Journal of Clinical Neuroscience 19 (2012) 975–979

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Journal of Clinical Neuroscience

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Clinical Study

Transtentorial herniation in patients with hypertensive putaminal haemorrhageis predictive of elevated intracranial pressure following haematoma removal

Ke Wang, Yajun Xue, Xianzhen Chen, Daming Cui, Meiqing Lou ⇑Department of Neurosurgery, Shanghai Tenth People’s Hospital, Tongji University, 301 Middle Yanchang Road, Zhabei District, Shanghai 200072, China

a r t i c l e i n f o a b s t r a c t

Article history:Received 2 August 2011Accepted 21 September 2011

Keywords:Decompressive craniectomyHypertensive putaminal haemorrhageIntracranial pressureSurgical treatmentTranstentorial herniation

0967-5868/$ - see front matter � 2011 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.jocn.2011.09.027

⇑ Corresponding author. Tel./fax: +86 021 6630735E-mail address: 071105344@fudan.edu.cn (M. Lou

We investigated surgical outcomes of haematoma evacuation in patients with hypertensive putaminalhaemorrhage, with emphasis on the development of postoperative refractory intracranial hypertension.Twenty-two consecutive patients with hypertensive putaminal haemorrhage underwent microsurgicalclot removal without decompressive craniectomy. Medical histories, radiographic findings, and surgicalnotes were reviewed. Twenty patients survived to discharge. Twelve patients with preoperative transten-torial herniation, demonstrating a greater haematoma volume and lower Glasgow Coma Scale (GCS)score, had significantly elevated postoperative intracranial pressure. Five of these patients developedrefractory intracranial hypertension (42%), and two of these patients died. Conversely, none of the 10patients without preoperative transtentorial herniation experienced refractory intracranial hypertension,and they had a better outcome at discharge. The preoperative presence of clinical transtentorial hernia-tion may predict the development of postoperative refractory intracranial hypertension, which mayrequire decompressive craniectomy.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Hypertensive putaminal haemorrhage is a form of spontaneousintracerebral haemorrhage (ICH) with particularly high mortalityand morbidity despite optimal treatment.1 Although the efficacyof surgical treatment for ICH remains contentious, it is recognizedas a life-saving choice in clinically deteriorating patients.2 Opencraniotomy to remove the haematoma is the standard surgical ap-proach used to treat spontaneous ICH, and patients with hyperten-sive putaminal haematomas larger than 30 mL usually benefit fromthis operation.3 However, clot removal alone appears to be inade-quate for some patients, and an additional decompressive craniec-tomy may be required.4

Decompressive craniectomy involves removing a large piece ofthe skull and opening the underlying dura to allow the brain to ex-pand. The procedure is usually performed to treat brain disorderswith elevated intracranial pressure (ICP), such as severe traumaticbrain injury,5 massive middle cerebral artery infarction,6 and aneu-rysmal subarachnoid haemorrhage.7 Several studies recommendusing this technique alone or in combination with clot removalfor the treatment of spontaneous ICH.4,8–10 However, decompres-sive craniectomy can have severe side effects.11,12 Thus, clarifyingthe conditions predictive of elevated ICP could validate the use of

ll rights reserved.

9.).

decompressive craniectomy in patients with hypertensive putami-nal haemorrhage.

We suggest that only patients at high risk of developing postop-erative refractory intracranial hypertension will benefit from anadditional decompressive craniectomy after haematoma evacua-tion. To identify these patients, we evaluated the surgical outcomesof haematoma evacuation in 22 consecutive patients with hyper-tensive putaminal haemorrhage, paying special attention to thedevelopment of postoperative refractory intracranial hypertension.Preoperative transtentorial herniation was associated with signifi-cantly higher postoperative ICP, suggesting that this patient sub-group may benefit from decompressive craniectomy.

2. Materials and methods

We examined the records of 22 patients who underwent micro-surgical removal of hypertensive putaminal haematomas withoutdecompressive craniectomy at the Neurosurgical Department ofthe Shanghai Tenth People’s Hospital between January 2010 andMay 2011. The main inclusion criteria were a preoperative Glas-gow Coma Scale (GCS) score of 12 or less and a haematoma volumeof 30 mL or more, which was estimated using the formulaA � B � C/2.13 Patients with severe systemic diseases, such aschronic heart failure, pulmonary insufficiency, or liver and renaldysfunction were excluded. Informed consent was obtained fromthe patients’ next of kin.

