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Stereotactic aspiration of intracerebral haematoma: significance of surgical timing and haematoma volume reduction
Journal of Clinical Neuroscience (2003) 10(4), 439–443 ª 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0967-5868(03)00061-4
Clinical study
Stereotactic aspiration of intracerebral haematoma: significance of surgical timing and haematoma volume reduction Jung-Il Lee MD, Do-Hyun Nam MD, Jong-Soo Kim Whan Eoh MD, Jong Hyun Kim MD
MD,
Seung-Chyul Hong
MD,
Hyung-Jin Shin
MD,
Kwan Park
MD,
Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
Summary We reviewed 63 patients with primary intracerebral haemorrhage (PICH) in basal ganglia treated by computed tomography (CT)guided stereotactic aspiration to evaluate the impact of surgical timing and degree of haematoma volume reduction on neurological outcome evaluated with Glasgow Outcome Score (GOS). In 19 patients operation was performed within 24 h from the symptom onset with more than 60% of haematoma volume reduction. At 3 weeks 11 patients (58%) achieved a favorable outcome (GOS 4 or 5). In the other 44 patients only 10 (23%) recovered to GOS 4 or 5. These differences were statistically significant. At 6 months a still larger proportion of patients with early radical decompression showed favorable outcome, however, the difference was not statistically significant. The results demonstrate that early and radical stereotactic aspiration provided a better neurological outcome at the early recovery phase, though the beneficial effect on the final outcome was not significant statistically. ª 2003 Elsevier Science Ltd. All rights reserved. Keywords: intracerebral haemorrhage, stereotactic aspiration, surgical treatment
INTRODUCTION The role of stereotactic surgery in the treatment of primary intracerebral haemorrhage (PICH) is still controversial. Several previous reports demonstrated no significant difference in outcomes between open surgery and medical therapy alone in PICH.1–4 Stereotactic surgery was in 1965, introduced as a less invasive alternative.5 Several reports suggested the beneficial role of stereotactic aspiration in PICH,6–8 however, they could not give a definite answer because they were not randomised trials for direct comparison between stereotactic surgery and medical therapy. Only a randomised trial of endoscopic surgery in 1989 demonstrated surgical benefit compared with medical treatment alone.9 Meanwhile, more results were published in which traditional computed tomography (CT)-guided stereotactic method was replaced or combined with various adjunctive techniques such as thrombolytic therapy with urokinase or recombinant tissue plasminogen activator10–12 or intraoperative magnetic resonance imaging (MRI).13 However, the benefit of surgery compared with medical therapy alone or the indication of surgical treatment have to be defined through a large scale randomised study. Despite unsolved questions, stereotactic surgery for PICH became a common practice in some countries and the authors have used stereotactic aspiration under the hypothesis that early effective removal of haematoma might be beneficial at least in some selected patient groups. A recent trial of early craniotomy or stereotactic surgery in a small number of patients suggested that early surgical intervention may lessen the 3 month morbidity in
Received 11 June 2002 Accepted 9 September 2002 Correspondence to: Jung-Il Lee, Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 IlwonDong, Kangnam-Gu, Seoul 135-710, Republic of Korea. Tel.: +82-2-3410-3494; Fax: +82-2-3410-0048; E-mail: [email protected]
patients with supratentorial intracerebral haemorrhage.14 Meanwhile ultra-early craniotomy within 4 h of symptom onset was complicated by rebleeding and potential increase of mortality.15 We report our experience with a consecutive 63 cases of PICH in basal ganglia treated by stereotactic aspiration. Though this is not a prospective randomised controlled trial, the purpose of this retrospective study is to identify the factors affecting the neurological outcome of the patients treated with stereotactic surgery and to provide information which may be helpful for surgical trials in the future. MATERIALS AND METHODS Between January 1995 and December 2000, 780 patients with PICH were diagnosed and treated at our institution. Among them 184 patients underwent surgical intervention including craniotomy, stereotactic aspiration and extraventricular drainage. Stereotactic surgery was performed only in the patients with PICH of thalamus or basal ganglia. In this study we retrospectively analyzed only the data of 63 patients with basal ganglia PICH who were treated by stereotactic aspiration and thrombolysis. Stereotactic surgery was recommended for the patients with PICH in basal ganglia without brain stem involvement, Glasgow Coma Scale (GCS) score P5, haematoma volume P25 ml with neurological signs and symptoms, no hemorrhagic diathesis or serious uncontrollable medical illness, and without underlying diseases such as vascular malformation or brain tumour. Data from stereotactic surgery for the thalamic haemorrhage were not included for the analysis in this paper. There were no patients with large volume intraventricular haemorrhage. The decision to operate was made immediately after the first investigation by a neurosurgeon and all the patients fulfilling the above criteria were operated on except those patients who refused operation. Under the hypothesis that early surgery would give a better outcome, the operative procedure was performed as soon as possible. However, delayed transportation from the regional hospitals or the availability of a neurosurgeon and an operating suite in our institution resulted in 439
440 Lee et al.
the variable time interval from the symptom onset to the operation. There were no patients in whom decision of operation was made following deterioration during the observation period.
