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Minimally Invasive Neurosurgery for Spontaneous Intracerebral Hemorrhage—10 Years of Working Progress at National Taiwan University Hospital

Minimally Invasive Neurosurgery for Spontaneous Intracerebral Hemorrhage—10 Years of Working... ORIGINAL RESEARCH published: 20 May 2022 doi: 10.3389/fneur.2022.817386 Minimally Invasive Neurosurgery for Spontaneous Intracerebral Hemorrhage—10 Years of Working Progress at National Taiwan University Hospital 1,2† 3† 4 4 Chiu-Hao Hsu , Sheng-Chieh Chou , Lu-Ting Kuo , Sheng-Jean Huang , 4 4 4 Shih-Hung Yang , Dar-Ming Lai and Abel Po-Hao Huang * Department of Surgery, National Taiwan University Hospital Hsin-Chu Branch, Biomedical Park Hospital, Hsin-Chu, Taiwan, 2 3 Graduate Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan, Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital, and National Taiwan University College of Medicine, Taipei, Taiwan, Division of Hematology, Department of Internal Medicine, National Taiwan University Hospital, and National Taiwan University College of Medicine, Taipei, Taiwan Edited by: Jean-Claude Baron, Intracerebral hemorrhage (ICH) is a life-threatening disease with a global health burden. University of Cambridge, Traditional craniotomy has neither improved functional outcomes nor reduced mortality. United Kingdom Minimally invasive neurosurgery (MIN) holds promise for reducing mortality and improving Reviewed by: Nicholas Morris, functional outcomes. To evaluate the feasibility of MIN for ICH, a retrospective analysis University of Maryland, United States of patients with ICH undergoing endoscopic-assisted evacuation was performed. From Brian Jankowitz, University of Pennsylvania, 2012 to 2018, a total of 391 patients who underwent ICH evacuation and 76 patients who United States received early (<8 h) MIN were included. The rebleeding, mortality, and morbidity rates *Correspondence: were 3.9, 7.9, and 3.9%, respectively, 1 month after surgery. At 6 months, the median Abel Po-Hao Huang [email protected] [interquartile range (IQR)] Glasgow Coma Scale score was 12 (4.75) [preoperative: 10 (4)], the median (IQR) Extended Glasgow Outcome Scale score was 3 (1), and the median These authors have contributed equally to this work and share first (IQR) Modified Rankin Scale score was 4 (1). The results suggested that early (<8 h) authorship endoscope-assisted ICH evacuation is safe and effective for selected patients with ICH. The rebleeding, morbidity, and mortality rates of MIN in this study are lower than those Specialty section: of traditional craniotomy reported in previous studies. However, the management of This article was submitted to Stroke, intraoperative bleeding and hard clots is critical for performing endoscopic evacuation. a section of the journal With this retrospective analysis of MIN cases, we hope to promote the specialization of Frontiers in Neurology ICH surgery in the field of MIN. Received: 18 November 2021 Accepted: 20 April 2022 Keywords: functional outcome, intracerebral hemorrhage, minimally invasive neurosurgery, mortality, early Published: 20 May 2022 surgery Citation: Hsu C-H, Chou S-C, Kuo L-T, Huang S-J, Yang S-H, Lai D-M and INTRODUCTION Huang A-H (2022) Minimally Invasive Neurosurgery for Spontaneous The optimal treatment for intracerebral hemorrhage (ICH) remains among the most controversial Intracerebral Hemorrhage—10 Years topics in neurosurgery. ICH is associated with high morbidity and mortality rates and imposes of Working Progress at National a substantial economic burden worldwide. Recent studies have reported that compared with Taiwan University Hospital. traditional craniotomies, minimally invasive treatments resulted in more favorable outcomes (1–3). Front. Neurol. 13:817386. doi: 10.3389/fneur.2022.817386 These treatments include minimally invasive clot evacuation with stereotactic or endoscopic Frontiers in Neurology | www.frontiersin.org 1 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage aspiration with or without thrombolytic usage. Minimally they had incomplete medical records (n = 4), did not undergo invasive treatments cannot only reduce mortality but also postoperative follow-up imaging (n = 5), or were lost to long- improve neurological recovery in selected patients (3–5), which term follow-up (n = 3). Finally, 76 patients were included in this is rarely observed and encouraging for the treatment of ICH. study (Figure 1). Taiwan has a highly dense population and many hospitals. Patients with ICH can arrive at the hospital shortly after ictus. Rationale for Surgical Management of This is especially true in Taipei City, the capital of Taiwan, where Patients With Intracerebral Hemorrhage our hospital, National Taiwan University Hospital (NTUH), is Currently, we have four attending neurosurgeons in the NTUH located. The majority of surgeries were performed within 4 h after ICH team, which is the only dedicated ICH team in the country. ictus (6). We have performed minimally invasive neurosurgery This specialized team aims to improve functional outcomes, (MIN) under endoscopic guidance for ICH evacuation since quality of care, and quality of life for patients. The minimally 2008. For more than 10 years, we have been continuously refining invasive endoscopic-assisted ICH evacuation was performed in the surgical technique, equipment, protocol, and workflow in the approximately 70% of our surgical cases. On the basis of our pursuit of clinical excellence and improved outcomes. With the extensive experience and the literature review, we have developed paradigm shifting toward minimally invasive surgery, we share guidelines for the optimal treatment of patients with ICH in our experience in this retrospective analysis. NTUH. Recent studies have suggested that early surgery for ICH is associated with satisfactory functional outcomes and low MATERIALS AND METHODS mortality (8–12). This finding is concordant with our practice at NTUH where we performed surgery in more than 80% of Study Design patients with ICH within 4 h after ictus (6). We prefer the This retrospective study was conducted at NTUH after obtaining endoscopic-assisted evacuation over stereotactic thrombolytic the approval from the Ethical Review Board of our institute. We therapy because of its earlier decompression, high hematoma extracted and analyzed clinical data from the medical charts of clearance rate, and cost-effectiveness (13). patients with spontaneous supratentorial ICH who received early The selection of the surgical method depended on our MIN (within 48 h after ictus) from 2012 to 2018. This study clinical experience and the literature review. MIN was mostly was performed in compliance with applicable local regulations performed for deep-seated early ICH (such as the basal ganglia and the ethical principles of the Declaration of Helsinki. All and thalamus, with ICH volume ranging from 20 to 80 ml). the experimental protocols were approved by the Institutional For superficial (subcortical or lobar) ICH, minicraniotomy using Review Board of NTUH. Because of the retrospective nature of microscopic evacuation or endoscopic-assisted MIN was both this study, the requirement of informed consent was waived. feasible. For delayed cases (>72 h after ictus), craniectomy with Informed consent for surgery was obtained from each patient per ICH evacuation was preferred because such cases usually have routine practice. substantial brain edema and massive blood clots that favor decompressive craniectomy as the primary treatment instead Patient Selection of MIN. A series of experiences presented in this study represents the working progress of 6 years following a previously published series of our experiences from 2008 to 2011 (6). Between 2012 and Surgical Procedure 2018, a total of 391 patients underwent ICH evacuation at NTUH. Various MIN techniques have been developed for ICH evacuation We included patients with spontaneous supratentorial ICH who (14). We adopted the endoscopic-assisted approach where received early MIN (within 48 h after ictus). A cutoff of<48 h was suction is applied on the side of the endoscope inside a selected on the basis of the finding of a meta-analysis that patients 10–12-mm port or sheath that creates the working space who underwent MIN within 72 h were two times more likely (also known as the port-based approach). By contrast, the to achieve functional independence (7). In this experience, ICH pure endoscopic approach [e.g., the stereotactic intracerebral evacuation after 48 h of ictus may lead to significant brain edema hemorrhage underwater blood aspiration (SCUBA) technique] and massive blood clots that favor decompressive craniectomy as uses the aspiration device inside the endoscope (through its the primary treatment instead of MIN. working channel) with a 19-F peel-away sheath. We excluded patients with etiology related to structural Clot evacuation could be smoothly performed with one hand lesions or nonprimary lesions (cerebral aneurysm, arteriovenous holding the endoscope and the other hand holding a suction malformation, and cavernous malformation), cerebellar device. We