Prehospital Predictors of Emergent Intervention After Helicopter Transfer for Spontaneous Intraparenchymal Hemorrhage

Prehospital Predictors of Emergent Intervention After Helicopter Transfer for Spontaneous Intraparenchymal Hemorrhage

Original Article Prehospital Predictors of Emergent Intervention After Helicopter Transfer for Spontaneous Intraparenchymal Hemorrhage Erin D’Agostin...

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Original Article

Prehospital Predictors of Emergent Intervention After Helicopter Transfer for Spontaneous Intraparenchymal Hemorrhage Erin D’Agostino1, Jennifer Hong2, Chad Sudoko1, Nathan Simmons2, Stuart Scott Lollis3

OBJECTIVE: Helicopter transport may shorten transportation times for emergent neurosurgical intervention. The usefulness of helicopter transport after spontaneous intraparenchymal hemorrhage is not well studied. This study seeks to clarify factors that are associated with urgent surgical intervention in patients with spontaneous intracerebral hemorrhage following helicopter transport.

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METHODS: Records were reviewed for patients with spontaneous intraparenchymal hemorrhage transported by helicopter to Dartmouth-Hitchcock Medical Center between January 2008 and December 2011. Records were evaluated for factors associated with emergent tertiarylevel care intervention during the first 24 hours of admission.

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RESULTS: A total of 107 patients met inclusion criteria, with a mean age of 67.2 years. At presentation, 79 (75.24%) were hypertensive, 22 (21.57%) had an increased international normalized ratio, and 47 (45.19%) were intubated. Thirty-three patients (30.8%) underwent 1 or more neurosurgical interventions within 24 hours of arrival, with an additional 6 (5.6%) patients undergoing neurosurgical intervention after 24 hours after admission. On univariate analysis, age, Glasgow Coma Scale (GCS) score, and clot volume were significant predictors of neurosurgical intervention within 24 hours of interfacility helicopter transport. A lobar clot, presence of intraventricular hemorrhage, and presence of >1 cm of midline shift were also associated with neurosurgical intervention within 24 hours. On

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Key words Helicopter transport - Interfacility - Intraparenchymal hemorrhage - Prehospital predictors - Spontaneous -

Abbreviations and Acronyms DHART: Dartmouth-Hitchcock Advanced Response Team DHMC: Dartmouth-Hitchcock Medical Center GCS: Glasgow Coma Scale IVH: Intraventricular hemorrhage PAT: Potentially avoidable transfer SAH: Subarachnoid hemorrhage

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multivariate analysis, younger age, GCS score of 3e8, and lobar hemorrhage were independent predictors of neurosurgical intervention within 24 hours. CONCLUSIONS: Two thirds of patients did not undergo any surgical intervention during the first 24 hours of admission after interfacility helicopter transfer. Factors associated with urgent neurosurgical intervention included younger age, low GCS score, and presence of lobar hemorrhage.

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INTRODUCTION

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nterfacility helicopter transfer of patients with neurosurgical indications is a common but understudied phenomenon.1-3 Patients with spontaneous intraparenchymal hemorrhage (sIPH) are often initially evaluated and stabilized at community hospitals, then subsequently transferred to tertiary-care centers for further workup or definitive treatment. These patients may be selected for helicopter transport because of concerns of potential rapid deterioration, need for time-sensitive treatment, or lack of available ground-transport options. In many cases, it is unclear what criteria are used for helicopter triage, and no published evidence-based guidelines exist for sIPH. The lack of clear parameters for helicopter transport likely results in ad hoc case-by-case decision making, dependent more on referring physician unease than data. This situation may cause overuse of an expensive and scarce medical resource.1,4-6 Unnecessary helicopter transport also poses a potential threat to patient care by exposing

sIPH: Spontaneous intraparenchymal hemorrhage TBI: Traumatic brain injury From the 1Geisel School of Medicine, Dartmouth College, Hanover, New Hampshire; 2 Dartmouth-Hitchcock Medical Center, Section of Neurosurgery, Lebanon, New Hampshire; and 3 University of Vermont Medical Center, Section of Neurosurgery, Burlington, Vermont, USA To whom correspondence should be addressed: Stuart Scott Lollis, M.D. [E-mail: [email protected]; [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.050 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.