OPERATIVE TECHNIQUE Operations were performed under local anaesthesia or under general anaesthesia when endotracheal intubation was necessary due to impaired consciousness. Localisation of haematoma and a catheter placement were performed with Cosman-Roberts-Wells (Radionics, Burlington, MA) stereotactic frame under CT-guidance. Stereotactic head frame was applied to the patients under local anaesthesia and axial CT scan was obtained with 5-mm slice thickness. X, Y, and Z coordinates of target point relative to the stereotactic frame were acquired and approached through an ipsilateral frontal burr hole located 3 cm lateral from the midline and just anterior to the coronal suture. The target point for the catheter insertion was a point at the junction of the anterior two-third and the posterior one-third of anteroposterior diameter of haematoma expecting that it would maximize haematoma aspiration at supine position. Initially a rigid metal cannula of 2.5 mm diameter was inserted and the haematoma was aspirated using a syringe applying negative pressure manually. The rigid cannula was removed and replaced with a soft ventricular catheter of 2 mm inner diameter. The catheter was connected to a closed drainage system. CT scan was performed again immediately after aspiration. Thrombolytic therapy with urokinase instillation was done in case of remaining haematoma volume more than 20 ml measured with immediate postoperative CT scan. Five thousands IU of urokinase in 1 ml of sterile saline was injected into the catheter and the catheter was clamped for 1 h, and then opened and drained naturally. The procedure was repeated every 6 h for 1–3 days. Table 1
PRE- AND POST-OPERATIVE EVALUATION All patients were treated in a neurosurgical intensive care unit until the thrombolytic therapy was finished and neurologic status became stable. Bedside physiotherapy and rehabilitation therapy were started as soon as possible, usually within 2 weeks after the operation. GCS score was evaluated before and 12 h after operation. Neurological outcome of surgery was evaluated at 3 weeks and 6 months after the operation using Glasgow Outcome Scale (GOS) score.16 Volume of haematoma was calculated from the baseline CT scan, CT scan with the stereotactic frame before aspiration, and CT scan obtained immediately after aspiration using A B C=2 formula.17 A represents the largest diameter of the haematoma on axial CT image, B the diameter of haematoma perpendicular to A on the same slice, and C the vertical dimension of haematoma converted from the number of slices showing haematoma and slice thickness. The patients were grouped by surgical timing and the degree of haematoma volume reduction by surgery. The patients who underwent surgery within 24 h from symptom onset were included in the early surgery group and the others in the late surgery group. Also, the patients were divided into 2 groups with more than 60% and 60% or less reduction of haematoma volume by aspiration. The cut-off point of 60% was chosen simply for the convenience of statistical management.The data were analyzed by the v2 test, Student’s t test, and Mann– Whitney U test for the comparison of results from patients group. RESULTS The age of the 63 patients ranged 37–78 years (mean 55 years) and all of them had haemorrhage in the basal ganglia. Mean haematoma volume before aspiration was 46 ml (ranging from 25 to 95 ml). Ten patients (16%) showed 5–40% increase of haematoma volume between the initial diagnostic CT scan and CT
Characteristics of early and late surgery group Early surgery
Time to operation from symptom onset (hours) Nunber of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS (range) Reduction of haematoma volume after aspiration (%, mean SD)
O24 37 29:8 54:5 9:3 19:18 45 20 11 (6–15) 53 29
Late surgery >24 26 15:11 55:2 10:8 20:6 48 24 12 (8–15) 60 26
p Value
NSa NSb <0.05a NSb NSc NSb
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 2
Neurological outcome in early and late surgery group (number of patients)
Neurological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
3 weeks
6 months
Early surgery
Late surgery
Early surgery
Late surgery
0 3 18 11 5 16 (43%)
0 4 17 4 1 5 (19%) p < 0:05a
0 1 10 17 9 26 (70%)
0 1 10 12 3 15 (58%) NSa
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
Journal of Clinical Neuroscience (2003) 10(4), 439–443
ª 2003 Elsevier Science Ltd. All rights reserved.
Stereotactic aspiration of intracerebral haematoma
Table 3
441
Characteristics of patients group according to the degree of haematoma volume reduction by surgery Radical decompression
Reduction of haematoma volume after aspiration No. of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS (range) Time to operation from symptom onset (hours, mean SD)
Moderate decompression
p Value
O60% 33 21:12 56 9:7 22:11 47 19 12 (6–15) 34 33
>60% 30 23:7 54 10 17:13 46 25 11.5 (7–15) 36 42
NSa NSb NSa NSb NSc NSb
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 4
Neurological outcome of patients group according to degree of haematoma volume reduction by surgery (number of patients)
Neurological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
Three weeks
Six months
>60%
O60%
>60%
O60%
0 3 13 8 6 14 (44%) p < 0:05a
0 4 22 7 0 7 (21%)
0 0 11 10 9 19 (63%) NSa
0 2 9 19 3 22 (67%)
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
scan with stereotactic frame. Mean time to sterotactic aspiration from symptom onset was 35 h (ranging from 4 to 120 h). Mean reduction of haematoma volume measured from the CT scan obtained immediately after aspiration was 56% (ranging from 0 to 99%). Thrombolytic therapy was performed in 16 patients (25%). It continued from 24 to 72 h (mean 14 h). Median GCS score was 12 (range 6–15) before the operation and 13 (range 7–15) at 12 h after the operation. At 3 weeks after the operation 7 patients remained vegetative (GOS 2), 35 were dependent (GOS 3), 15 were independent but moderately disabled (GOS 4), and 6 achieved a good recovery (GOS 5). At 6 months the numbers of patients in each category were 2 (GOS 2), 20 (GOS 3), 29 (GOS 4), and 12 (GOS 5). There was no mortality until 6 months after the operation. Table 1 summarises the characteristics and neurological outcome of the patient groups classified by surgical timing. Thirty seven patients underwent operation within 24 h from the symptom onset. Compared with the other 26 patients who were operated on later than 24 h there was no statistically significant difference except laterality of haematoma. Left-sided haematoma was more frequent in the early surgery group. At 3 weeks 11 (30%) and 5 (14%) of 37 patients with early surgery were GOS 4 and 5 each, respectively (Table 2). Meanwhile only 4 (15%) and 1 (4%) of 26 patients with late surgery were GOS 4 and 5 each, respectively. The difference was statistically significant (p < 0:05). At 6 months still larger proportion of patients with early surgery recovered to GOS 4 and 5. However, it was not statistically significant. Tables 3 and 4 summarise the characteristics and neurological outcome of the patient groups classified by degree of immediate haematoma volume reduction by stereotactic aspiration. More than 60% of haematoma was aspirated in 30 patients and 60% or ª 2003 Elsevier Science Ltd. All rights reserved.
