ICH Score

ICH Score

The ICH Score: What It Is and What It Is Not 1).

Simple and reliable clinical grading score that is used for predicting the early mortality of patients with intracerebral hemorrhage (ICH).

The ICH Score has become the standard for risk-stratification of 30-d mortality in patients with intracerebral hemorrhage (ICH), but treatment has evolved over the last 17 yr since its inception.

The ICH score is a useful tool for predicting 30-day mortality both in patient who use and patients who do not use OAC. Although OAC use is an independent predictor of 30-day mortality, addition of OAC use to the existing ICH score does not increase the prognostic performance of this score 2)

The ICH Score is the sum of individual points assigned as follows:

GCS

GCS score 3 to 4 (=2 points),

5 to 12 (=1),

13 to 15 (=0)

Age

Age >/=80 years yes (=1), no (=0);

Localization

Infratentorial origin yes (=1), no (=0);

ICH volume >/=30 cm(3) (=1), <30 cm(3) (=0);

Intraventricular hemorrhage yes (=1), no (=0).

Patient 68 years old GCS 4: ICH 4 score

All 26 patients with an ICH Score of 0 survived, and all 6 patients with an ICH Score of 5 died. Thirty-day mortality increased steadily with ICH Score (P<0.005) 3).


Malinova et al. evaluated the reproducibility of the ICH-score in ICH patients undergoing fibrinolytic therapy.

They performed a retrospective analysis of patients with supratentorial ICH managed by fibrinolytic therapy and evaluated the 30-day mortality. The ICH-score was then applied to match the mortality in the patients with the mortality predicted by the ICH-score. The ICH-score is based on parameters available at admission: age, hematoma volume, intraventricular expansion, and clinical status according to the Glasgow Coma Scale.

A total of 233 patients were analyzed. The 30-day mortality rate was 30% (70/233). An age of ≥80 years was associated with a significantly higher mortality rate (OR 2.26, chi-square test p = 0.01). A hematoma volume of ≥30 mL led significantly more often to 30-day mortality (OR 3.72, chi-square test p = 0.01). The mortality was significantly higher in patients with intraventricular hemorrhage (2.97, chi-square test p = 0.003). The ICH-score showed a significant correlation with mortality (chi-square test, p < 0.0001). The following mortality rates were estimated using the ICH-score in our cohort: 1 = 0% (0/13), 2 = 0% (0/51), 3 = 1.3% (1/82), 4 = 43% (13/31), 5 = 100% (56/56). : The ICH-score not only allowed a reliable estimation of the 30-day mortality in patients with ICH treated conservatively but also treated by clot lysis. Compared to conservative treatment, fibrinolytic therapy reduced the 30-day mortality in patients with ICH-scores 1-4. Patients with ICH-score 5 do not have a benefit of fibrinolytic therapy and should no longer be considered to be candidates for fibrinolytic therapy 4).


The original ICH score did not accurately predict the mortality rate in the series of the Department of Neurosurgery, Emory University, AtlantaGeorgia. Patient survival exceeded ICH Score-predicted mortality regardless of surgical intervention. Reevaluation of predictive scores could be useful to aid in more accurate prognoses 5).

References

1)

Hemphill JC 3rd. The ICH Score: What It Is and What It Is Not. World Neurosurg. 2018 Dec 20. pii: S1878-8750(18)32883-3. doi: 10.1016/j.wneu.2018.12.060. [Epub ahead of print] PubMed PMID: 30580061.
2)

Houben R, Schreuder FHBM, Bekelaar KJ, Claessens D, van Oostenbrugge RJ, Staals J. Predicting Prognosis of Intracerebral Hemorrhage (ICH): Performance of ICH Score Is Not Improved by Adding Oral Anticoagulant Use. Front Neurol. 2018 Feb 28;9:100. doi: 10.3389/fneur.2018.00100. eCollection 2018. PubMed PMID: 29541054; PubMed Central PMCID: PMC5836590.
3)

Hemphill JC III, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;14:891–897. doi: 10.1161/01.STR.32.4.891.
4)

Malinova V, Iliev B, Mielke D, Rohde V. Intracerebral Hemorrhage-Score Allows a Reliable Prediction of Mortality in Patients with Spontaneous Intracerebral Hemorrhage Managed by Fibrinolytic Therapy. Cerebrovasc Dis. 2019 Nov 13:1-6. doi: 10.1159/000504246. [Epub ahead of print] PubMed PMID: 31722333.
5)

McCracken DJ, Lovasik BP, McCracken CE, Frerich JM, McDougal ME, Ratcliff JJ, Barrow DL, Pradilla G. The Intracerebral Hemorrhage Score: A Self-Fulfilling Prophecy? Neurosurgery. 2018 May 14. doi:

Hydrocephalus after aneurysmal subarachnoid hemorrhage

Hydrocephalus after aneurysmal subarachnoid hemorrhage

Epidemiology

Hydrocephalus complicates the clinical course of greater than 20% of patients with aneurysmal subarachnoid hemorrhage 1) 2) , and its onset can be acute, within 48 hours after SAH, or rarely chronic, occurring in a delayed fashion weeks and even months after the hemorrhage.

Etiology

The etiology of hydrocephalus following aSAH has yet to be fully elucidated, but is likely to include the following: obstruction of CSF flow within the basal cisterns and/or ventricles by clotted blood, diminished absorption at the arachnoid granulations, and inflammation 3) 4) 5) 6).

Na et al. found that higher sodium, lower potassium, and higher glucose levels were predictive values for shunt-dependent hydrocephalus from postoperative day (POD) 1 to POD 12-16 after subarachnoid hemorrhage. Strict correction of electrolyte imbalance seems necessary to reduce shunt-dependent hydrocephalus. Further large studies are warranted to confirm the findings 7).

