Accepted Manuscript

Pediatric Stroke Clinical Pathway Improves the Time to Diagnosis in an Emergency

Department

Amy M. DeLaroche, MBBS, Lalitha Sivaswamy, MD, Ahmad Farooqi, MPhil,

Nirupama Kannikeswaran, MD

PII: S0887-8994(16)30399-X
DOI: 10.1016/[Link].2016.09.005
Reference: PNU 8989

To appear in: Pediatric Neurology

Received Date: 4 June 2016

Accepted Date: 6 September 2016

Please cite this article as: DeLaroche AM, Sivaswamy L, Farooqi A, Kannikeswaran N, Pediatric Stroke
Clinical Pathway Improves the Time to Diagnosis in an Emergency Department, Pediatric Neurology
(2016), doi: 10.1016/[Link].2016.09.005.

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to
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 ACCEPTED MANUSCRIPT
Pediatric Stroke Clinical Pathway

Pediatric Stroke Clinical Pathway Improves the Time to Diagnosis in an Emergency

Department

Amy M. DeLaroche, MBBS1, Lalitha Sivaswamy MD1, Ahmad Farooqi MPhil2, Nirupama
Kannikeswaran, MD1

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Affiliations: 1Department of Pediatrics, Division of Emergency Medicine, Children’s Hospital of
Michigan, 3901 Beaubien St, Detroit, Michigan, 48201; 2School of Medicine, Wayne State
University, 540 E Canfield St, Detroit, Michigan, 48201

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Email Addresses: AD – adelaroc@[Link]
LS – lsivaswa@[Link]

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AF – afarooqi@[Link]
NK – nkannike@[Link]

Address correspondence to: Amy DeLaroche, Department of Pediatrics, Division of

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Emergency Medicine, Children’s Hospital of Michigan, 3901 Beaubien Street, Detroit,
Michigan, 48201, 313-745-5260 (phone), 313-993-7166 (fax), adelaroc@[Link]
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Word Count: 3178

Funding Source: No funding was secured for this study.

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Financial Disclosure: The authors have no financial relationships relevant to this article
to disclose.
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Conflicts of interest: The authors have no conflicts of interest to disclose.

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Pediatric Stroke Clinical Pathway

Abstract

Background: Identified barriers to the diagnosis of pediatric stroke include delays in provider
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recognition and definitive neuroimaging [magnetic resonance imaging (MRI)]. Clinical pathways

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are recommended to address these barriers; yet, few studies have evaluated their impact. Aim:

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Describe the impact of a pediatric stroke clinical pathway (PSCP) on the diagnosis of stroke in

patients presenting with focal neurologic dysfunction to a pediatric emergency department.

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Methods: The PSCP was implemented in our level 1 pediatric emergency department in June

2014 for children aged 1 month to 18 years. Demographic and clinical data were collected for

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patients ultimately diagnosed with stroke using the PSCP, and compared to data collected on
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patients diagnosed with stroke prior to implementation of the PSCP. Results: The PSCP was

activated for 36 patients. Stroke was diagnosed in 11 (33%) patients, of whom 55% were male
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with a median age of 11 ± 7 years. Focal deficits (82%) and headache (55%) were common
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presenting complaints. There was a significant improvement in the median time to MRI from
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arrival to the emergency department [pre-PSCP: 17 hours (IQR 6, 22) versus post-PSCP: 4 hours

(IQR 3, 12); p = 0.02]. Conclusions: The PSCP improved time to definitive diagnosis and
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streamlined the care provided to children presenting to the pediatric emergency department with

focal neurologic dysfunction.

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Keywords: Pediatric Stroke; Clinical Pathway; Diagnosis: Magnetic Resonance Imaging

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Pediatric Stroke Clinical Pathway

Introduction

Stroke is an acute neurological insult that has traditionally been conceptualized as an adult

disease. Although comparatively rare in the pediatric population, with an incidence of 2 to 13 per
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100,000 children,1 stroke is at least as common as brain tumors in children.2 With up to three-

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quarters of patients being discharged from the acute care setting with neurological deficits,

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pediatric stroke results in significant morbidity.3 Consequently, pediatric stroke leads to

substantial health care expenses given the cumulative cost of care over a child's lifespan.4,5 Early