less in the other 33 patients. Clinical characteristics were not significantly different between the 2 groups. At 3 weeks 8 (26%) and 6 (20%) of 30 patients with radical decompression were GOS 4 and 5 each, respectively (Table 4). Seven (21%) of 33 patients with moderate decompression belonged to GOS 4 and no patient recovered to GOS 5. The difference was statistically significant (p < 0:05). At 6 months more patients with radical decompression recovered to GOS 5 (9/30, 33% vs. 3/33, 9%). However, it did not reach the statistical significance. Tables 5 and 6 show the comparison between early radical decompression and late moderate decompression. In 19 patients the operations were performed within 24 h from symptom onset and more than 60% of haematoma was removed. In these patients neurological outcome was significantly better at 3 weeks compared with that of the other 44 patients with late surgery or 60% or less reduction of haematoma volume (p < 0:05). At 6 months the same tendency persisted, but it was not statistically significant. Haematoma volume increased in 4 patients after aspiration. All of them underwent stereotactic aspiration within 12 h from the symptom onset. Three of them subsequently underwent open craniotomy for evacuation of haematoma. There was no case of increasing haematoma or infection related with thrombolytic therapy. DISCUSSION The controversies about surgical treatment of PICH can be resolved only by a prospective randomised controlled trial such as the Surgical Trial in Intracerebral Haemorrhage (STICH) which is still ongoing.18 Though the aim of our analysis is not very different from STICH and our experience described here suggests a beneficial role for stereotactic surgery, the limitation is that this is Journal of Clinical Neuroscience (2003) 10(4), 439–443
442 Lee et al.
Table 5
Characteristics of patients group with early radical (O24 h and >60%) and late moderate (>24 h or O60%) decompression Early radical
No. of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS
19 14:5 53 7 9:10 41 19 11 (8–15)
Late moderate
p Value
44 30:14 55 11 30:14 49 23 12 (6–15)
NSa NSb NSa NSb NSc
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 6 Neurological outcome of the patients group with early radical (O24 h and >60%) and late moderate (>24 h or O60%) decompression (number of patients) Neuological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
Three weeks Early radical 0 1 7 6 5 11 (58%) p < 0:05a
Six months Late moderate 0 6 28 9 1 10 (23%)
Early radical
Late moderate
0 0 5 7 7 14 (74%) NSa
0 2 15 22 5 27 (61%)
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
not a randomised study and it is essential to be confirmed through a randomised trial before generalization. In this study the authors tried to focus on the factors which could be changed by surgical manipulations and might influence the results of surgery. There are well known prognostic factors of PICH such as volume of haematoma, neurological condition, age of the patients, and the presence of other systemic illness.19–22 In addition to these preoperatively determined factors our results showed that early and radical stereotactic aspiration is related to the better functional outcome at the earlier phase. The advantage of evacuation of PICH or importance of surgical timing were suggested by animal studies23;24 and clinical reports.25–27 Our results partially support them. More patients recovered to an independent state (GOS 4 or 5) when the early radical decompression was performed. However, the differences in neurological outcome were statistically significant only at 3 weeks after the operation though the same tendency was shown at 6 months. Shortening of the early recovery phase has the advantage of reducing the cost and effort necessary for the care of the patients. The patients can begin the rehabiliation program earlier and it may be another beneficial factor for long-term recovery. If the final outcome is not significantly improved by surgical treatment, however, indication for surgery should be more strictly defined. Because the number of the patients included in this study is not sufficient, long-term benefit of the early radical surgery needs to be evaluated with a larger number of patients. The authors mainly focused on the aspiration procedure among the whole treatment schedule and thrombolytic therapy is not systemically evaluated in this study. It might be a beneficial adjunctive of aspiration procedure, though the importance would be insignificant if the initial maneuver to reduce the volume of haematoma is sufficient. Concerning the early and radical intervention of PICH, the acute complications associated with the surgical procedure should Journal of Clinical Neuroscience (2003) 10(4), 439–443
be considered. It is well known that PICH expands not infrequently in the first 24 h.28;29 Our data revealed similar phenomenon because 10 patients (16%) showed expansion of haematoma during the period between initial baseline CT scan and CT scan with stereotactic frame just before the operation. Eight of the 10 patients underwent the initial CT scan within 2 h from the symptom onset and it seems that expansion of haematoma is more likely to be a naturally ongoing haematoma formation rather than provoked by the procedure of applying the stereotactic frame to the head of patients. The major concern is the possibility that the actual decompressive procedure would provoke rebleeding if it is performed during the unstable period. In our cases, there was no mortality caused by surgery. It seems to be extraordinary because case fatality rates for intracerebral haemorrhage is known to approach 50%. There are several reasons that we observed no mortality. All the patients included in this study had haemorrhage circumscribed in basal ganglia. A recent study described the subtypes of striatocapsular haemorrhage and their clinical outcome.30 Only the massive type of striatocapsular haemorrhage with mean diameter of 65 mm resulted in fatality rate of 49% regardless of the treatment modality. The fatality rates in the other subtypes of striatocapsular haemorrhage was not high, including the lateral type which is usually elliptical in shape with a mean long diameter of 53 mm and resulted in 7% of fatality. The mean haematoma volume of the cases analyzed in this study was 46 ml with less than 60 mm in long dimeter and most of them belonged to the lateral type of striatocapsular haemorrhage. Also, the patients with very low GCS score or other risk factors such as serious medical illness were not recommended for operation. Therefore no mortality in our series reflects a largely natural course of the disease. Though stereotactic surgery did not increase the risk of death in our series, the risk of rebleeding or expansion of haematoma during or after the surgery seems to be a significant problem. In 4 patients with increased ª 2003 Elsevier Science Ltd. All rights reserved.