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patients to risks of transport and by potentially misallocating limited resources at the tertiary-care center.4 To assess the usefulness of interfacility helicopter transfers for patients with sIPH, we reviewed records for all helicopter transfers to a tertiary-care center over a 5-year period, with specific attention to these patients. We hypothesized that most helicopter transports do not require emergent neurosurgical intervention, defined as ventriculostomy, craniotomy, conventional angiography, or endovascular treatment. We also analyzed pretransfer patient clinical and radiographic findings to evaluate factors that are significantly associated with neurosurgical intervention. Our goal was to focus on factors associated with intervention rather than patient outcome. METHODS Participants and Study Design Dartmouth-Hitchcock Medical Center (DHMC) hospital records, outside hospital imaging studies, and Dartmouth-Hitchcock Advanced Response Team (DHART) data bases were retrospectively searched for patients with sIPH who were transported by helicopter to DHMC for neurosurgical evaluation between January 1, 2008 and December 31, 2011. Determination of sIPH diagnosis was based on hospital discharge documentation and referral information. A total of 157 patients were initially identified as having been transported by helicopter for intraparenchymal bleed. Patients who had intraparenchymal hemorrhage secondary to history of trauma (n ¼ 10) or known tumor (n ¼ 18) were excluded. Patients with infratentorial or brainstem clot location (n ¼ 22) were also excluded. A total of 107 patients met the criteria for study inclusion. Air Ambulance System DHMC is a level I trauma center and tertiary referral center for northern New England, encompassing 22 hospitals primarily in New Hampshire and Vermont. DHART is the helicopter ambulance program operated by DHMC, which facilitates expedient transport in this area. It is comprised of 2 helicopters, 1 stationed at DHMC and 1 in Concord, New Hampshire, and is available at all times, weather permitting. The flight crew is composed of a pilot and 2 intensive care unit nurses. The decision to transport a patient by helicopter is made by the referring physician based on New Hampshire patient care protocols.7 Clinical Variables and Outcomes Assessment Pertinent information from retrospective chart review was sought regarding presentation, transport, and hospital admission and then subsequently analyzed for factors associated with emergent tertiary-level care intervention. Data collected included age, sex, presenting symptoms, time to presentation, clinical examination results, vital signs, coagulation studies, past medical history, medications, Glasgow Coma Scale (GCS) score, radiographic studies, evidence of deterioration during transport (changes in pupils, vital signs, imaging, intubation), transport time, interventions (medical and surgical), time to intervention, hospital length of stay, and disposition. Imaging from the outside hospital was evaluated when possible. Imaging was evaluated for clot

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location, clot volume, evidence of hydrocephalus (defined by Evans index 0.3)8 and midline shift. Time for transport by air was compared with time by ground, using DHART flight log records to calculate flight time and Google Maps to calculate average 1-way driving times. Time to intervention was calculated based on arrival documented by DHART flight log and procedure start times indicated by anesthesia operative log or operative note. Time to intervention was categorized as occurring within 24 hours or after 24 hours, fully within the time range that a patient could be transported by ground. Neurosurgical intervention was defined as ventriculostomy, craniotomy, or formal angiography. Statistical Analysis All statistical tests were performed using the publicly available software R (www.r-project.com [R Foundation for Statistical Computing, Vienna, Austria]). A predetermined P value of 0.05 was deemed statistically significant. Any missing data were imputed using the mean value of the group for continuous variables, namely clot volume, and number of comorbidities. For the categories of hemorrhage location (lobar vs. deep), presence of intraventricular hemorrhage (IVH), the value chosen was the one most likely to be associated with intervention. Univariate analysis was performed for all clinical variables of interest for the primary outcome of intervention within 24 hours of arrival to the hospital versus no intervention during the same period. For comparison of continuous variables, a 2-tailed Student t test was conducted. For categorical variables, contingency tables were created and c2 tests were performed. For 2  2 tables, the 2-sided Fisher exact t test was used. For variables with >2 categories, the Pearson c2 test was used. Multivariate logistic regression was performed for the outcome of intervention within 24 hours of arrival at the hospital, incorporating all variables deemed to be statistically significant by univariate analysis. RESULTS Participants Records of all interfacility helicopter transfers for neurosurgical consultation between January 2007 and December 2011 to a tertiary-care hospital in rural New England were reviewed. From 873 flights, 140 patients were identified as having a diagnosis of spontaneous intracerebral hemorrhage. Nine were excluded because of a history of trauma; 18 were excluded because of infratentorial or brainstem clot location; and 6 were excluded because of multifocal hemorrhage, resulting in 107 patients included in the study. Descriptive Data All descriptive data are summarized in Table 1. The median age of our cohort was 71 years (range, 6e90 years). Seventy-nine patients (75.24%) were hypertensive at presentation. GCS scores on presentation were 13e15 in 49 patients (50%), 9e12 in 11 patients (11.2%), and 3e8 in 38 patients (38.8%). Twenty-two patients (21.57%) had an increased international normalized ratio. Fortyseven patients (45.19%) arrived intubated. Comorbidities included stroke (16 patients), myocardial infarction (5 patients),

