Neurosurg Rev DOI 10.1007/s10143-015-0606-6

REVIEW

Minimally invasive endoscopic surgery for treatment of spontaneous intracerebral haematomas Christopher Beynon & Patrick Schiebel & Julian Bösel & Andreas W. Unterberg & Berk Orakcioglu

Received: 26 April 2013 / Accepted: 16 November 2014 # Springer-Verlag Berlin Heidelberg 2015

Abstract Spontaneous intracerebral haemorrhage (ICH) is a devastating disease with a mortality rate of more than 40 % and a high morbidity rate with 10–15 % of survivors remaining fully dependent [11]. The role of surgical treatment of ICH remains a matter of controversy and ongoing investigation. Advances in neurosurgical techniques such as endoscopy and neuronavigation have been established in various fields of neurosurgery. Results of reported case series have suggested that some patients with ICH may benefit from haematoma evacuation through minimally invasive endoscopic procedures. In this article, we focus on the pathophysiologic rationales behind minimally invasive haematoma evacuation through endoscopic surgery and provide an overview of technical developments and reported patient series. In addition, the modalities of the surgical procedure at the authors’ institution are described. Controlled clinical trials are needed to evaluate the full potential and limitations of this promising technique. Keywords Intracerebral haemorrhage . Endoscopic surgery . Haematoma evacuation . Neuronavigation . Minimally invasive surgery Introduction In cases of intraventricular haemorrhage (IVH), it is well recognized that an external ventricular drainage (EVD) should be Electronic supplementary material The online version of this article (doi:10.1007/s10143-015-0606-6) contains supplementary material, which is available to authorized users. C. Beynon : P. Schiebel : A. W. Unterberg : B. Orakcioglu (*) Department of Neurosurgery, Heidelberg University Hospital, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany e-mail: [email protected] J. Bösel Department of Neurology, Heidelberg University Hospital, Heidelberg, Germany

inserted in patients with decreased level of consciousness in order to avoid or treat increased intracranial pressure (ICP) [24]. Surgical haematoma evacuation is recommended for patients with cerebellar haemorrhage who deteriorate clinically or who have brainstem compression on computed tomography (CT) images. The role of surgical treatment for supratentorial intracerebral haemorrhage is much less established and the decision whether to evacuate these haematomas remains controversial [22]. Systematic reviews of clinical studies have failed to prove beneficial effects of surgical haematoma evacuation in patients with ICH [36]. The international Surgical Trial of Intracerebral Haemorrhage (STICH) has recruited 1033 patients with ICH [20] and until now, it remains the most important trial regarding the role of surgery in this disease. Patients were randomized to best medical treatment or early surgical haematoma evacuation within 96 h. Analysis showed that there was no overall benefit from surgery while subanalyses revealed that there was a trend towards a better outcome in surgically treated patients if haematomas were located superficially. These findings had initiated the follow-up trial STICH II which randomized 601 patients with superficial ICH to early surgery or initial conservative treatment. Although results failed to reach significance, they suggest that early surgery might have a small survival advantage for patients with ICH especially in cases of impaired consciousness (Glasgow Coma Scale score 9–12) [21]. Rationale behind minimally invasive endoscopic haematoma evacuation Pathophysiologic background In the majority of cases, chronic damage of the cerebral vasculature due to long-standing arterial hypertension is the underlying pathophysiological mechanism leading to ICH [13].

