This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hankey, G. J. Articles by Hon, C. Search for Related Content PubMed PubMed Citation Articles by Hankey, G. J. Articles by Hon, C.

(Stroke. 1997;28:2126-2132.)
© 1997 American Heart Association, Inc.

Articles

Surgery for Primary Intracerebral Hemorrhage: Is It Safe and Effective?

A Systematic Review of Case Series and Randomized Trials

Graeme J. Hankey, MD, FRCP(Edin), FRACP; Christine Hon

From the Stroke Unit, Department of Neurology, Royal Perth Hospital (Western Australia, Australia).

Correspondence to Dr Graeme J. Hankey, Stroke Unit, Department of Neurology, Royal Perth Hospital, Wellington St, Perth, Western Australia, Australia 6001. E-mail gjhankey{at}cyllene.uwa.edu.au

	Abstract

Top Abstract Introduction Methods Results Discussion References

 
Background and Purpose The surgical treatment of primary intracerebral hemorrhage (PICH) varies thoughout the world, mainly because of the lack of evidence of its safety and effectiveness. This study compares the outcome of patients with PICH who are treated surgically with those who are not.

Methods We conducted a systematic overview (meta-analysis) of all studies of the outcome of surgery for PICH by means of a Medline search of relevant randomized trials and case series published since 1966. Cited references and presentations were also reviewed.

Results The 15 case series of surgery for PICH involving a total of 1524 patients (654 treated surgically) are potentially confounded and the results inconclusive. The pooled results of the three randomized controlled trials of open craniotomy and one trial of endoscopic evacuation for supratentorial PICH in a total of 349 patients (173 treated surgically) indicate a nonsignificant increase in odds of death and dependency at 6 months for patients treated surgically (odds ratio, 1.23; 95% confidence interval, 0.77 to 1.98). The odds of death or dependency at 6 months were 2.1 (1.1 to 4.1) for patients undergoing craniotomy and 0.45 (0.2 to 1.0) for endoscopic evacuation.

Conclusions There is insufficient evidence of the risks and benefits of surgery for PICH. Further randomized trials are needed to identify whether there is a favorable treatment effect of surgery, the types of PICH and patients who are likely to benefit and not benefit, and the safety and effectiveness of the different surgical interventions.

Key Words: cerebral hemorrhage • meta-analysis • stereotactic aspiration • surgical treatment

	Introduction

Top Abstract Introduction Methods Results Discussion References

 
Primary intracerebral hemorrhage (PICH) is an important stroke subtype because it is common (affecting approximately 35/100 000 population annually^1–3), it has a high early case-fatality rate (38% to 52% at 30 days^1,2,4–12), and it is amenable to potentially effective surgical treatment in the hazardous acute phase.

Surgical techniques include open craniotomy and CT-guided stereotaxic aspiration for decompressing and evacuating supratentorial PICH and suboccipital craniectomy and/or external ventricular drainage for infratentorial PICH.¹³ Open craniotomy, with or without ventricular drainage, has been facilitated by the development of transtemporal and transsylvian approaches to the basal ganglia and thalamus and the use of good illumination, magnification, and gentle retraction. Stereotaxic aspiration involves CT imaging of the patient's head in a stereotaxic frame, direct localization of the hematoma, and computerized calculation of the route for accessing the clot by means of a 3- to 5-mm cannula or standard ventricular catheter. Alternatively, an endoscope can be positioned stereotaxically or inserted under echographic guidance and then clamped onto a Sugita head fixation system. A fresh hematoma can be simply aspirated with the application of a vacuum. Organized hematomas can be morcellated physically by a rotating screw in the cannula, a guillotine-type cutting instrument in the aspirating needle, a tubular vent, and irrigation with fluid at high pressure, or chemically liquefied by fibrinolytic agents such as urokinase and tissue plasminogen activator. Fibrinolytic agents may also be injected at 6- to 12-hour intervals through an indwelling cannula, followed on each occasion by attempted aspiration. Hemostasis may be promoted by means of laser.

Despite recent advances in the application of imaging, endoscopy, and fibrinolytic agents in the surgical treatment of PICH, controversy remains regarding its safety and effectiveness because of the lack of reliable evidence. Consequently, there is wide variation in the management of PICH among different neurosurgeons and neurologists throughout the world and even in single centers.^14,15

The aim of this study was to systematically review the totality of evidence, in increasing order of rigor, for the risks and benefits of surgical treatment for PICH (compared with supportive medical treatment alone) and consider the implications of the results on current clinical practice and future research endeavors.

