Objectives: This study assesses the benefits of adapting minimal invasive techniques (MIT) to selected patients with spontaneous supratentorial intracerebral hematomas (SSICHs).
Methods: The study compares the post-operative residual clot volume and clinical outcome of 89 selected, MIT evacuated SSICH-patients to those of 138 unselected cases operated in our department. Selection criteria includes patient age, early admission and MIT treatment. MIT treatment included: 28 patients with deep SSICHs smaller than 30 cm^sup 3^ associated with intraventricular bleeding who underwent neuronavigation-guided stereotactic catheter lysis, 37 patients with deep hematomas larger than 30 cm^sup 3^ and 24 patients with a lobar hemorrhage compressing eloquent regions who underwent microsurgical (endoscopic or neuronavigation assisted) clot aspiration.
Results: In eight (9%) of the patients in the MIT group, the CT scan control showed a residual clot smaller than 30% of the initial hemorrhage. The neurological condition 3 months later revealed 24 (26.9%) of these patients having a severe disability and 46 (51.6%) patients independent or slightly disabled. Nineteen patients (21.9%) died or remained vegetative. In the control group, 48 (34.7%) cases showed residual clots (
Conclusions: Adapting minimally invasive techniques to case selection improves the effectiveness of clot removal and the outcome of the patients with SSICHs. [Neurol Res 2005; 27: 755-761]
Keywords: Minimal invasive techniques; spontaneous intracerebral hematomas
INTRODUCTION
All over the world, considerable differences in the treatment of supratentorial spontaneous intracerebral hematomas (SSICHs) make it difficult to establish which patients could benefit from early clot removal and which techniques should be employed1,2. In the past, the employment of traditional surgical techniques was usually associated with considerable operative trauma and residual hematoma3. In fact, different minimally invasive techniques (MIT) such as computer tomography (CT)-guided thrombolysis and aspiration4-8, endoscopic clot removal9-11 and neuronavigation guided microsurgical removal12 can be adapted to the required urgency and accuracy of the hematoma evacuation in order to improve results. On the other hand, it is well known that accompanying factors like age of the patient, Glasgow coma scale (GCS) score at admission, the volume, depth and site of the hematoma, have a negative influence on the patient's outcome13,14. Nevertheless, the medical literature remains irresolute about the value of some of these factors as pre-operative selection criteria for surgery. Taking into account that the recognized trials about the surgical management of intracerebral hematomas3,11,15-17' neither make an exhaustive analysis of the potential advantage of setting patients selection criteria nor of the role of modern minimally invasive techniques, we compared the real benefit of their combined employment on the postoperative residual clot volume and clinical outcome in a single center retrospective investigation.
MATERIAL AND METHODS
Among 227 patients with SSICHs, who were operated in our department between April 1996 and April 2004, 89 deteriorating patients (55 male, 34 female), aged 22-65 years with a Glasgow coma scale (CCS) 4-12, filled the selection and treatment criteria for this retrospective evaluation. The results were compared to those obtained in 138 unselected operated cases. Selection criteria included patient's age (less than 65 years old), early admission and MIT treatment (6-24 hours for microsurgical or stereotactic lysis, respectively) and neurological deterioration with exclusion of primary deep comatose patients.
Deterioration was defined as any kind of neurological deficit progression, with or without disturbance of consciousness, clearly related to the hematoma volume and location, developed between the initial bleeding and the course of the next hours. cases conservatively treated, initially deep comatose patients, arteriovenous malformations and aneurysms, terminal medical illness, coagulopathy accounting for the hemorrhage or traumatic ICH were all excluded from both groups in this report. The diagnosis of SSICH was made on acute onset of neurological symptoms and signs in the absence of trauma and confirmed by CT scan.
Hematoma volume was calculated with the ABC/2 formula in all patients18.
In the MIT group, 28 deteriorating patients with deep SSICHs smaller than 30cm^sup 3^ volume associated with intraventricular bleeding were treated early (first 24 hours after bleeding) with a neuronavigation guided stereotactic catheter for lysis, using multiplanar targets (1-3). Actilyse was administered daily (1 mg for each cm of the largest clot diameter) depending on the residual clot volume measured with CT scan. Alter injection the catheter was clamped 2 hours before it was connected to a cerebrospinal fluid (CSF) drainage system. Long axis hematoma evacuation or lysis (with periodical catheter withdrawal) was preferred in most of these patients.
