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Figure.
Computed Tomographic Scans Demonstrating Characteristic Brain Hemorrhages in the Patient Cohort
Computed Tomographic Scans Demonstrating Characteristic Brain Hemorrhages in the Patient Cohort

A, Patient with left-sided hemiparesis that resolved within 6 hours. B, Patient with left-sided hemiparesis that resolved within 12 hours. C, Patient with severe anomia that resolved in 30 minutes. D, Patient with recurrent right-sided paresthesias lasting less than 24 hours. E, Patient with speech arrest that largely resolved within 15 minutes. F, Patient with right-sided hemiparesis and aphasia that resolved within 8 hours.

Table.  
Baseline Characteristics of the Patient Cohort
Baseline Characteristics of the Patient Cohort
1.
van Asch  CJ, Luitse  MJ, Rinkel  GJ, van der Tweel  I, Algra  A, Klijn  CJ.  Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis.  Lancet Neurol. 2010;9(2):167-176.PubMedGoogle ScholarCrossref
2.
Hemphill  JC  III, Greenberg  SM, Anderson  CS,  et al; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology.  Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association.  Stroke. 2015;46(7):2032-2060.PubMedGoogle ScholarCrossref
3.
Khirwadkar  H, Thomas  C, Fardy  M, Hourihan  M.  Postoperative subdural haematoma and pneumocephalus mimicking TIA [published online August 30, 2011].  BMJ Case Rep. doi:10.1136/bcr.03.2011.3965.PubMedGoogle Scholar
4.
Kumar  S, Goddeau  RP  Jr, Selim  MH,  et al.  Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies.  Neurology. 2010;74(11):893-899.PubMedGoogle ScholarCrossref
5.
Kothari  RU, Brott  T, Broderick  JP,  et al.  The ABCs of measuring intracerebral hemorrhage volumes.  Stroke. 1996;27(8):1304-1305.PubMedGoogle ScholarCrossref
6.
Moon  JS, Janjua  N, Ahmed  S,  et al.  Prehospital neurologic deterioration in patients with intracerebral hemorrhage.  Crit Care Med. 2008;36(1):172-175.PubMedGoogle ScholarCrossref
7.
Fan  JS, Huang  HH, Chen  YC,  et al.  Emergency department neurologic deterioration in patients with spontaneous intracerebral hemorrhage: incidence, predictors, and prognostic significance.  Acad Emerg Med. 2012;19(2):133-138.PubMedGoogle ScholarCrossref
8.
Kernan  WN, Ovbiagele  B, Black  HR,  et al; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology; Council on Peripheral Vascular Disease.  Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association.  Stroke. 2014;45(7):2160-2236.PubMedGoogle ScholarCrossref
9.
Goldstein  LB, Bian  J, Samsa  GP, Bonito  AJ, Lux  LJ, Matchar  DB.  New transient ischemic attack and stroke: outpatient management by primary care physicians.  Arch Intern Med. 2000;160(19):2941-2946.PubMedGoogle ScholarCrossref
10.
Roebers  S, Wagner  M, Ritter  MA, Dornbach  F, Wahle  K, Heuschmann  PU.  Attitudes and current practice of primary care physicians in acute stroke management.  Stroke. 2007;38(4):1298-1303.PubMedGoogle ScholarCrossref
11.
Edlow  JA, Kim  S, Pelletier  AJ, Camargo  CA  Jr.  National study on emergency department visits for transient ischemic attack, 1992-2001.  Acad Emerg Med. 2006;13(6):666-672.PubMedGoogle Scholar
12.
Wardlaw  JM, Keir  SL, Dennis  MS.  The impact of delays in computed tomography of the brain on the accuracy of diagnosis and subsequent management in patients with minor stroke.  J Neurol Neurosurg Psychiatry. 2003;74(1):77-81.PubMedGoogle ScholarCrossref
13.
Allen  CM.  Clinical diagnosis of the acute stroke syndrome.  Q J Med. 1983;52(208):515-523.PubMedGoogle Scholar
14.
Poungvarin  N, Viriyavejakul  A, Komontri  C.  Siriraj stroke score and validation study to distinguish supratentorial intracerebral haemorrhage from infarction.  BMJ. 1991;302(6792):1565-1567.PubMedGoogle ScholarCrossref
Original Investigation
March 2016

