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Minimally Invasive Evacuation of Spontaneous Cerebellar Intracerebral Hemorrhage
Original Article
Minimally Invasive Evacuation of Spontaneous Cerebellar Intracerebral Hemorrhage Christopher P. Kellner1, Frank Moore1,2, Marc S. Arginteanu1,2, Alfred A. Steinberger1,2, Kevin Yao1,2, Jacopo Scaggiante1, J Mocco1, Yakov Gologorsky1,2
OBJECTIVE: Spontaneous cerebellar intracerebral hemorrhage (scICH) constitutes w10% of all cases of spontaneous ICH, with a mortality of 20%e50%. Suboccipital craniectomy (SOC) is commonly performed for scICH causing brainstem compression or hydrocephalus. However, SOC requires long anesthesia times and results in a high complication rate. We present a series of patients who minimally invasive scICH evacuation as an alternative to traditional SOC.
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METHODS: We retrospectively reviewed the operative records for patients presenting to a single center from January 1, 2009 to March 1, 2017. All patients who had undergone evacuation of scICH were included in the present study. Clinical and radiographic variables were collected, including admission and postoperative Glasgow coma scale (GCS) scores, preoperative and postoperative hematoma volumes, and modified Rankin scale (mRS) scores at long-term follow-up.
mortality rate was 10% and mean long-term follow-up mRS score was 2. CONCLUSIONS: Minimally invasive scICH hematoma evacuation is a feasible alternative to SOC with numerous advantages that could lead to improved radiographic and clinical results.
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RESULTS: We identified 10 patients who had presented with scICH requiring surgery. All scICH evacuations were performed through a minicraniectomy positioned in the suboccipital area as close to the hematoma as possible. The mean patient age was 64.1 years. The mean presenting GCS score was 8.6, the mean initial hematoma volume was 25.4 mL, the mean procedure time was 57 minutes, and the mean postoperative hematoma volume was 2.8 mL. The
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Key words Craniectomy - Evacuation - Infratentorial - Intracerebral hemorrhage - Minimally invasive -
Abbreviations and Acronyms CT: Computed Tomography GCS: Glasgow coma scale ICH: Intracerebral hemorrhage mRS: Modified Rankin scale PCE: Pericavity edema PHE: Perihematomal edema
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INTRODUCTION
I
ntracerebral hemorrhage (ICH) is the most devastating form of stroke, with a 6-month mortality >40% and few effective treatment options. Spontaneous cerebellar ICH (scICH) represents 5%e10% of all cases of spontaneous ICH and results in even greater morbidity and mortality.1 Current American Heart Association guidelines have specified that scICH is the only evidence-based indication for surgical treatment and have advised surgery for those who are deteriorating neurologically or with brainstem compression and/or hydrocephalus from ventricular obstruction.2 The current surgical standard for scICH is to perform suboccipital craniectomy (SOC) with or without dural closure. However, SOC has resulted in an overall reported complication risk of w32%, including the risk of pseudomeningocele, hydrocephalus, cerebrospinal fluid leak, hematoma recurrence, infection, and long operative times in the range of 215e230 minutes.3-5
scICH: Spontaneous cerebellar intracerebral hemorrhage SOC: Suboccipital craniectomy From the 1Department of Neurosurgery, Icahn School of Medicine at Mount Sinai, New York, New York; and 2Department of Neurosurgery, Englewood Hospital and Medical Center, Englewood, New Jersey, USA To whom correspondence should be addressed: Christopher P. Kellner, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.145 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Published by Elsevier Inc.
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ORIGINAL ARTICLE CHRISTOPHER P. KELLNER ET AL.
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Figure 1. A 5-cm linear incision overlying the area at which most of the hematoma was situated and where it came closest to the surface was marked.
Recently, a substantial effort has been made to evaluate minimally invasive strategies for supratentorial ICH evacuation, including the ongoing MISTIE (minimally invasive surgery plus recombinant tissue plasminogen activator for intracerebral hemorrhage evacuation), the ENRICH trial (early minimally invasive removal of ICH), and the INVEST (minimally invasive endoscopic surgical treatment with Apollo for supratentorial intracerebral hemorrhage) trial.6-8 These same minimally invasive evacuation techniques could improve outcomes when applied to the posterior fossa. We present the results from a single-center series to
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demonstrate the feasibility of a minimally invasive technique for the treatment of scICH. METHODS The institutional board review approved the present study. A retrospective review was conducted of all surgeries performed for the treatment of cerebellar ICH at a single center from January 1, 2009 to July 1, 2017. All hemorrhages secondary to tumor, hemorrhagic transformation of ischemic stroke, or vascular malformation
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Figure 2. A 2e3-cm craniectomy was created over the hematoma, and all bone dust and bone chips were saved to fill in the minicraniectomy at the end of the procedure.
were excluded. The records were identified by meticulous review of our practice logs and billing data and confirmed by the hospital medical records department. A total of 10 operations were identified. Surgical Indications The indications for surgery included the following: computed tomography (CT) evidence of a parenchymal hematoma measuring
Figure 3. The underlying dura was opened in a stellate fashion.
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Figure 4. A 1-cm malleable retractor was used to deepen the exposure and facilitate aspiration of the clot.
3 cm or brainstem compression. A poor initial Glasgow coma scale (GCS) score did not affect the decision to perform surgery, because these patients are capable of profound and rapid recovery once the brainstem compression, intracranial hypertension, and/ or hydrocephalus have been corrected. All patients were admitted through the emergency room within 6 hours of symptom onset, and all 10 patients underwent surgery within 6 hours of presentation.
Clinical and Radiographic Data The demographic data collected included age, sex, ethnicity, medical comorbidities, pertinent medications, hospital length of stay, admission GCS score, GCS score on postoperative day 1, GCS score at discharge, and modified Rankin scale (mRS) score at long-term follow-up. The need for any secondary surgical procedures was also documented. All patients had undergone imaging studies on admission to the emergency room. All but 1 patient had postoperative scans available, and most patients had multiple follow-up scans performed. Most patients also had undergone vascular imaging, preoperatively, postoperatively, or as an outpatient. The hematoma and edema volumes were calculated using semiautomatic threshold-guided volume assessment with the AnalyzePro software (AnalyzeDirect Inc., Overland Park, Kansas, USA). All CT scan volumetric segmentation was performed by 2 independent raters (C.P.K. and J.S.) who were unaware of the patient details and the other rater’s findings. The calculations from each reviewer were averaged. For the threshold-guided segmentation, a Hounsfield range of 40e80 was used to identify the presence of hemorrhage and 5e33 to identify perihematomal edema (PHE) on the preoperative scans and pericavity edema (PCE) on the postoperative scans.9,10 The term PCE is introduced here to describe edema that surrounds the cavity
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Table 1. Patient Details GCS Score Patient
Age (Years)
Sex
HV (mL)
Admission
Postoperative
Discharge
Long-Term mRS Score
Preoperative
Postoperative
OT (Minutes)
1
78
F
10
11
12
2
23
2.5
67
2
47
M
11
14
15
1
32
0
77
3
63
F
3
3
NA
6
40
NA
65
4
82
F
13
14
15
2
14
0
70
5
70
F
15
15
15
2
13
5.8
58
6
62
M
4
10
10
3
24
9.1
52
7
67
M
3
13
14
2
39
0
50
8
49
F
4T
13
15
0
19
3.9
57
9
68
F
14
14
15
1
26
0
37
10
55
F
4T
15
15
1
24
3.7
38
GCS, Glasgow coma scale; mRS, modified Rankin scale; HV, hematoma volume; OT, operative time; F, female; M, male; NA, not available (patient 3 did not undergo postoperative imaging).
