact with intermittent headaches. She had no further seizures. A year after discharge, she remained neurologically intact and a CTA demonstrated complete resolution of her PRES-associated cerebral edema as well as no recurrence of her aneurysm or vasospasm (Fig. 4).
Fig. 3
Fig. 3

a Axial FLAIR demonstrating significant amount of predominantly left-sided parieto-occipital vasogenic edema. b Axial FLAIR demonstrating significant amount of predominantly left-sided parieto-occipital vasogenic edema. c T2 axial MRI demonstrating significant amount of predominantly left-sided parieto-occipital vasogenic edema. d T2 axial MRI demonstrating significant amount of predominantly left-sided parieto-occipital vasogenic edema

Fig. 4
Fig. 4

CTA reconstructions at 6 months post-hemorrhage demonstrating persistently occluded aneurysm and resolution of vasospasm

Discussion

Hyperdynamic therapy is often utilized in prophylaxis and treatment of cerebral vasospasm after aneurysmal subarachnoid hemorrhage (aSAH) to prevent DIND. PRES is an uncommon but clinically significant syndrome that has been described in numerous case reports. The current hypothesis for a mechanism of PRES involves capillary leak in the setting of damaged endothelium. At high pressures, the intrinsic cerebral autoregulatory system fails and vessels are forcibly dilated leading to arteriolar distention and rupture of vascular endothelial cell connections. Extravasation of plasma proteins induces a vasogenic edema [35]. Etiologies include hypertension, pre-eclampsia, toxic drugs, immunosuppression, lupus, and renal failure. Symptoms vary widely, but most are often reversible with a reduction in blood pressure [6]. PRES typically localizes to the parieto-occipital region, an area believed to be less capable of autoregulation secondary to less sympathetic innervation [7]. Symptoms localize to the area affected and include altered mental status, seizures, visual changes, weakness, and if in the dominant hemisphere, aphasia.

Management of PRES and cerebral vasospasm together presents a treatment challenge. The treatment for each is in direct conflict with the pathophysiology of each other. We presented a patient with unilateral vasospasm of the right ACA and MCA, with complications of vasogenic edema arising in the contralateral hemisphere. While most reports of PRES demonstrate bilateral posterior occipito-parietal hemispheric involvement, a few case reports offer similar reports of unilateral vasospasm and contralateral vasogenic edema [2, 8]. As Dhar et al. proposed, this presentation is likely the result of persistent vasospasm on one side lowering perfusion pressure effectively presenting the development of PRES on the ipsilateral site. The unaffected hemisphere however, remains vulnerable to PRES-induced edema [8].

A literature review was performed of hyperdynamic therapy-associated PRES in patients with aSAH. The relative paucity of literature is likely secondary to the lack of standard MRI imaging performed in aneurysm patients. Awori et al. attempted to extrapolate common risk factors for patients with aSAH and triple-H-associated PRES. However, upon an extensive literature review, the cases are too few in number to establish significant risk factors [9]. As demonstrated in Table 1, PRES seems to occur more frequently in females and on average, occurs about 8 days after initiation of hyperdynamic therapy.
Table 1

Reports of PRES with aSAH-associated vasospasm

Author

Age, gender

Aneurysm location

Vasospasm location

Edema distribution

Treatment

Vasospasm treatment

Baseline BP (MAP)

Target BP (mmHg)

PRES (days after SAH)

PRES (days after HT)

Hx of HTN

mRS

Symptoms during PRES/CVS

Amin 1999 [10]

52, F

L MCA

Not described.

Bilateral occipital

Clipping

Hyperdynamic

Dobutamine

150/70 (97)

SBP 200

13

7

N

1

Lethargy

66, M

X

 

Bilateral occipital

 

Hyperdynamic

Dobutamine

NA

SBP 200

12

10

Y

6

Lethargy aphasia Seizure R hemiparesis

Sanelli 2005 [11]

49, F

AComm

Bilateral ACA

Bilateral occipital R occipital ICH

Clipping

HHH

NA

SBP 140–200

17

13

NA

1

Lethargy

Wartenberg 2006 [12]

73, F

L ICA

L ACA and MCA

Bilateral occipital parietal

Clipping

HHH

145–175

SBP 140–200

10

7

Y

4

Coma with decorticate posturing

Jang 2010 [13]

65, F

PComm

Not described.