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intervention is advocated as a means of minimizing the physical and economic burden of this

disease,6 but timely diagnosis is hampered by the non-specific clinical presentation of pediatric

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stroke, and delays in both health care provider recognition of stroke and acquisition of timely
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definitive neuroimaging with magnetic resonance imaging (MRI).7-11
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To address these challenges, institutional protocols with development of a “stroke team” have
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been recommended as part of a multipronged approach toward improving the diagnosis of

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pediatric stroke.6,12 The “pediatric stroke alert” has recently been described, and this standardized

approach to providing evidence based care has the potential to improve an institution's
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capabilities to evaluate and manage acute pediatric stroke.12 However, few studies characterize

the success and limitations of a pediatric stroke protocol,13 and the impact of standardized care
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pathways on the diagnosis of pediatric stroke is not well known. Thus, the aim of this study is to
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describe our institution's experience in implementing a pediatric stroke clinical pathway (PSCP)

and to evaluate the impact of this PSCP on the diagnosis of stroke in a pediatric emergency

department.
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Pediatric Stroke Clinical Pathway

Methods

This study was conducted at a freestanding children’s hospital in Detroit, Michigan with over

90,000 emergency department visits and 10,000 hospital admissions annually. Pediatric
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neurologists are available 24 hours a day, 7 days per week for consultation. Two cohorts of

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children were included in this study: (1) patients who were diagnosed with stroke prior to

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implementation of the PSCP (pre-PSCP) and (2) patients diagnosed with stroke and managed

following implementation of the PSCP (post-PSCP).

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Patients in the pre-PSCP group were identified through a query of the electronic medical record

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using ICD – 9 codes (434.91, 434.11, 434.01). Children aged 1 month to 18 years evaluated in
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the pediatric emergency department with neurological deficits and admitted to our institution

between 2009 and 2013 with a final discharge diagnosis of ischemic stroke (arterial or venous)
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were included. Patients in the post-PSCP group were those who presented to the pediatric
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emergency department with neurological deficits for whom the PSCP was activated and the final
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diagnosis was ischemic (arterial or venous) or hemorrhagic stroke with radiologic confirmation

(MRI). Hemorrhagic stroke included venous sinus thrombosis, hemorrhagic transformation of an

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arterial stroke and primary non-traumatic intracerebral lobar hemorrhage. There were no patients

with spontaneous subarachnoid hemorrhage. Patients were identified through retrospective

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review of the PSCP pager log. The pager log is accessed monthly by the institution’s
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communications specialist and emailed to the principal investigator.

The PSCP resulted from a multidisciplinary collaboration between hospital administration and

the departments of anesthesia, critical care, emergency medicine, hematology, neurology,

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Pediatric Stroke Clinical Pathway

pharmacy, and radiology. Following literature review, discussion with other institutions with

established protocols, and input from participating departments, the PSCP was implemented in

June 2014 following hospital wide lectures and small group sessions directed at nurses and
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physicians at all levels of training. Implementation was evaluated by a core team of physicians

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with real-time data used for further education and reinforcement as needed.

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The PSCP can be activated for patients aged 1 month to 18 years presenting to the pediatric

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emergency department with a positive “stroke screen” within 72 hours of symptom onset. A

positive stroke screen for the protocol was defined as one or more of the following: (1) sudden

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onset of a focal neurological deficit, which may be motor (gait disturbance, hemiparesis, facial
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weakness) or non-motor (visual field impairment, sensory symptoms) in nature; (2) new onset

seizure followed or preceded by a persistent focal neurological deficit; or (3) unexplained

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alteration of mental status in the presence of a risk factor for stroke. Risk factors were itemized
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on the PSCP for clinician reference and include a history of one of the following: (1) prior
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stroke, (2) congenital heart disease, (3) sickle cell disease, (4) head trauma in the past week (5)

arteriovenous malformation, (6) hypercoaguability, (7) cranial radiation, (8) acute lymphoblastic
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leukemia receiving L-asparaginase, (9) Down Syndrome, (10) moyamoya disease, (11)

mitochondrial encephalopathy with lactic acidosis and stroke like episodes, and (12) varicella or
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any significant infection of the head or neck in the preceding three months (Appendix 1).
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Clinicians activate the PSCP using a single fan out page to alert attending physicians from the

departments of anesthesia, critical care, neurology, and radiology in order to expedite imaging

and hospital admission. Trainees are not involved in the PSCP in an effort to streamline clinical
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Pediatric Stroke Clinical Pathway

care. With activation of the PSCP, a standardized protocol is initiated. For patients with sickle

cell disease, early exchange transfusion is initiated followed by MRI. For patients without sickle

cell disease, an urgent CT is followed by MRI. Standard guidelines for pre-sedation fasting are
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generally followed but general anesthesia is administered by the on call pediatric anesthesiologist

