Each year, an estimated 1.7 million people experience. Comprehensive Assessment of Isolated Traumatic Subarachnoid Hemorrhage

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1 JOURNAL OF NEUROTRAUMA 31:1 15 (April 1, 2014) ª Mary Ann Liebert, Inc. DOI: /neu Comprehensive Assessment of Isolated Traumatic Subarachnoid Hemorrhage Jonathan J. Lee, 1 David J. Segar, 1 and Wael F. Asaad 1 4 Abstract Recent studies have shown that isolated traumatic subarachnoid hemorrhage (tsah) in the setting of a high Glasgow Coma Scale (GCS) score (13 15) is a relatively less severe finding not likely to require operative neurosurgical intervention. This study sought to provide a more comprehensive assessment of isolated tsah among patients with any GCS score, and to expand the analysis to examine the potential need for aggressive medical, endovascular, or open surgical interventions in these patients. By undertaking a retrospective review of all patients admitted to our trauma center from , we identified 661 patients with isolated tsah. Only four patients (0.61%) underwent any sort of aggressive neurosurgical, medical, or endovascular intervention, regardless of GCS score. Most tsah patients without additional systemic injury were discharged home (68%), including 53% of patients with a GCS score of 3 8. However, older patients were more likely to be discharged to a rehabilitation facility ( p < 0.01). There were six (1.7%) in-hospital deaths, and five patients of these patients were older than 80 years old. We conclude that isolated tsah, regardless of admission GCS score, is a less severe intracranial injury that is highly unlikely to require aggressive operative, medical, or endovascular intervention, and is unlikely to be associated with major neurologic morbidity or mortality, except perhaps in elderly patients. Based upon our findings, we argue that impaired consciousness in the setting of isolated tsah should strongly compel a consideration of non-traumatic factors in the etiology of the altered neurological status. Key words: head injury; hospital transfer; subarachnoid hemorrhage; traumatic brain injury Introduction Each year, an estimated 1.7 million people experience traumatic brain injury (TBI) in the United States, resulting in 1.4 million emergency department (ED) visits, 275,000 hospitalizations, and 53,000 deaths. 1 The general incidence of TBI in developed countries is estimated to be about 200 per 100,000 per year, typically counting only hospital admissions, 2 and the yearly economic burden of these injuries is estimated to be a total of $76.5 billion in the United States. 3 Given these substantial figures, there has been increasing interest in the management of TBI over the past few decades. Much of this interest has focused on discriminating among different subtypes of TBI to improve triage and management specifically, which patients require admission to the intensive care unit (ICU), admission at all, follow-up brain imaging, or transfer from community hospitals to Level 1 or 2 trauma centers with specialized services Traumatic subarachnoid hemorrhage (tsah) is a common subtype of TBI. The advancement of computerized tomography (CT) scanning has improved the detection and classification of tsah. 12,13 Servadei and colleagues found that of 750 head injury patients, 41% showed evidence of tsah on admission CT scan. 14 Mattioli and colleagues found an incidence of tsah in 61% of 169 head-injured patients admitted to the ICU. 13 More recently, Holmes and colleagues found that tsah was the second most frequent TBI in patients visiting the ED for blunt head injury. 15 Although past studies have shown that the presence of tsah in addition to other traumatic findings on an admission head CT scan ( non-isolated tsah) portends a worse outcome, 14,16,17 more recent studies have focused on the notion that isolated tsah in the setting of a high Glasgow Coma Scale (GCS) score (GCS 13 15) portends relatively better outcomes, compared with other forms of intracranial injury. For example, Levy and colleagues reported that patients with mild isolated tsah were much more likely to be admitted to the ICU, yet had significantly shorter ICU length of stay (LOS), and had no significant differences in hospital LOS and mortality rate, compared with concussion patients. 18 Similarly, Quigley and colleagues concluded that patients with isolated tsah and a GCS score of 13 or higher, without other significant trauma or clinical deterioration, do not require routine follow-up brain imaging or ICU admission. 19 Several studies have found that patients with mild tsah are highly unlikely to undergo neurosurgical 1 Warren Alpert Medical School, Brown University, 3 Brown Institute for Brain Science, Providence, Rhode Island. 2 Department of Neurosurgery, 4 Norman Prince Neurosciences Institute, Rhode Island Hospital, Providence, Rhode Island. 1

2 2 LEE ET AL. intervention Consequently, the need to transfer patients with tsah from community medical facilities to specialized centers has been questioned. 6,21 23 However, these studies did not examine the possibility that patients with tsah might have required other intensive (i.e., non-neurosurgical) medical, or procedural interventions, and did not consider patients with a GCS score lower than 13. Given the accumulating evidence that mild (GCS 13 15) isolated tsah is unlikely to be of major clinical significance, one objective of the current study was to investigate if this notion holds true for isolated tsah patients with any GCS score. In other words, if tsah is indeed a less severe finding, why are some patients with isolated tsah admitted with lower GCS scores, and is isolated tsah in this setting a more severe form of brain injury? We examined the likelihood of neurosurgical intervention in these patients, and also recorded the use of angiography and incidence of endovascular procedures. In addition, we examined the use of aggressive medical therapies that might have reflected severe brain injury and thus would have warranted specialized care at a tertiary center. To understand why some patients might have required aggressive measures, we more closely reviewed those particular cases. More generally, we inquired whether patient outcomes from isolated tsah differed by age. Finally, we wished to examine the characteristics of tsah patients transferred from a referring treatment center to our ED versus tsah