Data suggest that the volume of the third ventricle in the initial CT is a strong predictor for shunt dependency after aSAH 8).

Diagnosis

Early recognition of its signs and symptoms and accurate interpretation of computed tomography (CT) studies are important for the management of patients with SAH. Clinically, a poor neurologic grade has the highest correlation with an increased incidence of hydrocephalus. Radiographically, the bicaudate index on CT studies has emerged as the best marker of this condition. Although further studies are needed to understand the complex pathophysiology of this condition, hydrocephalus after SAH can be treated effectively using current technology 9).


Most readmissions after aneurysmal subarachnoid hemorrhage (SAH) relate to late consequences of hemorrhage, such as hydrocephalus, or medical complications secondary to severe neurological injury. Although a minority of readmissions may potentially be avoided with closer medical follow-up in the transitional care environment, readmission after SAH is an insensitive and likely inappropriate hospital performance metric 10).

Data demonstrate that gender influences acute hydrocephalus development in a rat SAH model. Future studies should determine the role of estrogen in SAH-induced hydrocephalus 11).

Hydrocephalus might cause gradual obtundation in the first few hours or days; it can be treated by lumbar puncture or ventricular drainage, dependent on the site of obstruction

Aneurysmal subarachnoid hemorrhage (SAH) has been reported to induce an intrathecal inflammatory reaction reflected by cytokine release, particularly interleukin-6 (IL-6), which correlates with early brain damage and poor outcome.

Treatment

Hydrocephalus might cause gradual obtundation in the first few hours or days; it can be treated by lumbar puncture or ventricular drainage, dependent on the site of obstruction 12).

Outcome

Hydrocephalus is a common and potentially devastating complication of aneurysmal subarachnoid hemorrhage (SAH).

Hydrocephalus leads to prolonged hospital and ICU stays, well as to repeated surgical interventions, readmissions, and complications associated with ventriculoperitoneal shunts, including shunt failure and shunt infection. Whether variations in surgical technique at the time of aneurysm treatment may modify rates of shunt dependency remains a matter of debate 13).

Shunt dependency

The indication for and the timing of a permanent shunt operation in patients following acute hydrocephalus (HC) after subarachnoid hemorrhage (SAH) remains controversial because risk factors for chronic HC fail to predict permanent shunt dependency. The amount of cerebrospinal fluid (CSF) drained via an external ventricular drain (EVD) may predict shunt dependency.

Results suggest that the daily amount of external CSF drainage volume in the acute state of SAH might influence the development of HC 14).


CSF IL-6 values of ≥10,000 pg/ml in the early post-SAH period may be a useful diagnostic tool for predicting shunt dependency in patients with acute posthemorrhagic hydrocephalus. The development of shunt-dependent posthemorrhagic hydrocephalus remains a multifactorial process 15).

Reliable prognostic tools to estimate the case fatality rate (CFR) and the development of chronic hydrocephalus (CHC) in aneurysmal subarachnoid hemorrhage (SAH) are not well defined.

Graeb Score or LeRoux score improve the prediction of shunt dependency and in parts of CFR in aneurysmal SAH patients therefore confirming the relevance of the extent and distribution of intraventricular blood for the clinical course in SAH 16).

Case series

One-hundred and fifty-two patients who had undergone an operation for SAH were enrolled in this study. Clinical data, radiological data, and procedural data were investigated. Procedural data included the operating technique (clipping vs. EVT) and the use of additional procedures (no procedure, lumbar drainage, or EVD). Delayed hydrocephalus was defined as a condition in which the Evan’s index was 0.3 or higher, as assessed using brain computed tomography more than 2 weeks after surgery, requiring shunt placement due to neurological deterioration.

Of the 152 patients, 45 (29.6%) underwent surgical clipping and 107 (70.4%) underwent EVT. Twenty-five (16.4%) patients developed delayed hydrocephalus. Age (p = 0.019), procedure duration (p = 0.004), and acute hydrocephalus (p = 0.030) were significantly correlated with the incidence of delayed hydrocephalus. However, the operation technique (p = 0.593) and use of an additional procedure (p = 0.378) were not significantly correlated with delayed hydrocephalus incidence.

No significant difference in the incidence of delayed hydrocephalus was associated with operation technique or use of an additional procedure in patients with SAH. However, delayed hydrocephalus was significantly correlated with old age, long procedural duration, and acute hydrocephalus. Therefore, they recommend that additional procedures should be discontinued as soon as possible 17).

2017

Winkler et al. conducted a retrospective review of 663 consecutive patients with aSAH treated from 2005 to 2015 by open microsurgery via a pterional or orbitozygomatic craniotomy by the senior author (M.T.L.). Data collected from review of the electronic medical record included age, Hunt and Hess grade, Fisher grade, need for an external ventricular drain, and opening pressure. Patients were stratified into those undergoing no fenestration and those undergoing tandem fenestration of the LT and MoL at the time of surgical repair. Outcome variables, including VP shunt placement and timing of shunt placement, were recorded and statistically analyzed. RESULTS In total, shunt-dependent hydrocephalus was observed in 15.8% of patients undergoing open surgical repair following aSAH. Tandem microsurgical fenestration of the LT and MoL was associated with a statistically significant reduction in shunt dependency (17.9% vs 3.2%, p < 0.01). This effect was confirmed with multivariate analysis of collected variables (multivariate OR 0.09, 95% CI 0.03-0.30). Number-needed-to-treat analysis demonstrated that tandem fenestration was required in approximately 6.8 patients to prevent a single VP shunt placement. A statistically significant prolongation in days to VP shunt surgery was also observed in patients treated with tandem fenestration (26.6 ± 19.4 days vs 54.0 ± 36.5 days, p < 0.05). CONCLUSIONS Tandem fenestration of the LT and MoL at the time of open microsurgical clipping and/or bypass to secure ruptured anterior and posterior circulation aneurysms is associated with reductions in shunt-dependent hydrocephalus following aSAH. Future prospective randomized multicenter studies are needed to confirm this result 18).