	Methods

Top Abstract Introduction Methods Results Discussion References

 
We reviewed all case series and randomized controlled trials assessing the effect of surgical treatment for PICH by means of a Medline search of articles published between January 1966 and June 1997 using the terms intracerebral hemorrhage, PICH, cerebellar hemorrhage, pontine hemorrhage, thalamic hemorrhage, and brain stem hemorrhage. References and reports cited in identified articles and all published epidemiological studies and reviews were also examined.

The studies were classified, in increasing order of rigor, as retrospective case series without controls, prospective case series without controls, case series with literature controls, case series with historical controls, case series with concurrent controls, case series with concurrent controls assessed by multiple regression analysis to adjust for important prognostic factors, and randomized controlled trials.

Patient outcome was recorded according to the definitions of the authors, which, besides death, were inconsistent. An effort was made to discern whether patient outcome was assessed by an observer who was blinded to the patient's treatment, but frequently this was not stated or did not occur.

The results of randomized trials are expressed as odds ratios (OR) with 95% confidence intervals (CIs), calculated by standard methods. The data from all the trials were pooled together with the use of current methods of systematic overview.^16,17

	Results

Top Abstract Introduction Methods Results Discussion References

 
Case Series With Controls of Any Type
We identified 15 case series that aimed to determine whether surgical treatment (combined with the supportive medical treatment) improves the outcome of patients with PICH^18–32 (Table 1). Only one study was population-based³⁰ and one prospective.³¹ The diagnosis of PICH was made by CT or MRI scan in all studies. Four studies were restricted to surgery for supratentorial PICH,^18–21 8 were restricted to infratentorial PICH,^22–29 and 3 examined surgery for both supratentorial and infratentorial PICH.^30–32

View this table: [in this window] [in a new window]   Table 1. Summary of Case Series on the Effect of Surgery for Primary Intracerebral Hemorrhage (1980-1996)

Supratentorial PICH
The four case studies of surgery for supratentorial PICH comprised a total of 421 patients (194 treated surgically).^18–21 All were retrospective, and two^20,21 were restricted to patients with putaminal hemorrhages. The selection criteria for surgery were described clearly in only one study.¹⁸ Surgical evacuation was performed by open craniotomy in all studies. Death was the only outcome measure common to all studies. All four studies concluded that surgery had no beneficial effect on supratentorial PICH.

Infratentorial PICH
The eight case studies of surgery for infratentorial PICH comprised a total of 405 patients (241 treated surgically). All studies were retrospective, and all but one²⁹ were restricted to patients with cerebellar hemorrhage. The surgical intervention comprised ventricular drainage and suboccipital craniectomy, but the timing of the surgery was variable. Death was the only outcome measure common to each study, but it was measured at different times (eg, at discharge, at 7 days, at 30 days). Two studies^22,29 reported surgery to have a beneficial effect in certain patients (conscious or drowsy but deteriorating patients with shift or obliteration of the fourth ventricle and hydrocephalus, or intraventricular blood and hydrocephalus²⁹), and one study²⁸ suggested that surgery had an overall beneficial effect. The other five series were either inconclusive or found no beneficial effect of surgery.

Supratentorial and Infratentorial PICH
The three case studies of surgery for both supratentorial and infratentorial PICH^30–32 comprised a total of 698 patients (219 treated surgically). One was prospective³¹ and one population-based.³⁰ The selection criteria for surgery varied. Open craniotomy, ventricular drainage, and suboccipital craniectomy were the main surgical procedures. Outcome was measured in terms of mortality and/or dependency at 30 days or 6 months. Broderick et al³⁰ reported no beneficial effect of surgery for either supratentorial or infratentorial PICH, in contrast to Coraddu et al.³¹ Kanno et al³² reported no beneficial effect of surgery for mild and severe PICH (defined by the location and size of the hematoma) but benefit for moderate PICH.

Randomized Controlled Trials
The four randomized trials of surgical treatment for PICH studied supratentorial PICH only (not infratentorial PICH).