patients who were transported directly from the field. To investigate these issues, we conducted a review of all isolated tsah patients admitted to our Level 1 trauma center over a 10-year span, from Methods Patient population Using the trauma registry database, we retrospectively identified all patients admitted to the Rhode Island Hospital ED during the 10- year period of January 1, 2003, to December 31, We queried the database using the International Classification of Diseases, Ninth Revision (ICD-9) codes for traumatic head injuries (THIs) including extra-axial and intra-axial hemorrhages and skull fractures (ICD-9 800, 801, 803, 804, , 900, 907, 950, and 951). We included skull fractures because these are potential causes of indirect brain injury (e.g., depressed fractures impinging the brain, fractures across venous sinuses, and fractures through the carotid canal causing arterial injury). We then identified patients within this THI cohort who had only isolated tsah (i.e., without additional intracranial abnormalities) as our goal was to study the effect of this injury alone. Thus, all tsah patients in this study had isolated tsah. We identified tsah patients by either ICD-9 code only, Abbreviated Injury Scale (AIS) code only, or both. We excluded patients who did not have a GCS score recorded. When the AIS or ICD-9 codes were discordant, we reviewed the individual records to determine if the patient truly had isolated tsah. We excluded patients who had penetrating head injuries or were found to have more than just tsah upon further review of their records. We referred to this initial population as the tsah population throughout our study. Additionally, in order to compare the effect of tsah with the effect of other THIs, we excluded all tsah patients from the THI cohort to form a new population; we referred to this population as the THI tsah population throughout our study. We defined two subgroups of tsah patients: those with major systemic injuries and those without major systemic injuries. We defined tsah without major systemic injuries as those having tsah without severe extracranial injuries, (i.e., allowing only minor injuries in this group, such as non-multiple fractures of the distal extremities). To form this subgroup ( tsah-m ), we excluded patients who had the following ICD 9 codes: , , , , , , and Throughout this study, we referred to tsah patients with and without major systemic injuries as the tsah + m population and tsah m population, respectively. Covariates We reviewed medical records to determine the following patient demographics: age, sex, GCS score, Injury Severity Score (ISS), mechanism of injury (motor vehicle accident, fall, or other), blood alcohol level (BAL), hospital transfer from a referring facility, ICU admission, length of ICU and hospital stay (if applicable), and posthospital disposition. We categorized post-hospital disposition as discharged home, rehabilitation, hospice, or expired. We classified patients who left the hospital against medical advice or were transferred to the psychiatry department as having been discharged home. In addition, we classified patients who were discharged to a short-term hospital, skilled nursing facility, or intermediate care facility as having been discharged to rehabilitation. Among the tsah population, we reviewed medical records for neurosurgical operative interventions, specifically craniotomy, craniectomy, external ventricular drain (EVD) placement, or intracranial pressure (ICP) monitor placement. The use of noninvasive angiography also was reviewed, and patients undergoing endovascular procedures were identified. Further, we identified all patients in the tsah population who received hypertonic medications, specifically mannitol and/or hypertonic saline. In addition, we reviewed the medical records of patients who expired in the tsah-m population to determine the specific circumstances of their deaths. Lastly, among each study population, we extracted all patients who were transferred to the ED from a referring medical facility. We reviewed medical records to determine patient demographics for these groups. Statistical analysis Bootstrap tests were performed to assess the significance of observed differences across groups. To compare the means of different groups, the group assignment of the individual values were randomly shuffled 10,000 times and the mean group differences were recalculated to produce a distribution of randomized values. The actual value could then be compared against this distribution to derive a p value. For a comparison of proportions within groups, a different bootstrap test was performed in which the likelihood (again, over 10,000 iterations) of producing the observed (or more extreme) numbers of group members was empirically determined using the actually-observed ratios and the exact number of group members. These bootstrap-permutation tests have an important advantage over parametric tests in that they do not assume the underlying distributions to be gaussian or even unimodal. A p value < 0.01 was considered significant in all cases. All statistical analyses were performed in MATLAB (Mathworks, Natick, MA). Results We identified 7,568 patients with THI by the initial trauma registry query. A flow chart depicting the subsequent process through which we applied the inclusion and exclusion criteria to this population to isolate the tsah population is shown in Figure 1. We identified 661 (8.7%) patients with isolated tsah (i.e., patients with tsah but no other abnormal intracranial findings on CT scan). According to the data systems case definition of traumatic brain injury 24 issued by the U.S. Centers for Disease Control and Prevention, (ICD-9 800, 801, 803, 804, and ), our THI cohort included 7,455 TBI patients (98.5% of the total THI cohort). Of