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Table 1. Pretransfer Demographic and Clinical Variables of Patients Transferred by Helicopter Ambulance with Spontaneous Intraparenchymal Hemorrhage to DartmouthHitchcock Medical Center, 2007e2011 Variable

Mean (Standard Deviation)

Median (Range)

N (%)

Patient-Specific Information Age, years Sex (male)

67.65 (14.9) —

71 (6e90) —

— 62 (58.5)

Clinical data at presentation Systolic blood pressure (mm Hg)

167.3 (35.9)

163 (97 e260)



Heart rate (beats/minute)

79.2 (16.9)

77 (39 e132)



224.8 (78)

213 (12 e429)







47 (46.1)

First platelet count Anticoagulation First international normalized ratio Glasgow Coma Scale score

1.59 (1.3)

Variable

n

Lobar clot

%

72

69.9

Temporal lobe clot

14

13.6

Frontal lobe clot

19

18.5

Parietal lobe clot

7

6.8

Occipital lobe clot

5

4.85

Multilobar clot

27

26.2

Deep clot

31

30.1

Intraventricular hemorrhage

55

51.4

Hydrocephalus

25

23.3

Midline shift >1 cm

27

25.2

Clot <1 cm from inner skull table

73

68.2

Hydrocephalus Defined by Evans Ratio 0.3. Deep defined by basal ganglia or thalamus.

1 (0.9e8.2) —

10.04 (5.05)

12.5 (3 e15)



3e8





38 (38.8)

9e12





11 (11.2)

13e15





49 (50)

previous intracranial hemorrhage (2 patients), and bleeding diathesis (4 patients). Interventions Before Arrival Forty-seven patients (45.19%) were intubated before arrival at the tertiary-care center. Before arrival, 17 patients (17.2%) were given fresh frozen plasma and 17 (16.4%) were given mannitol. Average transport time was 79 minutes (standard deviation, 28.82). Fortyseven patients (43.9%) had an interfacility helicopter transport time that exceeded 1-way drive times from the referring facility. Thirteen patients (12.4%) showed clinical decline during transport, as shown by pupillary change, intubation, or noted significant changes in vital signs. Imaging All patients underwent an initial noncontrast head computed tomography study with results summarized in Table 2. The locations of the hemorrhages were classified as lobar in 75 patients (70.1%) and deep in 32 (29.9%). Thirty patients (28.8%) had temporal lobe clots, 19 patients (17.7%) had frontal lobe clots, 7 patients (6.5%) had parietal lobe clots, and 27 patients (25.2%) had clots that encompassed multiple lobes. Intraventricular hemorrhage (IVH)

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Table 2. Imaging Characteristics of Patients with Spontaneous Intraparenchymal Hemorrhage Transferred from an Outside Facility by Helicopter Emergency Medical Services

was present in 55 patients (51.4%), hydrocephalus was present in 25 patients (23.3%), and >1 cm of midline shift was present in 27 patients (25.2%). The mean clot volume was 52.3 mL (range, 2.1e238.7 mL). Seventy-three patients (68.2%) had a hematoma within 1 cm of the inner table of the skull. Additional imaging including computed tomography angiography and conventional cerebral angiography identified 4 aneurysms and 9 other vascular malformations. Interventions Thirty-three patients (30.8%) underwent 1 or more neurosurgical interventions within 24 hours of arrival. Of these interventions, there were 20 craniotomies, 22 external ventricular drain placements, 5 subdural intracranial pressure monitor placements, and 7 conventional angiograms. Medical management of spontaneous intracranial hemorrhage included fresh frozen plasma transfusion in 17 patients, and platelet transfusion in 2 patients. Six patients underwent craniotomy during their admission, but >24 hours after admission. Three of these patients had undergone intervention during the first 24 hours of admission (2 had undergone external ventricular drain placement and 1 had undergone angiography) and then underwent craniotomy >24 hours after admission. Seventy-one patients (66.4%) did not undergo any neurosurgical intervention during their admission after interfacility helicopter transport and received medical management only, which included blood pressure monitoring and control, reversal of anticoagulation, and intubation. These data are seen in Figure 1. Of the patients who received no surgical interventions, 31.4% were deemed to have unsalvageable brain injuries after evaluation by a neurosurgeon and progressed to death or were discharged to hospice. None of the 9 patients older than 80 years with basal ganglia hemorrhage received any neurosurgical intervention during admission. In addition, none of the 3 patients older than 80