after the hematoma has been removed during minimally invasive ICH evacuation. The maximum dimension of the hematoma was measured directly. The minimum distance from the hematoma cavity to the surface was measured. The presence of intraventricular hemorrhage, ventricular casting, and hydrocephalus was noted. The presence of brainstem compression was documented. If preoperative CT angiography was performed, the presence of spot sign, density heterogeneity, margin irregularity, and a fluid-fluid level was noted.11 Postoperative scans were evaluated for residual hematoma and PCE. Operative Technique The surgical records were studied for the length of surgery, laterality of surgery, and placement of an external ventricular drain. The surgical technique varied slightly among the operative surgeons. Nonetheless, several themes were present. Ventricular drains were placed at the discretion of the surgeon and were placed immediately before or immediately after surgical evacuation of the hematoma. Depending on the position of the hematoma (i.e., vermian, paramedian, lateral), the patient was positioned supine with the head turned, lateral, or prone. A Mayfield clamp was rarely used. On preoperative imaging, the portion of the hematoma closest to the posterior cortical surface was identified, and this point was used to plan the corticectomy, craniectomy, and skin incision. A 5-cm linear incision was marked, overlying the area in which most of the hematoma was situated and where it came closest to the surface (Figure 1). The marked incision was infiltrated with 2% Marcaine, prepared, and draped in the usual sterile manner. Preoperative antibiotics were always administered. Mannitol was administered as soon as possible after the diagnosis. The incision was carried through fascia and muscle directly to the suboccipital bone. A periosteal elevator was then used to elevate the myocutaneous flap, and 1 or 2 curved Weitlaner retractors were placed under the periosteum on the bone. A high speed drill was
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used to thin out the suboccipital bone, and Kerrison rongeurs were used to create a small craniectomy, with a 2e3-cm diameter, depending on the size of the hemorrhage (Figure 2). All bone dust and bone chips were saved. The underlying dura was opened in a stellate fashion (Figure 3). A 1e2-cm corticotomy was performed. This was often overlying obvious cerebellar discoloration or thinning. A 1-cm malleable retractor was used to deepen the exposure and facilitate aspiration of the clot (Figure 4). If the fourth ventricle was entered, the intraventricular hemorrhage was gently aspirated. If a bleeding source were identified, it was coagulated with bipolar cautery. The cavity was filled with Floseal (Baxter Healthcare Corp., Deerfield, Illinois, USA) and packed with cottonoids for 1 minute. It was then irrigated thoroughly. If the fourth ventricle had been entered, a cottonoid was placed over it to prevent the entry of blood products and Floseal. The dura was then approximated, whenever possible. A piece of Gelfoam (Pfizer, New York, New York, USA) was placed over the dura and then covered with the collected bone dust and chips. Drains were left in place at the discretion of the operating surgeon. The wound was approximated in anatomic layers, with a running suture over the skin. Antibiotics were continued for 24 hours, unless an external ventricular drain was present, in which case the antibiotics were maintained until the drain had been removed.
RESULTS The data from 10 patients presenting consecutively with scICH from January 2009 to July 2017 who met the criteria for surgical evacuation were collected (Table 1). The mean age standard deviation was 64.1 11.5 years. The patient characteristics are listed in Table 2. Of the 10 patients, 7 were women; 5 patients were white, 2 were African-American, 2 were Asian, and 1 was Hispanic. All the patients presented with elevated blood pressure. The mean systolic blood pressure on presentation was 216 mm Hg, and
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Table 2. Patient Characteristics Variable Age (years)
Table 3. Surgical Results Value 64.1 11.5
Gender (n)
Mean SD
Variable Hematoma volume (mL) Preoperative
25.4 9.2
Postoperative
2.8 3.2
Male
3
Female
7
Evacuation percentage
85.7 17.0
Procedure time (minutes)
57.1 13.2
White
5 (50)
Burr hole width (mm)
25.2 8.3
African American
2 (20)
Brainstem compression (%)
Asian
2 (20)
Preoperative
90
Hispanic
1 (10)
Postoperative
0
Ethnicity
Medical history Hypertension
SD, standard deviation.
8 (80)
Diabetes
4 (40)
Hyperlipidemia
2 (20)
Coronary artery disease
1 (10)
Aspirin use
2 (20)
AC use
0 (0)
Admission GCS score
8.5 (3e15)
ICH score
3.0 (1.3)
Initial SBP (mm Hg)
216 (29)
mean residual hematoma was 2.8 mL (range, 0e9.1), for an average evacuation rate of 85.7%. The postoperative PCE averaged 23.1 6.8, for an average change in edema volume of 113%. All patients with preoperative brainstem compression showed radiographic resolution of compression. No patients developed repeat bleeding, pseudomeningocele, cerebrospinal fluid leak, or infection. The hospital length of stay in the present series was 10.6 days. The average postoperative GCS score was 12.2, and the average discharge GCS score was 14. The long-term follow-up duration ranged from 3 to 90 months, with an average mRS score of 2 (Table 4).
Initial CT findings Hematoma volume Hydrocephalus Distance from cortex
25.4 (9.2) 4 (40) 7.5 (5.6)
Presence of IVH
5 (50)
Brainstem compression
8 (80)
Data presented as mean standard deviation, n (%), or mean (range). AC, anticoagulation; GCS, Glasgow coma scale; ICH, intracerebral hemorrhage; SBP, systolic blood pressure; CT, computed tomography; IVH, intraventricular hemorrhage.
the mean diastolic blood pressure was 108 mm Hg. Of the 10 patients, 8 (80%) had known hypertension before presentation requiring medication. In addition, 4 patients had diabetes and 2 patients were taking aspirin. The mean GCS score on presentation was 8.6 (range, 3e15). The mean hematoma volume was 25.4 9.2 mL. The mean PHE volume was 20.8 4.5 mL. The average distance to the cortical surface was 7.5 5.6 mm. All patients had compression of the fourth ventricle. Also, 4 patients had hydrocephalus and 8 patients had a mass effect on the brainstem; 5 patients had intraventricular hemorrhage. The operative time averaged 57.1 13.2 minutes. The surgical results are presented in Table 3. The craniectomy diameter averaged 25.2 8.3 mm. Six patients received an external ventricular drain during the procedure. Of the 10 patients, 4 had complete evacuation. The
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Case Description Patient 1. A 68-year-old woman with a medical history notable for diabetes mellitus and hypertension was brought to the emergency room with severe headaches, nausea, and emesis after syncope at
Table 4. Outcome Measures Variable
Value
LOS (days)
10.6 4.5
Tracheostomy
1 (10)
PEG placement
1 (10)
VPS
1 (10)
Infection
0 (0)
Pseudomeningocele
0 (0)
Repeat bleeding
0 (0) 12.2 3.6
GCS score postoperatively GCS score at discharge
14 1.8
mRS score at long-term follow-up*
2 1.6
Data presented as mean standard deviation or n (%). LOS, length of stay; PEG, percutaneous endoscopic gastrostomy; VPS, ventriculoperitoneal shunt; GCS, Glasgow coma scale; mRS, modified Rankin scale. *Average follow-up duration was 33 months (range, 3e90).