3 TRAUMATIC SUBARACHNOID HEMORRHAGE 3 FIG. 1. Flow chart showing study inclusion and exclusion criteria. tsah, traumatic subarachnoid hemorrhage; AIS, Abbreviated Injury Scale; ICD-9, International Statistical Classification of Diseases, Ninth Revision; GCS, Glasgow Coma Scale. these, 8.9% of patients had isolated tsah. Within the tsah population (n = 661), we identified one patient by AIS code only, and three patients by ICD 9 code only. Excluded from this tsah population were 69 patients who did not have a GCS score recorded, three patients who had penetrating head injuries, and 13 patients who were found to have additional intracranial injuries upon further review of their records and initial imaging studies. We subtracted all 661 tsah patients from the THI cohort (n = 7,568) to identify 6,907 THI patients without tsah (THI tsah). In addition, we identified two subgroups of patients within the tsah population (n = 661): 311 patients who had tsah with major systemic injuries (tsah + m), and 350 patients who had tsah without major systemic injuries (tsah m). Demographics Table 1 summarizes patient demographics for the THI cohort, the tsah population, and the THI tsah, tsah + m and tsah m sub-populations. There were significant demographic differences between these three groups. The tsah populations were significantly older (tsah m vs. THI tsah, p < ; tsah + m vs. THI tsah, p < ) and were more equally distributed among

4 4 LEE ET AL. Table 1. Patient Demographics* tsah-m (n = 350) tsah + m (n = 311) THI-tSAH (n = 6,907) tsah (n = 661) THI cohort (n = 7,568) Mean age 62.8{ 57.2x 46.8{x Male 49% (173){ 54% (167)x 65% (4,489){x 51% (340) 64% (4,829) Admission GCS score** % (15){{ 13% (41){x 20% (1,241){x 8.5% (56) 19% (1,297) % (10){ 8.0% (25){ 6.4% (390) 5.3% (35) 6.3% (425) % (325){{ 79% (245){ 73% (4,447){ 86% (570) 74% (5,017) Mean 14.3{{ 13.1{x 12.3{x ISS** < 10 72% (253){{ 24% (76){ 28% (1,915){ 50% (329) 30% (2,244) % (97){{ 62% (192){x 50% (3,470){ 44% (289) 50% (3,759) > 24 0{ 14% (43)x 22% (1,502){x 6.5% (43) 21% (1,545) Mean 7.4{{ 16.4{ 16.6{ Mechanism of injury MVA 9.4% (33){{ 25% (77){ 21% (1,446){ 17% (110) 21% (1,556) Fall 73% (256){{ 48% (149){ 51% (3,508){ 61% (405) 52% (3,913) Other 17% (61){{ 27% (85){ 28% (1,953){ 22% (146) 28% (2,099) ICU admission 21% (72){{ 48% (150){x 39% (2,664){x 34% (222) 38% (2,886) Mean ICU days 0.81{{ 3.7{x 2.6{x Mean LOS 3.9{{ 10.5{ 8.6{ Post-hospital disposition** Discharge home 68% (237){ 52% (163){x 62% (4,274)x 61% (400) 62% (4,674) Rehabilitation 30% (105){ 38% (119){ 25% (1,718) 34% (224) 26% (1,942) Hospice 0.57% (2) 1.3% (4) 0.61% (42) 0.91% (6) 0.64% (48) Expired 1.7 (6){{ 8.0% (25){ 12% (853){ 4.7% (31) 12% (884) *Percentages may not sum to 100% due to rounding. {Significant difference between tsah-m and tsah + m populations: p < 0.01, bootstrap tests. {Significant difference between tsah-m and THI-tSAH populations; p < 0.01, bootstrap tests. xsignificant difference between tsah + m and THI-tSAH populations; p < 0.01, bootstrap tests. **Eight hundred twenty-nine THI and THI-tSAH patients did not have a GCS score recorded; percentages are out of 6,739 and 6,078, respectively. Twenty THI and THI-tSAH patients did not have an ISS recorded; percentages are out of 7,548 and 6,887, respectively. Twenty THI and THI-tSAH patients did not have a post-hospital disposition recorded; percentages are out of 7,548 and 6,887, respectively. tsah-m, traumatic subarachnoid hemorrhage without major systemic injuries; tsah + m, traumatic subarachnoid hemorrhage with major systemic injuries; THI-tSAH, traumatic head injury without traumatic subarachnoid hemorrhage; GCS, Glasgow Coma Scale; ISS, Injury Severity Score; MVA, motor vehicle accident; ICU, intensive care unit; LOS, length of stay. men and women (tsah m vs. THI tsah, p < ; tsah + m vs. THI tsah, p < ) than the THI tsah population. The tsah m population had a significantly greater proportion of patients who experienced falls (tsah m vs. THI tsah, p < ; tsah m vs. tsah + m, p < ), had a greater number of hospital transfers (tsah m vs. THI tsah, p < ; tsah m vs. tsah + m, p < ), had a lower rate of ICU admission (tsah m vs. THI tsah, p < ; tsah m vs. tsah + m, p < ), and had a lower mean ICU and hospital LOS (tsah m vs. THI tsah, p < ; tsah m vs. tsah + m, p < ) than both the THI tsah and tsah + m populations. Overall, there were 72 ICU admissions for tsah m patients; patients with mild tsah (GCS score of 13 15) accounted for 56 of these (78% of all ICU admissions for this population), resulting in a 17% overall ICU admission rate for mild tsah m patients. A smaller proportion of patients in the tsah m population were intoxicated than the tsah + m population ( p = ). GCS Scores The tsah m population had a significantly higher mean GCS score (tsah m vs. THI tsah, p < ; tsah m vs. tsah + m, p = ), a lower proportion of patients with low GCS scores (GCS 3 8, tsah m vs. THI tsah, p < ; GCS 3 8, tsah m vs. tsah + m, p < ), and a higher proportion of patients with high GCS scores (GCS 9 12, tsah m vs. THI tsah, p < ; GCS 9 12, tsah m vs. tsah + m, p < ; Fig. 2) than both the THI tsah and tsah + m populations. Figure 3 plots the distribution of ISSs among these groups, showing the expected differences between the tsah-m group and the other two groups, reflecting the selection criteria used to define these populations (ISS < 10, tsah m vs. THI tsah, p < ; ISS < 10, tsah m vs. tsah + m, p < ; ISS 10 24, tsah m vs. THI tsah, p < ; ISS 10 24, tsah m vs. tsah + m, p < ). When we analyzed GCS scores among all tsah patients (n = 661) by age, we found significant differences between age groups in the proportions of patients with GCS scores of 13 or higher and patients with lower GCS scores. We found that 19- to 39-year-olds had a lower proportion of patients with GCS scores of (73/108, 68%) than both 40- to 79-year-olds (279/316, 88%) and 80- to 100-year-olds (181/192, 94%; GCS 9 12, 19- to 39-yearolds vs. 40- to 79-year-olds, p < ; GCS 9 12, 19- to 39-yearolds vs. 80- to 100-year-olds, p < ; Fig. 4); a comparison between 19- to 39-year-olds and 0- to 18-year-olds did not reach significance (GCS 9 12, 19- to 39-year-olds vs. 0- to 18-year-olds, p = ). We also found that patients ages 19 to 39 were more likely to have lower GCS scores than 40- to 79-year-olds (GCS 3 8, p = ); comparisons between 19- to 39-year-olds and 0- to 18- year-olds and 80- to 100-year-olds did not reach significance (GCS 3 8, 19- to 39-year-olds vs. 0- to 18-year-olds, p = ; GCS

5 TRAUMATIC SUBARACHNOID HEMORRHAGE 5 FIG. 2. Bar graphs depicting (A) Glasgow Coma Scale (GCS) scores among the traumatic head injury without traumatic subarachnoid hemorrhage (THI-tSAH) population (n = 6,907); (B) tsah with major systemic injuries population (n = 311); and (C) tsah without major systemic injuries population (n = 350). Bar graphs were scaled to compare the relative proportions of GCS scores. 829 THI-tSAH patients did not have a GCS score recorded; percentages are out of 6,078.