Stereotactic aspiration of intracerebral haematoma
haematoma after the operation the procedure was performed between 6 and 12 h from the symptom onset. These findings suggest that aggressive decompression during the acute phase might be associated with the higher risk of rebleeding which has been suggested by other authors.15 In summary, it is suggested that the earlier and more radical decompression results in a better recovery in the early phase. Though the beneficial effect of aggressive approach on final outcome was not significant it needs to be further evaluated with a larger number of patients. Early and radical surgery with traditional CT-guided stereotactic method can be accompanied by the increased risk of rebleeding and other innovative techniques such as endoscopic evacuation or intraoperative MRI may be a useful methods in the future. Finally all the issues need to be clarified through a prospective randomised controlled trial.
REFERENCES 1. Batjer HH, Reisch JS, Allen BC, Plaizier LJ, Su CJ. Failure of surgery to improve outcome in hypertensive putaminal hemorrhage: a prospective randomized trial. Arch Neurol 1990; 47: 1103–1106. 2. Juvela S, Heiskanen O, Poranen A, Vltonen S, Kuurne T, Kaste M, Troupp H. The treatment of spontaneous intracerebral hemorrhage: a prospective randomized trial of surgical and conservative treatment. J Neurosurg 1989; 70: 755–758. 3. McKissock W, Richardson A, Taylor J. Primary intracerebral haemorrhage: a controlled trial of surgical and conservative treatment in 180 selected cases. Lancet 1961; 2: 221–226. 4. Morgenstern LB, Frankowski RF, Shedden P, Pasteur W, Grotta JC. Surgical treatment for intracerebral hemorrhage (STICH): a single-center, randomized clinical trial. Neurology 1998; 51: 1359–1363. 5. Benes V, Vladyka V, Zverina E. Stereotaxic evacuation of typical brain hemorrhage. Acta Neurochir 1965; 13: 419–426. 6. Matsumoto K, Hondo H. CT-guided stereotoxic evacuation of hypertensive intracerebral hematomas. J Neurosurg 1984; 61: 440–448. 7. Nizuma H, Shimizu Y, Yonemitsu T, Nakassato N, Suzuki J. Results of stereotactic aspiration in 175 cases of putaminal hemorrhage. Neurosurgery 1989; 24: 814–819. 8. Hondo H, Uno M, Sasaki K, Ebisudani D, Shichijo F, Toth Z, Matsumoto K. Computed tomography controlled aspiration surgery for hypertensive intracerebral hemorrhage: experience of more than 400 cases. Stereotact Funct Neurosurg 1990; 55: 432–437. 9. Auer LM, Deinsberger W, Niederkorn K, Gell G, Kleinert R, Schneider G, Holzer P, Bone G, Mokry M, Korner E, Kleinert G, Hanusch S. Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: a randomized study. J Neurosurg 1989; 70: 530–535. 10. Niizuma H, Otsuki T, Johkura H, Nakazato N, Suzuki J. CT-guided sterotactic aspiration of intracerebral hematoma: result of a hematoma-lysis method using urokinase. Appl Neurophysiol 1985; 48: 427–430. 11. Lippitz BE, Mayfrank L, Spetzger U, Warnke JP, Bertalanffy H, Gilsbach JM. Lysis of basal ganglia haematoma with recombinant tissue plasminogen activator (rtPA) after stereotactic aspiration: initial results. Acta Neurochir 1994; 127: 159–160.
ª 2003 Elsevier Science Ltd. All rights reserved.