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Figure 5. (A) Initial computed tomography (CT) scan demonstrating a left cerebellar intracerebral hemorrhage with intraventricular extension and mass effect on the brainstem. (B) Postoperative CT scan
work. Her vital signs were notable for blood pressure of 212/103 mm Hg. Her admission GCS score was 14. A CT scan showed a large left cerebellar parenchymal hemorrhage with intraventricular extension and adjacent edema and a mass effect on the brainstem (Figure 5A). She underwent urgent minimally invasive left craniectom for ICH evacuation. The total operative time was 37 minutes. The craniectomy width was approximately 15 mm. The postoperative CT scan demonstrated near complete clot evacuation (Figure 5B). The length of stay was 3 days, and her discharge GCS score was 15. The 3-month mRS score was 1, and the delayed CT findings were unremarkable (Figure 5C). Patient 2. A 67-year-old man, with a medical history notable for hypertension and diabetes mellitus, presented to the emergency
Figure 6. (A) Initial computed tomography (CT) scan demonstrating a large right cerebellar hematoma with mass effect on the brain stem, effacement of the fourth ventricle, and early hydrocephalus. (B) Postoperative CT scan showing excellent evacuation of hematoma, a widely patent fourth
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demonstrating near complete clot evacuation. (C) CT scan at long-term follow-up showing 1.5-cm craniectomy site with no residual hematoma or mass effect.
room with slurred speech, lethargy, and right-sided weakness. His blood pressure was 214/105 mm Hg. CT revealed a large right cerebellar hematoma with mass effect on the brain stem, effacement of the fourth ventricle, and early hydrocephalus (Figure 6A). On examination, he was somnolent, unable to follow commands, and minimally moving his left arm. His GCS score was 3. He was taken emergently to the operating room for minimally invasive right craniectomy for ICH evacuation and placement of a right frontal external ventricular drain. He awoke rapidly, and the ventriculostomy was weaned successfully over several days. The postoperative CT scan showed excellent evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus (Figure 6B). The bone windows showed bone chips placed in the craniectomy site (Figure 6C). He was discharged to rehabilitation
ventricle, and no hydrocephalus. (C) Bone windows showing bone chips placed in the craniectomy site. (D) Long-term follow-up CT scan demonstrating regrowth of suboccipital bone in previous craniectomy location.
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Figure 7. (A) Initial computed tomography (CT) scan showing a large left cerebellar hematoma with mass effect on the brainstem and hydrocephalus. (B) Postoperative CT scan demonstrating minimal residual
MINIMALLY INVASIVE SURGERY FOR CEREBELLAR ICH
hematoma and decompression of the fourth ventricle and brainstem. (C) CT scan performed at long-term follow-up examination showing regrowth of the bone across the minicraniectomy site.
on postoperative day 11. His discharge GCS score was 14, and the 3month mRS score was 2. The long-term follow-up CT scan demonstrated regrowth of the suboccipital bone in the location of the previous craniectomy (Figure 6D).
to home on postoperative day 9. Her discharge GCS score was 15, and her 3-month mRS score was 1.
Patient 3. A 49-year-old woman, with a medical history notable for severe hypertension and previous stroke, was brought by her husband to the emergency room in extremis. She had reported a headache and dizziness and then became somnolent. On examination, she was obtunded, with extensor posturing to noxious stimuli. The GCS score was 4T. The CT scan showed large left cerebellar hematoma with mass effect on the brainstem and hydrocephalus (Figure 7A). She underwent emergent minimally invasive left SOC, ICH evacuation, and placement of a right frontal external ventricular drain. She woke up quickly and was extubated the next day. The postoperative CT scan demonstrated minimal residual hematoma and decompression of the fourth ventricle and brainstem (Figure 7B). Her ventricular drain was removed, and she was discharged to rehabilitation on postoperative day 9. Her discharge GCS score was 15. The 3-month mRS score was 0, and the CT scan at that time demonstrated complete resolution of the hemorrhage and PHE, with regrowth of the bone across the minicraniectomy site (Figure 7C).
Without surgical intervention, scICH would be the most deadly form of ICH. Series from the pre-CT era reported 100% mortality without surgical intervention if signs of alteration of consciousness or brainstem compression were present.12 The only American Heart Association guidelines recommendation for surgery for spontaneous ICH is to perform surgical evacuation for posterior fossa hemorrhage with the presence of hydrocephalus from ventricular compression and/or brainstem compression.2 Most reports of the surgical management of scICH have described SOC. SOC, however, requires a high degree of tissue
Patient 4. A 55-year-old woman with a medical history notable for hypertension was brought to the emergency room by ambulance after developing severe nausea with vomiting and syncope while working. The initial examination showed profound lethargy with eyes closed. She required intubation for airway protection. Her blood pressure was 212/103 mm Hg and pulse was 47 bpm, consistent with a Cushing response. The CT scan revealed a large left vermian hematoma with mass effect on the brainstem, compression of the fourth ventricle, early hydrocephalus, and caudal displacement of the tonsils (Figure 8A). She was taken emergently to the operating room for minimally invasive left SOC and ICH evacuation. She awoke rapidly and recovered well over several days. The CT scan showed excellent evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus (Figure 8B). She was discharged
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DISCUSSION
Figure 8. (A) Preoperative computed tomography (CT) scan revealing large left vermian hematoma with mass effect on the brain stem, compression of the fourth ventricle, early hydrocephalus, and caudal displacement of the tonsils. (B) Postoperative CT scan showing near-complete evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus.