McKissock et al³³ (1961) randomized 180 of a series of 303 patients, aged 32 to 76 years, who were admitted to the Atkinson Morley Hospital (171 cases) or the National Hospital, Queen Square (9 cases), England, between January 1959 and June 1960. The diagnosis of supratentorial PICH was established by angiography in approximately 60% of cases and ventriculography in the remainder. Eighty-two patients were excluded because they died or recovered rapidly before diagnostic investigation; were found to have tumor, abscess, or posterior fossa hemorrhage; or because the patient was in extremis and urgent surgery was performed or surgery was demanded by the referring physician. Ninety-one patients were "randomly allocated" to best medical treatment and 89 to the surgery and best medical treatment, but the method of randomization was not described. The treatment groups were comparable in age and sex. Surgery was undertaken as soon as the diagnosis and localization of PICH were determined. Medical therapy comprised initial bed rest in a general intensive care unit, with or without antihypertensive drugs and urea, and active physiotherapy. The primary outcome event was death or level of independence among survivors at 6 months. Patients were classified as independent if they were able to resume their former occupation, partially disabled if they had residual neurological signs but were capable of an independent existence and in many cases light work, and totally disabled if they were incapable of taking care of themselves. "The survivors were seen six months after discharge by an independent neurologist who was in no way connected with the patient's management while in hospital." Surgical treatment was associated with an increased odds of being dead or dependent at 6 months (OR, 2.04; 95% CI, 1.04 to 3.98).

Juvela et al³⁴ (1989) randomized 52 patients, aged 15 to 65 years, who were admitted to the Department of Neurosurgery, Helsinki University Central Hospital, between 1982 and 1986. The diagnosis of supratentorial PICH was made by CT scan in all cases. Patients were included if they presented within 24 hours of onset of symptoms and were unconscious but reactive to pain or had severe hemiparesis or dysphasia. Patients were excluded if they did not react to pain; were clearly improving; had a cerebellar hemorrhage or hemorrhage due to trauma, a brain tumor, aneurysm, or arteriovenous malformation; or had a poor prognosis due to severe heart, lung, endocrine, or malignant disease. Twenty-six patients were "randomly allocated" to immediate frontotemporal craniotomy with the use of microsurgical techniques within 48 hours of admission and 26 to medical therapy, which was not described other than "corticosteroids were not used in the present study." The method of randomization was not described. The surgical and control groups were comparable with regard to sex, age, chronic hypertension, previous use of antihypertensive drugs, mean size of hematoma (milliliters), and unconsciousness (number of cases and mean duration [hours]), but they differed in terms of the median score on the Glasgow Coma Scale and presence of intraventricular bleeding. All survivors was assessed by one of the investigators "who did not perform the operation" for level of dependence at 1, 6, and 12 months, using the Glasgow Outcome Scale.³⁷ The results showed a trend toward a higher odds of death or dependency with surgical treatment (OR, 5.95; 95% CI, 0.64 to 55), but the 95% CI was wide and included an OR of unity.

Batjer et al³⁵ (1990) randomized 17 patients, aged 30 to 75 years, who were admitted to Parkland Memorial Hospital, Dallas, Tex, between December 1983 and March 1989. Patients were included if they had CT evidence of putaminal hemorrhage at least 3.0 cm in diameter with or without ventricular extension; were aged between 30 and 75 years; had a documented history of hypertension; and were hospitalized within 24 hours of onset of symptoms. Patients were excluded if angiography was required (to exclude an aneurysm, arteriovenous malformation, or tumor); if they were older than 75 years; had minimal neurological dysfunction; were deeply comatose with decorticate or decerebrate posturing; or had an unassociated neurological illness, end-stage systemic disease, or a coagulopathy of any cause. Eight patients were randomly allocated to surgery and nine to the control group. The two groups were comparable with regard to the level of consciousness at the time of admission, age, systolic and diastolic blood pressure, and time from onset of symptoms to arrival in the emergency department. Survivors were assessed at 3 and 6 months after onset by one of the investigators; it is not clear if the assessor was blind to the treatment allocation. The assessment comprised a neurological examination, discussion with the patient's family, and review of medical charts of patients followed up in other clinic systems or by telephone interview with family members. The level of independence was classified by the functional outcome scale as level 1 (dead or vegetative), level 2 (dependent at home or in an institution), level 3 (independent at home), and level 4 (return to prestroke level of activity but not necessarily to occupation). The results showed a trend toward a lower rate of death or level of dependence in the surgically treated patients (OR, 0.86; 95% CI, 0.09 to 8.1), but the 95% CIs were very wide.