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intervention. Presence of IVH, increasing clot volume, and presence of temporal lobe clot were not independent predictors of intervention within 24 hours of interfacility helicopter transport. These data are seen in Table 4. A rudimentary scoring system was developed using these 3 independent predictors (age <65 years, lobar hemorrhage, and GCS score <9). In patients with zero risk factors (n ¼ 13), the frequency of emergent surgical intervention was 0%. In patients with 1 risk factor (n¼42), the frequency of emergent surgical intervention was 26%. In patients with 2 risk factors (n¼41), the frequency of emergent intervention was 32%. In patients with 3 risk factors, (n¼11), the frequency of emergent intervention was 82%. DISCUSSION Figure 1. Interventions during the first 24 hours of admission after interfacility helicopter transport of patients with solitary spontaneous intraparenchymal hemorrhage. Interventions included craniotomy, external ventricular drain, subdural intracranial pressure (ICP) monitor, or other (clipping, coiling, conventional angiogram). Several patients received >1 intervention.

years with severe mass effect (defined as midline shift >15 mm) received any neurosurgical intervention during admission. Univariate Analysis On univariate analysis for factors associated with neurosurgical intervention within 24 hours of interfacility helicopter transfer, age, GCS score, clot volume, and change in pupillary examination results were all significant predictors. Patients who underwent interventions were significantly younger, had significantly lower GCS score, had significantly larger clot volumes on average, and showed deterioration as documented by a change in pupillary examination results by the time they arrived at our center. Presentation with anisocoria at the outside hospital did not predict intervention after transfer, but development of anisocoria or fixed pupils during transfer predicted increased likelihood of neurosurgical intervention. A lobar clot, presence of IVH, and presence of >1 cm of midline shift were also associated with neurosurgical intervention within 24 hours. Clinical and radiographic variables that did not significantly differ between the 2 groups included gender, systolic blood pressure and heart rate, number of comorbidities, presence of a temporal lobe clot, and transport times. These data are seen in Table 3. Multivariate Analysis Factors that were identified as statistically significantly associated with neurosurgical intervention within 24 hours were entered into a multivariate logistic regression to assess for independence. Age, a GCS score of 3e8, and a lobar hemorrhage were independent predictors of neurosurgical intervention within 24 hours. An odds ratio of 0.94 for age suggests that increased age is associated with a decreased likelihood of intervention. In comparison, a GCS score 8 and a lobar hemorrhage were both associated with an increased likelihood of

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Risk of rapid deterioration in neurosurgical patients with certain conditions has prompted increased attention to speed of transportation to definitive care at a tertiary center. For example, studies of ischemic stroke and spontaneous subarachnoid hemorrhage (SAH) have shown that expedited transport can improve outcomes.9-13 In accordance with efforts to reduce time to intervention, helicopter use for interfacility and scene transport has increased significantly in the past 2 decades. Attempts have been made to establish guidelines for triage on scene to expedite helicopter transport of patients with stroke and SAH to tertiary-care centers.14-16 Approximately 400,000 rotor wing transports and 150,000 fixed wing aircraft transports are used annually in the United States. The proliferation of helicopter transports has created the potential for overuse and unindicated high-risk flights. For time-sensitive conditions, some degree of overtriage has been deemed acceptable. The American College of Surgeons Committee on Trauma has stated that a rate of up to 35% overtriage for trauma is reasonable.4 This standard likely applies to neurosurgical indications, but investigation of which presenting features of patients predict necessity for intervention would allow for better allocation of critical resources. For some neurologic emergencies, including traumatic brain injury (TBI), randomized studies have been conducted examining the outcomes of craniectomy versus medical alone and have found that in certain patients, surgical intervention may not always result in better outcomes. Although these studies do not examine interfacility transport, they suggest that surgery may not always be necessary in our patient population.17,18 Guidelines are necessary to aid in determination of which patients at presentation will benefit from surgical intervention and therefore require rapid transport. For TBI, guidelines have been published19 and applied20 to more efficiently allocate helicopter resources. Transport guidelines do not exist for sIPH. Although a broader issue is whether a patient requires transfer, a starting point is how a patient is transferred. Deployment of ground transportation may result in the same use of emergent services as air transportation for many patients, without straining system resources to the same extent. Although outcomes are an important objective for further study, our study seeks to start by clarifying factors in these patients that are associated with urgent surgical intervention after helicopter transport.