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irrespective of these guidelines when clinically warranted. All patients undergo diffusion

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weighted imaging first with a complete MRI/MRA performed immediately after, or within a few

hours, at the discretion of the radiologist and neurologist as long as the patient is clinically stable.

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For both protocols, the goal is to obtain MRI brain within 4 hours of patient arrival to the

pediatric emergency department. When MRI was readily available, the pathway allowed for

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flexibility and omission of the CT. All neuroimaging, when obtained, was immediately
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interpreted by the attending neuroradiologist, reviewed by the neurologist, and conveyed to the

pediatric emergency department physician.

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The protocol delineates requisite laboratory studies, interventions to be performed in the

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pediatric emergency department, guidelines for neuroprotective strategies and nursing care.

Patients with confirmed stroke are admitted to the intensive care unit. A summary of the protocol
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for patients without sickle cell disease is attached in Appendix 1. Tissue-type plaminogen

activator is not routinely used at our institution; thus, standard definitive therapy included
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anticoagulant or antiplatelet therapy at the discretion of the pediatric hematologist and

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neurologist.

Demographic and clinical data, including presenting signs and symptoms, physical examination

findings, imaging results, and hospital length of stay were abstracted for both the pre and the
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Pediatric Stroke Clinical Pathway

post-PSCP groups using a standardized form. This study was approved by the Institutional

Review Board of Wayne State University School of Medicine.

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Statistical Analyses

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Categorical variables were reported in numbers (%), normally distributed continuous variables

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were reported as mean ± standard deviation (SD), and non-normally distributed continuous

variables as median and inter-quartile range (IQR). Pearson’s Chi-squared test was used to

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analyze the distribution of categorical variable by groups, provided a minimum expected number

of at least 5 in any cell, otherwise Fisher-Irwin test was used for the analysis. Normality for all

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continuous variables was tested using the Shapiro-Wilk test as sample size is less than 2000.
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Two group comparisons for normal continuous variables were conducted using Student t test,

whereas non-normally distributed continuous variables were compared using the Wilcoxon rank
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sum test. Friedman's two-way test was used to study time to neuroimaging performed outside of
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business hours. Median control chart was used to study time to MRI and time to CT. Data were
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analyzed using the statistical package for the social sciences (IBMSPSS version 23, IBM

Corporation, Armonk, New York) and SAS (version 9.4, SAS Institute Inc. Cary, North
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Carolina). Significance level was set at 0.05.

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Results
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Demographics and Symptomatology

Stroke was diagnosed in one third of patients (11/36, 31%) for whom the PSCP was activated

(Figure 1). The majority of these patients (7/11, 64%) had an ischemic stroke while 36% (4/11)

had a hemorrhagic stroke. There were no significant differences in the age, sex, race or time of
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Pediatric Stroke Clinical Pathway

pediatric emergency department presentation for patients with stroke pre and post PSCP

implementation (Table 1). However, a significantly higher proportion of patients were triaged as

higher acuity for immediate physician evaluation following implementation of the PSCP (Table
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1). A higher proportion of patients in the post-PSCP group lacked risk factors for stroke

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compared to the pre-PSCP group (7/11, 64% post-PSCP versus 8/30, 27% pre-PSCP). Focal

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neurological deficit and headache were the two most common presenting symptoms for patients

with stroke in the post-PSCP group (Figure 2).