976 K. Wang et al. / Journal of Clinical Neuroscience 19 (2012) 975–979

Haematoma removal was performed under the operating micro-scope using either a transsylvian or transcortical approach, depend-ing on the preference of the neurosurgeon. The involved vessels wereexamined if possible, and haemostasis in the cavity was achieved.The dura was tightly sutured, and the bone flap was returned in allpatients. If intraventricular haemorrhage (IVH) occurred, an intra-ventricular ICP-monitoring probe (Codman, Johnson & Johnson,Raynham, MA, USA) was inserted. Otherwise, a subdural ICP-moni-toring kit was used according to the manufacturer’s instructions.After surgery, patients were transferred to the Neurological Inten-sive Care Unit and received optimal medical treatment, includinghyperosmolar treatment (mannitol, 3% saline), mechanical ventila-tion, glycaemic control, blood pressure management, and analgesicsedation. All patients underwent head CT scans within 12 hours aftersurgery, and a series of CT scans was performed postoperatively.

We collected data including the GCS score and pupillary abnor-malities prior to surgery, preoperative head CT scan findings,haematoma volume before and after surgery, and outcomes at dis-charge. The presence of stupor or coma, combined with unilateralor bilateral fixed dilated pupils, was considered a sign of clinicaltranstentorial herniation. The volume of the remaining haematomawas assessed according to the CT scans taken within 12 hours aftersurgery. ICP values were recorded hourly, and daily mean ICP val-ues were calculated using the hourly values. Patient outcomeswere assessed at discharge according to the Glasgow OutcomeScale (GOS). A poor patient outcome was defined by GOS scoresof one, two, or three, while a good outcome was defined by GOSscores of four or five.

Continuous data were expressed as the mean ± standard devia-tions, and categorical data were expressed as the median ± inter-quartile range. The p values were derived from the two-tailedunpaired Student’s t-test, the Mann–Whitney test, or Pearson’schi-square test. Differences were considered significant if p < 0.05.

3. Results

Clinical characteristics, CT scan findings, and patient outcomesare summarized in Table 1. Fourteen male and eight female pa-tients were included in this study, ranging from 33 to 77 years ofage (mean = 54.4 years). The mean GCS score immediately beforesurgery was 7.0 ± 3.0. The mean time interval from ictus to surgerywas 8.4 ± 4.4 hours (range = 5–20 hours). Eighteen patients dem-onstrated IVH on preoperative head CT scans. The median ICHscore was 3.0 (range = 2–4). The mean haematoma volume asdetermined from the preoperative head CT scans was73.1 ± 31.3 mL, and the remaining volume after surgery was11.0 ± 3.0 mL. During the operation, all patients had a tense dura,indicative of elevated ICP, but the tension was completely relievedby the clot removal. The mean ICP value immediately after surgerywas 3.0 mmHg (range = 1–6 mmHg). ICP gradually increased overtime (Fig. 1). No rebleeding was observed in any patient aftersurgery.

Twelve patients showed signs of preoperative transtentorialherniation. Among them, eight patients had unilateral fixed dilatedpupils, and four had bilateral fixed dilated pupils. Five of these pa-tients developed postoperative refractory intracranial hyperten-sion caused by severe brain swelling. The two patients with apeak ICP level of 20–30 mmHg had a GOS score of three at dis-charge, while the patient with a peak ICP level of 30–40 mmHghad a GOS score of two at discharge. The remaining two patientswith a peak ICP level of over 40 mmHg died in hospital. Conversely,none of the 10 patients without signs of preoperative transtentorialherniation developed postoperative refractory intracranial hyper-tension, and three attained a good outcome (GOS score of four orfive) at discharge.

The postoperative ICP changes in the two groups of patientswere further analyzed. The mean ICP values immediately after sur-gery in the patients with preoperative transtentorial herniationwere not significantly different from those without preoperativetranstentorial herniation (2.8 ± 1.2 mmHg vs. 2.6 ± 1.2 mmHg,p > 0.05). On the days following surgery, however, the mean ICPvalues in the transtentorial herniation group were significantlyhigher than in patients without preoperative signs of herniation(Table 2, Fig. 1A). When preoperative clinical characteristics wereevaluated, the 12 patients with preoperative transtentorial hernia-tion had larger haematomas (90.2 ± 30.1 mL vs. 52.7 ± 18.0 mL,p = 0.003) and lower GCS scores (6.5 ± 3.0 vs. 8.0 ± 3.3, p = 0.032)than those without herniation. There were no significant differ-ences in age (54.7 ± 9.9 vs. 54.0 ± 12.5, p > 0.05), ICH scores(3.0 ± 0.0 vs. 3.0 ± 0.3, p > 0.05), or the remaining haematoma vol-ume between the two groups (11.1 ± 3.1 mL vs. 10.8 ± 3.1 mL,p > 0.05). Moreover, the outcome at discharge was significantlypoorer in the patients with preoperative transtentorial herniation(3.0 ± 1.0 vs. 3.0 ± 1.3, p = 0.019).