Transient Neurological Symptoms in Patients With Intracerebral Hemorrhage

Author Affiliations
  • 1Stroke Division, Department of Neurology, Beth Israel Deaconess Medical Center, Boston, Massachusetts
  • 2Harvard Medical School, Boston, Massachusetts
JAMA Neurol. 2016;73(3):316-320. doi:10.1001/jamaneurol.2015.4202
Abstract

Importance  Transient symptoms from an intracerebral hemorrhage (ICH) are not well recognized and have previously not been reported.

Objective  To describe the clinical presentations and neuroimaging findings in a subset of patients with ICH presenting with transient neurological signs and symptoms.

Design, Setting, and Participants  Clinical case series in which the hospital database of a large academic center in Boston, Massachusetts, was searched using International Classification of Diseases, Ninth Revision code 431 from June 1, 2000, to August 31, 2014, to identify patients with ICH who had transient deficits that resolved completely within 24 hours of symptom onset.

Main Outcomes and Measures  Clinical presentation, neuroimaging findings, and prognosis.

Results  Among 3207 consecutive patients with ICH initially screened, 17 fulfilled study criteria (median age, 65 years [interquartile range, 56-73 years]; 11 male). In most patients, recovery from neurological symptoms started within a few hours after onset. Most hemorrhages in this cohort were small, with a mean (SD) hematoma volume of 17 (9.9) mL, and were subcortical in location. One patient died of hemorrhage recurrence.

Conclusions and Relevance  Patients with ICH can present with rapidly resolving deficits resembling transient ischemic attacks. Recognition of these instances is important to avoid delays in investigations and to manage these cases appropriately.

Introduction

Quiz Ref IDIntracerebral hemorrhage (ICH) is a particularly ominous stroke subtype that carries high rates of mortality and morbidity.1 Prompt recognition and appropriate management are necessary to affect outcomes in these patients.2 Usually, ICH presents with an abrupt onset of neurological deficits that often progress over time; nausea, vomiting, impairment of consciousness, and significant hypertension at presentation are common features.2 However, in a significant number of patients, the deficits are less pronounced and brain imaging is needed to differentiate ICH from an ischemic stroke. Whereas temporary symptoms have been observed in patients with subdural hematomas and subarachnoid hemorrhages due to amyloid angiopathy,3,4 transient deficits resembling transient ischemic attacks (TIAs) have not been reported, to our knowledge, in patients with ICH.

We encountered a patient in our practice who had developed a transient language impairment from a left temporal hemorrhage mimicking a TIA. This prompted us to systematically search the medical records at our institution to assess the frequency of TIA-like presentations of ICH, analyze their presenting symptoms and signs as well as imaging patterns, and assess prognosis.

Box Section Ref ID

Key Points

  • Question: Do transient signs and symptoms occur with intracerebral hemorrhages?

  • Findings: In this case series involving 17 carefully selected hospitalized patients, rapidly resolving signs and symptoms resembling transient ischemic attacks were documented. All patients had normal results on neurological examination within 24 hours after symptom onset.

  • Meaning: Patients with rapidly resolving stroke-like symptoms should undergo prompt brain imaging, even in the context of normal findings on neurological examination, to rule out intracerebral hemorrhage, especially prior to initiating any antithrombotic or anticoagulant therapy.