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dissection, brain exposure, long operative times, the risk of meningitis, and the risk of pseudomeningocele or hydrocephalus, which could require a ventriculoperitoneal shunt. The total complication rate for suboccipital craniectomy versus craniotomy in a large series was 32.6% and 7%, respectively.3 The present case series has demonstrated the feasibility of using a minimally invasive craniectomy approach for scICH. In our case series, complete evacuation was achieved in 4 of 10 patients. The residual hematoma in the 6 patients ranged from 2.5 to 9.1 mL. The mean overall evacuation percentage was 85.7%. The mean operative time was 57 minutes (range, 37e77). The mean GCS score at the first evaluation in the emergency room was 8.6 (range, 3e15), the mean postoperative GCS score was 12.2, the mean discharge GCS score was 14, and the mean long-term mRS score was 2. Mortality was 10%, because 1 patient with a 39.6 mL hemorrhage and GCS score of 3 on arrival did not improve after surgery and died shortly after. Minimally invasive evacuation of scICH has been reported previously using various techniques. Stereotactic aspiration and thrombolysis was first reported in supratentorial ICH by Doi et al.13 and then 8 years later in cerebellar ICH by Mohadjer et al.14 This procedure involves creation of a 1e2-cm craniectomy, stereotactic catheter placement into the hematoma, aspiration, infusion of urokinase, and repeated aspiration and/or infusion over multiple days until the hematoma has been fully removed. In the series reported by Mohadjer et al.14 of 14 patients, 3 died within 3 months of the procedure for unrelated reasons, 1 was lost to follow-up, and 10 all had good functional status (mean Karnovsky score of 86) at an average follow-up duration of 19.6 months. One patient had symptoms of residual dizziness and gait imbalance. Tokimura et al.15 reported a series of 23 patients who had undergone emergent keyhole craniotomy for the evacuation of scICH. They defined keyhole craniotomy as a 3-cm craniotomy over the cortical surface closest to the hematoma. They reported a 96.6% mean evacuation rate and no postoperative complications. The operative time averaged 125 minutes, and the time from skin incision to initial hematoma evacuation was 36.3 minutes. The investigators argued that the craniotomy permits a faster incision to evacuation time, decreased operative time, and fewer postoperative complications. A comparative series of 23 patients undergoing minicraniectomy versus 25 patients undergoing craniectomy demonstrated similar outcomes but shorter operative times for the minicraniectomy group by a factor of w4 (215 minutes for the suboccipital craniectomy vs. 55 minutes for the minicraniectomy group).4
REFERENCES 1. Flaherty ML, Woo D, Haverbusch M, Sekar P, Khoury J, Sauerbeck L, et al. Racial variations in location and risk of intracerebral hemorrhage. Stroke. 2005;36:934-937. 2. Hemphill JC III, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, 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
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An endoscopic approach has also been described using a 1e2cm craniectomy, 1-cm sheath, endoscope, and a combined irrigation, suction, cautery device commonly used for endoscopeassisted ICH evacuations in Japan. This group performed a retrospective comparison of 10 endoscopic evacuations and 10 suboccipital decompressive craniectomies with similar preoperative clinical characteristics. The endoscopic group had shorter operative times (64.5 vs. 230.6 minutes), a greater evacuation rate (95.2% vs. 90.6%), fewer complications (0 vs. 6), and better overall outcomes.5 Study Limitations Supratentorial minimally invasive techniques emphasize the use of stereotactic navigation and aligning the access trajectory with the long axis of the clot. Stereotactic navigation is more challenging to set up with the patient in the prone position, and scICH cases are more likely to be emergent without time to set up and register the equipment. Although we experienced no difficulty in locating the hematoma in any of our patients, the lack of stereotaxy might have resulted in a greater incidence of unnecessary cerebellar injury or difficulty locating the hematoma. Ultrasonography is an option to improve localization. In addition, some hematomas can spread across a wide range of the cerebellum or reside superiorly, making them challenging to evacuate through a small craniectomy. The study limitations included the small numbers, single-center nature of the study, and that the clinical outcomes were self-reported without blinding. CONCLUSION Although the American Heart Association guidelines have recommended surgical evacuation for scICH and previous studies have demonstrated success with various evacuation techniques, minimally invasive scICH evacuation has not been commonly practiced. The present case series has demonstrated a simple and inexpensive technique that does not use stereotactic guidance, thrombolytic agents, or an endoscope, with good surgical and functional results. ACKNOWLEDGMENTS The authors would like to acknowledge and thank Christopher M. Smith, MA, CMI, Academic Medical Illustrator, Icahn School of Medicine at Mount Sinai, for the original artwork presented in our report.
American Heart Association/American Stroke Association. Stroke. 2015;46:2032-2060. 3. Legnani FG, Saladino A, Casali C, Vetrano IG, Varisco M, Mattei L, et al. Craniotomy vs. craniectomy for posterior fossa tumors: a prospective study to evaluate complications after surgery. Acta Neurochir. 2013;155:2281-2286. 4. Tamaki T, Kitamura T, Node Y, Teramoto A. Paramedian suboccipital mini-craniectomy for evacuation of spontaneous cerebellar hemorrhage. Neurol Med Chir. 2004;44:578-582 [discussion: 583].
5. Yamamoto T, Nakao Y, Mori K, Maeda M. Endoscopic hematoma evacuation for hypertensive cerebellar hemorrhage. Minim Invasive Neurosurg. 2006;49:173-178. 6. Hanley DF, Thompson RE, Muschelli J, Rosenblum M, McBee N, Lane K, et al, MISTIE Investigators. Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, phase 2 trial. Lancet Neurol. 2016;15:1228-1237. 7. Bauer AM, Rasmussen PA, Bain MD. Initial single-center technical experience with the
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BrainPath system for acute intracerebral hemorrhage evacuation. Oper Neurosurg (Hagerstown). 2017;13:69-76. 8. Fiorella D, Arthur AS, Mocco JD. 305 The INVEST trial: a randomized, controlled trial to investigate the safety and efficacy of image-guided minimally invasive endoscopic surgery with Apollo vs best medical management for supratentorial intracerebral hemorrhage. Neurosurgery. 2016;63(suppl 1): 1-187. 9. Smith EE, Rosand J, Greenberg SM. Imaging of hemorrhagic stroke. Magn Reson Imaging Clin N Am. 2006;14:127-140. 10. Urday S, Beslow LA, Goldstein DW, Vashkevich A, Ayres AM, Battey TWK, et al. Measurement of perihematomal edema in intracerebral hemorrhage. Stroke. 2015;46:1116-1119.
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11. Sporns PB, Schwake M, Schmidt R, Kemmling A, Minnerup J, Schwindt W, et al. Computed tomographic blend sign is associated with computed tomographic angiography spot sign and predicts secondary neurological deterioration after intracerebral hemorrhage. Stroke. 2016;48:131-135. 12. Brennan RW, Bergland RM. Acute cerebellar hemorrhage: analysis of clinical findings and outcome in 12 cases. Neurology. 1977;27:527-532. 13. Doi E, Moriwaki H, Komai N, Iwamoto M. [Stereotactic evacuation of intracerebral hematomas]. Neurol Med Chir. 1982;22:461-467. 14. Mohadjer M, Eggert R, May J, Mayfrank L. CTguided stereotactic fibrinolysis of spontaneous and hypertensive cerebellar hemorrhage: longterm results. J Neurosurg. 1990;73:217-222. 15. Tokimura H, Tajitsu K, Taniguchi A, Yamahata H, Tsuchiya M, Takayama K, et al. Efficacy and safety
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of key hole craniotomy for the evacuation of spontaneous cerebellar hemorrhage. Neurol Med Chir. 2010;50:367-372. Conflict of interest statement: This research was supported in part by a grant from Arminio and Lucyna Fraga and by a grant from Mr. and Mrs. Durkovic. C.K. is the director of a continuing medical education course, “Endoscopic Minimally Invasive Intracerebral Hemorrhage Evacuation,” funded by Penumbra. J.M. is the principal investigator of the INVEST trial funded by Penumbra and has financial interest in Rebound Therapeutics. Received 12 September 2017; accepted 16 July 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.145 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Published by Elsevier Inc.