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ICH is considered a complex, dynamic process with three hypothesized phases: (1) initial haemorrhage, (2) haematoma expansion and (3) enlargement of perihaematomal oedema. Although both the rate and extent of haematoma expansion vary between patients, a study demonstrated a significant increase of more than 33 % from baseline volume within 3 h from ictus in 38 % of patients [6]. Haematoma expansion is an important cause of early neurological deterioration and seems to depend on the original size of the haematoma. The final ICH volume is probably the most important outcome determinant. However, neither reliable predictors of haematoma expansion, with exception of the ‘spot sign’ on contrastenhanced CT, nor treatment options to avoid haematoma exp a n s i o n h a v e b e e n e s t a b l i s h e d s o fa r [ 4 2 ] . T h e perihaematomal brain oedema which develops after the initial bleed is considered the main cause of deterioration after the first day [19] and the existence of a perihaemorrhagic ‘penumbra-like’ zone has been suggested as a major cause of this oedema. Experimental and clinical studies have found no evidence of potentially salvageable ischemic brain tissue surrounding the haematoma [33, 39]. Nevertheless, several pathophysiological metabolic processes involved in the breakdown of blood components, for instance activated by thrombin, may contribute to oedema formation [14]. Cytotoxic mediators, disruption of the blood–brain barrier and inflammatory reactions contribute to the extent of perihaemorrhagic oedema [37, 47]. The rationale behind surgical evacuation of the haematoma is to reduce the mass effect on surrounding brain tissue and eliminate the toxic effects of blood degradation products. Through haematoma evacuation, the amount of cytotoxic mediators and the extent of perihaemorrhagic oedema are theoretically reduced. This rationale is supported by findings of a study by Broderick et al. who demonstrated a significant correlation between blood volume and 30-day mortality of patients with ICH [5]. Enlargement of the haematoma has been associated with increased mortality and morbidity [41], and the results of a recent study on 335 patients with ICH demonstrated that a 1-mL increase in haematoma growth leads to a 5 % higher risk of death or dependency [9]. Results from animal studies have suggested that surgical haematoma evacuation after experimental ICH may contribute to reduced mortality and improved neurological outcome. Altumbabic et al. induced ICH in rats through injection of bacterial collagenase into the caudate nucleus [1]. Haematoma aspiration 4 h after haemorrhage induction was associated with significantly reduced neuronal loss in the perihaematomal region of the striatum and better performance on a motor-behaviour evaluation than in controls. In a balloon-inflating experimental model of ICH, neuronal damage was higher in permanent inflation than in transient inflation suggesting that haematoma evacuation reduces neuronal damage [18].

Nevertheless, as mentioned before, a clear benefit through surgical haematoma evacuation for patients remains to be proven. Advantages of minimally invasive approaches Conventional surgical haematoma evacuation through craniotomy is an invasive procedure, and depending on existent comorbidities, the procedure itself may increase morbidity and mortality. A recent analysis of more than 45,000 patients who underwent surgical evacuation of spontaneous ICH demonstrated that the in-hospital mortality rate was 27.2 % and the complication rate (e.g., pulmonary, renal, and thromboembolic) was 41.2 % [35]. Although the influence of surgical procedures’ durations on mortality and morbidity has not been specifically studied for neurosurgical interventions, the results from a study on patients aged 80 years and older demonstrate that duration of surgical interventions may exacerbate detrimental effects of existing comorbidities [43]. Therefore, shortening of the surgical intervention’s duration through minimally invasive approaches may also reduce perioperative morbidity. The key advantage of minimally invasive brain surgery is a drastically reduced manipulation of viable brain tissue. Haematoma evacuation through conventional craniotomy often involves the use of brain retractors, and in order to visualize the haematoma cavity, significant compression of viable brain tissue is often inevitable. Especially in deeply located haematomas, this is an important issue as the distance through viable brain is increased and more retraction on brain tissue is necessary for sufficient visualization. In contrast, endoscopic techniques allow longer trajectories and access to deep haematomas without increased retraction of viable brain tissue. Furthermore, the use of neuronavigation easily facilitates access to the haematoma through considerable distances of non-eloquent brain tissue. Increased manipulation of viable brain tissue may offset beneficial effects of surgical haematoma evacuation. The STICH trial finding that surgical haematoma evacuation showed a trend towards improved outcome in patients with lobar haemorrhage but not in patients with ganglionic haemorrhage, may support this hypothesis. A further important advantage of minimally invasive approaches is the significantly faster access to the haematoma. Large space-occupying haematomas can lead to increased ICP, and this can be avoided through early evacuation of the haematoma. Haematoma access through conventional craniotomy is more time-consuming than through minimally invasive approaches, and in patients with impending cerebral herniation, this may have a significant impact on mortality and morbidity. It is quite striking that the vast majority of studies and reported case series on endoscopic haematoma evacuation in ICH originate from Asian countries. It is well recognized that