Methods

In this clinical case series, we identified all patients with ICH using International Classification of Diseases, Ninth Revision code 431 from our hospital database from June 1, 2000, to August 31, 2014. Discharge summaries of all records were individually reviewed to exclude patients with traumatic ICH, subarachnoid and subdural hemorrhages, secondary ICH from an underlying neoplasm, and ICH from hemorrhagic transformation of an ischemic infarct. We collected and analyzed demographic information as well as clinical and imaging findings on all remaining patients with a spontaneous ICH. Patients who had transient deficits (symptoms, signs, or both) from an ICH that had resolved on a repeated examination within 24 hours were eligible. The study was approved by the institutional review board at the Beth Israel Deaconess Medical Center. A waiver of informed consent was granted by the institutional review board owing to the low-risk, retrospective nature of this study.

Results

We identified 3207 patients with ICH using International Classification of Diseases, Ninth Revision code 431. Among these, 2137 patients had a spontaneous ICH without any coexisting subarachnoid or subdural hemorrhage, neoplasm, or secondary hemorrhagic transformation from a cerebral infarct. Of these, 34 patients had transient deficits, which were defined as clinical symptoms and signs that had resolved within 24 hours. These records were further reviewed to ascertain details of history and imaging findings and to discard records in which significant clinical information and details about the duration of symptoms were lacking (12 cases) or in which additional conditions may have confounded the clinical presentation (5 cases). A cohort of 17 patients was assembled (eAppendix in the Supplement). The baseline characteristics of this cohort are summarized in the Table.

The median age of the group was 65 years (interquartile range, 56-73 years); 11 of the 17 patients were men. All patients underwent a computed tomographic (CT) scan of the brain within 6 hours of symptom onset and had a documented detailed neurological examination at presentation as well as a subsequent progress note detailing the clinical course during the preceding 24 hours including a follow-up neurological examination within 24 hours.

Clinical Presentation

The trajectory of clinical improvement began early in all patients, usually within several minutes. In 9 patients, the deficits lasted less than 30 minutes, in 5 patients they lasted 6 hours or less, and only 1 patient had symptoms lingering more than 12 hours but less than 24 hours. The most common deficits were sensorimotor involving varying degrees of limb weakness, numbness, or incoordination. Three patients developed significant dysarthria and 2 others had major language impairment at onset; 3 patients had dizziness with gait unsteadiness. Quiz Ref IDThe typical symptoms of ICH including headache, nausea, vomiting, and reduction in levels of alertness were usually absent. Most patients had moderate to severe hypertension at presentation, although their neurological deficits were mild (mean [SD] National Institutes of Health Stroke Scale score, 2.3 [1.5]; range, 0-5) on initial neurological examination in the emergency department (Table). Five patients took antiplatelet medications either on their own accord or per the advice of their physicians prior to obtaining any imaging studies.

Imaging Findings

The prototypical imaging findings on CT scans at admission are shown in the Figure. Quiz Ref IDMost of the hemorrhages were subcortical involving the basal ganglia or neighboring white matter tracts. Two involved the temporal lobes. No patients had intraventricular hemorrhage or hydrocephalus. All hemorrhages were small, with a mean (SD) volume of 17 (9.9) mL as measured by the ABC/2 method.5 In addition to the initial head CT scans, 11 patients underwent brain magnetic resonance imaging and magnetic resonance angiography, 5 underwent CT angiography of the head, and 2 underwent conventional angiography. In 16 patients who underwent vascular imaging, only 1 had an abnormality consistent with a unilateral moyamoya-type pattern. Of the 11 patients who underwent brain magnetic resonance imaging, 7 showed varying degrees of leukoaraiosis on fluid-attenuated inversion recovery sequences; 2 showed scattered microbleeds on gradient echo sequences; 1 displayed characteristic features of a cavernoma; and 1 showed no other significant abnormality apart from the acute ICH.