6 6 LEE ET AL. FIG. 3. Bar graphs depicting (A) Injury Severity Scores (ISSs) among the traumatic head injury without traumatic subarachnoid hemorrhage (THI-tSAH) population (n = 6,907); (B) tsah with major systemic injuries population (n = 311); and (C) tsah without major systemic injuries population (n = 350). Bar graphs were scaled to compare the relative proportions of ISSs. 3 8, 19- to 39-year-olds vs. 80-to 100-year-olds, p = ). We hypothesized that the lower incidence of high GCS scores in 19- to 39-year-olds could be due to a higher prevalence of major systemic injury in these patients, requiring sedation or intubation and/or higher rates of intoxication in these patients. Indeed, we found that a higher proportion of patients ages 19 to 39 had an ISS of less than 24 (ISS > 24, 19- to 39-year-olds vs. 0- to 18-year-olds, p = 0.001; ISS > 24, 19- to 39-year-olds vs. 40- to 79-year-olds, p = ), although a comparison between 19- to 39-year-olds and 80- to 100- year-olds did not reach significance (ISS > 24, 19- to 39-year-olds

7 TRAUMATIC SUBARACHNOID HEMORRHAGE 7 FIG. 4. Bar graphs demonstrating Glasgow coma scale (GCS) score distribution among all traumatic subarachnoid hemorrhage patients (n = 661): (A) 0 18 years of age; (B) years of age; (C) years of age; and (D) years of age. Bar graphs were scaled to compare the relative proportions of GCS scores. vs. 80- to 100-year-olds, p = ). In addition, we found that tsah-m patients in this age group were less likely to have low GCS scores (GCS 3 8, tsah m vs. tsah + m, p < ), compared with tsah + m patients. Further, patients in this age group were more likely to be intoxicated (intoxicated patients, 19- to 39-year olds vs. 0- to 18-year-olds: p < ; 19- to 39-year-olds vs. 40- to 79-year-olds, p < ; Fig. 5); the comparison between 19- to 39-year-olds and 80- to 100-year-olds was not significant (intoxicated patients, 19- to 39-year-olds vs. 80- to 100-year-olds, p = ). These findings are consistent with the notion that the greater prevalence of apparent neurologic impairment (GCS 3 8) in this age group was not necessarily related to traumatic brain injury (isolated tsah). Use of non-invasive angiography In the tsah-m sub-group, 10 of 350 patients (2.9%) underwent non-invasive angiography (CT-angiogram or magnetic resonance [MR]-angiogram) to rule out a potential aneurysmal source for the SAH, while only five of 311 patients (1.6%) in the tsah + m group had neuro-vascular imaging. In only two cases was an aneurysm discovered, and one was likely incidental as it was not clearly FIG. 5. Graph showing the percent of intoxicated patients by age among all traumatic subarachnoid hemorrhage patients (n = 661). The vertical axis depicts the percent of intoxicated patients (blood alcohol level 0.08 g/100 ml) in each age range.

8 8 LEE ET AL. Table 2A. Aggressive Procedural Interventions Among All tsah Patients (n = 661) All isolated tsah (n = 661) GCS score 3 8 (n = 56) GCS score 9 12 (n = 35) GCS score (n = 570) ISS < 10 (n = 329) ISS (n = 289) ISS > 24 (n = 43) Craniotomy Craniectomy EVD placement 0.15% (1) 1.8% (1) % (1) 0 ICP monitor placement 0.15% (1) 1.8% (1) % (1) 0 Endovascular intervention* 0.15% (1) 0 2.9% (1) % (1) 0 0 Total 0.45% (3) 3.6% (2) 2.9% (1) % (1) 0.69% (2) 0 *Figure 7 shows a head CT scan of this patient. tsah, traumatic subarachnoid hemorrhage; GCS, Glasgow Coma Scale; ISS, Injury Severity Score; EVD, external ventricular drain; ICP, intracranial pressure. Table 2B. Aggressive Medical Interventions Among all tsah Patients (n = 644)* All isolated tsah (n = 644) GCS score 3 8 (n = 55) GCS score 9 12 (n = 34) GCS score (n = 555) ISS < 10 (n = 324) ISS (n = 277) ISS > 24 (n = 43) 3% Hypertonic saline 0.16% (1) 1.8% (1) % (1) 0 Mannitol 0.31% (2) 3.6% (2) % (2) 0 Total 0.47% (3) 5.4% (3) % (3) 0 *Seventeen patient records contained no confirmation of medical intervention incidence; percentages are out of 644. Overall, there were 4 patients who received aggressive neurosurgical, endovascular, or medical interventions; 1 patient who received an external ventricular drain placement was given both 3% hypertonic saline and mannitol. tsah, traumatic subarachnoid hemorrhage; GCS, Glasgow Coma Scale; ISS, Injury Severity Score. related to the distribution of the SAH. One patient without evidence of aneurysm underwent an additional CT-angiogram to assess for vasospasm (see below). Aggressive operative, endovascular, and medical interventions Table 2A and Table 2B detail aggressive neurosurgical, endovascular, and medical interventions among all tsah patients (n = 661). Two patients underwent a neurosurgical operative intervention (0.30%). No patients underwent a craniotomy or craniectomy. One patient underwent EVD placement (0.15%), and one other patient underwent ICP monitor placement (0.15%). One patient (0.15%) underwent an endovascular procedure to treat symptomatic vasospasm. Additionally, there was one recorded use of hypertonic saline (0.16%) and two recorded uses of mannitol (0.31%). In total, four patients (0.61%) who underwent any of these procedures or received hypertonic medications, as certain patients underwent more than one aggressive intervention. If, as we have been arguing, isolated tsah is a generally less severe category of intracranial injury, why would four patients have required aggressive surgical, endovascular or medical intervention? To more closely investigate this, we describe here the specific details of the four patients who underwent these procedures: Case 1: Neurosurgical intervention/evd placement. A 51-year-old woman with a history of hypertension and diabetes mellitus presented to the ED after a motorcycle accident. The patient was helmeted and experienced loss of consciousness at the time of the accident. Her arrival GCS score was 7 