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the incidence of ICH is significantly higher in Asian populations [16, 40] probably due to pathophysiologic differences from other populations. Minimally invasive techniques for endoscopic haematoma evacuation have not been studied in a large Caucasian population and results may differ due to different disease aetiologies. This review article focuses on minimally invasive approaches with the use of endoscopic devices, but other promising techniques have been developed and are currently investigated. For instance, stereotactic infusion of fibrinolytics such as recombinant tissue-plasminogen activator (rt-PA) into the haematoma cavity has shown promising results in preliminary studies [38]. Efficacy of this treatment is currently under investigation in the prospective ‘Minimally Invasive Surgery plus rt-PA for Intracerebral Hemorrhage Evacuation (MISTIE)’ trial (http://clinicaltrials.gov/ct2/show/ NCT00224770). Minimally invasive endoscopic surgical haematoma evacuation Technical developments and short-term outcome The first reports of endoscopic haematoma evacuation were published in 1985 [2, 3], and therefore, it is difficult to transfer the study results to today’s clinical situation. CT images were studied and a surgical approach through the shortest distance of viable brain was chosen to evacuate the haematoma. An endoscope was inserted into the haematoma cavity through a burr hole. The cavity was continuously rinsed with artificial fluid through one channel, and at regular intervals, the mixture of this fluid and blood clots was removed by suction through a separate endoscope channel. The whole surgical procedure was performed under visual control through a video camera attached to the endoscope. Several technical improvements have been reported in the last two decades. Nishihara et al. [31] reported the use of a transparent sheath, which is inserted into the haematoma cavity. This technique has important advantages in comparison to the endoscope-only approach. The visualization of the surgical field is significantly increased and a ‘working channel’ is created. Identification of the haematoma-brain border is improved through this transparent sheath and the ‘working channel’ enables the insertion and use of instruments, e.g., for coagulation of bleeding vessels, without damaging brain tissue. This transparent sheath has been used by the same group for further studies [30, 29] and was adopted by several other groups [26, 48, 17, 34, 50]. Other authors have reported the use of stainless steel tubes in their studies [7, 8, 15]. Ochalski et al. used an endoscopic port system with a bullet-shaped dilator which is passed into the centre of the haematoma after insertion of a stereotactic needle [32]. Waran et al. [45] developed an expandable cannula system which is introduced like a conventional brain cannula that

can be opened up after insertion into the haematoma cavity. It also enables using other instruments and its size is adjustable as necessary. The same group also used neuronavigation, a technique which proved beneficial in several other fields of neurosurgery [44]. Neuronavigation improves intraoperative orientation and was used for endoscopic haematoma evacuation initially by Miller et al. [23]. It was also used in a further study on ICH patients with coagulopathies [34]. Dye and colleagues have used frameless stereotactic guidance for endoscopic evacuation of ICH in a series of six patients [12]. Nagasaka and colleagues [25] developed a combined irrigation-coagulation-suction tube which enables a cavity inflation-deflation method for identifying residual parts of the haematoma. After removal of major parts of the haematoma, the haematoma cavity collapses and residual haematoma may be hidden from the visual field. By the latter method described however, the cavity is inflated with saline and, thus, visualization is improved and bleeding vessels are easily identified. In a further series, the same group described a balanced irrigation-suction technique for endoscopic haematoma removal [27]. With the combined irrigationcoagulation-suction tube, irrigation and suction volumes are balanced through the hand-piece, thus keeping the visual field clear of fluid and blood. Nakano et al. [28] used an ultrasonic aspirator for haematoma removal after insertion of a sheath. Bakshi and colleagues reported the use of a three-in-one endoscope which combines a telescope, an irrigation cannula and a cautery electrode in one device [4]. Several groups have reported their experience with endoscopic techniques for the evacuation of intracerebral haematomas. Data regarding patient characteristics, surgical modalities, and short-term outcome are summarized in Table 1. Reported haematoma evacuation rates are impressive and in-hospital mortality and morbidity rates are considerably lower than the rates for ICH treatment through conventional surgical haematoma evacuation or conservative treatment reported in previous studies. Several limitations should however be kept in mind when interpreting the results of these reports. Most studies were retrospective and had very small patient numbers. Patients were highly selected and in some series, exclusion criteria included severe comorbidities and deep coma. Nevertheless, the results of these preliminary reports demonstrate that endoscopic surgery is a feasible method in haematoma evacuation. Technical developments have improved the intraoperative modalities with very low surgical complication rates. Prospective controlled clinical trials comparing this treatment modality with conventional haematoma evacuation through craniotomy and with conservative treatment are needed. Most importantly, effects on longterm mortality and functional outcome have to be analyzed, since these will define the role of endoscopic haematoma evacuation in ICH more than technical feasibility and effects on short-term outcome.