181 participants with a mean age of 54.4 years. Higher sodium (hazard ratio, 1.53; 95% confidence interval, 1.13-2.07; p = 0.005), lower potassium, and higher glucose levels were associated with higher shunt-dependent hydrocephalus. The receiver operating characteristic curve analysis showed that the areas under the curve of sodium, potassium, and glucose were 0.649 (cutoff value, 142.75 mEq/L), 0.609 (cutoff value, 3.04 mmol/L), and 0.664 (cutoff value, 140.51 mg/dL), respectively.

Despite the exploratory nature of this study, we found that higher sodium, lower potassium, and higher glucose levels were predictive values for shunt-dependent hydrocephalus from postoperative day (POD) 1 to POD 12-16 after subarachnoid hemorrhage. Strict correction of electrolyte imbalance seems necessary to reduce shunt-dependent hydrocephalus. Further large studies are warranted to confirm our findings 19).

2016

The study is designed to determine the efficacy of lamina terminalis fenestration on the reduction of SDH after aneurysm clipping.

METHODS/DESIGN: A total of 288 patients who meet the inclusion criteria will be randomized into single aneurysm clipping or aneurysm clipping plus FLT in the Department of Neurosurgery, West China Hospital. Follow-up was performed 1, 3, 6, and 12 months after aneurysm clipping. The primary outcome is the incidence of SDH and the secondary outcomes include cerebral vasospasm, functional outcome evaluated by the modified Rankin Scale and Extended Glasgow Outcome Scale, and mortality.

DISCUSSION: The FISH trial is a large randomized, parallel controlled clinical trial to define the therapeutic value of FLT, the results of which will help to guide the surgical procedure and resolve the long-puzzled debate in the neurosurgical community.

CONCLUSIONS: This protocol will determine the efficacy of FLT in the setting of aneurysmal subarachnoid hemorrhage 20).

2003

Seven hundred eighteen patients with aneurysmal subarachnoid hemorrhage who were treated between 1990 and 1999 were retrospectively studied, to identify factors contributing to shunt-dependent hydrocephalus. With these data, a stepwise logistic regression procedure was used to determine the effect of each variable on the development of hydrocephalus and to create a scoring system.

Overall, 152 of the 718 patients (21.2%) underwent shunting procedures for treatment of hydrocephalus. Four hundred seventy-nine of the patients (66.7%) were female. Of the factors investigated, the following were associated with shunt-dependent hydrocephalus, as determined with a variety of statistical methods: 1) increasing age (P < 0.001), 2) female sex (P = 0.015), 3) poor admission Hunt and Hess grade (P < 0.001), 4) thick subarachnoid hemorrhage on admission computed tomographic scans (P < 0.001), 5) intraventricular hemorrhage (P < 0.001), 6) radiological hydrocephalus at the time of admission (P < 0.001), 7) distal posterior circulation location of the ruptured aneurysm (P = 0.046), 8) clinical vasospasm (P < 0.001), and 9) endovascular treatment (P = 0.013). The presence of intracerebral hematomas, giant aneurysms, or multiple aneurysms did not influence the development of shunt-dependent hydrocephalus.

The results of this study can help identify patients with a high risk of developing shunt-dependent hydrocephalus. This may help neurosurgeons expedite treatment, may decrease the cost and length of hospital stays, and may result in improved outcomes 21).

2000

In 138 patients with ruptured cerebral aneurysms operated on within 48 to 72 hours after subarachnoid hemorrhage, an external ventricular drainage catheter was inserted before craniotomy and was used intermittently during the first week after surgery. In 51 patients, intracranial pressure (ICP) was measured intraoperatively. The majority of patients showed increased ICP intraoperatively irrespective of the preoperative Hunt and Hess grade and the amount of subarachnoid blood accumulation or intraventricular blood clot. Intraoperative drainage of cerebrospinal fluid allowed easy access for aneurysm dissection by making the brain slack in more than 90% of patients. Postoperative ICP measurements revealed that significant brain swelling did not occur in the majority of patients. In 7 patients, persistently elevated ICP (greater than 20 mm Hg) was recorded. Nine patients (8%) developed shunt-dependent hydrocephalus; all of these patients had suffered an intraventricular hemorrhage. Measurements of the volumes of cerebrospinal fluid drained did not allow prediction of shunt-dependent hydrocephalus 22).

1987

The incidence and clinical aspects of acute hydrocephalus were examined in 200 patients with recently ruptured intracranial aneurysms. The following conclusions were reached: Acute hydrocephalus is an important complication of aneurysmal subarachnoid hemorrhage that occurs in approximately 20% of all cases and exhibits an incidence that tends to parallel clinical grade (Grade I, 3%; Grade II, 5%; “Good” Grade III, 21%; “Bad”Grade III, 40%; Grade IV, 42%; Grade V, 26%). Impaired consciousness leading to a general downgrading of clinical status was the predominant clinical finding (93%), but neither this nor other nonspecific signs of increased intracranial pressure were distinguishable from the effects of the precipitating hemorrhage. The computed tomographic signs of acute hydrocephalus are distinctive and consist of selective ballooning of the frontal horns, rostral-caudal enlargement of the cerebral ventricles, and a halo of periventricular hyperdensity (edema) that evolves in sequence with ventricular changes. The treatment of choice is external ventricular drainage, which results in prompt and often dramatic improvement in approximately two-thirds of the patients 23).