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12. Shaller C, Rohde V, Meyer B, Hassler W. Stereotactic puncture and lysis of spontaneous intracerebral hemorrhage using recombinant tissue-plasminogen activator. Neurosurgery 1995; 36: 328–333. 13. Bernays RL, Kollias SS, Romanowski B, Valavanis A, Yonekawa Y. Near-realtime guidance using intraoperative magnetic resonance imaging for radical evacuation of hypertensive haematomas in the basal ganglia. Neurosurgery 2000; 47: 1081–1090. 14. Zuccarello M, Brott T, Derex L, Kothari R, Sauerbeck L, Tew J, Loveren HV, Yeh HS, Tomsick T, Pancioli A, Khoury J, Broderick J. Early surgical treatment for supratentorial intracerebral hemorrhage. A randomized feasibility study. Stroke 1999; 30: 1833–1839. 15. Morgenstern LB, Demchuk AM, Kim DH, Frankowski RF, Grotta JC. Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage. Neurology 2001; 56: 1294–1299. 16. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975; 1: 480–484. 17. Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J. The ABCs of measuring intracerebral hematoma volumes. Stroke 1996; 27: 1304–1305. 18. Major ongoing stroke trials. Stroke 2001;32:1449–1457. 19. Tuhrim S, Dambrosia JM, Price TR, Mohr JP, Wolf PH, Heyman A, Kase CS. Prediction of intracerebral haemorrhage survival. Ann Neurol 1988; 24: 258– 263. 20. Dixon AA, Holness RO, Howes WJ, Garner JB. Spontaneous intracerebral haemorrhage: an analysis of factors affecting prognosis. Can J Neurol Sci 1985; 12: 267–271. 21. Daveral P, Castel JP, Dartigues JF, Orgogozo JM. Death and functional outcome after spontaneous intracerebral haemorrhage. A prospective study of 166 cases using multivariate analysis. Stroke 1991; 22: 1–6. 22. Franke CL, van Swieten JC, Algra A, van Gijin J. Prognostic factors in patients with intracerebral haematoma. J Neurol Neurosurg Psychiatry 1992; 55: 653– 657. 23. Altumbabic M, Peeling J, Del Bigio MR. Intracerebral hemorrhage in the rat: effects of hematoma aspiration. Stroke 1998; 29: 1917–1922. 24. Wagner KR, Xi G, Hua Y, Zuccarello M, de Courten-Myers GM, Broderick JP, Brott T. Ultra-early clot aspiration after lysis with tissue plasminogen activator in a porcine model of intracerebral hemorrhage: edema reduction and blood–brain barrier protection. J Neurosurg 1999; 90: 491–498. 25. Kaneko M, Tanaka K, Shimada T, Sato K, Uemura K. Long-term evaluation of ultra-early operation for hypertensive intracerebral hemorrhage in 100 cases. J Neurosurg 1983; 58: 838–842. 26. Kanno T, Sano H, Shinomiya Y, Katada K, Nagata J, Hoshino M, Mitsuyama F. Role of surgery in hypertensive intracerebral hematoma. A comparative study of 305 nonsurgical and 154 surgical cases. J Neurosurg 1984; 61: 1091– 1099. 27. Waga S, Miyazaki M, Okada M, Tochio H, Matsushima S, Tanaka Y. Hypertensive putaminal hemorrhage: analysis of 182 patients. Surg Neurol 1986; 26: 159–166. 28. Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Cauerbeck L, Spilker J, Duldner J, Khoury J. Early growth in patients with intracerebral hemorrhage. Stoke 1997; 28: 1–5. 29. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage: incidence and time course. Stroke 1986; 27: 1783–1787. 30. Chung CS, Caplan LR, Yamamoto Y, Chang HM, Lee SJ, Song HJ, Lee HS, Shin HK, Yoo KM. Striatocapsular haemorrhage. Brain 2000; 123: 1850–1862.
Journal of Clinical Neuroscience (2003) 10(4), 439–443
Clinical study
Stereotactic aspiration of intracerebral haematoma: significance of surgical timing and haematoma volume reduction Jung-Il Lee MD, Do-Hyun Nam MD, Jong-Soo Kim Whan Eoh MD, Jong Hyun Kim MD
MD,
Seung-Chyul Hong
MD,
Hyung-Jin Shin
MD,
Kwan Park
MD,
Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
Summary We reviewed 63 patients with primary intracerebral haemorrhage (PICH) in basal ganglia treated by computed tomography (CT)guided stereotactic aspiration to evaluate the impact of surgical timing and degree of haematoma volume reduction on neurological outcome evaluated with Glasgow Outcome Score (GOS). In 19 patients operation was performed within 24 h from the symptom onset with more than 60% of haematoma volume reduction. At 3 weeks 11 patients (58%) achieved a favorable outcome (GOS 4 or 5). In the other 44 patients only 10 (23%) recovered to GOS 4 or 5. These differences were statistically significant. At 6 months a still larger proportion of patients with early radical decompression showed favorable outcome, however, the difference was not statistically significant. The results demonstrate that early and radical stereotactic aspiration provided a better neurological outcome at the early recovery phase, though the beneficial effect on the final outcome was not significant statistically. ª 2003 Elsevier Science Ltd. All rights reserved. Keywords: intracerebral haemorrhage, stereotactic aspiration, surgical treatment
INTRODUCTION The role of stereotactic surgery in the treatment of primary intracerebral haemorrhage (PICH) is still controversial. Several previous reports demonstrated no significant difference in outcomes between open surgery and medical therapy alone in PICH.1–4 Stereotactic surgery was in 1965, introduced as a less invasive alternative.5 Several reports suggested the beneficial role of stereotactic aspiration in PICH,6–8 however, they could not give a definite answer because they were not randomised trials for direct comparison between stereotactic surgery and medical therapy. Only a randomised trial of endoscopic surgery in 1989 demonstrated surgical benefit compared with medical treatment alone.9 Meanwhile, more results were published in which traditional computed tomography (CT)-guided stereotactic method was replaced or combined with various adjunctive techniques such as thrombolytic therapy with urokinase or recombinant tissue plasminogen activator10–12 or intraoperative magnetic resonance imaging (MRI).13 However, the benefit of surgery compared with medical therapy alone or the indication of surgical treatment have to be defined through a large scale randomised study. Despite unsolved questions, stereotactic surgery for PICH became a common practice in some countries and the authors have used stereotactic aspiration under the hypothesis that early effective removal of haematoma might be beneficial at least in some selected patient groups. A recent trial of early craniotomy or stereotactic surgery in a small number of patients suggested that early surgical intervention may lessen the 3 month morbidity in
Received 11 June 2002 Accepted 9 September 2002 Correspondence to: Jung-Il Lee, Department of Neurosurgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 IlwonDong, Kangnam-Gu, Seoul 135-710, Republic of Korea. Tel.: +82-2-3410-3494; Fax: +82-2-3410-0048; E-mail: [email protected]