used 8-Fr suction to remove the clot because suction hemorrhage, traumatic ICH, tumor bleeding, hemorrhagic with a smaller caliber would lead to the ineffective removal of transformation after ischemic stroke or postoperative bleeding, ICH. In the presence of a hard clot, the alligator punch was used or primary intraventricular hemorrhage (IVH). In addition, to pass through the sheath for piecemeal removal. In extreme we excluded patients who underwent traditional craniotomy, cases, we used the cavitron ultrasonic surgical aspirator (CUSA) external ventricular drainage, or decompressive craniectomy as to remove the hard clot. The CUSA is a surgical device used the primary treatment. in neurosurgical procedures. The CUSA is coupled with low- We carefully reviewed the medical records of the remaining 88 frequency ultrasound that helps operators to dissect or fragment patients who underwent minimally invasive endoscope-assisted tissues or pathologies. The CUSA was used to manage ICH cases ICH evacuation. Furthermore, we excluded 12 patients because with hard clots that could not be removed with suction only. Frontiers in Neurology | www.frontiersin.org 2 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage FIGURE 1 | Flowchart of patient selection. Apollo, Artemis, and Myriad are not available in Taiwan; thus, these techniques were time-consuming. Moreover, achieving we have no experience in using these devices. hemostasis by using these techniques was difficult. Later, we Regarding hemostasis during surgery, we initially used an used local hemostatic agents that remarkably reduced the time endoscopic bipolar or a suction coagulation device; however, of hemostasis, with a low rebleeding rate. In our experience, Frontiers in Neurology | www.frontiersin.org 3 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage no active bleeding requiring coagulation was noted in more suction and irrigation is crucial for bleeder identification and than 90% of cases and local hemostatic agents [e.g., FLOSEAL hemostasis (16). Hemostatic Matrix (Baxter Healthcare Corporation, Fremont, For brain access, most neurosurgeons used the 12-mm California, USA), a gelatin–thrombin matrix] yielded satisfactory outer diameter transparent trocar. The peel-away sheath was hemostasis (15). occasionally used by neurosurgeons who were comfortable When an active bleeder was encountered during surgery, with ventriculoscopic techniques (6). In our experience, we suctioned out blood, used irrigation to identify the active only 10%−15% of the cases had intraoperative bleeding bleeder, contacted it with the suction tip, and performed requiring hemostasis and most of the small arterial bleeding cauterization by using a metallic suction tube. The importance from thalamostriate perforators could be stopped using local of a balanced suction irrigation technique in the minimally hemostatic agents (8). During surgery, similar to the SCUBA invasive surgery of ICH was described in detail in a previous technique, we alternated between air and water phases; we study (16). After hemostasis, we placed an external ventricular found this technique to be useful for preventing the hematoma drain if the frontal horn was entered during surgery; otherwise, cavity from collapsing with resultant residual ICH and for we inserted an intracranial pressure (ICP) monitor [fiber identifying the bleeder (19). Cauterization was required in <5% optic devices (e.g., Camino ICP Monitor) and strain gauge of cases and was easily performed using traditional suction at the devices (e.g., Codman Microsensor and Raumedic Neurovent- bleeding point (vessel) with unipolar cauterization touching the P ICP sensor)] through the surgical corridor created by handle of the sucker (poor man’s suction bipolar). Alternatively, the trocar under direct vision in the perihematoma zone commercialized suction bipolar devices can be used (6). If all of the brain parenchyma. A surgical biopsy of the brain these attempts failed, the next step was to change to a larger parenchyma was performed, if amyloid angiopathy was trocar (Vycor, with a diameter of >2 cm used for traditional suspected (17). bipolar cauterization). We rarely converted to craniotomy, which In terms of surgical techniques, we recommend using was only performed in three out of more than 400 ICH cases. the penetrating technique (Huang’s technique) instead of the circumferential technique used in our previous studies (6, 8) Perioperative Care for ICH removal because it prevents collateral brain damage In the perioperative period, we observed that dexmedetomidine when using the trocar or port inside the normal brain tissue. substantially reduced blood pressure fluctuations. This reduction For typical basal ganglia ICH, we used modified Kocher’s point is associated with a decreased rebleeding rate, as demonstrated (1 cm lateral to Kocher’s point). A 2.5-cm incision was vertically in various experiences and other major surgeries (20). The effect made on modified Kocher’s point, creating a 1.5–2.0-cm burr of dexmedetomidine on patients with ICH was reported in a hole. After dural opening, either the trans-sulcal or transcortical clinical trial (21). For cases with a high risk of rebleeding, approach was used. The intraoperative Aloka burr-hole type we may consider tranexamic acid and recombinant factor VIIa ultrasound was selectively used to verify the trajectory and (NovoSeven) (22). Currently, we routinely perform CT within depth of ICH before puncturing with the trocar (we used a 24 h after surgery to confirm the residual hematoma and the transparent trocar with an outer diameter of 12 mm and length degree of evacuation. of 10 cm for putaminal ICH) (6). For thalamic ICH, we used Cognitive enhancers and neural stimulants were reported a considerably different surgical approach. Initially, our team to improve cognitive and behavioral impairments in patients used an aggressive approach involving the use of the endoscopic with putaminal ICH and traumatic brain injury (23). We used technique to remove thalamic ICH in the brain parenchyma. methylphenidate in patients with ICH who were comatose However, the surgical outcome was poor and most of the patients before the surgery to improve neurological outcomes. In our remained comatose after evacuation. Therefore, our current goal experience of 58 patients, methylphenidate was safe and effective was to relieve hydrocephalus and remove IVH to minimize and was associated with faster consciousness recovery, greater shunt dependency. We only dived into thalamic ICH in the chance of successful extubation, and shorter intensive care unit brain parenchyma when we observed the rupture side during (ICU) stay. However, a study reported the rare side effects of endoscopic surgery. The first step was to determine whether methylphenidate, such as serotonin syndrome, in patients with to use the frontal or occipital approach; we occasionally used ICH (24). the contralateral approach (18). The rupture side could be determined through preoperative CT performed to choose the surgical approach. The thalamostriate vein was required to be Data Collection carefully preserved to prevent iatrogenic infarction. We collected data on the following characteristics of the patients: We applied the concepts of the SCUBA technique in our hematoma location and volume, presence of IVH, sex, age, time MIN for ICH evacuation. The SCUBA technique differs from of operation, operative blood loss, and hematoma evacuation minimally invasive ICH intervention because it combines two rate. All the patients underwent preoperative head CT and a separate neuroendoscopic strategies in two phases: the first follow-up head CT within 1 week after surgery. The estimated is using dry-field conditions and the second is using a wet- hematoma volume was calculated using the ABC/2 method (A: field strategy (19). This prevents the collapse of the hematoma maximum length in the axial cut of CT, B: width perpendicular to cavity and allows for complete clot removal. This technique is A on the same CT cut, and C: the number of slices multiplied by useful for bleeder identification. During the procedure, balancing the slice thickness). Frontiers in Neurology | www.frontiersin.org 4 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage TABLE 1 | Characteristics of patients. Putaminal Thalamic Subcortical All (n = 56) (n = 9) (n = 11) Male, n (%) 42 (75.0) 5 (55.6) 6 (54.5) 53 (69.7) Age (year), median (IQRs) 58 (17.25) 66 (6) 62 (32) 59 (18) ICH score, median (IQRs) 2 (1) 3 (1) 2 (1.5) 2 (1) IVH, n (%) 26 (46.4) 6 (66.7) 4 (36.4) 36 (47.4) Anticoagulants and antiplatelets, n (%) Antiplatelet agents 6 (10.7) 1 (11.1) 3 (27.3) 10 (13.2) Anticoagulant agents 1 (1.8) 0 (0) 0 (0) 1 (1.3) Both 2 (3.6) 0 (0) 0 (0) 2 (2.6) Operative time (min), median (IQRs) 108 (50.25) 109 (63) 104 (34.5) 107 (50.25) Preoperative ICH volume (ml), median (IQRs) 45 (28.75) 35 (15) 50 (20) 42.5 (25) Operative blood loss (ml), median (IQRs) 50 (12.5) 50 (0) 50 (0) 50 (0) ICU length of stay (day), median (IQRs) 16 (14.5) 13.5 (15.25) 19 (3) 16 (13) Hospital length of stay (day), median (IQRs) 30 (23.5) 29 (25.25) 