1985

Hydrocephalus, defined as a bicaudate index above the 95th percentile for age, was found in 34 (20%) of 174 prospectively studied patients with subarachnoid hemorrhage (SAH) who survived the first 24 hours and who underwent computerized tomography (CT) scanning within 72 hours. The occurrence of acute hydrocephalus was related to the presence of intraventricular blood, and not to the extent of cisternal hemorrhage. The level of consciousness was depressed in 30 of the 34 patients. Characteristic clinical features were present in 19 patients, including a gradual obtundation after the initial hemorrhage in 16 patients and small nonreactive pupils in nine patients (all with a Glasgow Coma Scale score of 7 or less). In the remaining 15 patients (44%), the diagnosis could be made only by CT scanning. After 1 month, 20 of the 34 patients had died: six from rebleeding (four after shunting), 11 from cerebral infarction (eight after an initial improvement), and three from other or mixed causes. Only one of nine patients in whom a shunt was placed survived, despite rapid improvement in all immediately after shunting. The mortality rate among patients with acute hydrocephalus was significantly higher than in those without, with the higher incidence caused by cerebral infarction (11 of 34 versus 12 of 140 cases, respectively; p less than 0.001). Death from infarction could not be attributed to the extent of cisternal hemorrhage, the use of antifibrinolytic drugs, or failure to apply surgical drainage, but could often be explained by the development of hyponatremia, probably accompanied by hypovolemia 24).

1984

Seventeen patients suffering from SAH and/or intraventricular hemorrhage were studied; all were admitted in Grades II to V according to Hunt and Hess. Eleven patients had a proven aneurysm. The ICP, monitored via an intraventricular catheter, was above 15 mm Hg (2 kPa) during part of the monitoring period in all patients. B-waves at 1/min were noted in all patients. Resistance to outflow of CSF was determined by the following techniques: 1) bolus injection; 2) constant-rate steady-state infusion; or 3) controlled withdrawal (“inverse infusion”). Resistance to outflow of CSF was increased in all patients, ranging from 11.5 to 85 mm Hg/ml/min. The ICP was linearly correlated with outflow resistance. Four (50%) of the eight survivors required a shunt. Neither the presence of hydrocephalus on admission, nor the level of ICP, nor the magnitude of resistance to outflow of CSF was clearly related to the requirement of a permanent CSF diversion 25).

References

1)

Wilson CD, Safavi-Abbasi S, Sun H, Kalani MY, Zhao YD, Levitt MR, et al: Meta-analysis and systematic review of risk factors for shunt dependency after aneurysmal subarachnoid hemorrhage. J Neurosurg 126:586–595, 2017
2)

Yamada S, Nakase H, Park YS, Nishimura F, Nakagawa I: Discriminant analysis prediction of the need for ventriculo- peritoneal shunt after subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 21:493–497, 2012
3) , 22)

Auer LM, Mokry M. Disturbed cerebrospinal fluid circulation after subarachnoid hemorrhage and acute aneurysm surgery. Neurosurgery. 1990 May;26(5):804-8; discussion 808-9. PubMed PMID: 2352599.
4)

Dorai Z, Hynan LS, Kopitnik TA, Samson D: Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 52:763–771, 2003
5)

Massicotte EM, Del Bigio MR. Human arachnoid villi response to subarachnoid hemorrhage: possible relationship to chronic hydrocephalus. J Neurosurg. 1999 Jul;91(1):80-4. PubMed PMID: 10389884.
6) , 24)

van Gijn J, Hijdra A, Wijdicks EF, Vermeulen M, van Crevel H. Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg. 1985 Sep;63(3):355-62. PubMed PMID: 4020461.
7)

Na MK, Won YD, Kim CH, Kim JM, Cheong JH, Ryu JI, Han MH. Early variations of laboratory parameters predicting shunt-dependent hydrocephalus after subarachnoid hemorrhage. PLoS One. 2017 Dec 12;12(12):e0189499. doi: 10.1371/journal.pone.0189499. eCollection 2017. PubMed PMID: 29232410; PubMed Central PMCID: PMC5726740.
8)

Pinggera D, Kerschbaumer J, Petr O, Ortler M, Thomé C, Freyschlag CF. The Volume of the Third Ventricle as a Prognostic Marker for Shunt Dependency After Aneurysmal Subarachnoid Hemorrhage. World Neurosurg. 2017 Dec;108:107-111. doi: 10.1016/j.wneu.2017.08.129. Epub 2017 Sep 1. PubMed PMID: 28867328.
9)

Germanwala AV, Huang J, Tamargo RJ. Hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am. 2010 Apr;21(2):263-70. doi: 10.1016/j.nec.2009.10.013. Review. PubMed PMID: 20380968.
10)

Greenberg JK, Washington CW, Guniganti R, Dacey RG Jr, Derdeyn CP, Zipfel GJ. Causes of 30-day readmission after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2016 Mar;124(3):743-9. doi: 10.3171/2015.2.JNS142771. Epub 2015 Sep 11. PubMed PMID: 26361278.
11)

Shishido H, Zhang H, Okubo S, Hua Y, Keep RF, Xi G. The Effect of Gender on Acute Hydrocephalus after Experimental Subarachnoid Hemorrhage. Acta Neurochir Suppl. 2016;121:335-9. doi: 10.1007/978-3-319-18497-5_58. PubMed PMID: 26463971.
12)

van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007 Jan 27;369(9558):306-18. Review. PubMed PMID: 17258671.
13) , 18)