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ORIGINAL ARTICLE ERIN D’AGOSTINO ET AL.

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Table 3. Univariate Analysis of Factors Associated with Urgent Neurosurgical Intervention After Interfacility Helicopter Transfer for Solitary Spontaneous Intraparenchymal Hemorrhage Intervention Within 24 Hours (n [ 33)

No Intervention Within 24 Hours (n [ 74)

P Value

61.3 (18.0)

70.4 (12.3)

0.0031*

<50

4 (37.0)

21 (94.0)

0.04

<65

18 (54.5)

52 (71.2)

0.09

Variable Clinical variables Mean age, years

<80

28 (84.8)

70 (95.9)

0.08

Female

13 (46.0)

31 (42.5)

0.833

Systolic blood pressure, mm Hg

167.9 (6.6)

167.1 (4.2)

0.9052*

Heart rate, beats/minute

78.4 (3.1)

79.6 (1.9)

0.7330*

Number of comorbidities

0.0945

1

7 (21.2)

12 (16.2)

2e3

16 (48.5)

23 (31.1)

4

10 (30.3)

39 (52.7)

Mean Glasgow Coma Scale score

7.8 (4.7)

11.0 (4.9)

0.0031*

3e8

22 (66.6)

26 (35.1)

0.007079y

9e12

3 (9.1)

7 (9.5)

13e15

8 (24.3)

41 (55.4)

6 (18.2)

2 (2.7)

0.009

Number with lobar clot vs. deep

29 (87.9)

46 (62.2)

0.0073

Number with temporal lobe clot

13 (39.4)

17 (22.9)

0.103

Number with intraventricular hemorrhage

23 (69.7)

32 (43.2)

0.022

Number with midline shift >1 cm

18 (54.5)

9 (12.2)

0.0007

Number with pupillary change during transfer Radiographic variables

Mean clot volume, mL

64.11 (37.8)

44.26 (48.19)

0.0245*

<10

1 (3.1)

19 (25.7)

0.0293y

10e30

8 (24.2)

16 (21.6)

31e50

8 (24.2)

18 (24.3)

>50

16 (48.5)

21 (28.4)

Number with hydrocephalus Mean transport times, minutes

13 (38)

21 (62)

0.372

83.3 (6.2)

77.2 (3.0)

0.3259*

Bold values are expressed as mean (SD), all other data expressed as n (%). All other statistical tests are Fisher exact test, 2 sided. A P value 0.05 is considered statistically significant. SD, standard deviation. *Student t test, 2-tailed. yPearson c2 test.

Key Results In our experience, most patients (74.4%) with spontaneous solitary supratentorial sIPH who are referred to our medical center via interfacility helicopter transfer do not receive any neurosurgical intervention. Of these patients who received no surgical interventions, 31.4% were diagnosed with unsalvageable brain

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injuries and progressed to death or were discharged to hospice. Many transferred patients received medical management alone, often initiated and managed at an outside emergency department. It is likely that for this subset of patients, a helicopter transfer was unnecessary and ground transport would not have altered outcome. Only 13 patients (12.4%) had an acute decline in their

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Table 4. Multivariate Logistic Regression for Factors Associated with Urgent Neurosurgical Intervention After Interfacility Helicopter Transfer for Solitary Spontaneous Intraparenchymal Hemorrhage Variable

Odds Ratio (95% Confidence Interval)

Younger age

0.948 (0.908e0.983)*

Lobar location

5.81 (1.520e29.353)y

Limitations The primarily limitation of our study is its retrospective nature, which introduces significant selection bias. We do not completely understand the reasons behind why these patients were transferred via helicopter as opposed to ground transport. If referring physicians were using criteria other than clinical and radiographic factors, we were not able to assess these with this study. Another important limitation of our study is that we are not able to comment on whether helicopter transfer of our patients resulted in improved outcomes because we did not include a matched ground-transport cohort. We deliberately chose to examine the narrow question of how frequently helicopter transfer results in neurosurgical intervention for sIPH because any comparison of ground versus helicopter transport that is not randomized would be highly confounded.