Etiology

Etiology of the hemorrhage was determined based on discharge diagnosis and review of all discharge summaries and neuroimaging findings. In 8 patients the bleed was likely hypertensive; 2 patients had probable amyloid angiopathy; 1 patient had moyamoya disease; 1 had bleeding from a cavernous angioma; 2 cases were likely anticoagulant related; and a definite etiology for hemorrhage could not be determined in 3 cases.

Follow-up

One patient died during hospitalization of recurrence of a massive ICH 4 days after admission. This patient had a pacemaker and did not undergo brain magnetic resonance imaging or vascular imaging. The etiology of her hemorrhage was unclear. Detailed follow-up information was available in 9 patients. The follow-up varied between 1 and 8 months. In all these patients there was no recurrence of symptoms suggestive of a stroke or TIA.

Discussion

Quiz Ref IDWhereas clinical deterioration after ICH has been shown in several studies,6,7 to our knowledge no studies have reported rapid improvement in clinical deficits in patients with ICH. We adopted a 24-hour threshold for labeling a deficit as transient as this time cutoff has traditionally been used for defining TIAs.8 In most patients the improvement started early, usually within several minutes, and the symptoms and signs had resolved well before our adopted time threshold. This is likely an unusual presentation of ICH, although rapid improvement of symptoms with relatively minor deficits may have contributed to a referral bias and led to an underascertainment of cases. Only a prospective population-based study with detailed early neurological assessment and close monitoring can estimate the true incidence.

Quiz Ref IDOur report carries significant clinical relevance. First, it shows that transient deficits from a minor ICH can mimic a TIA or minor infarct and thus require brain imaging for differentiation. Some of our patients received antiplatelet medications prior to any imaging. While we did not observe any harm in this small group of patients, prescription of these agents can be hazardous in this situation. Second, this study highlights a need to obtain prompt brain imaging in all patients with suspected TIAs. In many settings, patients with TIAs are not routinely admitted for admission or referred to the emergency department.9,10 Previous reports have shown that even in patients presenting to the emergency department with symptoms of a TIA, CT scans are underused and only 50% to 70% of such patients undergo a scan.11 Delays in obtaining head CTs can substantially reduce the sensitivity of detecting a hemorrhage especially beyond a week.12 Third, in resource-limited settings, clinical scores to diagnose ICH have been derived and validated.13,14 It is worth noting that only a small minority of our patients could reliably be suspected of having an ICH based on their presenting features such as diminished consciousness, nausea, vomiting, headache, and severe hypertension. Our findings urge caution regarding the reliability of these clinical tools in identifying minor hemorrhages.

The biological underpinning driving such an early recovery after ICH is intriguing. The rapid resolution of symptoms may suggest a hemodynamic cause with spontaneous reduction in local mass effect from redistribution of blood along the tracts, especially in patients with subcortical bleeds. In 2 of our patients with lobar hemorrhages, focal seizures with postictal deficits may have played a role. Neuroplastic changes with cortical reorganization are also a possibility, although the time course is less typical.

The major limitation of our work lies in its retrospective nature, where documentation of a detailed neurological evaluation at predefined regular intervals was unavailable. Thus, we relied on the admission and progress notes as well as discharge summaries to record timing of recovery. We meticulously excluded cases in which this information was unavailable. The etiology of the hemorrhage was based on clinician impression, although we independently reviewed all records and imaging studies for corroboration. Routine follow-up information was not available in some of our patients and brain imaging was not repeated in many patients. Most patients with available information fared well, although there was 1 death from recurrent ICH.

Conclusions

This study highlights a previously unrecognized presentation of ICH and emphasizes its clinical relevance for patient care. Further studies are needed to better estimate its true incidence and understand the pathophysiological basis of this presentation.

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Article Information

Corresponding Author: Sandeep Kumar, MD, Stroke Division, Department of Neurology, Beth Israel Deaconess Medical Center, 185 Pilgrim Rd, Palmer 127, Boston, MA 02215 (skumar@bidmc.harvard.edu).

Accepted for Publication: November 4, 2015.

