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Peter Hutchinson, Ivan Timofeev, and Peter Kirkpatrick

✓Brain edema is a common pathophysiological process seen in many neurosurgical conditions. It can be localized in relation to focal lesions or generalized in diffuse types of brain injury. In addition to local adverse effects occurring at a cellular level, brain edema is associated with raised intracranial pressure (ICP), and both phenomena contribute to poor outcome in patients. One of the goals in treating patients with acute neurosurgical conditions in intensive care is to control brain edema and maintain ICP below target levels. The mainstay of treatment is medical therapy to reduce edema, but in certain patients—for example, those with diffuse severe traumatic brain injury (TBI) and malignant middle cerebral artery infarction—such treatment is not effective. In these patients, opening the skull (decompressive craniecto-my) to reduce ICP is a potential option. In this review the authors discuss the role of decompressive craniectomy as a surgical option in patients with brain edema in the context of a variety of pathological entities. They also address the current evidence for the technique (predominantly observational series) and the ongoing randomized studies of decompressive craniectomy in TBI and ischemic stroke.

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Paul S. Slosberg

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Carole L. Turner, Susan Tebbs, Piotr Smielewski, and Peter J. Kirkpatrick

Object. Applanation tonometry is a noninvasive method of assessing both peripheral and central arterial blood pressure (BP) profiles. In this study the authors examine whether there are differences in these profiles in patients with intracranial aneurysms when compared with age-matched controls.

Methods. Carotid artery (CA) and derived aortic BP waveforms were obtained using a pulse wave analysis system. The ratio of the pressure wave amplitude above the systolic shoulder to the total systolic BP (augmentation index [AI]) was recorded.

One hundred seventy-three patients with intracranial aneurysms (23 unruptured lesions) and 173 healthy control volunteers were examined. For the patients with aneurysms the right and left CA AIs (mean ± standard deviation) were 125.6 ± 23.1% and 128.3 ± 22.1%, respectively. Corresponding values for the control group were 118.4 ± 22.6% and 119.4 ± 21.8%. The calculated AI for the ascending aorta was 29.8 ± 10.5% and 25.6 ± 12.2% for patients with aneurysms and control volunteers, respectively. Significant asymmetry in CA AI was seen in patients with aneurysms, the left being greater (p = 0.002). No significant differences were seen in mean BP (108 ± 14 mm Hg in patients with aneurysms compared with 106 ± 16 mm Hg in controls; p = 0.2). Multivariate analysis excluded the influence of BP and other potential confounding vascular risk factors for increased AI.

Conclusions. Significant differences in AI, both in magnitude and symmetry, were identified in patients with intracranial aneurysms when compared with matched controls.

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Ming-Yuan Tseng, Peter J. Hutchinson, and Peter J. Kirkpatrick

Object

In a previous randomized controlled trial, the authors demonstrated that acute erythropoietin (EPO) therapy reduced severe vasospasm and delayed ischemic deficits (DIDs) following aneurysmal subarachnoid hemorrhage. In this study, the authors aimed to investigate the potential interaction of neurovascular protection by EPO with age, sepsis, and concurrent statin therapy.

Methods

The clinical events of 80 adults older than 18 years and with < 72 hours of aneurysmal subarachnoid hemorrhage, who were randomized to receive 30,000 U of intravenous EPO-β or placebo every 48 hours for a total of 3 doses, were analyzed by stratification according to age (< or ≥ 60 years), sepsis, or concomitant statin therapy. End points in the trial included cerebral vasospasm and impaired autoregulation on transcranial Doppler ultrasonography, DIDs, and unfavorable outcome at discharge and at 6 months measured with the modified Rankin Scale and Glasgow Outcome Scale. Analyses were performed using the t-test and/or ANOVA for repeated measurements.

Results

Younger patients (< 60 years old) or those without sepsis obtained benefits from EPO by a reduction in vasospasm, impaired autoregulation, and unfavorable outcome at discharge. Compared with nonseptic patients taking EPO, those with sepsis taking EPO had a lower absolute reticulocyte count (nonsepsis vs sepsis, 143.5 vs. 105.8 × 109/L on Day 6; p = 0.01), suggesting sepsis impaired both hematopoiesis and neurovascular protection by EPO. In the EPO group, none of the statin users suffered DIDs (p = 0.078), implying statins may potentiate neuroprotection by EPO.

Conclusions

Erythropoietin-related neurovascular protection appears to be attenuated by old age and sepsis and enhanced by statins, an important finding for designing Phase III trials.

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Nahal Mavaddat, Barbara J. Sahakian, Peter J. A. Hutchinson, and Peter J. Kirkpatrick

Object. This study was conducted to define neuropsychological changes following operation for subarachnoid hemorrhage (SAH) caused by rupture of an anterior communicating artery (ACoA) aneurysm and to assess the influence of the timing of surgery to clip the aneurysm.

Methods. Cognitive outcome was evaluated using the Cambridge Neuropsychological Test Automated Battery in patients with an ACoA aneurysm that had caused an SAH. Adult patients younger than 70 years of age who had achieved a favorable neurological outcome (Glasgow Outcome Scale scores of 4 or 5) were studied 6 to 24 months postsurgery. Patients were divided into early (Days 0–3) and late surgery groups (after Day 3) according to the timing of surgery after the ictus. Neuropsychological analysis was performed by reviewers who were blinded to the timing of surgery.