Thirty-seven patients with deep located hematomas (DLH) larger than 30 cm^sup 3^ and 24 patients with a lobar hemorrhage (LH) compressing eloquent regions underwent microsurgical (endoscopic or neuronavigation assisted) clot aspiration.
A narrow surgical corridor (1.2-1.5 cm), created by the intermittent deepening of the brain retractor and suction, assured the least injury to vital cortical areas, tracts and blood vessels.
Post-operative residual hematomas were investigated with a CT-scan control 24-72 hours after hematoma evacuation. Outcome was measured 3 months after demission using a 3-level scale: level 1, dead or vegetative; level 2, dependent (severe disability); level 3, independent (slight disability). CT-scan and outcome evaluation for this study were blind performed.
Surgical approaches and hematoma evacuation technique
The goal of the MIT was the complete removal of the clot. An enlarged burr hole was placed based in the area providing the least brain and blood vessel injury, trying to reach a long axis hematoma evacuation.
Surgical planning was performed with the Viewing-wand navigator in the first 3 years and with the Vector Vision2 Brain Lab device the last 5 years. Two Hawk Vision(TM) (rigid and flexible) endoscopes, Cordis Biot, Sophia Antipolis French, with diameters of 0.94-2.8 mm were employed in several patients as complementary technique to microscopy.
Commercially available statistical software (SPSS for Windows, Version 11.5.1) was used to compare the examined data. Patient's related variables, as well as data associated with the ICH volume and percentage of residual clot were analysed with a Chi-square and Kendall-Taub f-test. Correlations with a p value below 0.05 were defined as significant.
RESULTS
The characteristic data of the patients in the MIT and control groups (age, sex, clinical status, hematoma location and volume, status of progressive neurological deterioration and presence of chronic hypertension) are shown in Table 1. The median time from bleeding to operation for patients undergoing MIT was 4.7 and 15.6 hours for microscopic and stereotactic-treated cases, respectively. In the control group, the median time was 7.9 hours (range 3-72 hours). No significant differences were found between the groups in terms of the pre-operative clinical condition with only a minor percentage of patients with less pre-operative impaired consciousness and hemiparesis in the MIT group (Figure 1).
Residual clots larger than 30% of the original hematoma volume were not observed.
In 81 of 89 cases (MIT group), the clots were adequately removed (no measurable rest). Eight patients showed in the CT-scan control a residual clot (less than 30% of the initial hemorrhage), without requiring surgical revision. There were no major post-operative complications related to early rebleeding in patients treated with neuronavigation guided stereotactic catheter for lysis. In these patients with clots under 30 cm^sup 3^ volumes, a long axis hematoma lysis and the placement of the intraventricular stereotactic catheter for lysis of packed clots were easily calculated with navigation using multiplanar approaches (Figure 2). Seven patients received two drains and four patients three.
The pre-operative hematoma volume was reduced to less than one-third after 24 hours as CT-scan controls demonstrated. Four days after surgery the level of consciousness had improved in 22 of the 28 patients. Cerebrospinal fluid passage was restored within 3 days and only five patients subsequently needed ventricular shunting. Only one residual clot was diagnosed. This was related to misplacement of the lysis catheter. Two cortical bleedings without mass effect and one intraventricular infection were observed in these patients.
In patients who underwent microsurgical (endoscopie or neuronavigation assisted) clot aspiration, we observed two rebleedings. Residual hematomas were mostly related to laterally performed surgical approaches (seven cases). Post-operative infections were not observed in DLH or LH patients treated with MIT. The most common physical findings in patients with lobar hemorrhage were hemiparesis (21 cases), hemisensory syndrome (15 cases), visual defects (eight cases) and aphasia (seven cases). In selected deteriorating patients with DLH or LH, the individual surgical planning helped to reduce the operatively induced secondary brain damage as well as to promptly improve the post-operative quality of life in many cases (Figure 3). Patients with LH and symptoms such as hemiparesis and aphasia recovered well (promptly after surgery in 12 and five patients, and after rehabilitation in an additional six and two patients, respectively) or had only a minimal disability allowing the patients a sell-sufficient life. In patients with DLHs and LHs who were found to be severely disabled at the 3 months evaluation outcome, 15 (75%) were still able Io move (wheelchair) or communicate by gesticulation.