Winkler EA, Burkhardt JK, Rutledge WC, Rick JW, Partow CP, Yue JK, Birk H, Bach AM, Raygor KP, Lawton MT. Reduction of shunt dependency rates following aneurysmal subarachnoid hemorrhage by tandem fenestration of the lamina terminalis and membrane of Liliequist during microsurgical aneurysm repair. J Neurosurg. 2017 Dec 15:1-7. doi: 10.3171/2017.5.JNS163271. [Epub ahead of print] PubMed PMID: 29243978.
14)

Hayek MA, Roth C, Kaestner S, Deinsberger W. Impact of External Ventricular Drainage Volumes on Shunt Dependency after Subarachnoid Hemorrhage. J Neurol Surg A Cent Eur Neurosurg. 2016 Jul 22. [Epub ahead of print] PubMed PMID: 27448196.
15)

Wostrack M, Reeb T, Martin J, Kehl V, Shiban E, Preuss A, Ringel F, Meyer B, Ryang YM. Shunt-Dependent Hydrocephalus After Aneurysmal Subarachnoid Hemorrhage: The Role of Intrathecal Interleukin-6. Neurocrit Care. 2014 May 20. [Epub ahead of print] PubMed PMID: 24840896.
16)

Czorlich P, Ricklefs F, Reitz M, Vettorazzi E, Abboud T, Regelsberger J, Westphal M, Schmidt NO. Impact of intraventricular hemorrhage measured by Graeb and LeRoux score on case fatality risk and chronic hydrocephalus in aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2015 Jan 21. [Epub ahead of print] PubMed PMID: 25599911.
17)

Eom TO, Park ES, Park JB, Kwon SC, Sim HB, Lyo IU, Kim MS. Does Neurosurgical Clipping or Endovascular Coiling Lead to More Cases of Delayed Hydrocephalus in Patients with Subarachnoid Hemorrhage? J Cerebrovasc Endovasc Neurosurg. 2018 Jun;20(2):87-95. doi: 10.7461/jcen.2018.20.2.87. Epub 2018 Jun 30. PubMed PMID: 30370242; PubMed Central PMCID: PMC6196142.
19)

Na MK, Won YD, Kim CH, Kim JM, Cheong JH, Ryu JI, Han MH. Early variations of laboratory parameters predicting shunt-dependent hydrocephalus after subarachnoid hemorrhage. PLoS One. 2017 Dec 12;12(12):e0189499. doi: 10.1371/journal.pone.0189499. eCollection 2017. PubMed PMID: 29232410.
20)

Tao C, Fan C, Hu X, Ma J, Ma L, Li H, Liu Y, Sun H, He M, You C. The effect of fenestration of the lamina terminalis on the incidence of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage (FISH): Study protocol for a randomized controlled trial. Medicine (Baltimore). 2016 Dec;95(52):e5727. doi: 10.1097/MD.0000000000005727. PubMed PMID: 28033279; PubMed Central PMCID: PMC5207575.
21)

Dorai Z, Hynan LS, Kopitnik TA, Samson D. Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2003 Apr;52(4):763-9; discussion 769-71. PubMed PMID: 12657171.
23)

Milhorat TH. Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1987 Jan;20(1):15-20. PubMed PMID: 3808257.
25)

Kosteljanetz M. CSF dynamics in patients with subarachnoid and/or intraventricular hemorrhage. J Neurosurg. 1984 May;60(5):940-6. PubMed PMID: 6716162.

Internal carotid artery bifurcation aneurysm

Internal carotid artery bifurcation aneurysm

Internal carotid artery bifurcation aneurysms are subtype of internal carotid artery aneurysm.

They settle in an area of ​​great hemodynamic stress. This characteristic, together with the fact that it affects young individuals, a tendency to growth and bleeding, a high rate of early bleeding and an unfavorable neck-bottom relationship, make these brain aneurysms good candidates for microsurgical treatment versus endovascular treatment. However, and even considering that the incidence of these aneurysms is relatively low, references in the literature on this subgroup of aneurysms are very scarce 1)2) 3) 4) 5) 6) 7) 8).

Sakamoto et al. studied the location of the aneurysm sac and showed that they somewhat deviate towards the exit of the A1, where hemodynamic stress would be higher 9).

Some cases have been described associated with agenesis or internal carotid fenestration 10).

Epidemiology

Internal carotid artery bifurcation aneurysms represent between 2.4% and 4% of all intracranial aneurysm11) 12) 13) 14).

Clinical Feaures

They are characterized clinically by their tendency to occur at a younger age.

The most frequent clinical presentation is subarachnoid hemorrhage, although in the Gonzalez-Darder et al. series most of the intervened cases were discovered by chance. In the literature, it is described that some patients present with the ophthalmologic clinic by compression of the optic belt. Since the aneurysm is buried in the sinus of the frontal lobe, the association of a frontal hematoma that rises towards the caudate is typical and can open to the lateral ventricle, often associating long-path deficits. As in the series described, most of our patients were female and many of them young. This last fact implies the need to study associated risk factors, especially vascular dysplasias, connective diseases, and polycystic kidney disease. At the time of diagnosis, aneurysms are usually medium or large in size, giant aneurysms being exceptional 15).

Complications

They frequently rupture at a younger age compared to other intracranial aneurysms 16).

Additionally, the increased hemodynamic stress at this level translates into a higher rate of recurrent aneurysm compared with aneurysms in other locations 17) 18)

Classification

Projection

Superior

Anterior

Posterior

Treatment

Treatment is recommended since they tend to bleed at a lower age than other aneurysms 19).