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Imaging

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There was no significant difference in the number of patients in the pre and post-PSCP groups
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evaluated with a CT (20/30, 67% pre-PSCP versus 8/11, 73% post-PSCP; p = 1.0). There was a

reduction in the median time to CT in the post-PSCP group compared to the pre-PSCP group
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although the difference was not statistically significant [46 minutes (IQR 34, 76) post PSCP
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versus 79 minutes (IQR 35, 107) pre-PSCP; p = 0.54)]. Most patients in both study periods
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underwent MRI (28/30, 96% pre-PSCP versus 11/11, 100% post-PSCP; p = 1.0), however only

7/11 patients in the post-PSCP group had an urgent MRI as outlined by the PSCP. MRI was
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deferred for two patients diagnosed with hemorrhagic stroke based on their CT, while one patient

with mitochondrial encephalomyopathy, lactic acidosis, and stroke-like episodes had treatment
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instituted in the emergency department prior to an inpatient MRI, which demonstrated acute
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stroke. Treatment was initiated for this patient prior to the MRI as the clinical presentation was

reminiscent of previous episodes of stroke. In the fourth patient, evolution of the neurological

symptoms and examination over the first 16 hours of the admission led to a diagnostic inpatient

MRI 21 hours after initial presentation. Considering only those patients where the MRI was
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Pediatric Stroke Clinical Pathway

urgently obtained per the PSCP (7/11), there was a significant improvement in the median time

to MRI from arrival to the pediatric emergency department [17 hours (IQR 6, 22) pre-PSCP

versus 4 hours (IQR 3, 12) post-PSCP; p = 0.02]. There was no significant difference in the time
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to MRI for patients diagnosed with stroke in the post-PSCP group based on the time of

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emergency department presentation [3.5 hours (IQR 3, 13.5) during the day (0700-1500 hours)

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versus 4 hours (IQR 2, 12) during the afternoon (1500-2300 hours); p = 1.0)]. Although only

marginally statistically significant, the time to MRI for patients diagnosed with stroke in the

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post-PSCP group was quicker on weekdays compared with weekends [3 hours (IQR 2, 3) on

weekdays versus 8 hours (IQR 4, 17.5) on weekends; p = 0.048].

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Disposition and Length of Stay

The proportion of patients admitted to the pediatric intensive care unit increased significantly in
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the post-PSCP period (15/30, 50% pre-PSCP versus 7/11, 64% post PSCP; p = 0.004). Both the
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median length of stay in the pediatric emergency department [3 hours 50 minutes (IQR: 2:38,
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4:56) pre-PSCP versus 4 hours 33 minutes (IQR 3:15, 5:56 post-PSCP; p = 0.17] and the overall

median hospital length of stay [117 hours (IQR:74, 201) pre-PSCP versus 143 hours (IQR 81,
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213) post-PSCP; p = 0.62) remained unchanged following implementation of the PSCP.

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Outcomes
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The majority of patients with stroke were discharged home (18/30, 60% pre-PSCP versus 7/11,

64% post-PSCP). One third of children in pre and post-PSCP periods were discharged to

inpatient rehabilitation following their acute hospitalization (10/30, 33% pre-PSCP and 4/11,

36% post-PSCP). There were no deaths in the post-PSCP group while two patients in the pre-
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Pediatric Stroke Clinical Pathway

PSCP group died. One patient had a mitochondrial disorder of unknown etiology and the other

had complex congenital heart disease.

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Discussion

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Our study demonstrates that a standardized institutional protocol can significantly improve the

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time to a diagnosis of acute stroke among children presenting to a tertiary care pediatric

emergency department with neurological deficits. Pediatric stroke teams with standardized care

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protocols have been developed at the 23 institutions involved with the Thrombolysis in Pediatric

Stroke (TIPS) study.14,15 Our institution was not among the 23 involved in the TIPS study; thus,

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the success of our institution’s protocol demonstrates the feasibility of this approach in a tertiary
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care center functioning outside the realm of multi-centered stroke research.
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This is an important achievement as primary adult stroke centers markedly improve the quality
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of care for individuals with stroke,16 and institutions participating in the TIPS study met many of
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the criteria required for this designation.15 Our institution was not among those involved in the

TIPS study, but even those hospitals planning to become stroke centers noted lower in-hospital
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mortality and readmission rates during the initial stroke certification phase.17 While emergency

departments in adult stroke centers focus on early imaging with the intent to administering timely
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thrombolytic therapy, we argue that similar emphasis on early imaging, achieved through a
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PSCP, can potentially lead to early intervention in children. Such intervention may be supportive

in nature, such as regulation of blood pressure, maintaining normothermia and normoglycemia

and starting anticonvulsant medication, or more definitive such as anticoagulation or surgical

intervention.
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Pediatric Stroke Clinical Pathway