Fifty per cent of the patients in this study underwent clot re-moval using the transsylvian approach, and the remaining patientsunderwent clot removal using the transcortical approach. Therewere no significant differences in the haematoma volume reduc-tion or the remaining haematoma volume between the two surgi-cal groups (81.3 ± 6.4% vs. 84.9 ± 6.6%, p > 0.05; 10.5 ± 2.6 mL vs.11.4 ± 3.4 mL, p > 0.05). The mean ICP values at different timepoints after surgery were not significantly different between thetwo surgical groups (Fig. 1B). Moreover, the outcome at dischargebetween the two surgical approach groups was not significantlydifferent (3.0 ± 1.0 vs. 3.0 ± 1.0, p > 0.05). These findings suggestthe two surgical approaches have similar effects.

3.1. Illustrative patient

A 33-year-old man with a history of hypertension developed asudden-onset headache followed by right-side hemiparesis and adepressed level of consciousness that developed over the followingsix hours. Upon arrival at the Emergency Department, he was ini-tially responsive to verbal stimulation but later became comatoseand had a GCS score of seven, with a left-dilated fixed pupil anda pinpoint right pupil. A head CT scan revealed a large (approxi-mately 76 mL) left putaminal haematoma extending into the tem-poral lobe, with prominent shift of the midline structures (greaterthan 1 cm) and effacement of the basal cisterns, suggesting se-verely elevated ICP. The haematoma was evacuated successfullyeight hours after the ictus using the transsylvian approach withoutdecompressive craniectomy and a subdural ICP probe was inserted.The left pupil contracted immediately after surgery and respondedto light 24 hours after surgery. A head CT scan eight hours aftersurgery showed recovery of the midline structures and reappear-ance of the basal cisterns, indicating relief of intracranial hyperten-sion. With optimal medical treatment, the ICP values of this patientwere maintained at an acceptable level, as reflected by the clearpresence of basal cisterns and mid-positioned septum pellucidumon CT scans performed on days three and seven after surgery(Fig. 2). Four weeks after the surgery, the patient was dischargedto a rehabilitation centre with a GOS score of three. He was livingindependently at the 6-month follow-up.

4. Discussion

The most efficacious surgical treatment for spontaneous ICH iscontentious, and the choice of treatment is further complicatedby a number of presurgical factors that impact the clinicaloutcome.1,14–17 If surgical candidates are appropriately selected,

Table 1Clinical characteristics, CT scan findings, surgical approaches, and outcomes at discharge in patients with hypertensive putaminal haemorrhage

Patientno.

Age(years),sex

PreoperativeGCS score

Pupillaryabnormalities

IVH Midline shift(P 1 cm)

ICHscore

Haematomavolume (mL)

Time tosurgery(hours)

Surgicalapproach

Residualvolume (mL)

Outcomes(GOS score)

1� 59, F 4 BFDP No Yes 3 98 5 TS 10 12 58, M 6 UFDP Yes No 3 65 20 TS 12 33 61, M 8 UFDP Yes Yes 3 53 9 TC 10 34 53, F 5 BFDP Yes Yes 3 118 5 TC 13 25 46, M 7 MPFP Yes No 3 35 14 TS 10 36� 60, M 6 BFDP Yes Yes 3 95 5 TC 8 27 47, M 8 UFDP Yes Yes 3 80 7 TC 10 28 35, M 12 NR No No 2 38 5 TC 12 59 58, F 9 NR Yes No 3 40 15 TC 8 310� 59, M 4 BFDP Yes Yes 4 165 5 TC 18 111 33, M 7 UFDP No Yes 2 76 6 TS 8 312 50, F 11 NR Yes Yes 3 58 9 TS 15 513 59, F 7 NR No Yes 2 99 6 TC 16 314 50, M 10 UFDP Yes Yes 3 65 8 TC 8 315 60, M 7 NR Yes No 3 50 7 TS 6 416 47, F 9 UFDP Yes Yes 3 72 6 TS 14 417 66, F 7 NR Yes No 3 54 5 TS 10 318 77, M 10 NR Yes No 3 56 16 TS 8 319� 58, M 7 UFDP Yes Yes 3 105 8 TC 9 320 40, M 8 NR Yes No 3 52 6 TS 11 321� 72, F 5 UFDP Yes Yes 3 90 13 TC 14 322 49, M 8 MPFP Yes No 3 45 5 TS 12 3