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Minimally Invasive Evacuation of Spontaneous Cerebellar Intracerebral Hemorrhage Christopher P. Kellner1, Frank Moore1,2, Marc S. Arginteanu1,2, Alfred A. Steinberger1,2, Kevin Yao1,2, Jacopo Scaggiante1, J Mocco1, Yakov Gologorsky1,2
OBJECTIVE: Spontaneous cerebellar intracerebral hemorrhage (scICH) constitutes w10% of all cases of spontaneous ICH, with a mortality of 20%e50%. Suboccipital craniectomy (SOC) is commonly performed for scICH causing brainstem compression or hydrocephalus. However, SOC requires long anesthesia times and results in a high complication rate. We present a series of patients who minimally invasive scICH evacuation as an alternative to traditional SOC.
-
METHODS: We retrospectively reviewed the operative records for patients presenting to a single center from January 1, 2009 to March 1, 2017. All patients who had undergone evacuation of scICH were included in the present study. Clinical and radiographic variables were collected, including admission and postoperative Glasgow coma scale (GCS) scores, preoperative and postoperative hematoma volumes, and modified Rankin scale (mRS) scores at long-term follow-up.
mortality rate was 10% and mean long-term follow-up mRS score was 2. CONCLUSIONS: Minimally invasive scICH hematoma evacuation is a feasible alternative to SOC with numerous advantages that could lead to improved radiographic and clinical results.
-
-
RESULTS: We identified 10 patients who had presented with scICH requiring surgery. All scICH evacuations were performed through a minicraniectomy positioned in the suboccipital area as close to the hematoma as possible. The mean patient age was 64.1 years. The mean presenting GCS score was 8.6, the mean initial hematoma volume was 25.4 mL, the mean procedure time was 57 minutes, and the mean postoperative hematoma volume was 2.8 mL. The
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Key words Craniectomy - Evacuation - Infratentorial - Intracerebral hemorrhage - Minimally invasive -
Abbreviations and Acronyms CT: Computed Tomography GCS: Glasgow coma scale ICH: Intracerebral hemorrhage mRS: Modified Rankin scale PCE: Pericavity edema PHE: Perihematomal edema
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INTRODUCTION
I
ntracerebral hemorrhage (ICH) is the most devastating form of stroke, with a 6-month mortality >40% and few effective treatment options. Spontaneous cerebellar ICH (scICH) represents 5%e10% of all cases of spontaneous ICH and results in even greater morbidity and mortality.1 Current American Heart Association guidelines have specified that scICH is the only evidence-based indication for surgical treatment and have advised surgery for those who are deteriorating neurologically or with brainstem compression and/or hydrocephalus from ventricular obstruction.2 The current surgical standard for scICH is to perform suboccipital craniectomy (SOC) with or without dural closure. However, SOC has resulted in an overall reported complication risk of w32%, including the risk of pseudomeningocele, hydrocephalus, cerebrospinal fluid leak, hematoma recurrence, infection, and long operative times in the range of 215e230 minutes.3-5
scICH: Spontaneous cerebellar intracerebral hemorrhage SOC: Suboccipital craniectomy From the 1Department of Neurosurgery, Icahn School of Medicine at Mount Sinai, New York, New York; and 2Department of Neurosurgery, Englewood Hospital and Medical Center, Englewood, New Jersey, USA To whom correspondence should be addressed: Christopher P. Kellner, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.145 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Published by Elsevier Inc.
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ORIGINAL ARTICLE CHRISTOPHER P. KELLNER ET AL.
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Figure 1. A 5-cm linear incision overlying the area at which most of the hematoma was situated and where it came closest to the surface was marked.
Recently, a substantial effort has been made to evaluate minimally invasive strategies for supratentorial ICH evacuation, including the ongoing MISTIE (minimally invasive surgery plus recombinant tissue plasminogen activator for intracerebral hemorrhage evacuation), the ENRICH trial (early minimally invasive removal of ICH), and the INVEST (minimally invasive endoscopic surgical treatment with Apollo for supratentorial intracerebral hemorrhage) trial.6-8 These same minimally invasive evacuation techniques could improve outcomes when applied to the posterior fossa. We present the results from a single-center series to
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demonstrate the feasibility of a minimally invasive technique for the treatment of scICH. METHODS The institutional board review approved the present study. A retrospective review was conducted of all surgeries performed for the treatment of cerebellar ICH at a single center from January 1, 2009 to July 1, 2017. All hemorrhages secondary to tumor, hemorrhagic transformation of ischemic stroke, or vascular malformation
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Figure 2. A 2e3-cm craniectomy was created over the hematoma, and all bone dust and bone chips were saved to fill in the minicraniectomy at the end of the procedure.
were excluded. The records were identified by meticulous review of our practice logs and billing data and confirmed by the hospital medical records department. A total of 10 operations were identified. Surgical Indications The indications for surgery included the following: computed tomography (CT) evidence of a parenchymal hematoma measuring
Figure 3. The underlying dura was opened in a stellate fashion.
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Figure 4. A 1-cm malleable retractor was used to deepen the exposure and facilitate aspiration of the clot.
3 cm or brainstem compression. A poor initial Glasgow coma scale (GCS) score did not affect the decision to perform surgery, because these patients are capable of profound and rapid recovery once the brainstem compression, intracranial hypertension, and/ or hydrocephalus have been corrected. All patients were admitted through the emergency room within 6 hours of symptom onset, and all 10 patients underwent surgery within 6 hours of presentation.
Clinical and Radiographic Data The demographic data collected included age, sex, ethnicity, medical comorbidities, pertinent medications, hospital length of stay, admission GCS score, GCS score on postoperative day 1, GCS score at discharge, and modified Rankin scale (mRS) score at long-term follow-up. The need for any secondary surgical procedures was also documented. All patients had undergone imaging studies on admission to the emergency room. All but 1 patient had postoperative scans available, and most patients had multiple follow-up scans performed. Most patients also had undergone vascular imaging, preoperatively, postoperatively, or as an outpatient. The hematoma and edema volumes were calculated using semiautomatic threshold-guided volume assessment with the AnalyzePro software (AnalyzeDirect Inc., Overland Park, Kansas, USA). All CT scan volumetric segmentation was performed by 2 independent raters (C.P.K. and J.S.) who were unaware of the patient details and the other rater’s findings. The calculations from each reviewer were averaged. For the threshold-guided segmentation, a Hounsfield range of 40e80 was used to identify the presence of hemorrhage and 5e33 to identify perihematomal edema (PHE) on the preoperative scans and pericavity edema (PCE) on the postoperative scans.9,10 The term PCE is introduced here to describe edema that surrounds the cavity
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Table 1. Patient Details GCS Score Patient
Age (Years)
Sex
HV (mL)
Admission
Postoperative
Discharge
Long-Term mRS Score
Preoperative
Postoperative
OT (Minutes)
1
78
F
10
11
12
2
23
2.5
67
2
47
M
11
14
15
1
32
0
77
3
63
F
3
3
NA
6
40
NA
65
4
82
F
13
14
15
2
14
0
70
5
70
F
15
15
15
2
13
5.8
58
6
62
M
4
10
10
3
24
9.1
52
7
67
M
3
13
14
2
39
0
50
8
49
F
4T
13
15
0
19
3.9
57
9
68
F
14
14
15
1
26
0
37
10
55
F
4T
15
15
1
24
3.7
38
GCS, Glasgow coma scale; mRS, modified Rankin scale; HV, hematoma volume; OT, operative time; F, female; M, male; NA, not available (patient 3 did not undergo postoperative imaging).
