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Hemorrhagic stroke
Original research
Yield of catheter angiography in patients with intracerebral hemorrhage with and without intraventricular extension
  1. Yasha Kadkhodayan,
  2. Josser E Delgado Almandoz,
  3. James E Kelly,
  4. Sushant P Kale,
  5. Bharathi D Jagadeesan,
  6. Christopher J Moran,
  7. DeWitte T Cross III,
  8. Colin P Derdeyn
  1. Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, Missouri, USA
  1. Correspondence to Dr Colin P Derdeyn, Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd, St Louis 63110, Missouri, USA; derdeync{at}mir.wustl.edu

Abstract

Background and aim The role of imaging for the detection of vascular lesions in patients with intracerebral hemorrhage (ICH) is poorly defined. A study was undertaken to compare the yield of digital subtraction angiography (DSA) in patients with ICH with intraventricular hemorrhage (IVH) and those without IVH.

Methods The DSA database at our institution was reviewed for patients who underwent DSA for acute spontaneous ICH over a period of 68 months. Patients with known vascular malformation or brain neoplasm, prior surgery, ischemic infarction, subarachnoid hemorrhage or isolated IVH were excluded. Patients were grouped into those with associated IVH (group A) and those without (group B). Baseline demographic and clinical data, non-contrast head CT (NCCT) probability for a vascular lesion and angiographic results were compared.

Results 293 patients met the inclusion and exclusion criteria (141 women, 152 men, mean age 57, range 18–88), 139 in group A and 154 in group B. Age and sex distributions were similar (p>0.05). Group A patients were more likely to be hypertensive or coagulopathic (p=0.001). Group B had more patients with high probability NCCT scans (p<0.001). Underlying vascular lesions were found in 21 patients (15.1%) in group A and 34 (22.1%) in group B (p>0.05).

Conclusion The presence of IVH in patients with acute spontaneous ICH is not associated with an increased risk of an underlying vascular lesion and should not be used to select patients for neurovascular evaluation.

  • Brain hemorrhage
  • intraventricular hemorrhage
  • cerebral angiography
  • aneurysm
  • coil
  • ct angiography
  • device
  • stent
  • subarachnoid
  • hemorrhage
  • arteriovenous malformation
  • angiography
  • angioplasty
  • stroke
  • flow diverter
  • stent
  • brain
  • intervention
  • artery
  • cervical
  • vasculitis
  • thrombectomy
  • catheter
  • balloon
  • stenosis

https://doi.org/10.1136/neurintsurg-2011-010077

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    Introduction

    Some patients with spontaneous intracerebral hemorrhage (ICH) have an underlying vascular etiology that may be amenable to treatment. These potentially treatable lesions include arteriovenous malformations (AVMs), aneurysms, arteriovenous fistulas (AVFs) and dural venous sinus thromboses. Diagnostic vascular imaging tools include digital subtraction angiography (DSA), multidetector computed tomographic angiography (CTA) and magnetic resonance angiography (MRA). DSA is the most accurate of these techniques but carries the highest risk and expense.

    A growing body of literature has focused on clinical factors and imaging features associated with the presence of an underlying vascular lesion as performing routine vascular imaging for all patients with spontaneous ICH, particularly with DSA, may not be cost-effective. For example, patients presenting with ICH are more likely to have a vascular lesion as an etiology of their hemorrhage if they are young, female, not hypertensive, have intact coagulation and lobar ICH location.1–17 Vascular imaging is important in this population, and DSA is commonly employed.

    An unpublished retrospective review of 63 consecutive patients aged >45 years presenting to our institution with ICH in the basal ganglia, thalamus, cerebellum or brainstem demonstrated a potentially important angiographic yield in those patients with extension into the ventricles (intraventricular hemorrhage, IVH). Five of the 26 patients with IVH (19.2%) had a positive angiogram while only one of the remaining 37 patients without IVH had a positive study (2.7%, overall yield of 9.5%: five AVMs and one aneurysm). Of note, all five of the patients with ICH with associated IVH with positive angiograms had a pre-existing diagnosis of hypertension in addition to belonging to an older patient population.

    As a consequence of this internal review, we adopted a protocol of performing DSA in older and hypertensive patients with ICH if there was associated IVH. However, this was not a protocol that was uniformly followed, and the decision to perform DSA in these patients was at the discretion of the clinical providers based on the patient's age, associated comorbidities and overall prognosis.

    The purpose of this study is to compare the yield of DSA in patients with acute spontaneous ICH and associated IVH with those without associated IVH in a series of 293 consecutive patients examined by DSA over a 68-month period following the adoption of this more liberal imaging protocol.