Prospective case series

9

Supratentorial

Supratentorial

CT scan assessment

68 Retrospective case series Supratentorial

Endoscopic port

Neuronavigation

18 Retrospective Case series

Supratentorial

Endoscopic sheath

CT scan assessment

28 Retrospective case series Supratentorial

a

Long-term outcome data available (see text)

81%

92%

NR

3.6%

0%

81%

Endoscopic sheath

0% 0%

99%

1.5%

NR

0%

0%

20%

Irrigation-suction tube 80–90%

Irrigation-suction

All: reduction (values NR) 93%

99%

99%

80%

0%

0%

23 Retrospective case series Supratentorial: 17 CT scan assessment Cerebellar: 6 4 Retrospective Supratentorial Neuronavigation case series 6 Retrospective case series Supratentorial Frameless stereotaxy

CT computed tomography, GCS Glasgow Coma Scale, NIHSS National Institutes of Health Stroke Scale

Nagasaka et al. [26] 2011 Orakcioglu et al. [34] 2011 Dye et al. [12] 2012 Zhu et al. [50] 2012 Ochalski et al. [32] 2013

Neuronavigation

Transparent sheath Irrigation-suction tube Transparent sheath Irrigation-suction Expandable cannula system Transparent sheath

CT scan assessment CT scan assessment

Transparent sheath

Neuronavigation

Prospective randomized Supratentorial controlled trial 14 Retrospective case series Supratentorial: 9 Cerebellar: 5 15 Retrospective case series Supratentorial: 11 Cerebellar: 4 6 Retrospective case series Supratentorial

6

Miller et al. [23] 2008 Nagasaka et al. [25] 2008 Nagasaka et al. [27] 2009 Waran et al. [45] 2009 Kuo et al. [17] 2011

Transparent sheath

95%

GOS 4-5 (3 months): 25%

All: improved GCS (discharge)

All: improved gcs (7 days)a

17.3%: good outcome (discharge)

Improvement mean GCS from 7.1 to 11 (7 days)

Nr

All: Improved GCS (7 days)

All: Improved GCS (postoperative)

30-d NIHSS: 18

Improved neurological grading (7 days)a

80%: good recovery / moderately disabled (discharge)

All: improved GCS (postoperative)

Nr

77%: improved GCS (3 days)

All: improved GCS (7 days)a

NR

Good recovery: 83 %

All: neurological improvement (7days)

Short-term outcome

At discharge: Survivors: GCS improved 33%

No surg. Mortality No surg. Mortality 7.1%

4.3%

No surg. Mortality 5.9%

0%

0%

20%

3.7%

95%

CT scan assessment

Transparent sheath

0%

3%

87%

CT scan assessment Transparent sheath Echoguided test punct. CT scan assessment Steel tube

0%

30.7%

0%

>80% reduction in 85% of patients 93% 0%

0%

0%

0%

0%

All 40 ml vol.

6

Nakano et al. [28] 2003 Bakshi et al. [4] 2004

Retrospective case series Supratentorial

ICH localization

Intra-op CT guided

9

Nishihara et al. [31] 2000

Study design

Retrospective case series Supratentorial

N

Modalities of case series and studies on endoscopic haematoma evacuation for treatment of ICH published within the last two decades