Bilateral temporal occipital

Coiling

HHH

130/80 (97)

SBP 165

7

1

N

1

Confusion, headache, and vision loss

Giraldo 2011 [14]

62, F

AComm

Circle of Willis and Bilateral ACA

Bilateral parietal occipital

Coiling

Hypertension

138/70 (93)

MAP 115

12

6

N

1

Confusion, headache, retro-orbital pain

70, F

AComm

NA

Bilateral temporal occipital

Coiling

Hypertension

Hypervolemia

149/58 (88)

MAP 120

12

11

Y

1

Lethargy seizure

62, M

AComm

NA

Bilateral temporal occipital cerebellar

Clipping

Hypertension

Hypervolemia

SBP 200

SBP 180

14

13

Y

4

Lethargy

Dhar 2011 [8]

47, F

R PComm

R MCA, bilateral ACA

L posterior temporal parietal

Clipping

Hypertension

MAP 65–75

MAP 120

13

7

N

1

Lethargy, confusion, L facial droop, aphasia, and HP

Voetsch 2011 [2]

35, F

R MCA

R MCA

Bilateral PCA

L MCA

Clipping

Hypertension

 

MAP 110

7

4

NA

3

Headadche, seizure, and declined arousal

Awori 2016 [9]

63, M

AComm

Basilar, MCA, PCA, ACA

Bilateral temporal occipital

Clipping

Hypertension

140/109

MAP 110

    

Mental status change, seizure

Current Study

33, F

R PComm

R ACA and MCA

L parietal occipital

Clipping

HHH

 

SBP 180–200

 

10

 

0

Wernicke’s aphasia, seizure

Total

10, F; 3, M

Avg age 57

        

Avg: 8 days

 

Avg mRS: 2.2

 

MAP mean arterial pressure; Hx OF HTN history of hypertension (Y= Yes, N = No, NA = Not reported); mRS modified rankin score

Dhar et al. present a very nearly identical case of a patient with right sided vasospasm receiving triple-H therapy [8]. Workup for new confusion and aphasia included negative EEG and angiograms. MRI demonstrated significant left parieto-occipital FLAIR changes. Mean arterial pressure (MAP) goals were decreased from 110 mmHG to 70 mmHg with rapid resolution of her aphasia, hemiparesis, and orientation. She was discharged without neurologic deficits. Dhar et al. argue that, in such situations should concerns for DIND exist, more aggressive but focal therapies such as balloon angioplasty or intra-arterial vasodilators may be safer in this particular subset of patients [8]. The authors are in agreement with this theory and suggest that should clinical presentation of both PRES and DIND be a concern, angiographic intervention may be safer for the patient.

Voetsch et al. present a similar case of a patient with right MCA spasm and DIND requiring hyperdynamic therapy and intra-arterial nicardipine [2]. Augmentation of blood pressure led to increasing headaches, lethargy, and ultimately two generalized seizures. MRI demonstrated bilateral occipital and left parietal FLAIR changes. Hyperdynamic therapy was discontinued. The right MCA territory ischemia did increase in size over the course of her hospitalization, and the patient was discharged with a moderate left hemiparesis.

A review of the literature was performed to synthesize a possible treatment paradigm [2, 8, 1014]. All authors initiated a relaxation of pressure parameters in their hyperdynamic therapy. Some reported immediate discontinuation of vasopressors while others performed a down-titration of vasopressors over several days. Most authors reported no occurrence of DIND upon a patient’s discharge. Voetsch et al. did report an increase in the size of one patient’s stroke territory after HHH therapy was discontinued [2].

Dhar et al. address the important concept that perhaps more focal treatments in the setting of PRES and significant vasospasm may be more beneficial than the conventional systemic treatments of HHH therapy [8]. Our patient underwent focal intra-arterial verapamil treatments and also received 48 h of intrathecal nicardipine in attempts to address both her vasospasm and her PRES. Though research remains to be performed, perhaps therapies that have conventionally functioned as second line treatments (intra-arterial vasodilators and intrathecal vasodilators) may be beneficial as earlier treatments in the setting of vasospasm given the systemic difficulties and complications associated with HHH therapy.

A review of the English literature found eight studies that reported on the use of intraventricular or cisternal administration of nicardipine for the treatment of aneurysmal SAH-associated vasospasm (Table 2). Few of these studies were sufficient in number and outcomes data to know when in the treatment algorithm, intra-thecal nicardipine should be implemented. These studies show however that the use of nicardipine is not associated with significant complications. Rates of ventricular-associated infections or meningitis varied and were not consistently reported. There is some evidence that TCD velocities are improved and maintain this improvement after administration [15, 16]. In patients where traditional HHH therapy may be contraindicated including patients with PRES, this treatment modality can function as a useful resource. Anecdotally, some patients experience nausea and emesis associated with administration. Others are also unable to tolerate prolonged EVD clamp times after administration of the drug.
Table 2

Summary of studies that have utilized intraventricular or cisternal nicardipine for the treatment of aSAH-associated vasospasm

Author

Study type

Vasopasm diagnosis

IVTN treatment

Patients (control)

Aneurysm

HH grade

Fisher grade

Aneurysm treatment

Results

Patient outcomes

Complications

Acute treatment for vasopasm

 Ko 2016 [16]

Retrospective case series

Study of hemodynamic changes during intraventricular nicardipine treatment (IVTN) in refractory vasospasm

Multimodality monitoring, brain oxygen tension, CBF, brain metabolism

4 mg, q8 nicardipine solution

Clamp EVD for 1 h

Mean 4.9 doses/patient

11 (0) Age mean: 49 8 female

3 male

NA

IV: 5

V: 6

3: 7 pt.