Auer et al³⁶ (1989) randomized 100 patients, aged 30 to 80 years, who were admitted to the Departments of Neurosurgery and Neurology, University of Graz, Austria, between June 1983 and August 1986 with a diagnosis of supratentorial PICH confirmed by CT scan. Patients were included if they were aged between 30 and 80 years, presented with neurological deficits or disturbed consciousness; were able to undergo unilateral carotid angiography; were otherwise fit for surgery; the volume of the hematoma (calculated from CT scans) exceeded 10 mL; the interval between stroke onset and start of treatment was less than 48 hours; and hemorrhage due to ruptured aneurysm, arteriovenous malformation, tumor, or trauma had been excluded. One hundred patients were "randomly allocated" to stereotaxically guided endoscopic evacuation of the PICH within 48 hours of admission plus standard medical therapy or to standard medical therapy alone. The two groups were comparable in terms of sex, age, level of consciousness, history of hypertension, and site, size, and side of hematoma. The primary outcome event was death or level of dependence at 6 months after the PICH. Dependency level was classified as grade 1 (patient leads a full and independent life without neurological deficit), grade 2 (patient leads a full and independent life with minimal neurological deficit), grade 3 (patient has neurological or intellectual impairment but is independent and able to work part time), grade 4 (patient has neurological deficit, is unable to work but is capable of self-care), grade 5 (patient is conscious but totally dependent on others for daily activities), and grade 6 (dead). The results were that surgical treatment was associated with a lower odds of death or dependency at 6 months (OR, 0.45; 95% CI, 0.19 to 1.04), but the 95% CI included unity.

Grotta et al³⁸ have published, in abstract form, the preliminary results of a randomized trial of surgery versus medical treatment in 26 of a series of 58 adults who presented within 12 hours of onset of lobar or putaminal PICH. One of 11 surgically treated patients died (9%) compared with 4 of 15 (27%) medically treated patients (OR, 0.28; 95% CI, 0.03 to 2.9). The type of surgical treatment, timing of outcome assessment, and functional outcome of survivors were not stated. Consequently, the results of this study have not been included in this overview (but should be included when they become known).

Systematic Overview
A formal statistical overview (meta-analysis) of the results of the four randomized controlled trials among a total of 173 patients in the surgically treated groups and 176 patients in the control groups indicates that surgery for supratentorial PICH is associated with a nonsignificant trend toward a higher odds of death or dependency at 6 months (OR, 1.23; 95% CI, 0.77 to 1.98) (Table 2, Figure).

View this table: [in this window] [in a new window]   Table 2. Summary of Randomized Controlled Trials of the Effect of Surgery for Supratentorial Primary Intracerebral Hemorrhage

View larger version (8K): [in this window] [in a new window]   Figure 1. Odds ratio of being dead or dependent 6 months after surgical treatment (active treatment) for supratentorial primary intracerebral hemorrhage. with intersecting line indicates trial results and 95% confidence intervals (area of proportional to amount of information contributed; , overview results and 95% confidence intervals. Dashed vertical line represents odds ratio of 1.23 suggested by overview of all four trial results. Solid vertical line represents odds ratio of unity (no treatment effect). Data from McKissock et al,33 Juvela et al,34 Batjer et al,35 and Auer et al.36

The pooled evidence of the three trials of open craniotomy showed that the odds of being "dead or dependent" at 6 months after supratentorial PICH were 2.10 (95% CI, 1.07 to 4.12) times greater among patients undergoing open craniotomy than those who were not surgically treated (Table 2).

The single trial of stereotaxically guided endoscopic evacuation showed that the odds of being "dead or dependent" at 6 months after supratentorial PICH was 0.45 (95% CI, 0.19 to 1.04) times less among patients undergoing this operation than those who were not surgically treated (Table 2).

	Discussion

Top Abstract Introduction Methods Results Discussion References

 
The 15 case series that describe the outcome of surgically treated patients with PICH are potentially confounded because the control groups with which they are compared may not have been comparable in terms of all of the other factors (besides treatment) that may influence patient outcome, such as the patient's age, level of consciousness, severity of limb paresis, and continence status; the site, size, volume, and mass effect of the hemorrhage; and the presence or absence of rupture of blood into the ventricles or subarachnoid space.^1,12 In addition, all but one of the case series were retrospective and thus hampered by several problems, both administrative (clinical notes or crucial data missing) and methodological (haphazard patient selection, nonstandard diagnostic and outcome criteria, variation in follow-up frequency and adequacy, and possible bias due to nonblind reviewers). Consequently, the results are inconclusive.