Glasgow Coma Scale score 13e15

Ref

9e12

2.27 (0.377e12.268)

3e8

3.72 (1.093e13.667)y

Clot volume (mL) <10

Ref

10e30

2.73 (0.302e60.939)

31e50

6.58 (0.922e135.88)

>50

3.41 (0.449e71.621)

Intraventricular hemorrhage

2.49 (0.772e8.455)

*P value ¼ 0.01. yP value ¼ 0.05.

neurologic examination result en route. Overall, patients who arrived at our facility after helicopter transport tended to present with either a good neurologic examination result and excellent neurologic prognosis (GCS score 13e15) and were “stably good” or with a poor neurologic examination result and terrible neurologic prognosis (GCS score 3e8) and were “stably bad” (see Table 1). This latter group was predominantly comprised of patients with hemorrhages that were nonoperative because of futility or family wishes. A shorter interfacility transport time would have been unlikely to affect the potential interventions or outcomes of these patients. We found that a poor GCS score (3e8), and a lobar hemorrhage location were independent predictors of neurosurgical intervention. This finding suggests that the patients who are most likely to benefit from expedited helicopter transport are those who are very symptomatic secondary to hemorrhages that are more superficial. This association, although intuitive, has not been shown in this cohort of transferred patients. Neither midline shift >1 cm nor hydrocephalus was an independent predictor of emergent surgical intervention. Univariate analysis did identify midline shift as a correlate of emergent intervention; however, on multivariate analysis, this factor became nonsignificant. This situation is likely because shift can be caused by large deep clots (which often are not evacuated) or by large superficial clots (which often are evacuated). Thus, the driving factor seems to be lobar position rather than mass effect. Regarding hydrocephalus, the explanation may relate to its definition in the context of this study. To ensure objectivity and uniformity, hydrocephalus was deemed to be present when pretransport imaging showed an Evans index 0.3. For elderly patients with significant brain atrophy, such a measurement may

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reflect chronic ex vacuo changes, rather than true posthemorrhagic hydrocephalus. Conversely, among younger patients with fuller brains at baseline, clinically significant hydrocephalus may occur when the Evans index remains within a supposedly normal range. However, the decision to perform ventriculostomy is typically driven by clinical status, and this may explain why GCS score was an independent predictor of intervention, whereas the radiographic suggestion of hydrocephalus was not.

Interpretations Beyond being potentially unnecessary, overtriage of patients to tertiary-care centers can have negative consequences. Unnecessary transfer can cause disruptions in patient care, displaces patients from family and home, and adds cost burden to health care. Transport also exposes patients to risks of transport, stresses patient support networks, and may disrupt critical resources at the tertiary-care center.4 An argument can be made for use of rightsize resources for care. Ground transport by ambulance has been shown to cost between $800 and $6160 and air ambulance by helicopter between $11,760 and $25,000.1,3,5,6 These costs are not always covered by insurance and patients can be left responsible for this fee.21 Transport of potentially avoidable transfer (PAT) patients, especially by helicopter, should be limited when possible. The most recent Cochrane adult major trauma guidelines state that evidence from 38 nonrandomized studies examining use of helicopter for transport is of “very low quality,” and that no composite estimate of benefit could be determined.22 Selection of appropriate patients for helicopter transport will become important as institutions and insurance companies face pressure to reduce health care spending. Appropriate transport triage has already been the subject of investigation for many other neurosurgical diagnoses. For patients with spontaneous SAH transferred to a tertiary-care center via helicopter, a GCS score of 15 at presentation predicted no emergent intervention, suggesting that ground transport would be safe for this population.5 Similarly, in the case of traumatic SAH with mild presenting deficit, neurosurgical intervention has been found to be rarely required. A recent study showed that none of the 67 patients transferred with traumatic SAH and presenting with a GCS score of 13e15 were found to require neurosurgical intervention.1 In another study of 300 patients transferred with mild TBI (GCS