� Five patients developed postoperative refractory intracranial hypertension. BFDP = bilateral fixed dilated pupil, F = female, GCS = Glasgow Coma Scale, GOS = GlasgowOutcome Scale, ICH = intracerebral haemorrhage, IVH = intraventricular haemorrhage, M = male, MPFP = midposition fixed pupil, NR = normal reaction, TC = transcortical,TS = transsylvian, UFDP = unilateral fixed dilated pupil.

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however, positive results can be achieved. Studies have shown thatpatients with ICH with a haematoma volume of more than 30 mLand a GCS score of less than 12 will benefit from surgicaltreatment3,18; all the patients included in this study met thesecriteria.

The goal of surgical treatment is to achieve complete clot re-moval as soon as possible with the least amount of surgical trauma.Hypertensive putaminal haemorrhage is one of the most devastat-ing forms of ICH because it frequently involves eloquent areas ofthe brain. Deep clots are relatively difficult for neurosurgeons toreach without damaging overlying structures. Advances in micro-surgical techniques have made it possible to minimize surgicaltrauma while still achieving satisfactory haematoma reduction.In this study, a near-complete (>90%) evacuation was achieved intwo patients, 80–90% in 15 patients, 70–80% in four patients, and<70% in only one patient. The mean haematoma volume reductionwas 84.9%, and preoperative intracranial hypertension was com-pletely relieved by clot removal.

Reduction of the intracranial volume buffering capacity and se-verely increased ICP are the most important predictors of poorprognosis after spontaneous ICH.19,20 Previous studies have shownthat a select group of patients with spontaneous ICH benefit fromhaematoma evacuation combined with decompressive craniec-tomy.4,19 However, there has been no clear statistical validationfor this treatment option or standard inclusion criteria. Unfortu-nately, the decision to perform an additional decompressive crani-ectomy after clot removal usually depends on the individualexperiences of the treating neurosurgeon.9,21 It is reasonable to as-sume that only patients who experience postoperative refractoryintracranial hypertension will benefit from an additional decom-pressive craniectomy. A number of clinical factors influence post-operative ICP levels, including brain oedema caused by blooddegradation products and surgical trauma, rebleeding of rupturedvessels, mass effect of residual haematoma, obstructive hydro-cephalus caused by intraventricular extension of the haematoma,and unfavourable systemic factors. The formation of brain oedema,as an important prognostic factor in patients with spontaneous

ICH,22 has been the subject of numerous studies.23–25 Althoughearly haematoma evacuation attenuates brain oedema forma-tion,26 the adequacy of this procedure to maintain an acceptablepostoperative ICP remains unknown. In this study, patients withpreoperative transtentorial herniation were more likely to developsevere brain swelling after clot removal, resulting in refractoryintracranial hypertension. The incidence of postoperative refrac-tory intracranial hypertension in patients with a unilateral fixed di-lated pupil and in those with bilateral fixed dilated pupils was 25%(two of eight) and 75% (three of four), respectively. Further analysisrevealed that the patients with preoperative clinical transtentorialherniation had larger haematomas and lower GCS scores prior tosurgery than patients without signs of herniation. These findingssuggest that the preoperative presence of clinical transtentorialherniation is associated with a more severe primary injury to thebrain and may serve as a predictor for the development of postop-erative refractory intracranial hypertension.