    Methods

    Institutional review board approval was obtained for the study and signed informed consent was obtained for DSA as part of routine clinical care. The neuroradiology DSA quality assurance database at our institution was retrospectively interrogated. Patients who underwent angiography for the indication of acute spontaneous ICH over a 68-month period from 1 December 2004 to 31 July 2010 were included. Patients with (1) known intracranial vascular malformation, (2) known brain neoplasm, (3) surgical evacuation and/or exploration prior to angiography, (4) imaging findings suggestive of ischemic infarction on admission (5) subarachnoid hemorrhage in the sylvian fissures or basal cisterns or (6) isolated IVH were excluded.

    Admission non-contrast head CT (NCCT) images were reviewed by neuroradiology fellows (YK, JEK) or a stroke fellow (SK) to assess for the presence of ICH with and without intraventricular extension. The NCCTs were categorized by two neuroradiologists (JDA, BDJ) blinded to the clinical data and final diagnosis into high, intermediate and low probability for the presence of an underlying vascular lesion following the criteria detailed below.13 ,14 This categorization is part of the secondary intracerebral hemorrhage score (SICH), a recently validated practical scoring system for patients with ICH further described in the Discussion section.

    A high probability NCCT was defined as an examination in which there were either (1) enlarged vessels or calcifications along the margins of the ICH or (2) hyperattenuation within a dural venous sinus or cortical vein along the presumed venous drainage path of the hemorrhage. A low probability CT was defined as an examination in which none of the findings of a high probability NCCT were present and the hemorrhage was located within the basal ganglia, thalamus or brainstem (deep hemorrhage). An indeterminate NCCT was defined as an examination that did not meet the criteria for a high or low probability NCCT, most commonly a lobar or cerebellar ICH. All differences in reader interpretations were resolved by consensus.

    Electronic medical records were reviewed by four physicians (JDA, YK, JEK, SK) and the following demographic and clinical information was recorded: age, sex, history of hypertension defined by documented diagnosis or known use of antihypertensive medications, and indicators of coagulopathy defined by daily antiplatelet therapy with aspirin or clopidogrel, international normalized ratio >3.0, activated partial thromboplastin time >80 s or platelet count <50 000 cells/mm3 of blood. Hypertension and impaired coagulation were considered together as it was the absence of both factors that was found to be an independent predictor of an underlying vascular lesion in a recent multiple variable logistic regression analysis.14

    Catheter angiography was performed within 1 week of admission on one of two dedicated biplane neuroangiographic units (Axiom Artis, Siemens, Erlangen, Germany). The procedures were performed by one of three neurointerventional staff (CJM, DTC, CPD) and house staff, including radiology and neurosurgery residents, diagnostic neuroradiology fellows and/or a neurointerventional fellow. All catheter angiograms included biplanar intracranial images after selective catheterization and contrast injection (Optiray 320, Covidien, Hazelwood, Missouri, USA) of the vessels of interest as dictated by the vascular supply to the site of ICH demonstrated on NCCT. For suspected lesions of the anterior circulation, common carotid injections were routinely employed with selective internal or external carotid injections generally reserved for cases where the additional diagnostic information would be needed for treatment planning.

    Patients were grouped into those with and without associated IVH, and their angiographic results were compared using the χ2 test or Fisher exact test (substituted for the χ2 test if any frequency was below 1 or less than 5 in more than 20% of the cells for 2×2 or 3×2 matrices) for statistical significance (defined as p<0.05). Baseline demographic and clinical data as well as NCCT probability for an underlying vascular lesion were also compared. Patients with IVH and an underlying vascular lesion at DSA were similarly compared with patients with IVH and negative angiograms.

    Results

    A total of 317 patients underwent DSA for acute spontaneous ICH over the 68-month study period. Twenty-four of these patients (7.6%) were excluded (7 for known intracranial vascular or mass lesion, 4 for imaging findings suggestive of ischemic infarction on admission and 13 for subarachnoid hemorrhage). Of note, an additional 49 patients underwent emergency surgical evacuation for acute spontaneous ICH at our institution over the same time period. These patients may or may not have had intraoperative or postoperative DSA; however, all of these patients were also excluded.

    Two hundred and ninety-three consecutive patients (141 women and 152 men) of mean age 57 years (range 18–88) met the inclusion and exclusion criteria. One hundred and thirty-nine patients (47.4%) had intraventricular extension (group A) and the remaining 154 patients (52.6%) did not (group B). Both groups had similar age and sex distributions (p>0.05, table 1). Those in group A were more likely to have had an underlying diagnosis of hypertension or impaired coagulation (p=0.001).

    View this table:
    Table 1

    Demographic characteristics of study patients

    The difference between NCCT probability for an underlying vascular lesion according to the criteria described above was highly significant between the two groups (p<0.001). Of the 10 patients with high probability NCCT, three were in group A and seven were in group B. Conversely, of the 116 patients with low probability NCCT, 78 (67.2%) were in group A and 38 (32.8%) were in group B. Deep hemorrhages, defined as those in the basal ganglia, thalamus and brainstem, were more likely to be associated with IVH (p<0.001).