after the hematoma has been removed during minimally invasive ICH evacuation. The maximum dimension of the hematoma was measured directly. The minimum distance from the hematoma cavity to the surface was measured. The presence of intraventricular hemorrhage, ventricular casting, and hydrocephalus was noted. The presence of brainstem compression was documented. If preoperative CT angiography was performed, the presence of spot sign, density heterogeneity, margin irregularity, and a fluid-fluid level was noted.11 Postoperative scans were evaluated for residual hematoma and PCE. Operative Technique The surgical records were studied for the length of surgery, laterality of surgery, and placement of an external ventricular drain. The surgical technique varied slightly among the operative surgeons. Nonetheless, several themes were present. Ventricular drains were placed at the discretion of the surgeon and were placed immediately before or immediately after surgical evacuation of the hematoma. Depending on the position of the hematoma (i.e., vermian, paramedian, lateral), the patient was positioned supine with the head turned, lateral, or prone. A Mayfield clamp was rarely used. On preoperative imaging, the portion of the hematoma closest to the posterior cortical surface was identified, and this point was used to plan the corticectomy, craniectomy, and skin incision. A 5-cm linear incision was marked, overlying the area in which most of the hematoma was situated and where it came closest to the surface (Figure 1). The marked incision was infiltrated with 2% Marcaine, prepared, and draped in the usual sterile manner. Preoperative antibiotics were always administered. Mannitol was administered as soon as possible after the diagnosis. The incision was carried through fascia and muscle directly to the suboccipital bone. A periosteal elevator was then used to elevate the myocutaneous flap, and 1 or 2 curved Weitlaner retractors were placed under the periosteum on the bone. A high speed drill was
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used to thin out the suboccipital bone, and Kerrison rongeurs were used to create a small craniectomy, with a 2e3-cm diameter, depending on the size of the hemorrhage (Figure 2). All bone dust and bone chips were saved. The underlying dura was opened in a stellate fashion (Figure 3). A 1e2-cm corticotomy was performed. This was often overlying obvious cerebellar discoloration or thinning. A 1-cm malleable retractor was used to deepen the exposure and facilitate aspiration of the clot (Figure 4). If the fourth ventricle was entered, the intraventricular hemorrhage was gently aspirated. If a bleeding source were identified, it was coagulated with bipolar cautery. The cavity was filled with Floseal (Baxter Healthcare Corp., Deerfield, Illinois, USA) and packed with cottonoids for 1 minute. It was then irrigated thoroughly. If the fourth ventricle had been entered, a cottonoid was placed over it to prevent the entry of blood products and Floseal. The dura was then approximated, whenever possible. A piece of Gelfoam (Pfizer, New York, New York, USA) was placed over the dura and then covered with the collected bone dust and chips. Drains were left in place at the discretion of the operating surgeon. The wound was approximated in anatomic layers, with a running suture over the skin. Antibiotics were continued for 24 hours, unless an external ventricular drain was present, in which case the antibiotics were maintained until the drain had been removed.
RESULTS The data from 10 patients presenting consecutively with scICH from January 2009 to July 2017 who met the criteria for surgical evacuation were collected (Table 1). The mean age standard deviation was 64.1 11.5 years. The patient characteristics are listed in Table 2. Of the 10 patients, 7 were women; 5 patients were white, 2 were African-American, 2 were Asian, and 1 was Hispanic. All the patients presented with elevated blood pressure. The mean systolic blood pressure on presentation was 216 mm Hg, and
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Table 2. Patient Characteristics Variable Age (years)
Table 3. Surgical Results Value 64.1 11.5
Gender (n)
Mean SD
Variable Hematoma volume (mL) Preoperative
25.4 9.2
Postoperative
2.8 3.2
Male
3
Female
7
Evacuation percentage
85.7 17.0
Procedure time (minutes)
57.1 13.2
White
5 (50)
Burr hole width (mm)
25.2 8.3
African American
2 (20)
Brainstem compression (%)
Asian
2 (20)
Preoperative
90
Hispanic
1 (10)
Postoperative
0
Ethnicity
Medical history Hypertension
SD, standard deviation.
8 (80)
Diabetes
4 (40)
Hyperlipidemia
2 (20)
Coronary artery disease
1 (10)
Aspirin use
2 (20)
AC use
0 (0)
Admission GCS score
8.5 (3e15)
ICH score
3.0 (1.3)
Initial SBP (mm Hg)
216 (29)
mean residual hematoma was 2.8 mL (range, 0e9.1), for an average evacuation rate of 85.7%. The postoperative PCE averaged 23.1 6.8, for an average change in edema volume of 113%. All patients with preoperative brainstem compression showed radiographic resolution of compression. No patients developed repeat bleeding, pseudomeningocele, cerebrospinal fluid leak, or infection. The hospital length of stay in the present series was 10.6 days. The average postoperative GCS score was 12.2, and the average discharge GCS score was 14. The long-term follow-up duration ranged from 3 to 90 months, with an average mRS score of 2 (Table 4).
Initial CT findings Hematoma volume Hydrocephalus Distance from cortex
25.4 (9.2) 4 (40) 7.5 (5.6)
Presence of IVH
5 (50)
Brainstem compression
8 (80)
Data presented as mean standard deviation, n (%), or mean (range). AC, anticoagulation; GCS, Glasgow coma scale; ICH, intracerebral hemorrhage; SBP, systolic blood pressure; CT, computed tomography; IVH, intraventricular hemorrhage.
the mean diastolic blood pressure was 108 mm Hg. Of the 10 patients, 8 (80%) had known hypertension before presentation requiring medication. In addition, 4 patients had diabetes and 2 patients were taking aspirin. The mean GCS score on presentation was 8.6 (range, 3e15). The mean hematoma volume was 25.4 9.2 mL. The mean PHE volume was 20.8 4.5 mL. The average distance to the cortical surface was 7.5 5.6 mm. All patients had compression of the fourth ventricle. Also, 4 patients had hydrocephalus and 8 patients had a mass effect on the brainstem; 5 patients had intraventricular hemorrhage. The operative time averaged 57.1 13.2 minutes. The surgical results are presented in Table 3. The craniectomy diameter averaged 25.2 8.3 mm. Six patients received an external ventricular drain during the procedure. Of the 10 patients, 4 had complete evacuation. The
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Case Description Patient 1. A 68-year-old woman with a medical history notable for diabetes mellitus and hypertension was brought to the emergency room with severe headaches, nausea, and emesis after syncope at
Table 4. Outcome Measures Variable
Value
LOS (days)
10.6 4.5
Tracheostomy
1 (10)
PEG placement
1 (10)
VPS
1 (10)
Infection
0 (0)
Pseudomeningocele
0 (0)
Repeat bleeding
0 (0) 12.2 3.6
GCS score postoperatively GCS score at discharge
14 1.8
mRS score at long-term follow-up*
2 1.6
Data presented as mean standard deviation or n (%). LOS, length of stay; PEG, percutaneous endoscopic gastrostomy; VPS, ventriculoperitoneal shunt; GCS, Glasgow coma scale; mRS, modified Rankin scale. *Average follow-up duration was 33 months (range, 3e90).