Author Year

Table 1

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Effects on long-term outcome Only limited data are available regarding the effects of endoscopic haematoma evacuation on the long-term outcome of ICH patients as the evidence from the last 20 years is based on case series with limited numbers of included patients. Chen et al. [7] analyzed seven patients in whom putaminal haemorrhage was endoscopically evacuated. Follow-up examination 6 months after surgery showed that six patients had a good outcome assessed by the Glasgow Outcome Scale (GOS), while one patient had remained in a vegetative state. The series reported by Nishihara et al. [29] showed a mortality rate of 3.7 % at 6 months and 44 % of cases had a poor outcome (GOS: 1–3). Moderate disability (GOS: 4) was seen in 22 % while 33 % of patients made a full recovery. Kuo and colleagues [17] analyzed 68 ICH patients treated with surgical endoscopic haematoma evacuation within 12 h of ictus. Follow-up examination 6 months after surgery revealed a mortality rate of 5.9 % and a mean GOS-extended score of 4.9 (range: 1–8). It has to be kept in mind that patients were highly selected and accounted for only 34 % of all ICH patients treated at the authors’ institution. Patients with coagulopathies, antiplatelet medication, liver cirrhosis, or an initial GCS score of less than 4 were not included in the study.

Fig. 1 Image sets are fused with a neuronavigation system for defining the optimum entrypoint and trajectory route (a). After trepanation with a burr hole trepan (b), a transparent sheath is inserted into the haematoma cavity and the haematoma is visualized through the endoscopic system (c, d). Intraoperative video sequences are available in the online version of this article

Furthermore, numbers of patients that were lost to follow-up are not reported. In light of these data, no conclusion can be drawn regarding the effects of endoscopic haematoma evacuation on long-term outcome of ICH patients. Reported data samples have been too small or have been significantly influenced by exclusion criteria. Treatment modalities at the authors’ institution Guidelines regarding the decision whether to surgically evacuate haematomas in patients with ICH are not available. Therefore, at our institution, every patient is discussed on an individual basis between treating neurosurgeons and neurologists. Many factors regarding the patient’s general condition, comorbidities, neurological status, signs of increased ICP, surgical risks as well as extent and localization of ICH are considered when tailoring a patient-specific decision. In general, all ICH patients with decreased vigilance and haematoma volumes of above 30 ml are subjected to this discussion. CT angiography is performed in every ICH patient treated at our institution since this examination procedure allows identification of underlying pathologies such as cerebral aneurysms and vascular malformations [46]. Furthermore, the presence of

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active contrast extravasation (‘spot sign’) is a significant predictor of haematoma expansion [10]. The dataset obtained through this examination is suitable for planning navigation modalities and for this purpose, image sets are fused with the neuronavigation system (BrainLab AG, Feldkirchen, Germany or Stryker Navigation System II, Stryker GmbH, Duisburg, Germany). The optimum entry point and trajectory are planned on the software system. The optimum trajectory is planned along the long axis of the haematoma through the shortest distance of viable brain while eloquent areas are avoided. The surgical procedure is performed with patients under general anaesthesia and in the supine position. In order to maximize the accuracy of the neuronavigation system, the patient’s head is fixed in a three-pin head holder (Mayfield® Triad Skull Clamp, Integra Neurosciences, Plainsboro, NJ, USA). At the trajectory entry site, a large burr hole is made. After incision and coagulation of the dura mater, a transparent sheath is inserted into the haematoma cavity under visual control. The endoscope is inserted through this sheath into the haematoma cavity. The haematoma is then evacuated through an intra-haematomal evacuation technique. By use of the balanced irrigation-suction technique as described by Nagasaka and colleagues [27], a sufficient visualization of the haematoma cavity is ensured. Within this device, a monopolar coagulation tip is incorporated which can be used for coagulation of bleeding vessels. Intraoperative orientation is enabled through the use of the neuronavigation system. Additionally, the tip of the endoscope can be incorporated into intraoperative neuronavigation images if the Stryker neuronavigation system is used (Fig. 1). As we have previously reported, our primary goal of haematoma evacuation is not the maximum removal of the haematoma [34]. Small haematoma remnants are not evacuated aggressively since this may offset the advantages of a minimally invasive approach by injuring viable surrounding brain tissue. After evacuation of the haematoma, the burr hole is covered with absorbable gelatin sponge and