The evaluation of the patient's neurological condition 3 months later in the MIT group revealed 24 (26.9%) of the patients having a severe disability and 46 (51.6%) patients being independent or slightly disabled. Nineteen patients (21.9%) died or remained vegetative.
In the control group (unselected cases traditionally operated), 48 (34.7%) patients showed residual clots (volume
DISCUSSION
Craniotomy has been the standard approach to remove SSICHs. This method may lead to further brain damage and does not really improve the effectiveness of the clot removal. Complications such as rebleeding or infection additionally increase with the size of the surgically exposed area. Today, the employment of MIT is demonstrated to be a safe, accurate and effective alternative for clot removal, particularly during acute stages19. However, the evacuation of mass occupying clots without patient selection, achieves functional independence in only a quarter of patients if they had stupor or coma, loss of pontomesencephalic brainstem reflexes or radiological signs of herniation20. Therefore, it is important to consider the individual level of urgency to decrease the local mass effect and the intracranial pressure, particularly in patients who still have a potential for clinical recovery.
Regarding treatment implementation, there is no doubt that conservative medical treatment should always be instituted first in all patients without a depressed level of consciousness, with minor focal neurological deficits and with a small hematoma volume on CT scan. However, in deteriorating patients, the location and volume of the hematoma must be carefully related to other factors, such as patient's age and clinical condition, in order to perform a prompt hematoma evacuation if required. Although, in our study, in both groups no significant differences were found between the pre-operative clinical condition and hematoma volumes, their post-operative condition confirmed a significant increased number of deadvegetative and dependent patients as well as a slightly reduced number of independent patients in the control group compared to selected MIT-operated cases. Today, it is well known that many untreated patient with large basal ganglia hematomas rapidly deteriorate due to the local clot mass effect and globally increased ICP21. A secondary clinical neurological deterioration (approximately 12 hours after the onset of supratentorial ICH) occurs in one-third of ICH patients and seems to be related to the hematoma volume22,23. Mechanical injury caused by elevated local tissue pressures, reduction of cerebral blood flow (CBF)24-26, infiltration of plasma27, inflammation related to clotting proteins28, protease induction29, blood-brain barrier disruption, and secondary hemorrhages from capillaries and venules30,351, have been demonstrated to be responsible for this kind of secondary injury. Histological damage occurs mainly in the adjacent perihemorrhage region32 and persists over at least 3 days after bleeding. Precise, acute and complete removal of the clot reduces mass effect24,33-35, lowers intracranial pressure (ICP)36 and improves perfusion in the affected hemisphere37. Unfortunately, surgical benefit tends to be limited or non-existent in older patients (>65 years of age), as well as in those with a very low Glasgow coma score and with additional comorbiditiy factors14,38-40.
Hematomas smaller than 30 cm^sup 3^ mean that the urgency and invaseiness of the procedure can be adapted to suit the patient's characteristics and the location of the hematoma. Hematomas with low mass effect, but with ventricular filling can be progressively evacuated within a few days using catheter lysis. Particularly older patients tolerate such procedures better than microsurgery. Kanaya and Kuroda41 reported a better functional outcome in patients undergoing stereotactic aspiration than in those with conventional evacuation, if the patient's pre-operative consciousness was normal or stuporous. Stereotactic procedures employing thrombolysis and aspiration combine the benefits of surgical clot removal, limited tissue damage, a shorter surgery and the use of local anesthesia4-8,42. An additional factor that plays a role in the improved outcome of these patients is the simultaneous use of multiple targets, resulting in additional early relief of intraventricular clots. Unfortunately, this technique is frequently employed in the sub-acute phase of the bleeding, after the secondary damage has already occurred. In this study, neuronavigation combined with stereotactic long axis ICH lysis and drainage of ventricular clots accelerated ICH evacuation, improved the patients' neurological condition and reduced the number of shunt implantations. On the other hand, it has to be remarked, that stereotactic catheter lysis takes longer to reduce clot-mass effect and, therefore, should be seldom considered in young deteriorating patients with large hematomas and little ventricular compromise.