and her ISS was 11. In addition to her head injury, she presented with an eye laceration, a dilated, unreactive ( blown ) pupil and external facial trauma. While her initial CT report was pending, the patient was empirically given mannitol and 3% hypertonic saline. The first head CT scan showed diffuse SAH without any other intracranial abnormality. However, given the mechanism of injury, there was a concern for diffuse axonal injury (DAI) that was suggested but not definitively identified on CT. An EVD was placed in the ED. She was admitted to the neurosurgical service and taken to the neuro- ICU. Hyperosmolar therapy for cerebral edema, including mannitol and 3% hypertonic saline, was administered on a daily basis to control her ICP, which spiked transiently as high as 47 mm H 2 O; at each instance, the hyperosmolar therapy was effective at reducing the ICP to normal levels. An ophthalmology consult ascribed her abnormal pupillary exam to iris sphincter injury. On Day 12, the EVD was discontinued and the patient was transferred to a general floor. The patient was discharged to a rehabilitation facility on Day 39. Upon discharge, she was minimally verbal and unable to follow commands. Case 2: Neurosurgical intervention/icp monitor placement. A 14-year-old male presented to the ED after a motorcycle accident, resulting in a loss of consciousness. He was noted to have seizure activity as well as vomiting during transport. His arrival GCS score was 8 and his ISS was 11. He was intubated upon arrival to the ED. His initial CT showed trace SAH with no other intracranial abnormalities. A cervical spine CT showed a non-displaced facet fracture. While still in the trauma bay, he continued to have seizure activity and emesis, and his mental status was reported to deteriorate. The patient was started on anti-seizure medication and transported to the pediatric ICU (PICU) where an ICP monitor was placed on Day 2. This was discontinued the next day. The patient s mental status improved, leading to his transfer out of the PICU to a general pediatric floor on Day 5. The patient was discharged home on Day 6 without apparent neurological sequelae. Case 3: Endovascular intervention/intra-arterial treatment of vasospasm. A 56-year-old woman with morbid obesity, newly diagnosed breast cancer, and a history of deep venous thrombosis and pulmonary embolism, for which she was on

9 TRAUMATIC SUBARACHNOID HEMORRHAGE 9 FIG. 6. Axial computed tomography scan of the 56-year-old female who underwent endovascular procedure for right middle cerebral artery vasospasm. warfarin, presented to the ED after a fall from standing. She was unresponsive in the field according to the emergency medical service report, and was intubated prior to transport. Her initial GCS upon presentation was 11T. A CT demonstrated SAH in the right Sylvian fissure (Fig. 6). CT-angiogram, MR-angiogram, and direct catheter angiogram were all negative for an aneurysmal source. She had been kept intubated despite an improving neurologic exam until the catheter angiogram had been completed; she was extubated on hospital day 3. She then developed left side weakness responsive to induced hypertension and doppler plus radiographic evidence of right middle cerebral artery vasospasm on Day 7. She was started on oral nimodipine and underwent intra-arterial treatment for vasospasm with nicardipine, resulting in both radiographic and clinical benefit, though later imaging revealed a small lenticulostriate infarct. She was ultimately discharged to rehabilitation on Day 27, with residual mild left facial and upper extremity weakness. Case 4: Aggressive medical intervention/hypertonic fluid administration. A 28 year-old female without significant past medical history was transferred from a referring hospital after a sustaining injury in a roll-over motor vehicle accident. Per report, she had been awake and combative, with a GCS score of 14 at the referring facility; she was sedated and intubated there to prevent secondary injury. Upon arrival here, her GCS was 10T, and her right pupil was noted to be 7 mm in diameter and unreactive to light. She was empirically given mannitol until a CT scan was obtained, which revealed only isolated tsah and no evidence of mid-brain compression. An ophthalmology consult later determined her blown pupil to be a result of traumatic third nerve injury. She was extubated on Day 2 and discharged to home on Day 3. Post-hospital disposition Unsurprisingly, as shown in Table 1, the tsah m population had a greater proportion of patients who were discharged home than the tsah + m population ( p < ) and a lower proportion of expired patients than both the THI tsah and tsah + m population (tsah-m vs. THI-tSAH, p < ; tsah-m vs. tsah + m, p = ). Among the 350 tsah-m patients, most patients were discharged home (237; 68%), 105 patients (30%) were discharged to rehabilitation, two patients (0.57%) were discharged to a hospice, and six patients (1.7%) expired (Table 3). As expected, the majority of patients with GCS scores of were discharged home (221/ 325, 68%). Yet, even the majority of patients with GCS scores of 3 8 (8/15, 53%) and GCS 9 12 (8/10, 80%) were ultimately discharged home. Note that one patient was transferred to the psychiatry service and four patients left against medical advice; these patients were grouped with those discharged home. We analyzed post-hospital disposition by age among the tsah m population. Among 0 18, 19 39, and year-olds, the majority of patients were discharged home (97%, 86%, and 75%, respectively). Among year olds, 50% of patients were discharged to rehabilitation, and a slightly smaller proportion of patients were discharged home (44%). In general, the proportion of patients discharged to rehabilitation increased by age group (Fig. 7).