The most reliable evidence for the effectiveness of surgical evacuation for supratentorial PICH on patient outcome comes from large, randomized, single-blind, controlled trials and a systematic overview (meta-analysis) of all trials, published and unpublished.

This systematic overview identified four published randomized controlled trials aimed at determining whether surgical treatment combined with the best medical therapy would improve the survival and quality of life of patients presenting with supratentorial PICH compared with best medical therapy alone. The trials were conducted in four different countries (England, Finland, the United States, and Austria) and at different periods of time. Several aspects of the trials, such as the diagnostic process and surgical interventions, were not uniform. For example, the diagnosis of PICH was based on CT scan in the three latter trials, but in the study by McKissock et al³³ diagnosis was based on clinical examination, cerebral angiography, and examination of the cerebrospinal fluid. It was not stated in any of the trials whether the process of randomization was concealed. Medical therapy was described to some extent in three trials^33,35,36 and was really no more than supportive care; there have been no randomized trials proving or disproving the benefit of specific medical therapies in PICH such as mechanical ventilation, blood pressure control, and the use of osmotic diuretics such as mannitol. Although the surgical and control groups were comparable in terms of several known prognostic factors, there were significant differences in the initial Glasgow Coma Scale scores and frequency of intraventricular hemorrhage between the two groups studied by Juvela et al.³⁴ Three trials evaluated the effect of removal of PICH at open craniotomy,^33–35 and one evaluated stereotaxically guided endoscopic evacuation.³⁶ In all trials, surgical intervention was performed within 48 hours of the onset of symptoms, and the primary outcome event was death and level of dependence 6 months after surgery (although the definitions of dependency varied).

None of the trials were large enough individually to have the statistical power to reliably quantify the risks and benefits of surgery. A systemic review of the four trials suggests that overall there is no clear benefit or risk from surgery; the odds of being "dead or dependent" at 6 months after supratentorial PICH was 1.2 (95% CI, 0.8 to 2.0) times greater among patients undergoing surgical evacuation than those who were not treated surgically, but the extremes of the 95% CIs of the OR are consistent with surgery having a favorable effect (OR, 0.8) and an unfavorable effect (OR, 2.0). However, there was significant heterogeneity of the treatment effect; craniotomy appeared to have qualitatively different effects than stereotaxic endoscopic aspiration. The pooled evidence of the three trials of craniotomy showed that the odds of being dead or dependent at 6 months after supratentorial PICH was 2.1 (95% CI, 1.1 to 4.1) times greater among patients undergoing craniotomy than those who were not treated surgically, whereas the single trial of endoscopic evacuation showed that odds of patients being dead or dependent at 6 months after supratentorial PICH was 0.45 (95% CI, 0.2 to 1.0) times that of patients who were not treated surgically. Within the three trials of craniotomy, one trial³³ was performed in the pre-CT era, and it is therefore possible that diagnostic errors may have increased the hazard of surgery; patients with nonhemorrhagic stroke may have undergone a risky treatment (craniotomy) from which they were unlikely to benefit. Whether these results reflect publication bias is also open to question.

In conclusion, the role of stereotaxic surgery for supratentorial PICH has not been adequately studied in randomized trials and remains uncertain. Furthermore, there have been no randomized controlled trials evaluating surgical techniques for the treatment of posterior fossa hematoma. Consequently, clinical practice is haphazard; the indications for surgery are uncertain (large lobar hematomas, small subcortical hematomas, none at all), the technique is uncertain (stereotaxic or endoscopic, conventional craniotomy), and the risks and benefits of the different techniques for different indications are uncertain. The uncertainty in clinical practice and the magnitude of this controversy are the ideal platforms from which to launch another randomized trial that is collaborative throughout the world and therefore large enough to reliably identify the risks and benefits of surgery, for whom surgery is safe and effective, and for whom surgery is dangerous or ineffective.

Received May 21, 1997; revision received July 18, 1997; accepted August 26, 1997.