37 (21) 28 (11.5) IVH, intraventricular hemorrhage; IQR, interquartile range; ICU, intensive care unit; ICH, intracerebral hemorrhage. Clinical Outcome noted and IVH was found in 47.4% of the patients. Most of the Outcome measures included the hematoma evacuation rate, enrolled patients were aged from 57 to 60 years, except for those rebleeding, mortality rate, morbidity rate, the preoperative with thalamic ICH (median age: 66 years). The median operative and postoperative Glasgow Coma Scale (GCS) scores, the time ranged from 104 to 108 min. The ICH score (median: 2) and operative blood loss (median: 50 ml) were similar among the postoperative Extended Glasgow Outcome Scale (GOSE) scores, the Modified Rankin Scale (mRS), length of ICU stay, different types of ICH. The patients with putaminal ICH had the highest preoperative ICH volume (median: 45 ml). and the length of hospital stay. The hematoma evacuation rate was calculated as [(preoperative volume – postoperative Most of the patients (97%) underwent MIN within 4 h after volume)/(preoperative volume) × 100 (%)]. Mortality was ictus. Only two patients underwent surgery on the second day of defined as all-cause death occurring within 30 days after surgery. ictus because of hematoma expansion. Our hospital defines three Rebleeding and morbidity rates were examined 1 month after classes for emergent operation. The duration between notifying surgery. Rebleeding was defined as a postoperative hematoma the operation room to the start of operation is limited to 30 min, volume greater than the preoperative volume or a difference 2 h, and 4 h for first-class, second-class, and third-class emergent of <5 ml between preoperative and postoperative hematoma operations, respectively. ICH is classified as a third-class surgery, volume. Morbidity included wound dehiscence and surgical site which is mostly performed within 4 h. infection, including meningitis, ventriculitis, and brain abscess. Postoperative outcomes included the GCS scores at 1 and 6 Postoperative Outcomes months and the GOSE and the mRS scores at 6 months. Table 2 summarizes the surgical and functional outcomes, with no significant difference noted between the groups. The median Statistical Analysis (IQR) hematoma evacuation rate was 85.7% (16.7%) and the Descriptive statistics were used to present categorical data in median (IQR) postoperative ICH volume was 5 (5) ml. According numbers and percentages and continuous data in numbers, to the Minimally Invasive Surgery Plus Recombinant Tissue medians, and interquartile ranges (IQRs). The surgical and Plasminogen Activator for Intracerebral Hemorrhage Evacuation functional outcomes were analyzed using the Kruskal–Wallis III (MISTIE III) study, a reduction in clot size to ≤15 ml is test. A P-value of <0.05 was regarded as statistically significant. associated with improvement in functional outcomes (4). In Statistical analyses were performed using SPSS (version 25, our series, 64 (84.2%) patients reached the goal of a residual Chicago, Illinois, USA). hematoma volume of <15 ml. The overall rebleeding rate at 1 month after surgery was 3.9%. Three patients experienced rebleeding in the first postoperative follow-up [2 (3.6%) in the RESULTS putaminal group and 1 (11.1%) in the thalamic group]. Six Demographics and Baseline patients died eventually (the overall mortality rate: 7.9%): two Characteristics patients died from pneumonia and sepsis, two patients died from Table 1 summarizes the demographics of the patients. We postoperative central nervous system infection, and two patients divided the patients into three groups according to the hematoma died because their family members decided to withdraw life location: putaminal (n = 56), thalamic (n = 9), and subcortical support owing to the lack of clinical improvement. The morbidity (n = 11). The male predominance of approximately 69.7% was rate at 1 month after surgery was 3.9%; one patient developed Frontiers in Neurology | www.frontiersin.org 5 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage TABLE 2 | Outcomes. Putaminal Thalamic Subcortical P-Value All (n = 56) (n = 9) (n = 11) (n = 76) Rebleeding, n (%) 2 (3.6) 1 (11.1) 0 (0) 3 (3.9) Mortality, n (%) 5 (8.9) 0 (0) 1 (9.1) 6 (7.9) Morbidity, n (%) 3 (5.4) 0 (0) 0 (0) 3 (3.9) Hematoma evacuation rate (%), median (IQRs) 86.6 (11.9) 75.0 (19.0) 80.0 (20.8) 0.170 85.7 (16.7) Postoperative ICH volume (ml), median (IQRs) 5 (5) 10 (5) 10 (12.5) 5 (5) Postoperative hematoma volume <15 ml, n (%) 48 (85.7) 8 (88.8) 8 (77.8) 64 (84.2) GCS, median (IQRs) Pre-op 10 (4) 8 (3) 11 (3.5) 0.343 10 (4) Post-op 1 month 11 (4) 12 (5) 13 (4) 0.508 12 (4) Post-op 6 months 12 (4) 14 (6) 14 (3) 0.659 12 (4.75) GOSE, median (IQRs) Post-op 6 months 3 (1) 4 (2) 4 (1.5) 0.666 3 (1) mRS, median (IQRs) Post-op 6 months 4 (1) 4 (2) 4 (1) 0.997 4 (1) mRS 0–2, n (%) 7 (12.5) 1 (11.1) 3 (22.2) 11 (14.5) mRS 0–3, n (%) 21 (37.5) 4 (44.4) 3 (22.2) 28 (36.8) GCS, Glasgow coma scale; GOSE, Glasgow outcome scale extended; ICU, intensive care unit; mRS, modified rankin scale; OP, operation; IQR, interquartile range; ICH, intracerebral hemorrhage. scalp wound dehiscence, one patient developed meningitis and aspiration or endoscopic-assisted evacuation, is widely ventriculitis, and one patient developed brain abscess. used (27). Functional outcomes improved after surgery, with no Clinical Outcomes Compared With Prior significant differences observed between the groups (Table 2). The median (IQR) preoperative GCS score was 10 (4), which Minimally Invasive Neurosurgery Reports was numerically increased to 12 (4) at 1 month and 12 (4.75) In our series, early MIN within 48 h after ICH ictus resulted at 6 months. The median (IQR) GOSE score at the 6-month in a low rebleeding rate (3.9%), low mortality rate (7.9%), and follow-up was 3 (1). The median (IQR) mRS score at the 6-month low morbidity rate (3.9%); moreover, 36.8% of the patients follow-up was 4 (1). Satisfactory outcomes (mRS score: 0–3) were exhibited satisfactory functional outcomes (mRS score: 0–3) 6 noted in 36.8% of the patients. months after MIN. Although the overall median GOSE score indicated that the patients still required assistance to perform the activities of daily living (GOSE = 3) 6 months after MIN, the DISCUSSION patients with thalamic or subcortical ICH could occasionally be at home independently (GOSE = 4) and their overall GCS score The prevalence of ICH is especially high in Asia-Pacific regions, improved over time. Compared with those of patients included where ICH accounts for approximately 30%−40% of all stroke in other MIN studies, the postoperative outcomes of our patients cases. In the United States, ICH accounts for approximately only appeared to be more favorable. In the MISTIE III study (4), 44% 15% of all stroke cases (25). Each year in China alone, more than of patients achieved the mRS score of 0–3, 39% of patients had 150,000 patients receive minimally invasive treatment for ICH the GOSE score of ≥4 at 12 months, and the mortality rate at (8). Race and ethnicity appear to explain some of the variation 6 months was 15%. In the MISTIE III study, 33.4% of patients in clinical characteristics and outcomes after acute ICH; for achieved the mRS score of 0–3 and the mortality rate within 30 example, Caucasian patients with ICH are more likely to be older, days was 14.8% (31). In the intraoperative stereotactic CT-guided have a larger ICH volume, and have a higher mortality rate than endoscopic surgery (ICES) trial including six patients, 24% of Asian patients (26). patients achieved the mRS score of 0–3 and no patient died within The operation rate considerably varies worldwide, 30 days after surgery (3). ranging from 2 to 74% (27). In the United States, the early operation rate was previously 16% and decreased to Literature Support for Minimally Invasive 6% in 2005, presumably due to the results of the Surgical Neurosurgery Over Traditional Craniotomy Treatment for Ischemic Heart Failure (STICH) trial (28, 29). With the current increasing interest in surgical treatment, for Intracerebral Hemorrhage Evacuation the operation rate has increased to approximately 20% In patients with supratentorial ICH, compared with medical (1, 30). In the Asia-Pacific region, the operation rate ranges management alone, surgery in addition to medical management from 30 to 40% and the MIN method, either stereotactic reduced functional dependency and mortality more effectively Frontiers in Neurology | www.frontiersin.org 6 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage (1, 32). Moreover, two meta-analyses have demonstrated that in ICH and improve surgical outcomes (9). This finding is in selected patients benefited from MIN over other treatments contrast to the notion that early craniotomy for ICH leads to a (7, 33). The first meta-analysis of five randomized trials and high rebleeding rate (9, 35). These facts may cause a paradigm nine prospective studies observed a significant difference in shift for neurosurgeons to perform early MIN decompression the mortality rate between patients receiving MIN and those to reduce secondary brain injuries associated with ICH (e.g., receiving traditional craniotomy [odds ratio (OR), 0.76, 95% CI, perihematomal edema). 