10 10 LEE ET AL. Table 3. Post-Hospital Disposition Among tsah Patients Without Major Systemic Injuries* Discharged home Rehabilitation Hospice Expired Total Total 68% (237) 30% (105) 0.57% (2) 1.7% (6) 350 Admission GCS score % (8) 33% (5) 0 13% (2) % (8) 20% (2) % (221) 30% (98) 0.62% (2) 1.2% (4) 325 ISS < 10 64% (163) 34% (85) 0.79% (2) 1.2% (3) % (74) 21% (20) 0 3.1% (3) 97 > *Percentages may not sum to 100% due to rounding. tsah, traumatic subarachnoid hemorrhage; GCS, Glasgow Coma Scale; ISS, Injury Severity Score. Mortality There were six in-hospital deaths in the tsah-m subgroup, yielding a mortality rate of 1.7%. Table 4 provides details on these expired patients. The patients who died were 35, 82, 84, 86, 94, and 99 years old. Two patients had admission GCS scores of 7 or lower and four patients had GCS scores of 14 or higher; all patients experienced falls. Of these, four patients were made comfort measures only (CMO) by their families, and two died os cardiac arrest. There were 122 of 350 patients in the tsah m population who were 80 or older, resulting in a mortality rate of 4.1% (n = 5) in this age group. Further, two patients 80 or older (0.57%) were discharged to hospice. The overall peri-hospital mortality rate for tsah-m in patients 80 or older therefore was 5.7% (7/122). Hospital Transfers Given the observation that tsah was associated with predominantly good outcomes with minimal specialist intervention, we wondered if patients transferred from referring medical facilities were more likely to be severely injured than patients who were not. Table 5 outlines demographics of tsah-m patients who were transferred to our ED from referring treatment centers and tsah-m patients who were brought to our ED directly from the field. We found that transferred tsah-m patients showed little difference in demographic proportions relating to sex, admission GCS score, intoxication rates, ICU admission, and ICU and hospital LOS. The only statistically significant differences we found between these populations were that transferred tsah-m patients overall were older ( p = ), more likely to have low ISSs (ISS < 10, p = ), less likely to have high ISSs (ISS 10 24, p = ), and more likely to have experienced falls than tsah-m patients brought directly from the field (motor vehicle accidents, p = ; falls, p < ; other, p < ). Among patients in the tsah-m population who were transferred to the ED from a referring treatment center, most patients were either discharged home (132/201, 66%) or were sent to rehabilitation (65/201, 32%). The lower ISSs among transferred patients is consistent with appropriate field triage of more severely injured patients directly to higher-level trauma centers. Discussion Too often, any sort of traumatic intracranial hemorrhage is referred to simply as a head bleed by non-specialists involved in the initial care of these patients. Meanwhile, specialists such as neurosurgeons and neurologists learn from extensive experience that different categories of intracranial hemorrhage are associated with different clinical pictures and generally different outcomes. In this retrospective study of a large consecutive cohort of head-injured patients, we sought to characterize in detail a single type of injury, traumatic SAH without additional intracranial injury ( isolated tsah). We presented evidence that isolated tsah, on its own, is unlikely to be a cause of significant neurologic morbidity or mortality. FIG. 7. Graph demonstrating post-hospital disposition among traumatic subarachnoid hemorrhage (tsah) patients without major systemic injuries (tsah-m; n = 350) distributed by age.

11 TRAUMATIC SUBARACHNOID HEMORRHAGE 11 Table 4. Deaths Among tsah Patients Without Major Systemic Injuries Age Admission GCS score ISS Mechanism of injury Mechanism of death Other injuries Comorbidities Patient Fall Cardiac arrest Open wound of scalp Alcoholism Patient Fall CMO by family Open wound of forehead COPD, rheumatic heart disease, HTN, CAD Patient Fall CMO by family None HTN, CAD, pneumonectomy, diverticulitis Patient Fall CMO by family Open wound of scalp HTN Patient Fall CMO by family Abrasion to ear HTN, atrial fibrillation Patient Fall Cardiac arrest Skin abrasion to leg, face laceration CAD, HTN, seizures, TIA, squamous cell carcinoma tsah, traumatic subarachnoid hemorrhage; GSC, Glasgow Coma Scale; ISS, Injury Severity Score; CMO, comfort measures only; COPD, chronic obstructive pulmonary disease; HTN, hypertension; CAD, coronary artery disease; TIA, transient ischemic attack. The outcomes of patients with low GCS scores ( < 13) had not been assessed in previous studies. Here, only 7% of patients with isolated tsah without major systemic injury (tsah-m) had GCS scores lower than 13, whereas 21% of patients with isolated tsah with major systemic injury (tsah + m) had GCS scores lower than Table 5. Patient Demographics Among tsah Patients Without Major Systemic Injuries According to Transfer Status* tsah-m transferred from referring facility (n = 201) tsah-m brought directly from field (n = 149) Mean age 66.4{ 58.0{ Male 48% (96) 52% (77) Admission GCS score % (10) 3.4% (5) % (4) 4.0% (6) % (187) 93% (138) Mean ISS < 10 78% (156){ 65% (97){ % (45){ 35% (52){ > Mean Mechanism of injury MVA 6.0% (12){ 14% (21){ Fall 83% (167){ 60% (89){ Other 11% (22){ 26% (39){ Intoxication (BAL 12% (24) 18% (27) 7emsp; 0.08 g/100 ml) ICU admission 23% (47) 17% (25) Mean ICU days Mean LOS Post-hospital disposition Discharge home 66% (132) 70% (105) Rehabilitation 32% (65) 27% (40) Hospice 1.0% (2) 0 Expired 1.0% (2) 2.7% (4) *Percentages may not sum to 100% due to rounding. {Significant difference between populations; p < 0.01, bootstrap tests. tsah-m, traumatic subarachnoid hemorrhage without major systemic injuries; GSC, Glasgow Coma Scale; ISS, Injury Severity Score; MVA, motor vehicle accident; BAL, blood alcohol level; ICU, intensive care unit; LOS, length of stay. 13. One might attribute this difference to more severe forms of tsah in the tsah + m group (e.g., multi-focal or multi-lobar). However, we found that most patients with GCS scores lower than 13 were ultimately discharged to home, even including those with GCS scores of 3 8. If they had experienced neurologic morbidity as a result of brain injury, one would have expected more discharges to rehabilitation facilities. Most patients with low GCS scores were in the 19- to 39-year-old age group; this group had higher ISSs and the highest incidence of alcohol intoxication. Therefore, chemical intoxication (either self-administered or provided by firstresponders in the setting of major systemic injury) likely contributed to these lower admission GCS scores. These results suggest that poor neurologic status in a patient with only tsah on brain imaging should motivate careful consideration of non-traumatic causes. Only two of 661 tsah patients (0.3%) underwent neurosurgical operative intervention (placement of a intraparenchymal ICP monitor in one case, placement of an EVD in the other), and by the particular history of these cases, one of these two interventions was of questionable value (the patient s exam was limited by seizures, and the ICP monitor was discontinued after just one day). Only one patient in the tsah group (0.15%) was diagnosed with vasospasm and underwent an endovascular procedure. Likewise, very few patients received aggressive medical intervention in the form of hyperosmolar therapy (3/644, 0.47%), and two of these were cases in which this was done empirically (based upon initial clinical exam prior to brain