The presence of multiple perforators in this area along with the angle of origin often skewed toward the MCA or the anterior cerebral artery primarily can make treatment challenging 20).

They are surgically characterized by the technical difficulties posed by their domes being adherent to the frontal lobe, their location at the apex of the sylvian fissure, and their relation to myriad perforator complexes 21).

Surgical treatment

The surgical treatment of ICA bifurcation aneurysms is particularly challenging, due to their location at the highest point of the ICA and the presence of multiple perforators at this level that may be adherent to the back side of the aneurysm 22)

Endovascular treatment

Endovascular treatment of ICA bifurcation aneurysms is feasible and effective and is associated with high immediate angiographic occlusion rates. However, retreatment rates and procedure-related morbidity and mortality are non-negligible 23).

Periprocedural complications following endovascular treatment of ICA terminus aneurysms are not negligible. Aneurysms at this location are at a high risk of ischemic stroke in the territory of the ipsilateral MCA (either from distal emboli during the procedure or clot formation at the level of the neck with impairment of distal MCA flow), a potential source of serious morbidity and mortality 24) 25) 26).

In the meta-analysis of Morales-Valero et al., perioperative morbidity rates were approximately 4% and mortality rates were 3%. Perioperative stroke was a major contributor to morbidity and mortality, occurring in approximately 3% of patients. Although good long-term neurologic outcome was achieved in 90% of patients regardless of aneurysm rupture status, the periprocedural complication rate reported is not trivial. Particularly worrisome is the procedure-related mortality of 4% for unruptured and 6% for ruptured ICA bifurcation aneurysms. These findings stress the importance of proper patient selection because these aneurysms are often adequately and effectively treatable with surgical clip ligation. The high retreatment rate observed in the meta-analysis and in the own series is similar to that reported for aneurysms located in other bifurcation points 27).

Videos

Case series

2018

Fifty-one patients with ICAbifAs were treated in the study period out of which 40 patients underwent microsurgical clipping. The median age was 48 yr (range 14-68 yr). Nearly 95% of the patients presented in a good clinical grade (World Federation of Neurological Surgeons grade 1 and 2). At 6-mo follow-up, 36 patients (90%) had good clinical outcome (Glasgow Outcome Scale 4 and 5). According to their direction, ICAbifAs were grouped as anteriorly directed (10 cases), superiorly directed (23 cases), and posteriorly directed (7 cases). Operative techniques and nuances utilized depend on aneurysmal direction and are presented here.

An appropriate surgical strategy based on the direction of ICAbifAs as per the preoperative radiology, meticulous dissection of aneurysmal wall from adjacent perforators, and clip application with the aim of remodeling the ICA bifurcation are integral to achieving a good outcome 28).

2016

Fifty-nine patients with 61 unruptured ICAbifAs were included. Seven aneurysms were treated surgically (11.5 %), 22 underwent endovascular treatment (36 %), and 32 were managed conservatively (52.5 %). In the surgical group, short- and long-term complete aneurysm occlusion rates were 100 % with no cases of perioperative or long-term permanent morbidity or treatment-related mortality. In the endovascular group, two patients (11.7 %) with giant aneurysms had perioperative thromboembolic events with transient morbidity. There was one case of aneurysm rupture at follow-up in a giant aneurysm treated with partial coil embolization. Complete/near-complete occlusion rates were 63 %. There was one case of aneurysm rupture after 114 aneurysm-years of follow-up in the conservative management group (0.89 %/year), but no ruptures were observed in small aneurysms selected for conservative management.

Unruptured small ICAbifAs have a benign natural history. In patients selected for treatment, excellent results can be achieved in the vast majority of patients with judicious use of endovascular and surgical therapy 29).

2015

A total of 58 patients with ICA bifurcation aneurysms were treated. By interdisciplinary consensus, 30 aneurysms were assigned for coiling and 28 for clipping. Patients who underwent surgical clipping were younger and had larger aneurysms. More patients were assigned to coiling if their aneurysms originated only from the ICA bifurcation or projected superiorly. For the combined angiographic endpoint, complete and nearly complete occlusion (Raymond-Roy I + II), similar rates of 96% (coiling) or 100% (clipping) could be achieved. Raymond-Roy I occlusion occurred more often after clipping (79% vs 41% coiling). Follow-up of the endovascular group showed minor recanalization of the aneurysm neck (Raymond-Roy II) in 42%. One patient (4%) showed a major recanalization (Raymond-Roy III) and needed re-treatment. For incidental findings, no bleeding complications or new persistent neurological deficits occurred during follow-up.

Treatment of ICA bifurcation aneurysms after interdisciplinary assignment to clipping or coiling is effective and safe. Despite significantly more minor recanalizations after coiling, the re-treatment rate was very low, and no bleeding was observed during follow-up. Multivariate analysis revealed that origin only from the ICA bifurcation was an independent predictor of aneurysm recanalization after endovascular treatment 30).

2014

The records of 65 patients with 66 ICA BA were retrieved from data prospectively accrued between September 1999 and July 2013. Clinical and morphological outcomes of the aneurysms were assessed, including technical aspects of treatment.

The aneurysms under study were directed either superiorly (41/66, 62.1%), anteriorly (24/66, 36.4%), or posteriorly (1/66, 1.5%), and all were devoid of perforators. Aneurysmal necks were situated symmetrically at the terminal ICA (37/66, 56.1%) or slightly deviated to the proximal A1 segment (29/66, 43.9%). The steam-shaped S microcatheter (73.8%) was most commonly used to select the aneurysms, and the single microcatheter technique was most commonly applied (56.1%) to perform coil embolization, followed by balloon remodelling (21.2%), multiple microcatheter (15.1%), and stent-protection (7.6%). Successful aneurysmal occlusion was achieved in 100% of cases, with no procedure-related morbidity or mortality. Imaging performed in the course of follow-up (mean duration 27.3 months) confirmed stable occlusion of most lesions (47/53, 88.7%).