0.60–0.97] as well as a lower rate of rebleeding and a higher Many studies have enrolled patients with stable clots shown rate of satisfactory neurological recovery for the MIN approach on the CT scan performed 6 h post-onset, including the (33). The second meta-analysis of 15 randomized controlled MISTIE III study, the International Verapamil-Trandolapril trials reported that patients with ICH who received MIN within Study (INVEST), and the ICES trial (3, 9). The main reason for 24 h of ictus were 2.8 times more likely to achieve functional setting the selection criteria is because a previous study reported independence, whereas patients who received MIN within 72 h that ultra-early surgery within 4 h after ictus was associated with were two times more likely to reach functional independence (7). high rebleeding rates (35). However, we must be aware that the Traditional craniotomy requires brain retraction and is majority (25%) of patients with ICH deteriorate within the first highly invasive and traumatic. The problem with retraction few hours of ictus and may require clot evacuation within 4 h in neurosurgery should be emphasized and is often avoided, after ictus, especially for patients with a spot sign or black hole especially in deep-seated ICH, such as putaminal ICH (28, 34). In sign (39). our experience, retraction may lead to rebleeding. The rebleeding All the studies have reported that MIN performed within 8 h rate in open craniotomy using retraction was 15%−40% (35) and after ictus reduced the rebleeding rate (Supplementary Table 1). was significantly higher than that of 0%−3.3% in the MIN group Therefore, we suggest that minimally invasive surgical trials (6, 8, 12, 16, 36). Moreover, long-term brain atrophy after brain for ICH should not exclude patients operated within 4–6 h; retraction is alarming because retraction is associated with the instead, these are the patients with the most favorable functional chronic local thinning of the neocortex (37). outcome per our experience of more than 400 patients with MIN. Similarly, a single-arm surgical evaluation in 39 patients with ICH indicated that 52% of the patients achieved functional Early Minimally Invasive Neurosurgery for independence at follow-up and no mortality was noted (40). If Clot Evacuation, Hemostasis, and Low surgical evacuation is performed early, secondary injury from Rebleeding Rate ICH may be avoided. Moreover, if early clot evacuation can Rebleeding is the primary concern in MIN and usually occurs reduce the rebleeding rate and mass effect, MIN will most likely within 4 h of ictus. The American Heart Association/American benefit patients when it is performed early. In short, we strongly Stroke Association Guidelines for the Management of recommend early MIN (8 h postictus) for ICH because patients Spontaneous Intracerebral Hemorrhage in 2015 indicated will likely to be benefited from such surgery, especially in terms that ultra-early craniotomy (within 4 h of ictus) was associated of functional outcomes. with an increased risk of rebleeding. These data were from a The ideal approach to surgically treat ICH is to maintain study that performed ultra-early craniotomy in 24 patients and a balance among minimal invasiveness, completeness of clot the rebleeding rate was 40% (35). Because of the concern of removal, and secure hemostasis. In our experience, the vital a high rebleeding rate of ultra-early craniotomy, randomized questions are: (1) whether ICH volume can be reduced to < prospective trials have reported a timeframe for surgery that 15 ml, which may lead to improved functional outcomes (4); ranges from 6 to 24 h postictus. By contrast, early endoscopic (2) whether intraoperative bleeding is manageable (if traditional ICH evacuation has been performed in many patients, with low cauterization is necessary, if the working space is adequate for rebleeding rates of 0%−3.3% (6, 8, 12, 16, 36), suggesting that hemostasis, and if the trocar or probe needs to be changed to a MIN reduces the high rebleeding rate. In our previous study, larger one); and (3) whether progressive brain edema occurs after 84% of cases were operated within 4 h after ictus, resulting ICH removal. in a rebleeding rate of 1.5% (6). In this study, we included the patients using antiplatelet and anticoagulative agents and Limitations observed a rebleeding rate of 3.9%. Similarly, Chen et al. (12) This retrospective study has several limitations. First, this treated seven patients within 5 h after ICH and observed no single-center study analyzed the data of 76 patients only. postoperative rebleeding. Nakagasaka treated 23 patients at a These study results lack generalizability and can be applied median time of 4 h and noted no postoperative rebleeding (16). only to a narrow population or in a very specific situation; Nishihara treated 82 patients within 3 h after ICH and observed therefore, we suggest that MIN should be considered in early no postoperative rebleeding (11). Miki et al. treated 127 patients deep-seated ICH with volume ranging from 30 to 80 ml. On with early (<8 h) endoscopic-assisted ICH evacuation and the basis of the findings of previous studies, MIN should reported a postoperative rebleeding rate of 7.1% (38). be considered for deteriorating patients with ICH with a A meta-analysis of eight studies including 2,186 patients clot volume of > 25 ml (33, 41). In our experience, a clot demonstrated the improved functional outcome of surgery volume of > 80 ml is more difficult to treat minimally performed within 8 h of ictus (10). These findings indicated that invasively. Second, this study did not include the control early ICH evacuation using MIN may reduce the rebleeding rate group to detect the difference between MIN and traditional Frontiers in Neurology | www.frontiersin.org 7 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage craniectomy or medical treatment. Third, the patient cohort with ETHICS STATEMENT a small sample size was heterogeneous with different clinical The studies involving human participants were reviewed and decision-making among the four different surgeons. Finally, approved by Institutional Review Board of National Taiwan the lack of data integrity is inherent due to the nature of the University Hospital. Written informed consent for participation retrospective study. We did not manage missing data because was not required for this study in accordance with the national it reflected a real-world setting. Because of these limitations, legislation and the institutional requirements. these study outcomes should be interpreted with caution. These promising preliminary results warrant further large-scale and well-controlled investigations. AUTHOR CONTRIBUTIONS AH contributed to conceptualization, methodology, and formal CONCLUSION analysis. C-HH and S-CC investigated the study. L-TK, S-JH, S-HY, and D-ML contributed to resources. C-HH wrote the Early endoscope-assisted ICH evacuation is a safe and effective original draft and writing, reviewing, and editing the manuscript. treatment for selected patients with ICH. The rebleeding, All authors have read and agreed to the published version of morbidity, and mortality rates of our technique were lower than the manuscript. the reported outcomes of traditional craniotomy. DATA AVAILABILITY STATEMENT SUPPLEMENTARY MATERIAL The original contributions presented in the study are included The Supplementary Material for this article can be found in the article/Supplementary Material, further inquiries can be online at: https://www.frontiersin.org/articles/10.3389/fneur. directed to the corresponding author. 2022.817386/full#supplementary-material REFERENCES American Heart Association/American Stroke Association. Stroke. (2015) 46:2032essi doi: 10.1161/STR.0000000000000069 1. Gross BA, Jankowitz BT, Friedlander RM. 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(2008) 63:1113–7. discussion 7–8. doi: 10.1227/01.NEU.0000330414.56390.DE Publisher’s Note: All claims expressed in this article are solely those of the authors 29. Andaluz N, Zuccarello M. Recent trends in the treatment of spontaneous and do not necessarily represent those of their affiliated organizations, or those of intracerebral hemorrhage: analysis of a nationwide inpatient database. J the publisher, the editors and the reviewers. Any product that may be evaluated in Neurosurg. (2009) 110:403arel doi: 10.3171/2008.5.17559 this article, or claim that may be made by its manufacturer, is not guaranteed or 30. Munakomi S, Agrawal A. Advancements in managing intracerebral endorsed by the publisher. hemorrhage: transition from nihilism to optimism. Adv Exp Med Biol. (2019) 1153:1ol. doi: 10.1007/5584_2019_351 31. Hanley DF, Thompson RE, Muschelli J, Rosenblum M, McBee N, Lane K, et al. Copyright © 2022 Hsu, Chou, Kuo, Huang, Yang, Lai and Huang. This is an open- access article distributed under the terms of the Creative Commons Attribution Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the phase 2 trial. Lancet Neurol. (2016) 15:1228pson 32. Prasad K, Mendelow AD, Gregson B. Surgery for primary supratentorial original publication in this journal is cited, in accordance with accepted academic intracerebral haemorrhage. Cochrane Database Syst Rev. (2008) practice. No use, distribution or reproduction is permitted which does not comply with these terms. CD000200. doi: 10.1002/14651858.CD000200.pub2 Frontiers in Neurology | www.frontiersin.org 9 May 2022 | Volume 13 | Article 817386 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers in Neurology Unpaywall