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Figure 5. (A) Initial computed tomography (CT) scan demonstrating a left cerebellar intracerebral hemorrhage with intraventricular extension and mass effect on the brainstem. (B) Postoperative CT scan
work. Her vital signs were notable for blood pressure of 212/103 mm Hg. Her admission GCS score was 14. A CT scan showed a large left cerebellar parenchymal hemorrhage with intraventricular extension and adjacent edema and a mass effect on the brainstem (Figure 5A). She underwent urgent minimally invasive left craniectom for ICH evacuation. The total operative time was 37 minutes. The craniectomy width was approximately 15 mm. The postoperative CT scan demonstrated near complete clot evacuation (Figure 5B). The length of stay was 3 days, and her discharge GCS score was 15. The 3-month mRS score was 1, and the delayed CT findings were unremarkable (Figure 5C). Patient 2. A 67-year-old man, with a medical history notable for hypertension and diabetes mellitus, presented to the emergency
Figure 6. (A) Initial computed tomography (CT) scan demonstrating a large right cerebellar hematoma with mass effect on the brain stem, effacement of the fourth ventricle, and early hydrocephalus. (B) Postoperative CT scan showing excellent evacuation of hematoma, a widely patent fourth
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demonstrating near complete clot evacuation. (C) CT scan at long-term follow-up showing 1.5-cm craniectomy site with no residual hematoma or mass effect.
room with slurred speech, lethargy, and right-sided weakness. His blood pressure was 214/105 mm Hg. CT revealed a large right cerebellar hematoma with mass effect on the brain stem, effacement of the fourth ventricle, and early hydrocephalus (Figure 6A). On examination, he was somnolent, unable to follow commands, and minimally moving his left arm. His GCS score was 3. He was taken emergently to the operating room for minimally invasive right craniectomy for ICH evacuation and placement of a right frontal external ventricular drain. He awoke rapidly, and the ventriculostomy was weaned successfully over several days. The postoperative CT scan showed excellent evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus (Figure 6B). The bone windows showed bone chips placed in the craniectomy site (Figure 6C). He was discharged to rehabilitation
ventricle, and no hydrocephalus. (C) Bone windows showing bone chips placed in the craniectomy site. (D) Long-term follow-up CT scan demonstrating regrowth of suboccipital bone in previous craniectomy location.
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Figure 7. (A) Initial computed tomography (CT) scan showing a large left cerebellar hematoma with mass effect on the brainstem and hydrocephalus. (B) Postoperative CT scan demonstrating minimal residual
MINIMALLY INVASIVE SURGERY FOR CEREBELLAR ICH
hematoma and decompression of the fourth ventricle and brainstem. (C) CT scan performed at long-term follow-up examination showing regrowth of the bone across the minicraniectomy site.
on postoperative day 11. His discharge GCS score was 14, and the 3month mRS score was 2. The long-term follow-up CT scan demonstrated regrowth of the suboccipital bone in the location of the previous craniectomy (Figure 6D).
to home on postoperative day 9. Her discharge GCS score was 15, and her 3-month mRS score was 1.
Patient 3. A 49-year-old woman, with a medical history notable for severe hypertension and previous stroke, was brought by her husband to the emergency room in extremis. She had reported a headache and dizziness and then became somnolent. On examination, she was obtunded, with extensor posturing to noxious stimuli. The GCS score was 4T. The CT scan showed large left cerebellar hematoma with mass effect on the brainstem and hydrocephalus (Figure 7A). She underwent emergent minimally invasive left SOC, ICH evacuation, and placement of a right frontal external ventricular drain. She woke up quickly and was extubated the next day. The postoperative CT scan demonstrated minimal residual hematoma and decompression of the fourth ventricle and brainstem (Figure 7B). Her ventricular drain was removed, and she was discharged to rehabilitation on postoperative day 9. Her discharge GCS score was 15. The 3-month mRS score was 0, and the CT scan at that time demonstrated complete resolution of the hemorrhage and PHE, with regrowth of the bone across the minicraniectomy site (Figure 7C).
Without surgical intervention, scICH would be the most deadly form of ICH. Series from the pre-CT era reported 100% mortality without surgical intervention if signs of alteration of consciousness or brainstem compression were present.12 The only American Heart Association guidelines recommendation for surgery for spontaneous ICH is to perform surgical evacuation for posterior fossa hemorrhage with the presence of hydrocephalus from ventricular compression and/or brainstem compression.2 Most reports of the surgical management of scICH have described SOC. SOC, however, requires a high degree of tissue
Patient 4. A 55-year-old woman with a medical history notable for hypertension was brought to the emergency room by ambulance after developing severe nausea with vomiting and syncope while working. The initial examination showed profound lethargy with eyes closed. She required intubation for airway protection. Her blood pressure was 212/103 mm Hg and pulse was 47 bpm, consistent with a Cushing response. The CT scan revealed a large left vermian hematoma with mass effect on the brainstem, compression of the fourth ventricle, early hydrocephalus, and caudal displacement of the tonsils (Figure 8A). She was taken emergently to the operating room for minimally invasive left SOC and ICH evacuation. She awoke rapidly and recovered well over several days. The CT scan showed excellent evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus (Figure 8B). She was discharged
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DISCUSSION
Figure 8. (A) Preoperative computed tomography (CT) scan revealing large left vermian hematoma with mass effect on the brain stem, compression of the fourth ventricle, early hydrocephalus, and caudal displacement of the tonsils. (B) Postoperative CT scan showing near-complete evacuation of the hematoma, a widely patent fourth ventricle, and no hydrocephalus.