Through tailored technical strategies, ICA BA are amenable to safe and effective endovascular coil embolization, with a tendency for stable occlusion long-term 31).


Morales-Valero et al. performed a comprehensive literature search for reports on contemporary endovascular treatment of ICA bifurcation aneurysms from 2000 to 2013, and we reviewed our experience. We extracted information regarding periprocedural complications, procedure-related morbidity and mortality, immediate angiographic outcome, long-term clinical and angiographic outcome, and retreatment rate. Event rates were pooled across studies by using random-effects meta-analysis.

Including our series of 37 patients, 6 studies with 158 patients were analyzed. Approximately 60% of the aneurysms presented as unruptured; 88.0% (95% CI, 68.0%-96.0%) of aneurysms showed complete or near-complete occlusion at immediate postoperative angiography compared with 82.0% (95% CI, 73.0%-88.0%) at last follow-up. The procedure-related morbidity and mortality were 3.0% (95% CI, 1.0%-7.0%) and 3.0% (95% CI, 1.0%-8.0%), respectively. The retreatment rate was 14.0% (95% CI, 8.0%-25.0%). Good neurologic outcome was achieved in 93.0% (95% CI, 86.0%-97.0%) of patients.

Endovascular treatment of ICA bifurcation aneurysms is feasible and effective and is associated with high immediate angiographic occlusion rates. However, retreatment rates and procedure-related morbidity and mortality are non-negligible 32).

2007

Internal carotid artery (ICA) bifurcation aneurysms are relatively uncommon and frequently rupture at a younger age compared to other intracranial aneurysms.

Gupta et al treated a total of 999 patients for intracranial aneurysms, of whom 89 (8.9%) had ICA bifurcation aneurysms, and 42 of the 89 patients were 30 years of age or younger. The study analyzed the clinical records of 70 patients with ICA bifurcation aneurysms treated from mid 1997 to mid 2003. Multiple aneurysms were present in 15 patients. Digital subtraction angiography films were studied in 55 patients to identify vasospasm and aneurysm projection. The aneurysm projected superiorly in most of these patients (37/55, 67.3%).

They preferred to minimize frontal lobe retraction, so widely opened the sylvian fissure to approach the ICA bifurcation and aneurysm neck. Elective temporary clipping was employed before the final dissection and permanent clip application. Vasospasm was present in 24 (43.6%) of 55 patients. Forty-eight (68.6%) of the 70 patients had good outcome, 14 (20%) had poor outcome, and eight (11.4%) died. Patients with ICA bifurcation aneurysms tend to bleed at a much younger age compared to those with other intracranial aneurysms. Wide opening of the sylvian fissure and elective temporary clipping of the ICA reduces the risk of intraoperative rupture and perforator injury. Mortality was mainly due to poor clinical grade and intraoperative premature aneurysm rupture 33).

2002

A series of 25 patients treated by clipping under the operating microscope are analyzed and compared with previous cases. Twenty-five patients, 11 men and 14 women (mean age 51 years), were treated by the same neurosurgeon. Seventeen patients presented with subarachnoid hemorrhage (Hunt & Kosnik Grade I in three, II in five, III in two, IV in seven), five with unruptured ICA bifurcation aneurysms, and three with unruptured ICA bifurcation aneurysms but another ruptured aneurysm. There were 23 small, one large, and one giant ICA bifurcation aneurysms. The projection was superior in 12, anterior in seven, and posterior in six cases. Pterional approach was employed for all cases. Outcomes were evaluated at discharge with the Glasgow Outcome Scale. Favorable outcomes (good recovery (GR) and moderate disability (MD)) were obtained in ten of 17 patients with ruptured ICA bifurcation aneurysm. Favorable outcomes were significantly greater in Grades I and II (three in I, four in II) than in Grades III and IV (one in III, two in IV; P=0.0498). Seven of eight patients with unruptured ICA bifurcation aneurysm had favorable outcomes. Temporary clipping and projection of the aneurysm did not affect the outcome. Causative factors of unfavorable outcomes were primary brain damage in cases of small and large aneurysms and perforator damage in the case of giant aneurysm. Poor clinical grade and vasospasm are the causative factors of poor outcome in patients with ruptured ICA bifurcation aneurysm. Preservation of perforators is crucial in cases of giant aneurysm. Clipping of unruptured ICA bifurcation aneurysms is recommended since they tend to bleed at a lower age than other aneurysms 34).

Case reports

Mahajan et al. reported a unique case of recanalized left internal carotid artery aneurysm with thrombus adherent to the aneurysm neck and M1 origin diagnosed on 2-dimensional angiography causing embolic stroke in a 66-year-old female who was successfully treated with stent-assisted coiling. This is important to recognize as a cause of embolic stroke 35).

2015

A 70-year-old man with progressive visual disturbances, left superior quadrantanopsia, and right-sided papilledema underwent imaging that demonstrated a right internal carotid artery (ICA) terminus aneurysm with third-ventricle mass effect and ipsilateral optic nerve and chiasm compression. We performed a right modified orbitozygomatic craniotomy, with proximal control and dissection of the aneurysm and small perforator arteries. Temporary ICA and anterior cerebral artery (ACA) clips allowed placement of a large curved permanent clip, reconstructing the ICA bifurcation and maintaining adequate patency of the ACA and middle cerebral artery. Complete aneurysm obliteration was confirmed by intraoperative indocyanine green angiography and postoperative CT angiography. The video can be found here: http://youtu.be/5WEEgmA-g2A 36).