Published Online: January 4, 2016. doi:10.1001/jamaneurol.2015.4202.

Author Contributions: Dr Kumar had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Kumar, Selim.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Kumar.

Critical revision of the manuscript for important intellectual content: All authors.

Administrative, technical, or material support: Kumar, Marchina.

Conflict of Interest Disclosures: None reported.

References
1.
van Asch  CJ, Luitse  MJ, Rinkel  GJ, van der Tweel  I, Algra  A, Klijn  CJ.  Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis.  Lancet Neurol. 2010;9(2):167-176.PubMedGoogle ScholarCrossref
2.
Hemphill  JC  III, Greenberg  SM, Anderson  CS,  et al; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology.  Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association.  Stroke. 2015;46(7):2032-2060.PubMedGoogle ScholarCrossref
3.
Khirwadkar  H, Thomas  C, Fardy  M, Hourihan  M.  Postoperative subdural haematoma and pneumocephalus mimicking TIA [published online August 30, 2011].  BMJ Case Rep. doi:10.1136/bcr.03.2011.3965.PubMedGoogle Scholar
4.
Kumar  S, Goddeau  RP  Jr, Selim  MH,  et al.  Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies.  Neurology. 2010;74(11):893-899.PubMedGoogle ScholarCrossref
5.
Kothari  RU, Brott  T, Broderick  JP,  et al.  The ABCs of measuring intracerebral hemorrhage volumes.  Stroke. 1996;27(8):1304-1305.PubMedGoogle ScholarCrossref
6.
Moon  JS, Janjua  N, Ahmed  S,  et al.  Prehospital neurologic deterioration in patients with intracerebral hemorrhage.  Crit Care Med. 2008;36(1):172-175.PubMedGoogle ScholarCrossref
7.
Fan  JS, Huang  HH, Chen  YC,  et al.  Emergency department neurologic deterioration in patients with spontaneous intracerebral hemorrhage: incidence, predictors, and prognostic significance.  Acad Emerg Med. 2012;19(2):133-138.PubMedGoogle ScholarCrossref
8.
Kernan  WN, Ovbiagele  B, Black  HR,  et al; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology; Council on Peripheral Vascular Disease.  Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association.  Stroke. 2014;45(7):2160-2236.PubMedGoogle ScholarCrossref
9.
Goldstein  LB, Bian  J, Samsa  GP, Bonito  AJ, Lux  LJ, Matchar  DB.  New transient ischemic attack and stroke: outpatient management by primary care physicians.  Arch Intern Med. 2000;160(19):2941-2946.PubMedGoogle ScholarCrossref
10.
Roebers  S, Wagner  M, Ritter  MA, Dornbach  F, Wahle  K, Heuschmann  PU.  Attitudes and current practice of primary care physicians in acute stroke management.  Stroke. 2007;38(4):1298-1303.PubMedGoogle ScholarCrossref
11.
Edlow  JA, Kim  S, Pelletier  AJ, Camargo  CA  Jr.  National study on emergency department visits for transient ischemic attack, 1992-2001.  Acad Emerg Med. 2006;13(6):666-672.PubMedGoogle Scholar
12.
Wardlaw  JM, Keir  SL, Dennis  MS.  The impact of delays in computed tomography of the brain on the accuracy of diagnosis and subsequent management in patients with minor stroke.  J Neurol Neurosurg Psychiatry. 2003;74(1):77-81.PubMedGoogle ScholarCrossref
13.
Allen  CM.  Clinical diagnosis of the acute stroke syndrome.  Q J Med. 1983;52(208):515-523.PubMedGoogle Scholar
14.
Poungvarin  N, Viriyavejakul  A, Komontri  C.  Siriraj stroke score and validation study to distinguish supratentorial intracerebral haemorrhage from infarction.  BMJ. 1991;302(6792):1565-1567.PubMedGoogle ScholarCrossref
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