Fig. 2 CT images of a patient with extensive basal ganglia ICH (a). After endoscopic haematoma evacuation, only residual haematoma remnants are identified on CT images (b)

the skin incision is closed with an absorbable intracutanous suture. If patients were comatose prior to surgery, an intraparenchymal ICP probe (Neurovent-P®, Raumedic, Muenchberg, Germany) is placed into the haematoma cavity before skin closure. For cosmetic reasons, we make the skin incision in the hair-bearing scalp whenever possible and for this purpose, a longer skin incision may be needed to allow skin flap mobilization for reaching the entrypoint. Pre- and postoperative CT images of a patient treated at our institution are displayed in Figs. 1 and 2. Future perspectives In our opinion, the aforementioned pathophysiologic justifications of minimally invasive endoscopic evacuation of ICH and the reported results of case series operated by several groups justify further investigation of this promising technique. Zan and colleagues have recently announced the initiation of the randomized controlled trial ‘Endoscopic surgery versus conservative treatment for the moderate-volume haematoma in spontaneous basal ganglia haemorrhage (ECMOH)’ [49]. Motivated by our own initial experiences, we are currently preparing a prospective controlled clinical trial on minimally invasive endoscopic haematoma evacuation in ICH and are recruiting further centres for study participation.

Conclusion Reported case series and results of preliminary studies suggest that minimally invasive endoscopic surgery for evacuation of spontaneous ICH may improve mortality and morbidity rates. Utilization of surgical adjuncts such as neuronavigation and also technical refinements of endoscopic instruments have further improved surgical outcomes. Randomized controlled

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clinical trials are needed to evaluate this promising treatment option for patients with ICH. Acknowledgments We thank Dr. T. Nagasaka (Nagoya University Graduate School of Medicine, Aichi, Japan) for introducing the endoscopic balanced irrigation-suction technique with a multifunctional suction cannula to the Department of Neurosurgery at Heidelberg University Hospital.

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Comments Waleed A. Azab, New York, USA The manuscript by Dr. Beynon and colleagues deals with a relatively underutilized modality of surgical evacuation of spontaneous ICH. With the recent technical innovations like endoscopic transparent sheaths and irrigation-suction devices, endoscopic ICH evacuation is becoming technically more feasible. In a patient subpopulation where a short operating time and a limited yet effective procedure are evidently beneficial, endoscopic ICH evacuation seems to hold a great promise. Michael Buchfelder, Erlangen, Germany In this review, the authors discuss the current possibilities and limitations of endoscopic minimally invasive endoscopic surgery for spontaneous intracerebral haematomas. Whether surgical evacuation of spontaneous intracerebral haematomas at all causes an improvement of patient outcome in terms of mortality and neurological outcome and if so, which patients will profit from such an operation is an ongoing matter of controversy. During the last 30 years, gradually minimally invasive techniques, utilizing endoscopes, have been developed for haematoma evacuation that largely avoids major brain manipulation and retraction. This started with individual case report and expanded to small series. There are several technical variations and implementation of additional technology such as neuronavigation, ultrasonic aspiration, guiding tubes and other gadgets, which are excellently described in this review. Their utility is discussed as is the usefulness of the operation as far as the clinical outcome is concerned. Even the most sceptical reader will appreciate knowledge the availability and experience hitherto gained with this novel technique. For the final evaluation of its value for clinical practice, it seems to me that further studies, which include numerous patients, are awaited. Yavor Enchev, Varna, Bulgaria Currently, the treatment of spontaneous intracerebral haematomas (ICH) is controversial with respect to indications, timing, surgical techniques, and applied instruments and devices. Neuroendoscopy and neuronavigation have been proved their potential, effectiveness, reliability and advantages in most of the neurosurgical pathologies. Reasonably, similar results could be expected in the treatment of ICH. The authors thoroughly reviewed the published experience in this field. They discuss the rationales of the minimal invasive endoscopic evacuation of ICH, the existed technical directions and nuances, including their own experience, and the achieved outcomes. This rigorous and systematic review outlines the future trends of the pertinent research and the need of controlled clinical trials.

Minimally invasive endoscopic surgery for treatment of spontaneous intracerebral haematomas.

Spontaneous intracerebral haemorrhage (ICH) is a devastating disease with a mortality rate of more than 40 % and a high morbidity rate with 10-15 % of...
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