Minimally Invasive Neurosurgery for Spontaneous Intracerebral Hemorrhage—10 Years of Working Progress at National Taiwan University Hospital

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ORIGINAL RESEARCH published: 20 May 2022 doi: 10.3389/fneur.2022.817386 Minimally Invasive Neurosurgery for Spontaneous Intracerebral Hemorrhage—10 Years of Working Progress at National Taiwan University Hospital 1,2† 3† 4 4 Chiu-Hao Hsu , Sheng-Chieh Chou , Lu-Ting Kuo , Sheng-Jean Huang , 4 4 4 Shih-Hung Yang , Dar-Ming Lai and Abel Po-Hao Huang * Department of Surgery, National Taiwan University Hospital Hsin-Chu Branch, Biomedical Park Hospital, Hsin-Chu, Taiwan, 2 3 Graduate Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan, Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital, and National Taiwan University College of Medicine, Taipei, Taiwan, Division of Hematology, Department of Internal Medicine, National Taiwan University Hospital, and National Taiwan University College of Medicine, Taipei, Taiwan Edited by: Jean-Claude Baron, Intracerebral hemorrhage (ICH) is a life-threatening disease with a global health burden. University of Cambridge, Traditional craniotomy has neither improved functional outcomes nor reduced mortality. United Kingdom Minimally invasive neurosurgery (MIN) holds promise for reducing mortality and improving Reviewed by: Nicholas Morris, functional outcomes. To evaluate the feasibility of MIN for ICH, a retrospective analysis University of Maryland, United States of patients with ICH undergoing endoscopic-assisted evacuation was performed. From Brian Jankowitz, University of Pennsylvania, 2012 to 2018, a total of 391 patients who underwent ICH evacuation and 76 patients who United States received early (<8 h) MIN were included. The rebleeding, mortality, and morbidity rates *Correspondence: were 3.9, 7.9, and 3.9%, respectively, 1 month after surgery. At 6 months, the median Abel Po-Hao Huang [email protected] [interquartile range (IQR)] Glasgow Coma Scale score was 12 (4.75) [preoperative: 10 (4)], the median (IQR) Extended Glasgow Outcome Scale score was 3 (1), and the median These authors have contributed equally to this work and share first (IQR) Modified Rankin Scale score was 4 (1). The results suggested that early (<8 h) authorship endoscope-assisted ICH evacuation is safe and effective for selected patients with ICH. The rebleeding, morbidity, and mortality rates of MIN in this study are lower than those Specialty section: of traditional craniotomy reported in previous studies. However, the management of This article was submitted to Stroke, intraoperative bleeding and hard clots is critical for performing endoscopic evacuation. a section of the journal With this retrospective analysis of MIN cases, we hope to promote the specialization of Frontiers in Neurology ICH surgery in the field of MIN. Received: 18 November 2021 Accepted: 20 April 2022 Keywords: functional outcome, intracerebral hemorrhage, minimally invasive neurosurgery, mortality, early Published: 20 May 2022 surgery Citation: Hsu C-H, Chou S-C, Kuo L-T, Huang S-J, Yang S-H, Lai D-M and INTRODUCTION Huang A-H (2022) Minimally Invasive Neurosurgery for Spontaneous The optimal treatment for intracerebral hemorrhage (ICH) remains among the most controversial Intracerebral Hemorrhage—10 Years topics in neurosurgery. ICH is associated with high morbidity and mortality rates and imposes of Working Progress at National a substantial economic burden worldwide. Recent studies have reported that compared with Taiwan University Hospital. traditional craniotomies, minimally invasive treatments resulted in more favorable outcomes (1–3). Front. Neurol. 13:817386. doi: 10.3389/fneur.2022.817386 These treatments include minimally invasive clot evacuation with stereotactic or endoscopic Frontiers in Neurology | www.frontiersin.org 1 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage aspiration with or without thrombolytic usage. Minimally they had incomplete medical records (n = 4), did not undergo invasive treatments cannot only reduce mortality but also postoperative follow-up imaging (n = 5), or were lost to long- improve neurological recovery in selected patients (3–5), which term follow-up (n = 3). Finally, 76 patients were included in this is rarely observed and encouraging for the treatment of ICH. study (Figure 1). Taiwan has a highly dense population and many hospitals. Patients with ICH can arrive at the hospital shortly after ictus. Rationale for Surgical Management of This is especially true in Taipei City, the capital of Taiwan, where Patients With Intracerebral Hemorrhage our hospital, National Taiwan University Hospital (NTUH), is Currently, we have four attending neurosurgeons in the NTUH located. The majority of surgeries were performed within 4 h after ICH team, which is the only dedicated ICH team in the country. ictus (6). We have performed minimally invasive neurosurgery This specialized team aims to improve functional outcomes, (MIN) under endoscopic guidance for ICH evacuation since quality of care, and quality of life for patients. The minimally 2008. For more than 10 years, we have been continuously refining invasive endoscopic-assisted ICH evacuation was performed in the surgical technique, equipment, protocol, and workflow in the approximately 70% of our surgical cases. On the basis of our pursuit of clinical excellence and improved outcomes. With the extensive experience and the literature review, we have developed paradigm shifting toward minimally invasive surgery, we share guidelines for the optimal treatment of patients with ICH in our experience in this retrospective analysis. NTUH. Recent studies have suggested that early surgery for ICH is associated with satisfactory functional outcomes and low MATERIALS AND METHODS mortality (8–12). This finding is concordant with our practice at NTUH where we performed surgery in more than 80% of Study Design patients with ICH within 4 h after ictus (6). We prefer the This retrospective study was conducted at NTUH after obtaining endoscopic-assisted evacuation over stereotactic thrombolytic the approval from the Ethical Review Board of our institute. We therapy because of its earlier decompression, high hematoma extracted and analyzed clinical data from the medical charts of clearance rate, and cost-effectiveness (13). patients with spontaneous supratentorial ICH who received early The selection of the surgical method depended on our MIN (within 48 h after ictus) from 2012 to 2018. This study clinical experience and the literature review. MIN was mostly was performed in compliance with applicable local regulations performed for deep-seated early ICH (such as the basal ganglia and the ethical principles of the Declaration of Helsinki. All and thalamus, with ICH volume ranging from 20 to 80 ml). the experimental protocols were approved by the Institutional For superficial (subcortical or lobar) ICH, minicraniotomy using Review Board of NTUH. Because of the retrospective nature of microscopic evacuation or endoscopic-assisted MIN was both this study, the requirement of informed consent was waived. feasible. For delayed cases (>72 h after ictus), craniectomy with Informed consent for surgery was obtained from each patient per ICH evacuation was preferred because such cases usually have routine practice. substantial brain edema and massive blood clots that favor decompressive craniectomy as the primary treatment instead Patient Selection of MIN. A series of experiences presented in this study represents the working progress of 6 years following a previously published series of our experiences from 2008 to 2011 (6). Between 2012 and Surgical Procedure 2018, a total of 391 patients underwent ICH evacuation at NTUH. Various MIN techniques have been developed for ICH evacuation We included patients with spontaneous supratentorial ICH who (14). We adopted the endoscopic-assisted approach where received early MIN (within 48 h after ictus). A cutoff of<48 h was suction is applied on the side of the endoscope inside a selected on the basis of the finding of a meta-analysis that patients 10–12-mm port or sheath that creates the working space who underwent MIN within 72 h were two times more likely (also known as the port-based approach). By contrast, the to achieve functional independence (7). In this experience, ICH pure endoscopic approach [e.g., the stereotactic intracerebral evacuation after 48 h of ictus may lead to significant brain edema hemorrhage underwater blood aspiration (SCUBA) technique] and massive blood clots that favor decompressive craniectomy as uses the aspiration device