    Fifty-five of the 293 patients (18.8%) had an underlying vascular lesion at DSA that explained their hemorrhage, 21 of 139 (15.1%) in group A and 34 of 154 (22.1%) in group B (p>0.05). While deep hemorrhages were less likely to be due to an underlying vascular malformation (p<0.001), no statistically significant differences in angiographic yield were found between patients with and without IVH in subgroup analyses by hemorrhage location (145 lobar, 118 deep and 30 cerebellar hemorrhages, table 2).

    View this table:
    Table 2

    Hemorrhage locations

    Lesions found at angiography included 28 AVMs, nine aneurysms, six AVFs, six cases of dural venous sinus thromboses, four cases of vasculitis and two cases of moyamoya (table 3). The frequency of each lesion was not statistically different between the two groups. However, the only two cases of moyamoya occurred in group A (p=0.141).

    View this table:
    Table 3

    Positive angiographic findings

    Patients with IVH and angiographic findings that explained the hemorrhage (21 of 139, 15.1%) were compared with patients with IVH and negative angiograms in regard to their demographic and clinical data as well as their NCCT probability (table 4). While there was a trend towards younger patients in the group with positive angiograms, only the differences in rate of hypertension or impaired coagulation and the NCCT probability were found to be statistically significant (p=0.005 and p=0.006, respectively).

    View this table:
    Table 4

    Patients with ICH and associated IVH (group A)

    Discussion

    ICH accounts for 10–15% of patients having their first stroke with a 30-day mortality rate of 35–52%.18–20 Furthermore, those with associated IVH have poorer outcomes.21–24 Catheter angiography is often a component of the investigation of patients who present with acute spontaneous ICH. Patient age, a history of pre-existing hypertension and the site of hemorrhage can be helpful in predicting the likelihood of finding an underlying vascular lesion. Several previous studies have shown an increased likelihood of finding a vascular cause in younger patients, particularly those aged <45 years.1–17

    According to the latest American Stroke Association guidelines for the management of spontaneous ICH, established indications for DSA include subarachnoid hemorrhage, abnormal calcifications, obvious vascular abnormalities and blood in unusual locations such as the sylvian fissures.25 Catheter angiography may also be indicated in patients with no obvious cause of bleeding, such as those with isolated IVH. The yield of angiography declines in elderly patients with hypertension and a deep hematoma.

    In the case of primary IVH, defined as bleeding in the ventricular system without a discernable parenchymal component (rare), the yield of DSA was found to be quite high with 56% positive for a bleeding source in a recently published systematic review of the literature.26 The two most commonly identified causes among positive angiograms were AVMs (58%) and aneurysms (36%).

    At our institution, patients who presented with associated intraventricular extension of their intraparenchymal hemorrhage were considered for DSA despite old age and hypertension based on an unpublished retrospective review as detailed above. Over a 68-month period 139 patients presented with intraparenchymal hemorrhage with intraventricular extension (group A). Of these, 21 had underlying vascular lesions identified at DSA for a yield of 15.1%. Compared with 34 positive angiograms among 154 patients with isolated intraparenchymal hemorrhage (22.1% angiographic yield in group B), the presence of IVH was not found to be an independent predictor of a vascular lesion (table 1).

    However, the presence of IVH was highly associated with an underlying diagnosis of hypertension or impaired anticoagulation (p=0.001). The difference in the distribution of NCCT probabilities for a vascular lesion was also highly significant between groups A and B. Patients with isolated ICH (group B) were twice as likely to have a high probability NCCT and half as likely to have a low probability NCCT according to the criteria described in the Methods section, a component of the recently validated SICH.

    Taken together, these findings support the idea that group A simply includes a large subset of patients who have hemorrhagic risk factors rather than an increased risk of an underlying vascular lesion. The results even seem to suggest that patients with ICH whose ventricles are free of blood are less likely to have hemorrhagic risk factors and perhaps should be evaluated with greater suspicion. This is in contradiction to the unpublished review that inspired the present study. There are several possible explanations.

    The current cohort is relatively prospective. While not all patients with ICH and associated IVH underwent angiography, many more did under the new more liberal patient selection policy for angiography at our institution described above. On the other hand, in the retrospective review done previously, a significant selection bias was very likely. Conceivably, many of the patients had a suspicious clinical or CT finding that may have tipped the decision scale towards requesting DSA during a time when routine DSA was not performed.