imaging), and were ultimately of questionable value. Therefore, of the four patients who required aggressive intervention, only two (2/661 or 0.3%; one with DAI and high ICP spikes, the other with Sylvian tsah and vasospasm) clearly needed it. All of these patients were admitted with a GCS score lower than 13; so even among this group, the necessary intervention rate was only 2.3% (two of 89 patients with GCS scores of 3 12). These few cases with aggressive intervention highlight some potential pitfalls in the management of TBI. For example, a dilated and unreactive ( blown ) pupil may result from trauma to the cranial nerve III or to the eye itself, and so could incorrectly be attributed to brainstem compression (e.g., Cases #1 and #4). This is especially true when the neurological exam is hindered by sedation and/or paralytics. Likewise, an ictal or post-ictal state can alter exam findings, lowering a patient s apparent GCS score, thereby potentially leading to aggressive interventions such as placement of an intracranial pressure monitor (e.g., Case #2). These few cases also highlight rare but potentially significant delayed consequences of tsah. DAI is difficult to detect on brain CT, 25,26 and so this form of potentially severe injury may be present

12 12 LEE ET AL. in patients diagnosed as having only tsah by CT scan (e.g., Case #1). Further, in rare cases, tsah can lead to symptomatic vasospasm (e.g., Case #3). Therefore, delayed neurologic deterioration of patients with tsah should prompt consideration of these etiologies, and appropriate diagnostic tests should be performed (e.g., magnetic resonance imaging to assess for DAI; transcranial doppler or CT/MR catheter-angiogram for vasospasm). A possible exception to the general notion that isolated tsah is typically a benign condition is the relatively high mortality rate for tsah-m patients 80 or older (5.7%), and the increased likelihood of discharge to rehabilitation (50% vs. 2 to 25% for other age groups); this conforms to the generally higher rate of morbidity and mortality in elderly patients with TBI However, most of our elderly tsah patients were admitted with a high GCS score ( 14), again suggesting that neurological injury may not have been a prominent factor in the overall condition. Instead, just as hip fractures in the elderly have been associated with a high mortality despite their non life-threatening nature, 30 tsah in this population might be regarded as an indicator of generally declining health, leading to falls and other forms of minor injury and ultimately perhaps leading to family discussions regarding the overall goals of care. Indeed, 6/7 of these elderly patients were made CMO or discharged to hospice. Alternatively, differences in outcomes among elderly patients might be attributed to varying quality of care for patients across age groups. For example, one study found that increased morbidity and mortality among elderly patients with cerebral contusions may have stemmed at least in part from a lower likelihood of transfer to acute care facilities, as well as slower and less experienced care. 31 In our study, patients transferred from outside facilities tended to be older than those brought directly from the field; however, the significance of this finding is unclear, because it may arise from inappropriate initial triage from the field to those outside facilities, the need to transfer these patients from those facilities to our tertiary care center based upon medical comorbidities, or possibly even systemic factors unrelated to medical need, such as insurance status. 32 In any case, the lack of required specialist intervention for tsah and the circumstances under which elderly patients experienced mortality suggest that higher rates of morbidity and mortality are likely influenced by non-neurological factors, even in the setting of possible differences in care patterns. Despite the generally favorable prognosis of isolated tsah, more than half (57%) of all patients seen at our institution for this condition, even among those without additional major systemic injury (tsah-m), were transferred from a referring medical facility. The benefits of such transfers are unclear given the rare need for specialist intervention for this type of injury. Systemically, the costs of transfer and the additional burden placed on already crowded Level 1 and 2 trauma centers may be difficult to justify. Whether such patients, especially those with high GCS scores, benefit from hospital admission is uncertain. At our facility, those who are able and wish to be discharged home directly from the ED are allowed to do so after a short (6 8 h) period of observation, as long as isolated tsah is the only non-superficial injury. Some facilities routinely monitor such patients over a 23-hour observation period and yet others will admit all such patients, including by protocol, to an ICU. 19 Certainly, those of advanced age may require placement at a rehabilitation facility (see Fig. 7) and so admission is clearly warranted in such cases, though again, this is not necessarily a sequelum of neurological injury per se. Because this study considered only the index hospital admission and discharge status, it is blind to the possibility that some of these tsah patients could have been readmitted with or otherwise discovered to have previously unobserved intracranial injuries, such as delayed subdural hematomas or contusions. In that case, it may be that tsah might provide an early indicator of other potentially more severe forms of intracranial injury. Nevertheless, such findings would not alter the lack of need for high-level specialized care, at least in the short term. This possibility does, however, suggest that clinical follow-up to monitor for the appearance of new or worsening symptoms, such as worsening headache or new neurologic deficit, is prudent. Prior studies have examined the clinical significance of isolated tsah with similar results. Quigley and colleagues 19 reviewed 478 patients with isolated tsah and GCS scores of 13 15, finding that none required operative intervention. Likewise, Levy and colleagues 18 reported on 117 tsah patients with GCS scores of and found that none required operative intervention. More recently, Borczuk and colleagues. 20 found that of 75 isolated tsah patients with GCS scores of 13 15, only one exhibited a deterioration, which was non-neurological in nature. None of these studies reported on the use of aggressive medical interventions, such as mannitol or hypertonic saline, and none considered endovascular intervention. We found that none of our tsah patients admitted with GCS scores of required any of these forms of aggressive intervention. Interestingly, all 478 tsah patients in the Quigley and colleagues study and 47% of tsah patients in the Levy and colleagues study were admitted to the ICU, compared with 17% in our analogous tsah cohort (tsah-m, GCS 13 15). This highlights a striking lack of consensus across institutions in the management of isolated tsah. The value of scheduled repeat head imaging, regardless of changes in neurologic status, has been increasingly controversial. The rationale for this practice has been a concern that traumatic intracranial hemorrhages might progress radiographically prior to changes in the neurological exam, thereby allowing earlier intervention in such cases. 9 Consistent with this line of thinking, our institution repeated head CTs on all patients who showed findings on initial CTs during the years examined in this study. However, studies examining the value of scheduled repeat head CTs have not always differentiated between different forms of intracranial hemorrhage and are too often underpowered to detect differences across these groups. 