Secondly, the PSCP was successful in addressing the two main barriers to identification of

pediatric stroke cited in previous studies,6-9 namely provider recognition and timely definitive

imaging. The presence of a standardized protocol created a greater awareness of stroke as a

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potential diagnosis amongst pediatric emergency department physicians. A focal deficit,

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encapsulated in the FAST criteria (Facial droop, Arm weakness, Speech disturbance, Time to

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call 911) can identify 80% of childhood strokes.12 While the majority of patients both prior to

and following implementation of the PSCP presented with a focal deficit, only 30 children were

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identified over a 5 year period prior to the initiation of the PSCP (an average of 6 per year)

whereas the diagnosis of stroke was suspected 36 times in the 1.5 years after the protocol was

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implemented. The substantial value of a systematic check-list based approach has been
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documented in the surgical realm in several countries and across various types of interventions.18

We propose that the PSCP functioned in a similar vein by highlighting risk factors for stroke,
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identifying clear-cut time sensitive goals for the pediatric emergency department in terms of
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patient triaging, achieving diagnostic tests in an efficient manner, involving several sub-
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specialties at the outset and eliminating the need for individual consultations.
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MRI is the preferred imaging modality for pediatric stroke and with this pathway suspected

stroke can quickly be confirmed or ruled out as rapid access to MRI has been facilitated. This
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step is imperative as it has been previously reported that CT can be falsely reassuring in pediatric
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stroke.19 Similar to previous studies, 40% of our post-PSCP patients had an abnormal MRI with

a normal CT and 75% of these patients were diagnosed with stroke. Of note, one child presented

with headache and left sided weakness and numbness. Although her neurological examination

and CT were normal in the emergency department, she developed focal deficits 16 hours into her
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Pediatric Stroke Clinical Pathway

admission and was ultimately diagnosed with an acute posterior cerebral artery stroke on MRI.

Thus, emergency room physicians should not only strongly consider urgent MRI for pediatric

patients with focal deficits, irrespective of CT results, but a patient with an evolving neurological
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exam also warrants an urgent MRI.

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While the protocol uniformly reduced the time to definitive imaging irrespective of time of

pediatric emergency department presentation, there was still a marginally statistically significant

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difference to definitive imaging in weekday versus weekend presentations, with time to imaging

being shorter for weekday presentations. Weekend stroke presentations in a national sample

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occurred in 28% of children who then had higher odds of being discharged to an inpatient
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rehabilitation or nursing facility and higher mortality compared to children who presented on a

weekday.20 Although the PSCP now makes the mobilization of key personnel possible on the
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weekends, a standardized protocol alone does not mitigate the impact of the previously reported
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“weekend effect”.20 Differences in staffing may continue to play a role despite a standardized
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protocol, but further analysis of the various factors leading to delayed MRI on the weekends is

warranted so that the discrepancy in time to diagnosis of acute stroke can be addressed.
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We did not study the cost of implementation and maintenance of the protocol. It could be argued
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that greater utilization of imaging modalities, especially MRI in the PSCP period along with
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presence of additional on-call personnel for completion of such studies would translate into

greater health care costs. However, the protocol had "built in" checks that prevented ordering of

unnecessary emergent MRI by the emergency department physicians in that the PSCP could be

cancelled with neurologists’ input in patients for whom the imaging study did not result in a
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Pediatric Stroke Clinical Pathway

change in management (for example, mitochondrial encephalomyopathy, lactic acidosis, and

stroke-like episodes) or those patients for whom the definitive diagnosis could be established by

CT scan. While the PSCP may result in an increased cost of care for the acute presentation due to
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an increase in pediatric intensive care admissions with no change in overall length of stay, a true

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assessment of the economic impact of the PSCP is not possible without meaningful data related

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to long term patient outcomes given the substantial lifetime cost of pediatric stroke.4,5

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Limitations

This study has several notable limitations. First, this study was performed at a single institution

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with 24/7 pediatric neurology and radiology coverage. Access to subspecialty services limits
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generalizability to other practice settings. Second, the sample size is small and retrospective data

collection may have impacted the amount and quality of data available for analysis. Third, the
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PSCP was activated based on the individual pediatric emergency department clinician’s
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suspicion for stroke, which may have resulted in over or under activation of the PSCP. Thus, it is
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possible that the PSCP was not activated for patients in whom the ultimate diagnosis was stroke.