    Selecting patients for neurovascular evaluation can be challenging.27 While DSA at our institution has a relatively low permanent neurological complication rate of 0.12%,28 a less invasive alternative approach to DSA in low-risk populations with or without IVH would be multidetector CTA screening. Several recent retrospective series have shown that CTA is highly accurate in the detection of vascular abnormalities in the setting of ICH,10–13 ,17 with sensitivities ranging from 89% to 100% and overall accuracies ranging from 91% to 99%. Given the low-risk nature of CTA, many centers routinely employ CTA screening for all patients with ICH, thereby eliminating the difficulty of avoiding patient selection bias for DSA described above.

    The use of MRA has also been studied. Wong et al found high predictive values for MRA performed in the subacute phase in a retrospective review of 151 patients with ICH who underwent both MRA and DSA.15 They found 70 vascular lesions (46%) in this population, with MRA having a positive predictive value of 0.98 and a negative predictive value of 1. Interestingly, patients with vascular lesions in their cohort were more likely to have IVH. There are many possible reasons. Their mean age was 41.6 years compared with a mean age of 57 years in our study. In addition, only 34% of their patients were hypertensive compared with 63% of our cohort who had either hypertension or impaired coagulation. It is possible that IVH is a predictor of an underlying vascular lesion in young normotensive patients who would be studied anyway. As expected, their overall yield of 46% was also higher.

    A practical scoring system to stratify patients with ICH according to their risk of harboring a vascular etiology, the SICH score, has recently been reported.14 The validity of this scoring system was established using a prospective cohort of 222 patients evaluated with CTA at a center that routinely employs CTA screening for all patients with ICH. The SICH score (0–6 points) is based on age group (0–2 points), sex (0–1 point), neither known hypertension nor impaired coagulation (0–1 point) and NCCT probability (0–2 points). These factors, including the criteria for NCCT probability, were adapted for the analysis in this study (table 1).

    In the present study, 20 of the 21 patients in group A with an underlying vascular lesion had SICH scores of ≥2, corresponding to at least a chance of about 5% of a positive CTA (see two examples in figures 1 and 2). As such, neurovascular evaluation—at least with CTA—would have been reasonable using the SICH score even if the patients had not had intraventricular extension of their hemorrhage. These patients tended to be younger, were significantly more likely to be normotensive with intact coagulation and had higher probability NCCT (table 4). Based on the findings of this study, the use of IVH to select patients for neurovascular evaluation is not recommended; the SICH score may be a useful alternative. A diagnostic algorithm for the investigation of patients with hemorrhagic stroke using the SICH score has recently been proposed and is shown in figure 3.29 A SICH score threshold of 3 for DSA imaging was determined based on receiver operative characteristic curve analysis.14

    Figure 1
    Figure 1

    Twenty-six-year old woman with acute left hemiparesis, no history of hypertension or impaired coagulation. (A) Non-contrast head CT scan showing a large right frontoparietal hematoma with intraventricular extension and mild ventriculomegaly. (B) Lateral and oblique digital subtraction angiogram showing a 1.8×1.2 cm right parietal arteriovenous malformation with arterial feeders from a distal branch of the right middle cerebral artery and drainage to the superior sagittal sinus without associated aneurysm.

    Figure 2
    Figure 2

    Forty-six-year old man with headache and altered mental status, no history of hypertension or impaired coagulation. (A) Non-contrast head CT scan showing a 3.0×1.4 cm left thalamic hematoma with a large amount of intraventricular hemorrhage. (B) Lateral immediate and delayed arterial phase digital subtraction angiogram showing an early draining vein (arrow) arising from a distal posterior cerebral artery branch to the junction of the left transverse and sigmoid sinuses, thought to represent a pial arteiovenous malformation.

    Figure 3
    Figure 3

    Diagnostic algorithm for the investigation of patients with hemorrhagic stroke using the secondary intracerebral hemorrhage (SICH) score.29 CTA, CT angiography; DSA, digital subtraction angiography; ICH, intracerebral hemorrhage.

    A significant limitation of this study is the persistent patient selection bias due to the lack of uniformity in DSA utilization. The decision to perform DSA in patients with ICH was at the discretion of the referring physician and usually based on multiple clinical factors including patient age, associated comorbidities and overall prognosis. Another limitation is the post hoc analysis of risk factors for an underlying vascular lesion. One of these risk factors, hypertension, was also defined in a way that likely included patients with blood pressure well controlled by medication.

    Conclusion

    The presence of IVH in patients with acute spontaneous ICH is not associated with an underlying vascular lesion and should not be used to select patients for neurovascular evaluation. Our data support the routine use of DSA in young normotensive patients with intact coagulation in the setting of acute spontaneous ICH. CTA screening may be worth considering in selected older hypertensive patients regardless of the presence of IVH in light of its safer less invasive nature.

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    Footnotes

    • Competing interests None.

    • Ethics approval Washington University Human Research Protection Office.

    • Provenance and peer review Not commissioned; externally peer reviewed.