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score 13e15) and intraparenchymal hemorrhage or SAH, none required neurosurgical intervention or experienced neurologic decline.2 In the pediatric population, only 19% of those transferred for neurosurgical care receive neurosurgical intervention, without any association between transport time and outcome.23 Broader studies of neurosurgical conditions have shown a significant population of patients who qualify as PATs: patients who are transferred but undergo no neurosurgical diagnostic test intervention or intensive monitoring. Studies have identified 2 dichotomous groups that qualify as PATs: patients who are stably good or stably bad.3,6 One study of 916 potentially emergent neurosurgical candidate patients3 identified that 20% of all transfers qualify as PATs and that this group comprises patients with innocuous injury (most often transferred for headache or trauma) and patients with irrecoverable damage (most often transferred for nontraumatic intracerebral hemorrhage). The study, which included 916 patients transferred to a tertiary neurosurgical facility, estimated that $1.46 million over 2 years was spent on the transport of these patients, who did not benefit from transfer. Before transfer, consultation with a neurosurgeon via telephone discussion or telemedicine may prove particularly helpful in the context of these patients with poor prognosis. Our experience with interfacility helicopter transfer of patients with solitary supratentorial sIPH supports the findings of the previous studies. Of the 107 patients evaluated by the neurosurgical service for this indication, only a few required neurosurgical intervention, with the remaining patients falling into the same dichotomous categories of stably good or stably bad. Helicopter transport can be helpful for certain patients, but they should be thoughtfully selected. We have seen that a low GCS score (3e8), and a superficial hemorrhage (lobar location vs. deep location) are pretransfer variables that are significantly associated with intervention. In addition, in our population, none of the patients older

REFERENCES 1. Gates M, Mallory G, Planchard R, Nothdurft G, Graffeo C, Atkinson J. Triage patterns of traumatic subarachnoid hemorrhage: is referral to a tertiary care center necessary? World Neurosurg. 2017;100: 417-423. 2. Ditty BJ, Omar NB, Foreman PM, Patel DM, Pritchard PR, Okor MO. The nonsurgical nature of patients with subarachnoid or intraparenchymal hemorrhage associated with mild traumatic brain injury. J Neurosurg. 2014;123:1-5. 3. Kuhn EN, Warmus BA, Davis MC, Oster RA, Guthrie BL. Identification and cost of potentially avoidable transfers to a tertiary care neurosurgery service: a pilot study. Neurosurgery. 2016;79: 541-548. 4. Sequeira D, Martin-Gill C, Kesinger MR, Thompson LR, Jovin TG, Massaro LM, et al. Characterizing strokes and stroke mimics transported by helicopter emergency medical services. Prehosp Emerg Care. 2016;20:723-728.

than 80 years with basal ganglia hemorrhage or severe mass effect underwent any neurosurgical intervention during admission. These factors can easily be assessed by a referring physician and may guide patient selection for expedited transfer. In the future, a large multi-institutional prospective study using the studied specific criteria is necessary to validate the usefulness of these factors for triage, but for now, these factors may provide a basis for evaluating transfers of spontaneous intracerebral hemorrhage. Generalizability Our cohort of patients was drawn from a single tertiary-care center situated in a rural region. The availability of helicopter transport and transport distances and times are unique to our health care system and our findings are therefore less generalizable. Our triage and treatment algorithms are consistent with the standard of care for intraparenchymal hemorrhage (we adhered to recommendations from the intracranial hemorrhage trials17,18) and therefore our operation rates are likely broadly applicable across institutions. CONCLUSIONS Determining which patients benefit from interfacility transfer by helicopter for emergent neurosurgical intervention is challenging, and evaluation of clinical and radiographic features associated with intervention can aid in guiding appropriate allocation of these resources. Two thirds of patients with sIPH did not undergo any surgical intervention during the first 24 hours of admission after interfacility helicopter transfer. Factors associated with urgent neurosurgical intervention included younger age, low GCS score, and presence of lobar hemorrhage. ACKNOWLEDGMENTS We would like to acknowledge Sebastian Rubino, M.D. for his help with identifying patients relevant to this study.