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dissection, brain exposure, long operative times, the risk of meningitis, and the risk of pseudomeningocele or hydrocephalus, which could require a ventriculoperitoneal shunt. The total complication rate for suboccipital craniectomy versus craniotomy in a large series was 32.6% and 7%, respectively.3 The present case series has demonstrated the feasibility of using a minimally invasive craniectomy approach for scICH. In our case series, complete evacuation was achieved in 4 of 10 patients. The residual hematoma in the 6 patients ranged from 2.5 to 9.1 mL. The mean overall evacuation percentage was 85.7%. The mean operative time was 57 minutes (range, 37e77). The mean GCS score at the first evaluation in the emergency room was 8.6 (range, 3e15), the mean postoperative GCS score was 12.2, the mean discharge GCS score was 14, and the mean long-term mRS score was 2. Mortality was 10%, because 1 patient with a 39.6 mL hemorrhage and GCS score of 3 on arrival did not improve after surgery and died shortly after. Minimally invasive evacuation of scICH has been reported previously using various techniques. Stereotactic aspiration and thrombolysis was first reported in supratentorial ICH by Doi et al.13 and then 8 years later in cerebellar ICH by Mohadjer et al.14 This procedure involves creation of a 1e2-cm craniectomy, stereotactic catheter placement into the hematoma, aspiration, infusion of urokinase, and repeated aspiration and/or infusion over multiple days until the hematoma has been fully removed. In the series reported by Mohadjer et al.14 of 14 patients, 3 died within 3 months of the procedure for unrelated reasons, 1 was lost to follow-up, and 10 all had good functional status (mean Karnovsky score of 86) at an average follow-up duration of 19.6 months. One patient had symptoms of residual dizziness and gait imbalance. Tokimura et al.15 reported a series of 23 patients who had undergone emergent keyhole craniotomy for the evacuation of scICH. They defined keyhole craniotomy as a 3-cm craniotomy over the cortical surface closest to the hematoma. They reported a 96.6% mean evacuation rate and no postoperative complications. The operative time averaged 125 minutes, and the time from skin incision to initial hematoma evacuation was 36.3 minutes. The investigators argued that the craniotomy permits a faster incision to evacuation time, decreased operative time, and fewer postoperative complications. A comparative series of 23 patients undergoing minicraniectomy versus 25 patients undergoing craniectomy demonstrated similar outcomes but shorter operative times for the minicraniectomy group by a factor of w4 (215 minutes for the suboccipital craniectomy vs. 55 minutes for the minicraniectomy group).4
REFERENCES 1. Flaherty ML, Woo D, Haverbusch M, Sekar P, Khoury J, Sauerbeck L, et al. Racial variations in location and risk of intracerebral hemorrhage. Stroke. 2005;36:934-937. 2. Hemphill JC III, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, 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
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An endoscopic approach has also been described using a 1e2cm craniectomy, 1-cm sheath, endoscope, and a combined irrigation, suction, cautery device commonly used for endoscopeassisted ICH evacuations in Japan. This group performed a retrospective comparison of 10 endoscopic evacuations and 10 suboccipital decompressive craniectomies with similar preoperative clinical characteristics. The endoscopic group had shorter operative times (64.5 vs. 230.6 minutes), a greater evacuation rate (95.2% vs. 90.6%), fewer complications (0 vs. 6), and better overall outcomes.5 Study Limitations Supratentorial minimally invasive techniques emphasize the use of stereotactic navigation and aligning the access trajectory with the long axis of the clot. Stereotactic navigation is more challenging to set up with the patient in the prone position, and scICH cases are more likely to be emergent without time to set up and register the equipment. Although we experienced no difficulty in locating the hematoma in any of our patients, the lack of stereotaxy might have resulted in a greater incidence of unnecessary cerebellar injury or difficulty locating the hematoma. Ultrasonography is an option to improve localization. In addition, some hematomas can spread across a wide range of the cerebellum or reside superiorly, making them challenging to evacuate through a small craniectomy. The study limitations included the small numbers, single-center nature of the study, and that the clinical outcomes were self-reported without blinding. CONCLUSION Although the American Heart Association guidelines have recommended surgical evacuation for scICH and previous studies have demonstrated success with various evacuation techniques, minimally invasive scICH evacuation has not been commonly practiced. The present case series has demonstrated a simple and inexpensive technique that does not use stereotactic guidance, thrombolytic agents, or an endoscope, with good surgical and functional results. ACKNOWLEDGMENTS The authors would like to acknowledge and thank Christopher M. Smith, MA, CMI, Academic Medical Illustrator, Icahn School of Medicine at Mount Sinai, for the original artwork presented in our report.
American Heart Association/American Stroke Association. Stroke. 2015;46:2032-2060. 3. Legnani FG, Saladino A, Casali C, Vetrano IG, Varisco M, Mattei L, et al. Craniotomy vs. craniectomy for posterior fossa tumors: a prospective study to evaluate complications after surgery. Acta Neurochir. 2013;155:2281-2286. 4. Tamaki T, Kitamura T, Node Y, Teramoto A. Paramedian suboccipital mini-craniectomy for evacuation of spontaneous cerebellar hemorrhage. Neurol Med Chir. 2004;44:578-582 [discussion: 583].
5. Yamamoto T, Nakao Y, Mori K, Maeda M. Endoscopic hematoma evacuation for hypertensive cerebellar hemorrhage. Minim Invasive Neurosurg. 2006;49:173-178. 6. Hanley DF, Thompson RE, Muschelli J, Rosenblum M, McBee N, Lane K, et al, MISTIE Investigators. Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, phase 2 trial. Lancet Neurol. 2016;15:1228-1237. 7. Bauer AM, Rasmussen PA, Bain MD. Initial single-center technical experience with the
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BrainPath system for acute intracerebral hemorrhage evacuation. Oper Neurosurg (Hagerstown). 2017;13:69-76. 8. Fiorella D, Arthur AS, Mocco JD. 305 The INVEST trial: a randomized, controlled trial to investigate the safety and efficacy of image-guided minimally invasive endoscopic surgery with Apollo vs best medical management for supratentorial intracerebral hemorrhage. Neurosurgery. 2016;63(suppl 1): 1-187. 9. Smith EE, Rosand J, Greenberg SM. Imaging of hemorrhagic stroke. Magn Reson Imaging Clin N Am. 2006;14:127-140. 10. Urday S, Beslow LA, Goldstein DW, Vashkevich A, Ayres AM, Battey TWK, et al. Measurement of perihematomal edema in intracerebral hemorrhage. Stroke. 2015;46:1116-1119.
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11. Sporns PB, Schwake M, Schmidt R, Kemmling A, Minnerup J, Schwindt W, et al. Computed tomographic blend sign is associated with computed tomographic angiography spot sign and predicts secondary neurological deterioration after intracerebral hemorrhage. Stroke. 2016;48:131-135. 12. Brennan RW, Bergland RM. Acute cerebellar hemorrhage: analysis of clinical findings and outcome in 12 cases. Neurology. 1977;27:527-532. 13. Doi E, Moriwaki H, Komai N, Iwamoto M. [Stereotactic evacuation of intracerebral hematomas]. Neurol Med Chir. 1982;22:461-467. 14. Mohadjer M, Eggert R, May J, Mayfrank L. CTguided stereotactic fibrinolysis of spontaneous and hypertensive cerebellar hemorrhage: longterm results. J Neurosurg. 1990;73:217-222. 15. Tokimura H, Tajitsu K, Taniguchi A, Yamahata H, Tsuchiya M, Takayama K, et al. Efficacy and safety
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of key hole craniotomy for the evacuation of spontaneous cerebellar hemorrhage. Neurol Med Chir. 2010;50:367-372. Conflict of interest statement: This research was supported in part by a grant from Arminio and Lucyna Fraga and by a grant from Mr. and Mrs. Durkovic. C.K. is the director of a continuing medical education course, “Endoscopic Minimally Invasive Intracerebral Hemorrhage Evacuation,” funded by Penumbra. J.M. is the principal investigator of the INVEST trial funded by Penumbra and has financial interest in Rebound Therapeutics. Received 12 September 2017; accepted 16 July 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.145 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Published by Elsevier Inc.
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