	References

Top Abstract Introduction Methods Results Discussion References

 

1. Anderson CS, Chakera TMH, Stewart-Wynne EG, Jamrozik KD. Spectrum of primary intracerebral hemorrhage in Perth, Western Australia, 1989–90: incidence and outcome. J Neurol Neurosurg Psychiatry. 1994;57:936–940.[Abstract]
2. Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project —1981–86, II: incidence, case fatality rates and overall outcome at one year of cerebral infarction, primary intracerebral and subarachnoid hemorrhage. J Neurol Neurosurg Psychiatry. 1990;53:16–22.[Abstract]
3. Anderson CS, Jamrozik KD, Burvill PW, Chakera TMH, Johnson GA, Stewart-Wynne EG. Determining the incidence of different subtypes of stroke: results from the Perth Community Stroke Study, 1989–1990. MJA. 1993;158:85–89.
4. Herman B, Leyten ACM, van Luijk JH, Frenken CWGM, Op de Coul AAW, Schulte BPM. Epidemiology of stroke in Tilberg, the Netherlands: the population-based incidence register, II: incidence, initial clinical picture and medical care, and three week case fatality. Stroke. 1982;13:629–634.[Abstract/Free Full Text]
5. Ashok PP, Radhakrishnan K, Sridharan R, El-Mangoush MA. Incidence and pattern of cerebrovascular diseases in Benghazi, Libya. J Neurol Neurosurg Psychiatry. 1986;49: 519–523.
6. Broderick JP, Phillips SJ, Whisnant JP, O'Fallon WM, Bergstrahl EJ. Incidence rates of stroke in the eighties: the end of the decline in stroke? Stroke.. 1989;20:577–582.[Abstract/Free Full Text]
7. Kojima S, Omura T, Wakamatsu W, Kishi M, Yamazaki T, Iida M, Komachi Y. Prognosis and disability of stroke patients after 5 years in Akita, Japan. Stroke. 1990;21:72–77.[Abstract/Free Full Text]
8. Ricci S, Celani MG, La Rosa FL, Vitali R, Duca E, Ferraguzzi R, Paolotti M, Seppolino D, Caputo N, Chiurulla C, Scaroni R, Signorini E. SEPIVAC: a community-based study of stroke incidence in Umbria, Italy. J Neurol Neurosurg Psychiatry. 1991;54:695–698.[Abstract]
9. Giroud M, Gras P, Chadan N, Beuriat P, Milan C, Arveux P, Dumas R. Cerebral hemorrhage in a French prospective population study. J Neurol Neurosurg Psychiatry. 1991;54:595–598.[Abstract]
10. D'Alessandro G, Di Giovanni M, Roveyaz L, Iannizzi L, Compagnoni MP, Blanc S, Bottachi E. Incidence and prognosis of stroke in the Valle d'Aosta, Italy: first-year results of a community-based study. Stroke.. 1992;23:1712–1715.[Abstract/Free Full Text]
11. Fogelholm R, Nuutila M, Vuorela A-L. Primary intracerebral hemorrhage in the Jyvaskyla region, Central Finland, 1985–89: incidence, case fatality rate and functional outcome. J Neurol Neurosurg Psychiatry. 1992;55:546–552.[Abstract]
12. Counsell C, Boonyakarnkul S, Dennis M, Sandercock P, Bamford J, Burn J, Warlow C. Primary intracerebral hemorrhage in the Oxfordshire Community Stroke Project, II: prognosis. Cerebrovasc Dis. 1995;5:26–34.
13. Kaufman HH. Treatment of deep spontaneous intracerebral hematomas: a review. Stroke. 1993;24(suppl I):I-101-I-108.
14. Broderick J, Brott T, Tomsick T, Tew J, Duldner J, Huster G. Management of intracerebral hemorrhage in a large metropolitan population. Neurosurgery. 1994;34:882–887.[Medline] [Order article via Infotrieve]
15. Masdeu JC, Rubino FA. Management of lobar intracerebral hemorrhage: medical or surgical. Neurology. 1984;34:381–383.[Abstract/Free Full Text]
16. Antiplatelet Trialists' Collaboration. Secondary prevention of vascular disease by prolonged antiplatelet treatment. BMJ. 1988;296:320–331.
17. Cook DJ, Mulrow CD, Haynes RB. Systematic reviews: synthesis of best evidence for clinical decisions. Ann Intern Med. 1997;126:376–380.[Abstract/Free Full Text]