5. Hong J, Rubino S, Lollis SS. Prehospital Glasgow Coma Score predicts emergent intervention following helicopter transfer for spontaneous subarachnoid hemorrhage. World Neurosurg. 2016; 87:422-430. 6. Walcott BP, Coumans JV, Mian MK, Nahed BV, Kahle KT. Interfacility helicopter ambulance transport of neurosurgical patients: observations, utilization, and outcomes from a quaternary level care hospital. PLoS One. 2011;6:1-6. 7. New Hampshire Patient Care Protocols. Approved by the NH Medical Control Board January 2013. Available at: https://www.nh.gov/safety/divisions/ fstems/ems/advlifesup/documents/1NHPatientCare ProtocolsVersion7Final.pdf. Bureau of Emergency Medical Services 33 Hazen Drive Concord, NH 03305 603-223-4200 Copyright 2005, renewed 2007, 2009, 2011, 2013, New Hampshire Bureau of Emergency Medical Services. Accessed date: November 20, 2017. 8. Evans W. An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neur Psych. 1942;47:931-937.

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9. Conroy MB, Rodriguez SU, Kimmel SE, Kasner SE. Helicopter transfer offers a potential benefit to patients with acute stroke. Stroke. 1999; 30:2580-2584. 10. Silbergleit R, Scott PA, Lowell MJ, Silbergleit R. Cost-effectiveness of helicopter transport of stroke patients for thrombolysis. Acad Emerg Med. 2003; 10:966-972. 11. Svenson JE, O’Connor JE, Lindsay MB. Is air transport faster? A comparison of air versus ground transport times for interfacility transfers in a regional referral system. Air Med J. 2006;25: 170-172. 12. Lukovits TG, Von Iderstine SL, Brozen R, Pippy M, Goddeau RP, McDermott ML. Interhospital helicopter transport for stroke. Air Med J. 2013;32: 36-39. 13. Weyhenmeyer J, Guandique CF, Leibold A, Lehnert S, Parish J, Han W, et al. Effects of distance and transport method on intervention and mortality in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2018;128:490-498.

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14. Gupta R, Manuel M, Owada K, Dhungana S, Busby L, Glenn BA, et al. Severe hemiparesis as a prehospital tool to triage stroke severity: A pilot study to assess diagnostic accuracy and treatment times. J Neurointerv Surg. 2016;8:775-777. 15. Ishikawa K, Omori K, Takeuchi I, Jitsuiki K, Yoshizawa T, Ohsaka H, et al. A comparison between evacuation from the scene and interhospital transportation using a helicopter for subarachnoid hemorrhage. Am J Emerg Med. 2017;35:543-547. 16. Katz BS, Adeoye O, Sucharew H, Broderick JP, McMullan J, Khatri P, et al. Estimated impact of emergency medical service triage of stroke patients on comprehensive stroke centers: an urban population-based study. Stroke. 2017;48:2164-2170. 17. Cooper DJ, Rosenfeld J, Murray L, Arabi YM, Davies AR, D’Urso P, et al. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med. 2011;364:215-224. 18. Hutchinson PJ, Kolias AG, Timofeev IS, Corteen EA, Czosnyka M, Timothy J, et al. Trial of decompressive craniectomy for traumatic

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intracranial hypertension. N Engl J Med. 2016;375: 1119-1130. 19. Joseph B, Friese RS, Sadoun M, Aziz H, Kulvatunyou N, Pandit V, et al. The BIG (brain injury guidelines) project: defining the management of traumatic brain injury by acute care surgeons. J Trauma Acute Care Surg. 2014;76:965-969. 20. Capron GK, Voights MB, Moore HR, Wall DB. Not every trauma patient with a radiographic head injury requires transfer for neurosurgical evaluation: application of the brain injury guidelines to patients transferred to a level 1 trauma center. Am J Surg. 2017;214:1182-1185. 21. P. Eavis, Air Ambulancefile:///Users/scrabble/ Desktop/Dartmouth files/School work/Year 3.5/ NS/Hong projects/DHART/Protocols for transport.pdfs Offer a Lifeline, and Then a Sky-High Bill. New York Times. May 2015:1-5. Available at: https://www.nytimes.com/2015/05/06/business/ rescued-by-an-air-ambulance-but-stunned-at-thesky-high-bill.html?_r¼0. Accessed November 19, 2017.

22. Galvagno SM Jr, Thomas S, Stephens C, Floccare D, Stephens C, Beecher D, et al. Helicopter emergency medical services for adults with major trauma. Cochrane Database Syst Rev. 2015;3: CD009228. 23. Vedantam A, Hansen D, Briceño V, Moreno A, Ryan SL, Jea A. Interhospital transfer of pediatric neurosurgical patients. J Neurosurg Pediatr. 2016;18: 638-643. Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 16 May 2018; accepted 10 August 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.050 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.

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