4: 4 pt

NA

*Mean ICP increased slightly (2.5 ± 0.9 mmHg), peaking at 20 m

*ICP decreased 20–30 m after injection (3.7 ± 1.8 mmHg)

*MAP, PBO2, CBF, autoregulation indices did not change significantly

3 month follow up

mRS 5: 8 patients

mRS 6: 3 patients

Pneumonia (2)

Seizures (2)

Sepsis (2)

Globala cerebral edema (11)

Hydrocephalus (8)

MI (2)

 Lu 2012 [15]

Retrospective case-control

Monitored IVTN effects with TCD

TCDs

4 mg

Median 7 doses/patient (range 1–17)

14 (14)** Age mean: 45 12 female 2 male

ACOM: 3

PICA: 2

PCOM: 2

MCA: 2

Pericallosal: 1

Vertebral: 1

VB: 1

ICA: 1

ACA: 1

NA

3: 3 pt.

4: 11 pt

Coil: 8

Clip: 5

Stent: 1

*Mean flow velocity decreased after IVTN (R MCA: 120.2—> 82.0 cm/s, L MCA: 101.6—> 72.8 cm/s)

*No significant difference in clinical outcomes

No significant difference between control and treatment group at 30 and 90 days

No bleeding or infection incidents.

 Webb 2010 [24]

Retrospective case series

TCD measurement of changes post-IVTN

TCDs

4 mg q8–12

Clamp EVD for 30 m

Mean 6.7 doses/patient

64 (0) Age mean: 52

NA

I, II: 13

III: 30

IV, V: 21

2: 6 pt.

3: 45 pt.

4: 13 pt

Coil: 35

Clip: 29

*IVTN reduced mean flow velocity by 26.3 cm/s in MCA and 7.4 cm/s in ACA, maintained over 24 h with continued administration

*No change in ICP

Not described.

Ventricular-related infection: 4 clinically proven, 7 clinically possible

 Ehtisham 2009 [23]

Retrospective case series

Vasospasm refractory to standard medical and endovascular treatment.

TCDs

4 mg q12; stopped once MCA velocity < 120 cm/s

Clamp EVD for 30 m

6 (0) Age mean: 45 5 female

1 male

PCA: 2

ACA: 1

PICA: 1

VB: 1

Pericallosal: 1

II: 1

III: 2

IV: 2

V: 1

3: 2 pt.

4: 4 pt

Coil: 3

Clip: 3

*IVTN reduced MCA flow velocity by 43.1 ± 31.0 cm/s

Not described.

No major infection or reverse reaction.

 Goodson 2008 [25]

Retrospective case series

IVTN used in refractory vasospasm

Symptomatic

4 mg q12

Clamp EVD for 1 h

Length of treatment 9.5 days (5–17)

8 (0) Age mean: 51 7 female

1 male

ACA: 3

ACOM: 3

MCA: 1

PICA: 1

I: 4

II: 2

III: 2

4: 8 pt

Coil: 5

Clip: 3

*IVTN well-tolerated with minimal side effects

*7 moderate to good outcomes

*1 patient died in ICU

*Median modified rankin score: 2 (2–6)

1 had nausea and headache

PROPHYLACTIC TREAMENT FOR VASOSPASM

 Barth 2009 [26]

Prospective trial

Intraventricular nicardipine prolonged release implants (NPRI)

Angiogram or CT angiogram

6 or 10 pellets, 4 mg/pellet

31 (16)** Age mean: 52 20 female

11 male

ACA: 15

PCOM: 5

MCA: 4

VB: 2

PICA: 2

Pericallosal: 2 ICA: 1

I: 6

II: 11

III: 7

IV: 7

NA

Clip: 17

Coil: 14

*NRPI had larger mean diameter on DSA (90 ± 24% vs 80 ± 30% control)

*NPRI group had less moderate/severe vasospasm (41% vs 73% control)

*Effect not seen in coil group

*No difference in dose

Not described.