We did not collect information on stroke patients for whom the PSCP was not activated but none
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of the inpatients for whom the PSCP was activated had neurological symptoms in the ED.

Furthermore, the PSCP could be activated for patients presenting within 72 hours of symptom
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onset which exceeds the typical timeframe for acute intervention. Finally, the goal of obtaining
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an MRI within 4 hours of presentation exceeds the gold standard of one hour (G.A. deVeber,

email communication, June 2015). However, since our institution is not a center that is utilizing

thrombolytic therapy, a 4 hour timeframe was considered to be a reasonable timeframe to

complete definitive neuroimaging. Most importantly, the study did not evaluate the impact of the
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Pediatric Stroke Clinical Pathway

PSCP implementation on clinical outcomes of patients. While there was a trend toward more

patients being discharged home than to a rehabilitation unit following implementation of the

PSCP, our small sample size and absence of long term follow up of the study cohort prevents us
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from making any meaningful conclusions regarding patient outcomes.

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Conclusions

A standardized institutional protocol significantly improves the time to definitive diagnosis for

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children with stroke. Given that acute therapies are time sensitive, such prompt diagnosis of

pediatric stroke provides an opportunity for intervention. Additional studies are required to

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determine the impact of standardized protocols on clinical outcomes of individual children and
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the economic impact on pediatric health care delivery systems.
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5. Gardner MA, Hills NK, Sidney S, Johnston SC, Fullerton HJ. The 5-year direct medical
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deVeber GA. Delay to diagnosis in acute pediatric arterial ischemic stroke. Stoke

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11. Amlie-Lefond C, Rivkin MJ, Friedman NR, Bernard TJ, Dowling MM, deVeber G. The

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13. Ladner TR, Mahdi J, Gindville MC, Gordon A, Harris ZL, Crossman K, Pruthi S,
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Abramo TJ, Jordan LC. Pediatric acute stroke protocol activation in a children’s hospital

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14. Bernard TJ, Rivkin MJ, Scholz K, et al. Emergence of the primary pediatric stroke center.
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Impact of the Thrombolysis in Pediatric Stroke trial. Stroke 2014;45:2018-2023.

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15. Rivkin MJ, Bernard TJ, Dowling MM, Amlie-Lefond C. Guidelines for urgent managemt

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16. Hankey GJ, Warlow CP. Treatment and secondary prevention of stroke: evidence, costs,

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17. Ballard DW, Kim AS, Huang J, et al. Implementation of computerized physician order
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19. Elbers J, Wainwright MS, Amlie-Lefond C. The pediatric stroke code: early management

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inpatient sample. Stroke. 2016 Epub ahead of print. PMID 27118791.

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Table 1. Demographic characteristics of all patients with stroke before and after

implementation of the PSCP

Demographic Pre-PSCP Post-PSCP P value

Characteristic (n = 30) (n = 11)

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Age (years) 12 ± 10 11 ± 7 0.57
Median ± IQR
Male 50% 55% 1.0

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Race
African American 60% 45% 0.49
White 40% 55% 0.49

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Afternoon / 63% 55% 0.73
overnight
presentation
Weekday 73% 45% 0.14

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presentation
Emergency Severity 13% 55% 0.02
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Index Code 1
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Figure 1. Final diagnoses for all patients for whom the PSCP was activated

1 1
2
Stroke

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CNS metastases
3 11
Migraine

Transient neurological deficits with

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discrepant exam
2
Seizure

MELAS

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Psychosomatic
3

Demyelinating disease

Drug toxicity

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5 Moya Moya without stroke
4
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4
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Figure 2. Clinical characteristics of patients with stroke presenting pre and post PSCP

30
26
25

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Number of Patients

20

Pre-PSCP
15

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Post-PSCP
11 11
10 9 9
7

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6
5
2 2
1

U
0
Focal deficit Headache Seizure Altered mental Gait
status abnormalities
AN
M
D
TE
C EP
AC