The ICH score is a simple and reliable clinical grading scale forICH that stratifies patients based on 30-day mortality. The scoreis comprised of five components: (i) GCS score (3 or 4 = 2 points,5–12 = 1 point, 13–15 = 0 points); (ii) age P80 years (yes = 1,no = 0); (iii) infratentorial origin (yes = 1, no = 0); (iv) ICH volume(P30 mL = 1, < 30 mL = 0); and (v) IVH (yes = 1, no = 0). The ICHscore can range from zero to six, and an increase in the ICH scorepredicts an increase in the likelihood of 30-day mortality.27 Inthe initial study, the survival rate of patients with an ICH scoreof three was only 28%, whereas it was 94% (17 of 18 patients) inthis study. The difference in survival rate may be due to the carefulselection of surgical candidates in this study. Murthy et al. per-formed haematoma evacuation and decompressive craniectomyin a similarly selected group of patients who had large putaminalhaematomas, and the survival rate of the patients with an ICHscore of three was 90% (nine of 10 patients).8 These findings sup-port the view that performing an additional decompressive crani-ectomy after haematoma evacuation in patients without signs oftranstentorial herniation does not significantly improve the sur-vival rate.

Fig. 1. Graph showing changes in the mean daily intracranial pressure (ICP) values over the first week after surgery in patients with hypertensive putaminal haemorrhage. (A)Patients with preoperative clinical transtentorial herniation (Group 1) had higher ICP values than those without signs of herniation (Group 2). (B) No significant differences inICP values after surgery were observed between the patients treated using the transsylvian approach (Group 3) and those treated with the transcortical approach (Group 4).Error bars indicate standard errors. ⁄p < 0.05, ⁄⁄p < 0.01, ns = not significant.

Table 2Mean intracranial pressure for the first seven days after surgery in patients with putaminal hypertensive haemorrhage following haematoma removal

Intracranial pressure for 7 days after surgery (mmHg)

0 1** 2** 3** 4** 5* 6* 7*

TH (n = 12) 2.8 ± 1.6 9.8 ± 4.0 11.5 ± 3.5 18.9 ± 6.6 22.6 ± 10.2 24.5 ± 12.9 25.5 ± 16.0 25.6 ± 18.5No TH (n = 10) 2.6 ± 1.2 5.0 ± 1.3 7.4 ± 1.1 9.4 ± 2.3 12.2 ± 2.9 14.4 ± 2.7 13.6 ± 2.8 12.1 ± 2.0

TH = preoperative clinical transtentorial herniation.* p < 0.05.** p < 0.01.

Fig. 2. Axial head CT scans from the illustrative patient at the level of the lateral ventricles (top row) and basal cisterns (bottom row) before and after surgery. With optimalmedical treatment, no severe brain swelling was observed. The subdural intracranial pressure sensor is not visible in these planes.

978 K. Wang et al. / Journal of Clinical Neuroscience 19 (2012) 975–979

K. Wang et al. / Journal of Clinical Neuroscience 19 (2012) 975–979 979

The International Surgical Trial in Intracerebral Haemorrhageshowed that early surgical treatment for patients with ICH offersno significant benefit compared to initial conservative treatmentwith respect to six-month outcomes, which justifies initial conser-vative treatment for patients with ICH if the neurosurgeon isuncertain about the benefits of surgical treatment.14 Althoughmany clinical characteristics were balanced between the patientsrandomized to early surgery and those randomized to initial con-servative treatment, there was no indication that ICP was balancedbetween the two groups. Given that elevated ICP is associated withan increased risk of a poor outcome in patients with ICH,28 and thatdecreasing intracranial hypertension is the main goal of surgicaltreatment, it is reasonable to suggest that early surgical treatmentwill be beneficial for ICH patients with elevated ICP. In this study,all patients underwent surgery within 24 hours after ictus. Duringthe operation, all had a tense dura before clot removal, suggestinghigh ICP, and the brain and dura slackened once the haematomawas evacuated. We believe that early evacuation of haematomascausing elevated ICP contributed to acceptable postoperative ICPlevels in a large proportion (77.3%) of our patients and the rela-tively high survival rate (90.1%).

Our study has some limitations. This series of surgical haema-toma evacuation surgeries without decompressive craniectomy issmall and selected. Only patients expected to have a good chanceof recovery were offered surgery, as suggested by the relativelyyoung age of the patients. Despite these limitations, our studyindicates that microsurgical removal of hypertensive putaminalhaematomas is effective and adequate for patients without preop-erative transtentorial herniation with regards to postoperative ICPmanagement. However, the preoperative presence of clinical trans-tentorial herniation may predict the development of postoperativerefractory intracranial hypertension, which may require an addi-tional decompressive craniectomy after clot removal.

Acknowledgement

This study is funded by the Youth Foundation of Tongji Univer-sity, Shanghai, China. It is also partly supported by the NationalNatural Science Foundation of China (No. 81101909).

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