18. Bolander HG, Kourtopoulos H, Liliequist B, Wittboldt S. Treatment of spontaneous intracerebral hemorrhage: a retrospective analysis of 74 consecutive cases with special reference to computer tomographic data. Acta Neurochir (Wien).. 1983;67:19–28.[Medline] [Order article via Infotrieve]
19. Bambilla GL, Rodriguez Baeria R, Sangiovanni G, Rainoldi F, Locatelli D. Spontaneous intracerebral hemorrhage: medical or surgical treatment. J Neurol Sci. 1983;27:95–101.
20. 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.
21. Waga S, Yamamoto Y. Hypertensive putaminal hemorrhage: treatment and results. Is surgical treatment superior to conservative one? Stroke.. 1983;14:480–485.[Abstract/Free Full Text]
22. Mathew P, Teasdale G, Bannan A, Oluoch-Olunya D. Neurosurgical management of cerebellar hematoma and infarct. J Neurol Neurosurg Psychiatry. 1995;59:287–292.[Abstract]
23. Rosenthal D, Marquardt G, Sievert T. Spontaneous cerebellar hemorrhages: acute management and prognosis. Adv Neurosurg. 1993;21:61–68.
24. Van Loon J, Van Calenbergh F, Goffin J, Plets C. Controversies in the management of spontaneous cerebellar hemorrhage: a consecutive series of 49 cases and review of the literature. Acta Neurochir (Wien).. 1993;122:187–193.[Medline] [Order article via Infotrieve]
25. Firsching R, Kleindienst A. Cerebellar hematomas: prognosis and risk of upward transtentorial herniation. Adv Neurosurg. 1993;21:69–72.
26. Koziarski A, Frankiewicz E. Medical and surgical treatment of intracerebellar hematomas. Acta Neurochir (Wien). 1991;110:24–28.[Medline] [Order article via Infotrieve]
27. Firsching R, Huber M, Frowein RA. Cerebellar hemorrhage: management and prognosis. Neurosurg Rev. 1991;14:1991–1994.
28. Auer LM, Auer TH, Sayama I. Indications for surgical treatment of cerebellar hemorrhage and infarction. Acta Neurochir (Wien). 1986;79:74–79.[Medline] [Order article via Infotrieve]
29. Da Pian R, Bazzan A, Pasqualin A. Surgical versus medical treatment of spontaneous posterior fossa hematomas: a cooperative study on 205 cases. Neurol Res. 1984;6:145–151.[Medline] [Order article via Infotrieve]
30. Broderick J, Brott T, Tomsick T, Tew J, Duldner J, Huster G. Management of intracerebral hemorrhage in a large metropolitan population. Neurosurgery. 1994;34:882–887.
31. Coraddu M, Nurchi GL, Floris F, Meleddu V. Considerations about the surgical indication of the spontaneous cerebral hematomas. J Neurol Sci. 1990;34:35–39.
32. 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 non-surgical and 154 surgical cases. Neurosurgery. 1984;61:1091–1099.
33. McKissock W, Richardson A, Taylor J. Primary intracerebral hemorrhage: a controlled trial of surgical and conservative treatment in 180 unselected cases. Lancet. 1961;2:221–226.
34. Juvela S, Heiskanen O, Poranen A, Valtonen S, Kuurne T, Kaste M, Troupp H. The treatment of spontaneous intracerebral hemorrhage: a prospective randomised trial of surgical and conservative treatment. J Neurosurg. 1989;70:755–758.[Medline] [Order article via Infotrieve]
35. Batjer HH, Reisch JS, Allen BC, Plaizier LJ, Jen Su C. Failure of surgery to improve outcome in hypertensive putaminal hemorrhage: a prospective randomised trial. Arch Neurol. 1990;47:1103–1106.[Abstract]
36. 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 randomised study. J Neurosurg.. 1989;70:530–535.[Medline] [Order article via Infotrieve]
37. Jennett B, Bond M. Assessment of outcome after severe brain damage: a practical scale. Lancet.. 1975;1:480–484.[Medline] [Order article via Infotrieve]
38. Grotta J, Morgenstern L, Shedden P, Pasteur W. Randomised trial of early surgery for hemispheric intracerebral hemorrhage. Cerebrovasc Dis. 1996;6(suppl 2):21. Abstract.