patients with supratentorial intracerebral haemorrhage.14 Meanwhile ultra-early craniotomy within 4 h of symptom onset was complicated by rebleeding and potential increase of mortality.15 We report our experience with a consecutive 63 cases of PICH in basal ganglia treated by stereotactic aspiration. Though this is not a prospective randomised controlled trial, the purpose of this retrospective study is to identify the factors affecting the neurological outcome of the patients treated with stereotactic surgery and to provide information which may be helpful for surgical trials in the future. MATERIALS AND METHODS Between January 1995 and December 2000, 780 patients with PICH were diagnosed and treated at our institution. Among them 184 patients underwent surgical intervention including craniotomy, stereotactic aspiration and extraventricular drainage. Stereotactic surgery was performed only in the patients with PICH of thalamus or basal ganglia. In this study we retrospectively analyzed only the data of 63 patients with basal ganglia PICH who were treated by stereotactic aspiration and thrombolysis. Stereotactic surgery was recommended for the patients with PICH in basal ganglia without brain stem involvement, Glasgow Coma Scale (GCS) score P5, haematoma volume P25 ml with neurological signs and symptoms, no hemorrhagic diathesis or serious uncontrollable medical illness, and without underlying diseases such as vascular malformation or brain tumour. Data from stereotactic surgery for the thalamic haemorrhage were not included for the analysis in this paper. There were no patients with large volume intraventricular haemorrhage. The decision to operate was made immediately after the first investigation by a neurosurgeon and all the patients fulfilling the above criteria were operated on except those patients who refused operation. Under the hypothesis that early surgery would give a better outcome, the operative procedure was performed as soon as possible. However, delayed transportation from the regional hospitals or the availability of a neurosurgeon and an operating suite in our institution resulted in 439
440 Lee et al.
the variable time interval from the symptom onset to the operation. There were no patients in whom decision of operation was made following deterioration during the observation period.
OPERATIVE TECHNIQUE Operations were performed under local anaesthesia or under general anaesthesia when endotracheal intubation was necessary due to impaired consciousness. Localisation of haematoma and a catheter placement were performed with Cosman-Roberts-Wells (Radionics, Burlington, MA) stereotactic frame under CT-guidance. Stereotactic head frame was applied to the patients under local anaesthesia and axial CT scan was obtained with 5-mm slice thickness. X, Y, and Z coordinates of target point relative to the stereotactic frame were acquired and approached through an ipsilateral frontal burr hole located 3 cm lateral from the midline and just anterior to the coronal suture. The target point for the catheter insertion was a point at the junction of the anterior two-third and the posterior one-third of anteroposterior diameter of haematoma expecting that it would maximize haematoma aspiration at supine position. Initially a rigid metal cannula of 2.5 mm diameter was inserted and the haematoma was aspirated using a syringe applying negative pressure manually. The rigid cannula was removed and replaced with a soft ventricular catheter of 2 mm inner diameter. The catheter was connected to a closed drainage system. CT scan was performed again immediately after aspiration. Thrombolytic therapy with urokinase instillation was done in case of remaining haematoma volume more than 20 ml measured with immediate postoperative CT scan. Five thousands IU of urokinase in 1 ml of sterile saline was injected into the catheter and the catheter was clamped for 1 h, and then opened and drained naturally. The procedure was repeated every 6 h for 1–3 days. Table 1
PRE- AND POST-OPERATIVE EVALUATION All patients were treated in a neurosurgical intensive care unit until the thrombolytic therapy was finished and neurologic status became stable. Bedside physiotherapy and rehabilitation therapy were started as soon as possible, usually within 2 weeks after the operation. GCS score was evaluated before and 12 h after operation. Neurological outcome of surgery was evaluated at 3 weeks and 6 months after the operation using Glasgow Outcome Scale (GOS) score.16 Volume of haematoma was calculated from the baseline CT scan, CT scan with the stereotactic frame before aspiration, and CT scan obtained immediately after aspiration using A B C=2 formula.17 A represents the largest diameter of the haematoma on axial CT image, B the diameter of haematoma perpendicular to A on the same slice, and C the vertical dimension of haematoma converted from the number of slices showing haematoma and slice thickness. The patients were grouped by surgical timing and the degree of haematoma volume reduction by surgery. The patients who underwent surgery within 24 h from symptom onset were included in the early surgery group and the others in the late surgery group. Also, the patients were divided into 2 groups with more than 60% and 60% or less reduction of haematoma volume by aspiration. The cut-off point of 60% was chosen simply for the convenience of statistical management.The data were analyzed by the v2 test, Student’s t test, and Mann– Whitney U test for the comparison of results from patients group. RESULTS The age of the 63 patients ranged 37–78 years (mean 55 years) and all of them had haemorrhage in the basal ganglia. Mean haematoma volume before aspiration was 46 ml (ranging from 25 to 95 ml). Ten patients (16%) showed 5–40% increase of haematoma volume between the initial diagnostic CT scan and CT
Characteristics of early and late surgery group Early surgery
Time to operation from symptom onset (hours) Nunber of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS (range) Reduction of haematoma volume after aspiration (%, mean SD)
O24 37 29:8 54:5 9:3 19:18 45 20 11 (6–15) 53 29
Late surgery >24 26 15:11 55:2 10:8 20:6 48 24 12 (8–15) 60 26
p Value
NSa NSb <0.05a NSb NSc NSb
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 2
Neurological outcome in early and late surgery group (number of patients)
Neurological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
3 weeks
6 months
Early surgery
Late surgery
Early surgery
Late surgery
0 3 18 11 5 16 (43%)
0 4 17 4 1 5 (19%) p < 0:05a
0 1 10 17 9 26 (70%)
0 1 10 12 3 15 (58%) NSa
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
Journal of Clinical Neuroscience (2003) 10(4), 439–443
ª 2003 Elsevier Science Ltd. All rights reserved.