No different from control group

 Suzuki 2001 [22]

Prospective trial

Post operative intrathecal nicardipine

Symptomatic

angiogram

4 mg, q12 on post-op days 3–14 (via cisternal drain)

177 (0)

Age mean: 59

121 female

56 male

ICA: 66

ACOM: 58

MCA: 43

ACA: 6

VB: 4

I: 11

II: 112

III: 35

IV: 16

V: 2

NA

Clipped: 177

*20 (11.3%) with angiographic vasospasm

*10 (5.7%) with symptomatic vasospasm

*Low rates compared to literature (aVS 19–97%, sVS 5–90%)

mRS 2–3: 89.2% at 6 months

11 (6.2%) meningitis

 Shibuya 1994 [21]

Prospective trial

Post operative intrathecal nicardipine

Symptomatic

angiogram

2 mg, q8 for 10–14 days (via cisternal drain)

50 (91)**

Age mean: 54

ACA: 23

ICA: 13

MCA: 14

VB: 0

I: 0

II: 15

III: 25

IV: 10

NA

Clipped: 50

*Symptomatic vasospasm decreased by 26%

*Angiographic vasospasm decreased by 20%

*Neither are statistically significant

*Increased ‘good clinical outcome’ at 1 month post-bleed by 15%

Not described.

2 (4%) meningitis

4 (8%) hydrocephalus requiring shunts

**Historical controls; VS vasospasm; IVTN intraventricular nicardipine, PBO2 brain oxygen tension, CBF cerebral blood flow, HH Hunt Hess, TCDS transcranial dopplers study, M male, F female

Currently other agents including intravenous endothelin-1 receptor antagonists and intrathecal nimodipine, and milrinone are being studied as agents for the treatment of vasospasm. Endothelin receptor antagonists demonstrated potential in animal studies with reduction rates of vasospasm and increase in average vessel diameter; however, an updated meta-analysis has found that it does not demonstrate overall improved outcomes [17]. Levosimendan is a calcium channel sensitizer that has recently been shown to antagonize prostaglandin-induced vasoconstriction and upregulate the nitric oxide-cyclic guanosine monophosphate pathway thereby inducing increased vasorelaxation. Animal models have yet to be studied [18]. Intrathecal milrinone demonstrated a successful safety and feasibility study in a study of 170 patient receiving lumbar subarachnoid milrinone injections, but further trials are required to validate this protocol [19, 20]. Intrathecal nimodipine, nicardipine, and milrinone are not yet standards of care and have not yet been proven to improve overall outcomes in conventional research. However, these therapies have demonstrated utility in specific cases of patients where the use of conventional therapeutics, including HHH therapies, lead to unwelcome complications. Intrathecal administration of nicardipine demonstrates very little systemic effects [2123].

Conclusion

This case report and literature review suggest that the management paradigm of aSAH in the context of PRES should shift towards more focal modalities including intra-arterial vasodilators and intrathecal agents before reliance on HHH therapies due to the possibility of cardiopulmonary and neurologic complications. Early diagnosis of PRES in neurosurgical patients is essential for therapy modification to ensure better outcomes.

Abbreviations

ACA: 

Anterior cerebral artery

DIND: 

Delayed ischemic neurologic deficit

EVD: 

External ventricular drain

HHH: 

Hypertension, hypervolemia, and hemodilution

IA: 

Intra-arterial

ICA: 

Internal carotid artery

MAP: 

Mean arterial pressure

MCA: 

Middle cerebral artery

PRES: 

Posterior reversible encephalopathy syndrome

aSAH: 

Aneurysmal subarachnoid hemorrhage

TCD: 

Trans-cranial doppler

Declarations

Acknowledgements

Not applicable.

Funding

No funding was obtained for this work.

Availability of data and materials

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

Authors’ contributions

AR, JW, CHW, and JX have been involved in drafting the manuscript and revising it critically for important intellectual content. BM and YH have been involved in the conception of the report as well as revising manuscript critically for intellectual content. All authors have given final approval of the version to be published. All authors have agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Ethics approval and consent to participate

Approved by University Hospitals Cleveland Medical Center IRB department as non-human subjects research, as appropriate for case reports.

Consent for publication

Verbal and written consent for publication was obtained from patient.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
School of Medicine, Case Western Reserve University, 2109 Adelbert Road, Cleveland, OH 44106, USA
(2)
Department of Neurological Surgery, University of California Irvine SOM, 1001 Health Sciences Rd, Irvine, CA 92617, USA
(3)
Department of Neurological Surgery, University Hospitals Cleveland Medical Center, 11100 Euclid Avenue, Cleveland, OH 44106, USA
(4)
Department of Neurology, University of Minnesota, 420 Delaware St SE, Minneapolis, MN 55455, USA

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