This article has been cited by other articles:

				M. E Madden Diagnostic Imaging of Cerebrovascular Injury Radiol. Technol., July 1, 2008; 79(6): 535MR - 549MR. [Abstract] [Full Text] [PDF]

				M. L. Flaherty, M. Haverbusch, P. Sekar, B. Kissela, D. Kleindorfer, C. J. Moomaw, L. Sauerbeck, A. Schneider, J. P. Broderick, and D. Woo Long-term mortality after intracerebral hemorrhage Neurology, April 25, 2006; 66(8): 1182 - 1186. [Abstract] [Full Text] [PDF]

				K. Minematsu Evacuation of Intracerebral Hematoma Is Likely to Be Beneficial Stroke, June 1, 2003; 34(6): 1567 - 1568. [Full Text] [PDF]

				C. M. P. Rodrigues, S. Sola, Z. Nan, R. E. Castro, P. S. Ribeiro, W. C. Low, and C. J. Steer Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats PNAS, May 13, 2003; 100(10): 6087 - 6092. [Abstract] [Full Text] [PDF]

				O.P.M. Teernstra, S.M.A.A. Evers, J. Lodder, P. Leffers, C.L. Franke, and G. Blaauw Stereotactic Treatment of Intracerebral Hematoma by Means of a Plasminogen Activator: A Multicenter Randomized Controlled Trial (SICHPA) Stroke, April 1, 2003; 34(4): 968 - 974. [Abstract] [Full Text] [PDF]

				J. R. Carhuapoma, P. B. Barker, D. F. Hanley, P. Wang, and N. J. Beauchamp Human Brain Hemorrhage: Quantification of Perihematoma Edema by Use of Diffusion-Weighted MR Imaging AJNR Am. J. Neuroradiol., September 1, 2002; 23(8): 1322 - 1326. [Abstract] [Full Text] [PDF]

				A. A. Rabinstein, J. L. Atkinson, and E. F.M. Wijdicks Emergency craniotomy in patients worsening due to expanded cerebral hematoma: To what purpose? Neurology, May 14, 2002; 58(9): 1367 - 1372. [Abstract] [Full Text] [PDF]

				L.B. Morgenstern, A.M. Demchuk, D.H. Kim, R.F. Frankowski, and J.C. Grotta Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage Neurology, May 22, 2001; 56(10): 1294 - 1299. [Abstract] [Full Text] [PDF]

				H. M. Fernandes, B. Gregson, S. Siddique, and A. D. Mendelow Surgery in Intracerebral Hemorrhage : The Uncertainty Continues Stroke, October 1, 2000; 31(10): 2511 - 2516. [Abstract] [Full Text] [PDF]

				J. M. Montes, J. H. Wong, P. B. Fayad, and I. A. Awad Stereotactic Computed Tomographic-Guided Aspiration and Thrombolysis of Intracerebral Hematoma : Protocol and Preliminary Experience Stroke, April 1, 2000; 31(4): 834 - 840. [Abstract] [Full Text] [PDF]

				G. Gubitz and P. Sandercock Extracts from "Clinical Evidence": Acute ischaemic stroke BMJ, March 11, 2000; 320(7236): 692 - 696. [Full Text]

				R. Davenport and M. Dennis Neurological emergencies: acute stroke J. Neurol. Neurosurg. Psychiatry, March 1, 2000; 68(3): 277 - 288. [Abstract] [Full Text] [PDF]

				S. L. Hickenbottom, J. C. Grotta, R. Strong, L. A. Denner, J. Aronowski, and R. L. Macdonald Nuclear Factor-{kappa}B and Cell Death After Experimental Intracerebral Hemorrhage in Rats • Editorial Comment Stroke, November 1, 1999; 30 (11): 2472 - 2478. [Abstract] [Full Text] [PDF]

				M. O. McCarron, J. A.R. Nicoll, A. Izumihara, N. Iwamoto, K. Yamashita, H. Ito, and T. Ishihara Surgery for Cerebral Amyloid Angiopathy–Related Hemorrhage • Response Stroke, June 1, 1999; 30(6): 1291 - 1291. [Full Text] [PDF]

				M. Altumbabic, J. Peeling, M. R. Del Bigio, and R. L. Macdonald Intracerebral Hemorrhage in the Rat: Effects of Hematoma Aspiration • Editorial Comment Stroke, September 1, 1998; 29(9): 1917 - 1923. [Abstract] [Full Text] [PDF]

				Management soon after a stroke DTB, July 1, 1998; 36(7): 51 - 54. [Abstract] [Full Text] [PDF]

				J. L. Saver, G. J. Hankey, F. Edin, and C. S. Hon Surgery for Primary Intracerebral Hemorrhage: Meta-analysis of CT-Era Studies • Response Stroke, July 1, 1998; 29(7): 1477 - 1478. [Full Text]

This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hankey, G. J. Articles by Hon, C. Search for Related Content PubMed PubMed Citation Articles by Hankey, G. J. Articles by Hon, C.