Stereotactic aspiration of intracerebral haematoma
Table 3
441
Characteristics of patients group according to the degree of haematoma volume reduction by surgery Radical decompression
Reduction of haematoma volume after aspiration No. of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS (range) Time to operation from symptom onset (hours, mean SD)
Moderate decompression
p Value
O60% 33 21:12 56 9:7 22:11 47 19 12 (6–15) 34 33
>60% 30 23:7 54 10 17:13 46 25 11.5 (7–15) 36 42
NSa NSb NSa NSb NSc NSb
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 4
Neurological outcome of patients group according to degree of haematoma volume reduction by surgery (number of patients)
Neurological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
Three weeks
Six months
>60%
O60%
>60%
O60%
0 3 13 8 6 14 (44%) p < 0:05a
0 4 22 7 0 7 (21%)
0 0 11 10 9 19 (63%) NSa
0 2 9 19 3 22 (67%)
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
scan with stereotactic frame. Mean time to sterotactic aspiration from symptom onset was 35 h (ranging from 4 to 120 h). Mean reduction of haematoma volume measured from the CT scan obtained immediately after aspiration was 56% (ranging from 0 to 99%). Thrombolytic therapy was performed in 16 patients (25%). It continued from 24 to 72 h (mean 14 h). Median GCS score was 12 (range 6–15) before the operation and 13 (range 7–15) at 12 h after the operation. At 3 weeks after the operation 7 patients remained vegetative (GOS 2), 35 were dependent (GOS 3), 15 were independent but moderately disabled (GOS 4), and 6 achieved a good recovery (GOS 5). At 6 months the numbers of patients in each category were 2 (GOS 2), 20 (GOS 3), 29 (GOS 4), and 12 (GOS 5). There was no mortality until 6 months after the operation. Table 1 summarises the characteristics and neurological outcome of the patient groups classified by surgical timing. Thirty seven patients underwent operation within 24 h from the symptom onset. Compared with the other 26 patients who were operated on later than 24 h there was no statistically significant difference except laterality of haematoma. Left-sided haematoma was more frequent in the early surgery group. At 3 weeks 11 (30%) and 5 (14%) of 37 patients with early surgery were GOS 4 and 5 each, respectively (Table 2). Meanwhile only 4 (15%) and 1 (4%) of 26 patients with late surgery were GOS 4 and 5 each, respectively. The difference was statistically significant (p < 0:05). At 6 months still larger proportion of patients with early surgery recovered to GOS 4 and 5. However, it was not statistically significant. Tables 3 and 4 summarise the characteristics and neurological outcome of the patient groups classified by degree of immediate haematoma volume reduction by stereotactic aspiration. More than 60% of haematoma was aspirated in 30 patients and 60% or ª 2003 Elsevier Science Ltd. All rights reserved.
less in the other 33 patients. Clinical characteristics were not significantly different between the 2 groups. At 3 weeks 8 (26%) and 6 (20%) of 30 patients with radical decompression were GOS 4 and 5 each, respectively (Table 4). Seven (21%) of 33 patients with moderate decompression belonged to GOS 4 and no patient recovered to GOS 5. The difference was statistically significant (p < 0:05). At 6 months more patients with radical decompression recovered to GOS 5 (9/30, 33% vs. 3/33, 9%). However, it did not reach the statistical significance. Tables 5 and 6 show the comparison between early radical decompression and late moderate decompression. In 19 patients the operations were performed within 24 h from symptom onset and more than 60% of haematoma was removed. In these patients neurological outcome was significantly better at 3 weeks compared with that of the other 44 patients with late surgery or 60% or less reduction of haematoma volume (p < 0:05). At 6 months the same tendency persisted, but it was not statistically significant. Haematoma volume increased in 4 patients after aspiration. All of them underwent stereotactic aspiration within 12 h from the symptom onset. Three of them subsequently underwent open craniotomy for evacuation of haematoma. There was no case of increasing haematoma or infection related with thrombolytic therapy. DISCUSSION The controversies about surgical treatment of PICH can be resolved only by a prospective randomised controlled trial such as the Surgical Trial in Intracerebral Haemorrhage (STICH) which is still ongoing.18 Though the aim of our analysis is not very different from STICH and our experience described here suggests a beneficial role for stereotactic surgery, the limitation is that this is Journal of Clinical Neuroscience (2003) 10(4), 439–443
442 Lee et al.
Table 5
Characteristics of patients group with early radical (O24 h and >60%) and late moderate (>24 h or O60%) decompression Early radical
No. of cases Sex ratio (M:F) Age (years, mean SD) Side of haematoma (right:left) Volume of haematoma (ml, mean SD) Median GCS
19 14:5 53 7 9:10 41 19 11 (8–15)
Late moderate
p Value
44 30:14 55 11 30:14 49 23 12 (6–15)
NSa NSb NSa NSb NSc
GCS, Glasgow Coma Scale score; NS, not significant. a 2 v Test. b Student’s t test. c Mann–Whitney U test.