inside the endoscope (through its the primary treatment instead of MIN. working channel) with a 19-F peel-away sheath. We excluded patients with etiology related to structural Clot evacuation could be smoothly performed with one hand lesions or nonprimary lesions (cerebral aneurysm, arteriovenous holding the endoscope and the other hand holding a suction malformation, and cavernous malformation), cerebellar device. We used 8-Fr suction to remove the clot because suction hemorrhage, traumatic ICH, tumor bleeding, hemorrhagic with a smaller caliber would lead to the ineffective removal of transformation after ischemic stroke or postoperative bleeding, ICH. In the presence of a hard clot, the alligator punch was used or primary intraventricular hemorrhage (IVH). In addition, to pass through the sheath for piecemeal removal. In extreme we excluded patients who underwent traditional craniotomy, cases, we used the cavitron ultrasonic surgical aspirator (CUSA) external ventricular drainage, or decompressive craniectomy as to remove the hard clot. The CUSA is a surgical device used the primary treatment. in neurosurgical procedures. The CUSA is coupled with low- We carefully reviewed the medical records of the remaining 88 frequency ultrasound that helps operators to dissect or fragment patients who underwent minimally invasive endoscope-assisted tissues or pathologies. The CUSA was used to manage ICH cases ICH evacuation. Furthermore, we excluded 12 patients because with hard clots that could not be removed with suction only. Frontiers in Neurology | www.frontiersin.org 2 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage FIGURE 1 | Flowchart of patient selection. Apollo, Artemis, and Myriad are not available in Taiwan; thus, these techniques were time-consuming. Moreover, achieving we have no experience in using these devices. hemostasis by using these techniques was difficult. Later, we Regarding hemostasis during surgery, we initially used an used local hemostatic agents that remarkably reduced the time endoscopic bipolar or a suction coagulation device; however, of hemostasis, with a low rebleeding rate. In our experience, Frontiers in Neurology | www.frontiersin.org 3 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage no active bleeding requiring coagulation was noted in more suction and irrigation is crucial for bleeder identification and than 90% of cases and local hemostatic agents [e.g., FLOSEAL hemostasis (16). Hemostatic Matrix (Baxter Healthcare Corporation, Fremont, For brain access, most neurosurgeons used the 12-mm California, USA), a gelatin–thrombin matrix] yielded satisfactory outer diameter transparent trocar. The peel-away sheath was hemostasis (15). occasionally used by neurosurgeons who were comfortable When an active bleeder was encountered during surgery, with ventriculoscopic techniques (6). In our experience, we suctioned out blood, used irrigation to identify the active only 10%−15% of the cases had intraoperative bleeding bleeder, contacted it with the suction tip, and performed requiring hemostasis and most of the small arterial bleeding cauterization by using a metallic suction tube. The importance from thalamostriate perforators could be stopped using local of a balanced suction irrigation technique in the minimally hemostatic agents (8). During surgery, similar to the SCUBA invasive surgery of ICH was described in detail in a previous technique, we alternated between air and water phases; we study (16). After hemostasis, we placed an external ventricular found this technique to be useful for preventing the hematoma drain if the frontal horn was entered during surgery; otherwise, cavity from collapsing with resultant residual ICH and for we inserted an intracranial pressure (ICP) monitor [fiber identifying the bleeder (19). Cauterization was required in <5% optic devices (e.g., Camino ICP Monitor) and strain gauge of cases and was easily performed using traditional suction at the devices (e.g., Codman Microsensor and Raumedic Neurovent- bleeding point (vessel) with unipolar cauterization touching the P ICP sensor)] through the surgical corridor created by handle of the sucker (poor man’s suction bipolar). Alternatively, the trocar under direct vision in the perihematoma zone commercialized suction bipolar devices can be used (6). If all of the brain parenchyma. A surgical biopsy of the brain these attempts failed, the next step was to change to a larger parenchyma was performed, if amyloid angiopathy was trocar (Vycor, with a diameter of >2 cm used for traditional suspected (17). bipolar cauterization). We rarely converted to craniotomy, which In terms of surgical techniques, we recommend using was only performed in three out of more than 400 ICH cases. the penetrating technique (Huang’s technique) instead of the circumferential technique used in our previous studies (6, 8) Perioperative Care for ICH removal because it prevents collateral brain damage In the perioperative period, we observed that dexmedetomidine when using the trocar or port inside the normal brain tissue. substantially reduced blood pressure fluctuations. This reduction For typical basal ganglia ICH, we used modified Kocher’s point is associated with a decreased rebleeding rate, as demonstrated (1 cm lateral to Kocher’s point). A 2.5-cm incision was vertically in various experiences and other major surgeries (20). The effect made on modified Kocher’s point, creating a 1.5–2.0-cm burr of dexmedetomidine on patients with ICH was reported in a hole. After dural opening, either the trans-sulcal or transcortical clinical trial (21). For cases with a high risk of rebleeding, approach was used. The intraoperative Aloka burr-hole type we may consider tranexamic acid and recombinant factor VIIa ultrasound was selectively used to verify the trajectory and (NovoSeven) (22). Currently, we routinely perform CT within depth of ICH before puncturing with the trocar (we used a 24 h after surgery to confirm the residual hematoma and the transparent trocar with an outer diameter of 12 mm and length degree of evacuation. of 10 cm for putaminal ICH) (6). For thalamic ICH, we used Cognitive enhancers and neural stimulants were reported a considerably different surgical approach. Initially, our team to improve cognitive and behavioral impairments in patients used an aggressive approach involving the use of the endoscopic with putaminal ICH and traumatic brain injury (23). We used technique to remove thalamic ICH in the brain parenchyma. methylphenidate in patients with ICH who were comatose However, the surgical outcome was poor and most of the patients before the surgery to improve neurological outcomes. In our remained comatose after evacuation. Therefore, our current goal experience of 58 patients, methylphenidate was safe and effective was to relieve hydrocephalus and remove IVH to minimize and was associated with faster consciousness recovery, greater shunt dependency. We only dived into thalamic ICH in the chance of successful extubation, and shorter intensive care unit brain parenchyma when we observed the rupture side during (ICU) stay. However, a study reported the rare side effects of endoscopic surgery. The first step was to determine whether methylphenidate, such as serotonin syndrome, in patients with to use the frontal or occipital approach; we occasionally used ICH (24). the contralateral approach (18). The rupture side could be determined through preoperative CT performed to choose the surgical approach. The thalamostriate vein was required to be Data Collection carefully preserved to prevent iatrogenic infarction. We collected data on the following characteristics of the patients: We applied the concepts of the SCUBA technique in our hematoma location and volume, presence of IVH, sex, age, time MIN for ICH evacuation. The SCUBA technique differs from of operation, operative blood loss, and hematoma evacuation minimally invasive ICH intervention because it combines two rate. All the patients underwent preoperative head CT and a separate neuroendoscopic strategies in two phases: the first follow-up head CT within 1 week after surgery. The estimated is using dry-field conditions and the second is using a wet- hematoma volume was calculated using the ABC/2 method (A: field strategy (19). This prevents the collapse of the hematoma maximum length in the axial cut of CT, B: width perpendicular to cavity and allows for complete clot removal. This technique is A on the same CT cut, and C: the number of slices multiplied by useful for bleeder identification. During the procedure, balancing the slice thickness). Frontiers in Neurology | www.frontiersin.org 4 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage TABLE 1 | Characteristics of patients. Putaminal Thalamic Subcortical All (n = 56) (n = 9) (n = 11) Male, n (%) 42 (75.0) 5 (55.6) 6 (54.5) 53 (69.7) Age (year), median (IQRs) 58 (17.25) 66 (6) 62 (32) 59 (18) ICH score, median (IQRs) 2 (1) 3 (1) 2 (1.5) 2 (1) IVH, n (%) 26 (46.4) 6 (66.7) 4 (36.4) 36 (47.4) Anticoagulants and antiplatelets, n (%) Antiplatelet agents 6 (10.7) 1 (11.1) 3 (27.3) 10 (13.2) Anticoagulant agents 1 (1.8) 0 (0) 0 (0) 1 (1.3) Both 2 (3.6) 0 (0) 0 (0) 2 (2.6) Operative time (min), median (IQRs) 108 (50.25) 109 (63) 104 (34.5) 107 (50.25) Preoperative ICH volume (ml), median (IQRs) 45 (28.75) 35 (15) 50 (20) 42.5 (25) Operative blood loss (ml), median (IQRs) 50 (12.5) 50 (0) 50 (0) 50 (0) ICU length of stay (day), median (IQRs) 16 (14.5) 13.5 (15.25) 19 (3) 16 (13) Hospital length of stay (day), median (IQRs) 30 (23.5) 29 (25.25) 37 (21) 28 (11.5) IVH, intraventricular hemorrhage; IQR, interquartile range; ICU, intensive care unit; ICH, intracerebral hemorrhage. Clinical Outcome noted and IVH was found in 47.4% of the patients. Most of the Outcome measures included the hematoma evacuation rate, enrolled patients were aged from 57 to 60 years, except for those rebleeding, mortality rate, morbidity rate, the preoperative with thalamic ICH (median age: 66 years). The median operative and postoperative Glasgow Coma Scale (GCS) scores, the time ranged from 104 to 108 min. The ICH score (median: 2) and operative blood loss (median: 50 ml) were similar among the postoperative Extended Glasgow Outcome Scale (GOSE) scores, the Modified Rankin Scale (mRS), length of ICU stay, different types of ICH. The patients with putaminal ICH had the highest preoperative ICH volume (median: 45 ml). and the length of hospital stay. The hematoma evacuation rate was calculated as [(preoperative volume – postoperative Most of the patients (97%) underwent MIN within 4 h after volume)/(preoperative volume) × 100 (%)]. Mortality was ictus. Only two patients underwent surgery on the second day of defined as all-cause death occurring within 30 days after surgery. ictus because of hematoma expansion. Our hospital defines three Rebleeding and morbidity rates were examined 1 month after classes for emergent operation. The duration between notifying surgery. Rebleeding was defined as a postoperative hematoma the operation room to the start of operation is limited to 30 min, volume greater than the preoperative volume or a difference 2 h, and 4 h for first-class, second-class, and third-class emergent of <5 ml between preoperative and postoperative hematoma operations, respectively. ICH is classified as a third-class surgery, volume. Morbidity included wound dehiscence and surgical site which is mostly performed within 4 h. infection, including meningitis, ventriculitis, and brain abscess. Postoperative outcomes included the GCS scores at 1 and 6 Postoperative Outcomes months and the GOSE and the mRS scores at 6 months. Table 2 summarizes the surgical and functional outcomes, with no significant difference noted between the groups. The median Statistical Analysis (IQR) hematoma evacuation rate was 85.7% (16.7%) and the Descriptive statistics were used to present categorical data in median (IQR) postoperative ICH volume was 5 (5) ml. According numbers and percentages and continuous data in numbers, to the Minimally Invasive Surgery Plus Recombinant Tissue medians, and interquartile ranges (IQRs). The surgical and Plasminogen Activator for Intracerebral Hemorrhage Evacuation functional outcomes were analyzed using the Kruskal–Wallis III (MISTIE III) study, a reduction in clot size to ≤15 ml is test. A P-value of <0.05 was regarded as statistically significant. associated with improvement in functional outcomes (4). In Statistical analyses were performed using SPSS (version 25, our series, 64 (84.2%) patients reached the goal of a residual Chicago, Illinois, USA). hematoma volume of <15 ml. The overall rebleeding rate at 1 month after surgery was 3.9%. Three patients experienced rebleeding in the first postoperative follow-up [2 (3.6%) in the RESULTS putaminal group and 1 (11.1%) in the thalamic group]. Six Demographics and Baseline patients died eventually (the overall mortality rate: 7.9%): two Characteristics patients died from pneumonia and sepsis, two patients died from Table 1 summarizes the demographics of the patients. We postoperative central nervous system infection, and two patients divided the patients into three groups according to the hematoma died because their family members decided to withdraw life location: putaminal (n = 56), thalamic (n = 9), and subcortical support owing to the lack of clinical improvement. The morbidity (n = 11). The male predominance of approximately 69.7% was rate at 1 month after surgery was 3.9%; one patient developed Frontiers in Neurology | www.frontiersin.org 5 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage TABLE 2 | Outcomes. Putaminal Thalamic Subcortical P-Value All (n = 56) (n = 9) (n = 11) (n = 76) Rebleeding, n (%) 2 (3.6) 1 (11.1) 0 (0) 3 (3.9) Mortality, n (%) 5 (8.9) 0 (0) 1 (9.1) 6 (7.9) Morbidity, n (%) 3 (5.4) 0 (0) 0 (0) 3 (3.9) Hematoma evacuation rate (%), median (IQRs) 86.6 (11.9) 75.0 (19.0) 80.0 (20.8) 0.170 85.7 (16.7) Postoperative ICH volume (ml), median (IQRs) 5 (5) 10 (5) 10 (12.5) 5 (5) Postoperative hematoma volume <15 ml, n (%) 48 (85.7) 8 (88.8) 8 (77.8) 64 (84.2) GCS, median (IQRs) Pre-op 10 (4) 8 (3) 11 (3.5) 0.343 10 (4) Post-op 1 month 11 (4) 12 (5) 13 (4) 0.508 12 (4) Post-op 6 months 12 (4) 14 (6) 14 (3) 0.659 12 (4.75) GOSE, median (IQRs) Post-op 6 months 3 (1) 4 (2) 4 (1.5) 0.666 3 (1) mRS, median (IQRs) Post-op 6 months 4 (1) 4 (2) 4 (1) 0.997 4 (1) mRS 0–2, n (%) 7 (12.5) 1 (11.1) 3 (22.2) 11 (14.5) mRS 0–3, n (%) 21 (37.5) 4 (44.4) 3 (22.2) 28 (36.8) GCS, Glasgow coma scale; GOSE, Glasgow outcome scale extended; ICU, intensive care unit; mRS, modified rankin scale; OP, operation; IQR, interquartile range; ICH, intracerebral hemorrhage. scalp wound dehiscence, one patient developed meningitis and aspiration or endoscopic-assisted evacuation, is widely ventriculitis, and one patient developed brain abscess. used (27). Functional outcomes improved after surgery, with no Clinical Outcomes Compared With Prior significant differences observed between the groups (Table 2). The median (IQR) preoperative GCS score was 10 (4), which Minimally Invasive Neurosurgery Reports was numerically increased to 12 (4) at 1 month and 12 (4.75) In our series, early MIN within 48 h after ICH ictus resulted at 6 months. The median (IQR) GOSE score at the 6-month in a low rebleeding rate (3.9%), low mortality rate (7.9%), and follow-up was 3 (1). The median (IQR) mRS score at the 6-month low morbidity rate (3.9%); moreover, 36.8% of the patients follow-up was 4 (1). Satisfactory outcomes (mRS score: 0–3) were exhibited satisfactory functional outcomes (mRS score: 0–3) 6 noted in 36.8% of the patients. months after MIN. Although the overall median GOSE score indicated that the patients still required assistance to perform the activities of daily living (GOSE = 3) 6 months after MIN, the DISCUSSION patients with thalamic or subcortical ICH could occasionally be at home independently (GOSE = 4) and their overall GCS score The prevalence of ICH is especially high in Asia-Pacific regions, improved over time. Compared with those of patients included where ICH accounts for approximately 30%−40% of all stroke in other MIN studies, the postoperative outcomes of our patients cases. In the United States, ICH accounts for approximately only appeared to be more favorable. In the MISTIE III study (4), 44% 15% of all stroke cases (25). Each year in China alone, more than of patients achieved the mRS score of 0–3, 39% of patients had 150,000 patients receive minimally invasive treatment for ICH the GOSE score of ≥4 at 12 months, and the mortality rate at (8). Race and ethnicity appear to explain some of the variation 6 months was 15%. In the MISTIE III study, 33.4% of patients in clinical characteristics and outcomes after acute ICH; for achieved the mRS score of 0–3 and the mortality rate within 30 example, Caucasian patients with ICH are more likely to be older, days was 14.8% (31). In the intraoperative stereotactic CT-guided have a larger ICH volume, and have a higher mortality rate than endoscopic surgery (ICES) trial including six patients, 24% of Asian patients (26). patients achieved the mRS score of 0–3 and no patient died within The operation rate considerably varies worldwide, 30 days after surgery (3). ranging from 2 to 74% (27). In the United States, the early operation rate was previously 16% and decreased to Literature Support for Minimally Invasive 6% in 2005, presumably due to the results of the Surgical Neurosurgery Over Traditional Craniotomy Treatment for Ischemic Heart Failure (STICH) trial (28, 29). With the current increasing interest in surgical treatment, for Intracerebral Hemorrhage Evacuation the operation rate has increased to approximately 20% In patients with supratentorial ICH, compared with medical (1, 30). In the Asia-Pacific region, the operation rate ranges management alone, surgery in addition to medical management from 30 to 40% and the MIN method, either stereotactic reduced functional dependency and mortality more effectively Frontiers in Neurology | www.frontiersin.org 6 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage (1, 32). Moreover, two meta-analyses have demonstrated that in ICH and improve surgical outcomes (9). This finding is in selected patients benefited from MIN over other treatments contrast to the notion that early craniotomy for ICH leads to a (7, 33). The first meta-analysis of five randomized trials and high rebleeding rate (9, 35). These facts may cause a paradigm nine prospective studies observed a significant difference in shift for neurosurgeons to perform early MIN decompression the mortality rate between patients receiving MIN and those to reduce secondary brain injuries associated with ICH (e.g., receiving traditional craniotomy [odds ratio (OR), 0.76, 95% CI, perihematomal edema). 