8,33,34 One recent study reviewed 1,019 patients with all forms of traumatic intracranial hemorrhage, but lumped tsah with other extra-axial hemorrhages (subdural and epidural) for comparison against intra-axial (intraparenchymal) hemorrhage; they found that the likelihood of a worsened repeat CT scan was not different between these two groups. 10 Given their observed incidence of worsening subsequent head CTs, and the procedures triggered by these radiographic changes, they recommended continued use of routine scheduled repeat head CTs for all patients with traumatic intracranial hemorrhage, regardless of subtype. Unfortunately, the use of a heterogeneous extra-axial group that included tsah likely obscured real differences in the natural history of these lesions. We instead argue that given the generally favorable outcomes of isolated tsah, scheduled repeat head CTs are not necessary in this condition, particularly for patients with GCS scores of The typical management of tsah differs significantly from that of spontaneous (i.e., aneurysmal) SAH (ssah). A major concern with ssah, which usually occurs in or near the basal cisterns or major fissures, is vasospasm and the ensuing risk for stroke; treatment of ssah therefore is geared heavily towards recognizing

13 TRAUMATIC SUBARACHNOID HEMORRHAGE 13 and treating vasospasm aggressively. Meanwhile, vasospasm generally is not a prominent concern in the management of tsah, despite evidence it might be at least as common in this condition. 35,36 However, unlike in ssah, oral administration of the calcium channel blocker and vasodilator nimodipine has not proven to be of benefit in tsah. 37 Therefore, while there could be some subgroup of tsah patients who might indeed benefit from aggressive treatment of vasospasm, 38 there does not at this time appear to be a generalizable role for vasospasm-directed therapies in tsah. Some of the relatively infrequent morbidity in our tsah group could conceivably have been related to tsah-induced vasospasm and indeed, one patient in our cohort had diagnosed vasospasm that required aggressive endovascular treatment. Therefore, although seemingly rare, delayed neurological decline in patients with isolated tsah (especially perhaps in the major cisterns or fissures) should prompt consideration of a vasospastic etiology. Although most tsah injuries are ultimately neurologically benign, we do not argue that trauma patients with isolated tsah should be dismissed as minor trauma. These patients should be monitored for post-concussive symptoms that may severely impair quality-of-life for weeks or months. 39 Further, the notion of a vulnerable brain after even apparently mild trauma, especially in younger patients, has persisted since the earliest reports of catastrophic second-impacts 40 and is supported by non-human and human 44 studies. While there may not be a one-to-one correspondence between tsah and concussion, clinical similarities suggest it may nevertheless be wise to counsel patients regarding the avoidance of repeat head injury in at least the short-term. 18 In some cases, the severity of these symptoms alone may be indications for admission and observation. Traumatic SAH is defined by the presence of hemorrhage in the subarachnoid space, usually confined to the superficial sulci at the convexity of the brain. 45 Yet, despite the clinical frequency of tsah, the precise mechanisms by which this sort of injury may affect brain function is poorly understood. Specifically, due to the generally favorable prognosis of tsah, the lack of post-mortem studies, and the paucity of any experimental models specific to tsah, evidence for the exact pathophysiologic mechanisms of tsah has been limited. Nevertheless, some related experimental work provides hints about these potential mechanisms of injury. For example, a small prospective study has suggested that subarachnoid blood in patients with tsah likely correlates with posttraumatic vasospasm and delayed-ischemic symptoms. 46 Some authors have demonstrated similarities between post-traumatic vasospasm and aneurysmal vasospasm, supporting the hypothesis that these two injuries share a similar etiology. 47 However, significant differences do exist between these two categories of injury specifically, post-traumatic vasospasm has an earlier time of onset and a shorter duration than aneurysmal vasospasm. 48 Some of these differences may be explained by presence of mechanical injury to arteries during trauma, which has been experimentally correlated with short term vasospasm. 49 Most animal models used for investigating subarachnoid hemorrhage are designed to mimic ssah rather than tsah. Those that do focus on trauma often produce different constellations of intracranial injury rather than a pure cortical tsah phenomenon that typifies human injury in these cases Nevertheless, studies suggest that cortical spreading depression and depolarization waves, 53,54 as well as calcium-induced cell membrane injury, 55 play roles in the pathophysiology of tsah. Other studies propose that significant increases leukotriene production, 56 increases in brain metabolites such as choline and creatine, 57 and decreases in global and regional cerebral blood flow 58 also are particularly important. The relative contribution of functional derangements, such as these to the overall syndrome of injury, versus that caused by direct chemical injury by blood products, is unknown. Answering questions such as these represents an interesting and potentially beneficial area of research. In summary, this study adds to the growing body of evidence that isolated tsah is typically a less severe form of intracranial injury and extends those earlier findings to patients admitted with lower GCS scores than previously studied, and examines aggressive medical and endovascular as well as neurosurgical interventions. We found such interventions to be rare in this population and outcomes to be generally good, as even patients admitted with low GCS scores were more likely than not to be discharged home. We found a surprisingly high mortality and morbidity in elderly patients with isolated tsah, likely reflecting medical issues not directly arising from the trauma. In general, a lack of discrimination among different forms of traumatic intracranial hemorrhage may be to blame for the manner in which these injuries are typically managed and studied. In the case of relatively minor injuries such as isolated tsah, this lack of discrimination may lead to over-aggressive and costly measures, ranging from unnecessary routine repeat head CTs, overly cautious sedation and intubation, and inter-hospital transfers. Hopefully as tsah is better studied and understood, the few patients for whom more aggressive treatment might be warranted can be identified and triaged appropriately, while those for whom this injury is unlikely to be of significant consequence are given the most appropriate care. Acknowledgments The authors wish to thank the support of the Department of Neurosurgery, the Alpert Medical School of Brown University and Rhode Island Hospital. All authors participated in designing the study, performing the analyses and writing the manuscript. Author Disclosure Statement No competing financial interests exist. References 1. Faul, M., Xu, L., Wald, M.M., and Coronado, V.G. 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