Table 6 Neurological outcome of the patients group with early radical (O24 h and >60%) and late moderate (>24 h or O60%) decompression (number of patients) Neuological outcome GOS 1 2 3 4 5 Favorable outcome (GOS 4, 5)
Three weeks Early radical 0 1 7 6 5 11 (58%) p < 0:05a
Six months Late moderate 0 6 28 9 1 10 (23%)
Early radical
Late moderate
0 0 5 7 7 14 (74%) NSa
0 2 15 22 5 27 (61%)
GOS, Glasgow Outcome Scale score; NS, not significant. a 2 v Test.
not a randomised study and it is essential to be confirmed through a randomised trial before generalization. In this study the authors tried to focus on the factors which could be changed by surgical manipulations and might influence the results of surgery. There are well known prognostic factors of PICH such as volume of haematoma, neurological condition, age of the patients, and the presence of other systemic illness.19–22 In addition to these preoperatively determined factors our results showed that early and radical stereotactic aspiration is related to the better functional outcome at the earlier phase. The advantage of evacuation of PICH or importance of surgical timing were suggested by animal studies23;24 and clinical reports.25–27 Our results partially support them. More patients recovered to an independent state (GOS 4 or 5) when the early radical decompression was performed. However, the differences in neurological outcome were statistically significant only at 3 weeks after the operation though the same tendency was shown at 6 months. Shortening of the early recovery phase has the advantage of reducing the cost and effort necessary for the care of the patients. The patients can begin the rehabiliation program earlier and it may be another beneficial factor for long-term recovery. If the final outcome is not significantly improved by surgical treatment, however, indication for surgery should be more strictly defined. Because the number of the patients included in this study is not sufficient, long-term benefit of the early radical surgery needs to be evaluated with a larger number of patients. The authors mainly focused on the aspiration procedure among the whole treatment schedule and thrombolytic therapy is not systemically evaluated in this study. It might be a beneficial adjunctive of aspiration procedure, though the importance would be insignificant if the initial maneuver to reduce the volume of haematoma is sufficient. Concerning the early and radical intervention of PICH, the acute complications associated with the surgical procedure should Journal of Clinical Neuroscience (2003) 10(4), 439–443
be considered. It is well known that PICH expands not infrequently in the first 24 h.28;29 Our data revealed similar phenomenon because 10 patients (16%) showed expansion of haematoma during the period between initial baseline CT scan and CT scan with stereotactic frame just before the operation. Eight of the 10 patients underwent the initial CT scan within 2 h from the symptom onset and it seems that expansion of haematoma is more likely to be a naturally ongoing haematoma formation rather than provoked by the procedure of applying the stereotactic frame to the head of patients. The major concern is the possibility that the actual decompressive procedure would provoke rebleeding if it is performed during the unstable period. In our cases, there was no mortality caused by surgery. It seems to be extraordinary because case fatality rates for intracerebral haemorrhage is known to approach 50%. There are several reasons that we observed no mortality. All the patients included in this study had haemorrhage circumscribed in basal ganglia. A recent study described the subtypes of striatocapsular haemorrhage and their clinical outcome.30 Only the massive type of striatocapsular haemorrhage with mean diameter of 65 mm resulted in fatality rate of 49% regardless of the treatment modality. The fatality rates in the other subtypes of striatocapsular haemorrhage was not high, including the lateral type which is usually elliptical in shape with a mean long diameter of 53 mm and resulted in 7% of fatality. The mean haematoma volume of the cases analyzed in this study was 46 ml with less than 60 mm in long dimeter and most of them belonged to the lateral type of striatocapsular haemorrhage. Also, the patients with very low GCS score or other risk factors such as serious medical illness were not recommended for operation. Therefore no mortality in our series reflects a largely natural course of the disease. Though stereotactic surgery did not increase the risk of death in our series, the risk of rebleeding or expansion of haematoma during or after the surgery seems to be a significant problem. In 4 patients with increased ª 2003 Elsevier Science Ltd. All rights reserved.
Stereotactic aspiration of intracerebral haematoma
haematoma after the operation the procedure was performed between 6 and 12 h from the symptom onset. These findings suggest that aggressive decompression during the acute phase might be associated with the higher risk of rebleeding which has been suggested by other authors.15 In summary, it is suggested that the earlier and more radical decompression results in a better recovery in the early phase. Though the beneficial effect of aggressive approach on final outcome was not significant it needs to be further evaluated with a larger number of patients. Early and radical surgery with traditional CT-guided stereotactic method can be accompanied by the increased risk of rebleeding and other innovative techniques such as endoscopic evacuation or intraoperative MRI may be a useful methods in the future. Finally all the issues need to be clarified through a prospective randomised controlled trial.
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