0.60–0.97] as well as a lower rate of rebleeding and a higher Many studies have enrolled patients with stable clots shown rate of satisfactory neurological recovery for the MIN approach on the CT scan performed 6 h post-onset, including the (33). The second meta-analysis of 15 randomized controlled MISTIE III study, the International Verapamil-Trandolapril trials reported that patients with ICH who received MIN within Study (INVEST), and the ICES trial (3, 9). The main reason for 24 h of ictus were 2.8 times more likely to achieve functional setting the selection criteria is because a previous study reported independence, whereas patients who received MIN within 72 h that ultra-early surgery within 4 h after ictus was associated with were two times more likely to reach functional independence (7). high rebleeding rates (35). However, we must be aware that the Traditional craniotomy requires brain retraction and is majority (25%) of patients with ICH deteriorate within the first highly invasive and traumatic. The problem with retraction few hours of ictus and may require clot evacuation within 4 h in neurosurgery should be emphasized and is often avoided, after ictus, especially for patients with a spot sign or black hole especially in deep-seated ICH, such as putaminal ICH (28, 34). In sign (39). our experience, retraction may lead to rebleeding. The rebleeding All the studies have reported that MIN performed within 8 h rate in open craniotomy using retraction was 15%−40% (35) and after ictus reduced the rebleeding rate (Supplementary Table 1). was significantly higher than that of 0%−3.3% in the MIN group Therefore, we suggest that minimally invasive surgical trials (6, 8, 12, 16, 36). Moreover, long-term brain atrophy after brain for ICH should not exclude patients operated within 4–6 h; retraction is alarming because retraction is associated with the instead, these are the patients with the most favorable functional chronic local thinning of the neocortex (37). outcome per our experience of more than 400 patients with MIN. Similarly, a single-arm surgical evaluation in 39 patients with ICH indicated that 52% of the patients achieved functional Early Minimally Invasive Neurosurgery for independence at follow-up and no mortality was noted (40). If Clot Evacuation, Hemostasis, and Low surgical evacuation is performed early, secondary injury from Rebleeding Rate ICH may be avoided. Moreover, if early clot evacuation can Rebleeding is the primary concern in MIN and usually occurs reduce the rebleeding rate and mass effect, MIN will most likely within 4 h of ictus. The American Heart Association/American benefit patients when it is performed early. In short, we strongly Stroke Association Guidelines for the Management of recommend early MIN (8 h postictus) for ICH because patients Spontaneous Intracerebral Hemorrhage in 2015 indicated will likely to be benefited from such surgery, especially in terms that ultra-early craniotomy (within 4 h of ictus) was associated of functional outcomes. with an increased risk of rebleeding. These data were from a The ideal approach to surgically treat ICH is to maintain study that performed ultra-early craniotomy in 24 patients and a balance among minimal invasiveness, completeness of clot the rebleeding rate was 40% (35). Because of the concern of removal, and secure hemostasis. In our experience, the vital a high rebleeding rate of ultra-early craniotomy, randomized questions are: (1) whether ICH volume can be reduced to < prospective trials have reported a timeframe for surgery that 15 ml, which may lead to improved functional outcomes (4); ranges from 6 to 24 h postictus. By contrast, early endoscopic (2) whether intraoperative bleeding is manageable (if traditional ICH evacuation has been performed in many patients, with low cauterization is necessary, if the working space is adequate for rebleeding rates of 0%−3.3% (6, 8, 12, 16, 36), suggesting that hemostasis, and if the trocar or probe needs to be changed to a MIN reduces the high rebleeding rate. In our previous study, larger one); and (3) whether progressive brain edema occurs after 84% of cases were operated within 4 h after ictus, resulting ICH removal. in a rebleeding rate of 1.5% (6). In this study, we included the patients using antiplatelet and anticoagulative agents and Limitations observed a rebleeding rate of 3.9%. Similarly, Chen et al. (12) This retrospective study has several limitations. First, this treated seven patients within 5 h after ICH and observed no single-center study analyzed the data of 76 patients only. postoperative rebleeding. Nakagasaka treated 23 patients at a These study results lack generalizability and can be applied median time of 4 h and noted no postoperative rebleeding (16). only to a narrow population or in a very specific situation; Nishihara treated 82 patients within 3 h after ICH and observed therefore, we suggest that MIN should be considered in early no postoperative rebleeding (11). Miki et al. treated 127 patients deep-seated ICH with volume ranging from 30 to 80 ml. On with early (<8 h) endoscopic-assisted ICH evacuation and the basis of the findings of previous studies, MIN should reported a postoperative rebleeding rate of 7.1% (38). be considered for deteriorating patients with ICH with a A meta-analysis of eight studies including 2,186 patients clot volume of > 25 ml (33, 41). In our experience, a clot demonstrated the improved functional outcome of surgery volume of > 80 ml is more difficult to treat minimally performed within 8 h of ictus (10). These findings indicated that invasively. Second, this study did not include the control early ICH evacuation using MIN may reduce the rebleeding rate group to detect the difference between MIN and traditional Frontiers in Neurology | www.frontiersin.org 7 May 2022 | Volume 13 | Article 817386 Hsu et al. Minimally-Invasive Surgery for Intracerebral Hemorrhage craniectomy or medical treatment. Third, the patient cohort with ETHICS STATEMENT a small sample size was heterogeneous with different clinical The studies involving human participants were reviewed and decision-making among the four different surgeons. Finally, approved by Institutional Review Board of National Taiwan the lack of data integrity is inherent due to the nature of the University Hospital. Written informed consent for participation retrospective study. We did not manage missing data because was not required for this study in accordance with the national it reflected a real-world setting. Because of these limitations, legislation and the institutional requirements. these study outcomes should be interpreted with caution. These promising preliminary results warrant further large-scale and well-controlled investigations. AUTHOR CONTRIBUTIONS AH contributed to conceptualization, methodology, and formal CONCLUSION analysis. C-HH and S-CC investigated the study. L-TK, S-JH, S-HY, and D-ML contributed to resources. C-HH wrote the Early endoscope-assisted ICH evacuation is a safe and effective original draft and writing, reviewing, and editing the manuscript. treatment for selected patients with ICH. The rebleeding, All authors have read and agreed to the published version of morbidity, and mortality rates of our technique were lower than the manuscript. the reported outcomes of traditional craniotomy. DATA AVAILABILITY STATEMENT SUPPLEMENTARY MATERIAL The original contributions presented in the study are included The Supplementary Material for this article can be found in the article/Supplementary Material, further inquiries can be online at: https://www.frontiersin.org/articles/10.3389/fneur. directed to the corresponding author. 2022.817386/full#supplementary-material REFERENCES American Heart Association/American Stroke Association. Stroke. (2015) 46:2032essi doi: 10.1161/STR.0000000000000069 1. Gross BA, Jankowitz BT, Friedlander RM. 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This is an open- access article distributed under the terms of the Creative Commons Attribution Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the phase 2 trial. Lancet Neurol. (2016) 15:1228pson 32. Prasad K, Mendelow AD, Gregson B. Surgery for primary supratentorial original publication in this journal is cited, in accordance with accepted academic intracerebral haemorrhage. Cochrane Database Syst Rev. (2008) practice. No use, distribution or reproduction is permitted which does not comply with these terms. CD000200. doi: 10.1002/14651858.CD000200.pub2 Frontiers in Neurology | www.frontiersin.org 9 May 2022 | Volume 13 | Article 817386

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