A 64-year-old woman, with visual deficit, harboring a large wide-necked aneurysm located at the junction between left internal carotid artery and left A1 segment of anterior cerebral artery, was submitted to endovascular treatment. As she had pre-existing occlusion of left internal carotid, approach from the contralateral internal carotid was used to advance the pipeline embolization device through the anterior communicating artery and place the flow diverter horizontally across the neck (from M1 to A1). Coil embolization was also performed through a microcatheter navigated via posterior communicating artery. The intervention was uneventful, with total aneurysm occlusion. Patient presented with visual improvement on follow-up.

Horizontal deployment of pipeline embolization device appears to be an acceptable and feasible alternative to treat internal carotid bifurcation aneurysms. Long-term follow-up and a greater number of cases are mandatory to establish the safety of this strategy 37).


In a video presentation, a 68-year-old male with a large ruptured right ICA bifurcation aneurysm is presented. The patient’s neurological exam was rapidly deteriorating, therefore the patient was transferred to the operating theater after initial evaluation by CT and CT angiogram. A pterional craniotomy was performed, the frontal hematoma was partially removed and the aneurysm was clipped. Residual hematoma was removed after securing the aneurysm and the aneurysm dome was punctured(detail of surgical clipping in the video). Patient made a good recovery at 2 weeks post-op with complete recovery of left sided weakness, and some remaining cognitive deficit. The video can be found: http://youtu.be/dKFWptdgC4M 38).


Cikla et al. presented a 66-year-old man with seizures, aphasia, and hemiparesis. Work-up revealed a giant partially thrombosed aneurysm of the internal carotid artery bifurcation with surrounding vasogenic edema. He underwent clip reconstruction of the aneurysm via a cranio-orbital approach. Although they prepared for bypass with the radial artery and/or the superficial temporal artery, they were able to clip-reconstruct the aneurysm without bypass. The patient improved upon his pre-morbid state after surgery and made an excellent recovery. The video can be found in http://youtu.be/P_10hRQFuPo 39).

2012

A report of Zhang et al. documented the treatment of a giant aneurysm of the internal carotid artery bifurcation with a fistula to the cavernous sinus, which appeared following closed head trauma. A 39-year-old man suffered from blunt head trauma in an automobile accident. Two weeks after the trauma, progressive chemosis of the left eye was presented. Four months after the trauma, digital subtraction angiography showed an internal carotid artery bifurcation aneurysm, with drainage into the cavernous sinus. The lesion was successfully obliterated with preservation of the parent artery by using coils in conjunction with Onyx. Follow-up angiography obtained 3 months postoperatively revealed persistent obliteration of the aneurysm and fistula as well as patency of the parent artery. Endovascular treatment involving the use of coils combined with Onyx appears to be a feasible and effective option for treatment of this hard-to-treat lesion 40).

2011

A 55-year-old man presented with intracerebral hemorrhage (ICH) without subarachnoid hemorrhage (SAH) manifesting as acute onset of consciousness disturbance and right hemiparesis. Computed tomography showed ICH mainly localized in the left putamen, but no evidence of SAH. Magnetic resonance angiography demonstrated a cerebral aneurysm originating from the bifurcation of the left internal carotid artery, which was considered to be responsible for the ICH. The patient underwent emergent intravascular surgery for coil embolization of the aneurysm, and his neurological symptoms gradually recovered with rehabilitation after surgery. Although ICH without SAH is a rare presentation of a cerebral aneurysm, ruptured cerebral aneurysm should be considered as a potential cause of ICH. The localization and extent of ICH may be suggestive of a latent cerebral aneurysm in such cases 41).

2009

A surgical case of an eleven year old boy with excellent outcome is reported, with a subsequent review on the subject. Patients may present with classical subarachnoidal hemorrhage, but also with compressive signs with bigger and unruptured lesions. Initial management of these cases is basically the same of older patients, considering their age, weight and special intensive care for infants 42).

2006

A 58-year-old hypertensive woman presenting with mild headaches underwent computed tomography, which showed a nonruptured aneurysm of the left internal carotid artery. She subsequently underwent cerebral angiography, confirming that the aneurysm was located at the left terminal carotid segment with a wide neck. INTERVENTION: Using a cross-over approach from the contralateral internal carotid artery, a new self-expandable stent was advanced through the anterior communicating artery and placed horizontally across the aneurysm neck. Aneurysm occlusion was performed by subsequent trans-stent catheterization of the aneurysm and coil packing.

Successful stent placement allowed subtotal coil occlusion of the aneurysm with a good anatomic and clinical result. No complications were encountered. The new self-expandable stent is a highly flexible, low-profile device that can be safely navigated through tortuous intracranial vessels even in a crossover technique. Its radial force and closed cell design is suitable for stent-assisted coiling and may be superior to stents with an open cell design 43).

2005

Spontaneous pure acute subdural haematoma (ASDH) without intraparenchymal or subarachnoid haemorrhage caused by a ruptured cerebral aneurysm is extremely rare. The present case is the first report of an internal carotid artery bifurcation aneurysm presenting as pure ASDH. Suitable diagnostic investigations and therapeutic strategies are discussed. Arterial origin of bleeding should be considered in all cases of non-traumatic ASDH and a vascular anomaly has to be excluded. The neurological status on admission dictates the appropriate timing and methodology of the neuroradiological investigations 44).

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