Keyhole approaches are more appropriate in these young deteriorating patients with large DLHs or LHs compressing eloquent areas. Recently, Qiu et al.19 reported improved surgical results employing endoscopic-assisted keyhole operation. This technique was found to be safe and effective in their study. Keyhole approach patients with DLHs and sub-cortical LHs located in eloquent areas also gain a clear benefit from a precise clot location. Although neuronavigation, due to the increased intra-operative shift of the brain structure, prevents safe control of the deep areas, even experienced surgeons may profit from its employment. It helps to obtain an individual determination of the entry point on the cerebral cortex and to choose the appropriate surgical trajectory in clots of irregular configuration. In addition, it allows a three-dimensional reconstruction of the patient's important anatomical structures surrounding the hematoma. Taking into account that different reports43,44 describe the parietotemporal region as the brain area where lobar hemorrhages more commonly occur, the importance of avoiding additional functional damage does not need to be stressed. Many of these patients in our study, showed an impressively high percentage of function recovery within the first 24 hours after keyhole clot removal. On the other hand, particularly in this region, an improved pre-operative etiological diagnosis with the employment of thin radiological slices, helps to differentiate hematomas with initial different prognosis. It prevents surgeons from performing surgery in unsuitable candidates. As it is well known, patients with small hematomas in mass occupying arterial or venous cerebral infarctions and hematomas caused by vascular malformations do not benefit from a keyhole approach.
Keyhole approaches were not related to an increase in the rate of post-operative rebleeding in our study. Morgertern et al.45 reported that surgical hematoma evacuation within 4 hours of symptom onset was complicated in four of their 11 patients by rebleeding. Peresedov46 even reported the employment of a special balloon to be implanted into the hematoma cavity after evacuation to prevent recurrent bleeding. However, other authors46,47 have reported contradictory results regarding this. Although 68% of the hematomas in the MIT group in our study were microsurgically evacuated within the first 6 hours after bleeding, the rate of rebleeding employing minimally invasive techniques was only 3.2%. In this context, the critical need to identify the bleeding source, minimize the surgical damage and perform early hematoma removal, leads to significant differences in surgical results. Easy microsurgical aspiration is always possible during the early formation period of the clot, which avoids the employment of forceps and minimizes the surgical trauma and the rebleeding risk. Taking into account that SSICHs usually dissects along tissues planes and tracts, separating and compressing the nervous tissue, rather than destroying it, a well planned early surgical approach removes the clot completely without impairing the patient's deficits. Long axis clot removals are particularly facilitated by surgical planning. This not only helps to determine the entry point and the surgical trajectory, but to restrict the retraction-angle of the brain retractors to less than 20 . It increases the effectiveness of the clot suction without leaving a residual hematoma, prevents secondary brain injuries and follows the direction of the separated tracts12. Unfortunately, long axis approaches seem to be auto-limited by the length of the instruments employed, as well as by the accuracy of the surgical maneuvers performed at increased depth. Keyhole approaches performed where DLH have a subcortical expansion protruding the insular cortex laterally, have the advantage of a short transcerebral dissection47. However, an increased brain retraction is frequently required to expose the anterior and posterior hematoma edges due to the large anteroposterior expansion of such hematomas. It increases surgical trauma and requires an endoscopic-assisted control to avoid residual clots.
In conclusion, the accurate localization of the hemorrhage with neuronavigation, the combination of microscopic, stereotactic and endoscopie techniques applied to selected cases shows significant improvements in the effectiveness of clot removal and in the outcome of the patients with SSICHs.
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Mario Carvi y Nievas, Selim Toktamis*, Eberhard Haas and Hans-Georg Höllerhage
Department of Neurosurgery, Städtische Kliniken, Frankfurt am Main Höchst, and * Department of Neurosurgery, Städtische Kliniken, Krefeld, Germany
Correspondence and reprint requests to: Dr Med Mario Nazareno Carvi y Nievas, Oberarzt der Neurochirurgischen Klinik Städtische Kliniken, Frankfurt am Main, Höchst Akademisches Lehrkrankenhaus der J-W-Coethe-Universität FFM, 65929 Gotenstraße 6-8 [MCNievas@t-online.de Germany]. Accepted for publication February 2005.
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