Forty-seven patients whose mean age was 51.5 years were tested. They were compared with age- and intelligence quotient (IQ)—matched controls by using premorbid IQ as estimated on the National Adult Reading Test. Patients showed deficiencies in several tasks of verbal fluency, pattern recognition, and spatial working memory; this profile of deficits was similar to that seen in patients who underwent temporal lobe excisions. However, there was no significant difference in cognitive performance between the early and late surgery groups.

Conclusions. After open surgery for ruptured ACoA aneurysms, patients who have achieved a favorable neurological outcome still exhibit significant cognitive deficits, primarily in tests sensitive to temporal lobe dysfunction. However, early surgery does not carry a higher risk of neuropsychological disability.

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Ivan Timofeev, Marek Czosnyka, Jurgens Nortje, Peter Smielewski, Peter Kirkpatrick, Arun Gupta, and Peter Hutchinson

Object

Decompressive craniectomy is an advanced treatment option for intracranial pressure (ICP) control in patients with traumatic brain injury. The purpose of this study was to evaluate the effect of decompressive craniectomy on ICP and cerebrospinal compensation both within and beyond the first 24 hours of craniectomy.

Methods

This study was a retrospective analysis of the physiological parameters from 27 moderately to severely head-injured patients who underwent decompressive craniectomy for progressive brain edema. Of these, 17 patients had undergone prospective digital recording of ICP with estimation of ICP waveform–derived indices. The pressure-volume compensatory reserve (RAP) index and the cerebrovascular pressure reactivity index (PRx) were used to assess those parameters. The values of parameters prior to and during the 72 hours after decompressive craniectomy were included in the analysis.

Results

Decompressive craniectomy led to a sustained reduction in median (interquartile range) ICP values (21.2 mm Hg [18.7; 24.2 mm Hg] preoperatively compared with 15.7 mm Hg [12.3; 19.2 mm Hg] postoperatively; p = 0.01). A similar improvement was observed in RAP. A significantly lower mean arterial pressure (MAP) was needed after decompressive craniectomy to maintain optimum cerebral perfusion pressure (CPP) levels, compared with the preoperative period (99.5 mm Hg [96.2; 102.9 mm Hg] compared with 94.2 mm Hg [87.9; 98.9 mm Hg], respectively; p = 0.017). Following decompressive craniectomy, the PRx had positive values in all patients, suggesting acquired derangement in pressure reactivity.

Conclusions

In this study, decompressive craniectomy led to a sustained reduction in ICP and improvement in cerebral compliance. Lower MAP levels after decompressive craniectomy are likely to indicate a reduced intensity of treatment. Derangement in cerebrovascular pressure reactivity requires further studies to evaluate its significance and influence on outcome.

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Carole L. Turner, Ian B. Wilkinson, and Peter J. Kirkpatrick

Object

Patients with intracranial aneurysms tend toward raised blood pressure and abnormal pulse pressure profiles. The authors have investigated the influence of three antihypertension agents on blood pressure and pulse pressure waveforms in patients with known intracranial aneurysms, with a view to assessing the potential benefits of longterm antihypertension therapy on the progression of unruptured intracranial aneurysms.

Methods

Nineteen patients with a mean age of 56 years (range 38–76 years) were recruited for this study. All patients had confirmed intracranial aneurysms. A double-blind, randomized, crossover study was performed using perindopril, irbesartan, isosorbide mononitrate, and a placebo. Blood pressure and pulse pressure waveforms were assessed at the end of each 4-week treatment period.

Perindopril and irbesartan were well tolerated. For all measured parameters except heart rate (p = 0.03), no significant difference between baseline and placebo was identified. Each drug when compared with placebo reduced peripheral arterial blood pressure. Perindopril significantly decreased mean blood pressure by 10 mm Hg (p = 0.004), irbesartan by 9 mm Hg (p = 0.004), and isosorbide mononitrate by 13 mm Hg (p = 0.005).

The administration of each drug effected a significant reduction in the carotid artery augmentation index (AIX) compared with baseline values (perindopril p = 0.01, irbesartan p = 0.0002, and isosorbide mononitrate p = 0.03). There was also a significant difference in the AIX between irbesartan and the placebo (p = 0.05). Compared with the placebo, there was a significant difference in AIX (adjusted for heart rate) following the administration of irbesartan (p = 0.003) and isosorbide mononitrate (p = 0.01), but not with perindopril (p = 0.17).

Conclusions

Irbesartan appears to be the most effective treatment for the combined suppression of blood pressure and AIX in patients with intracranial aneurysms and has a high degree of patient tolerance.

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Piotr Smielewski, Marek Czosnyka, Peter Kirkpatrick, and John D. Pickard

✓ The transient hyperemic response test has been shown to provide an index of cerebral autoregulation in healthy individuals and in patients who have suffered a subarachnoid hemorrhage. In this study, the test was applied to patients who had received a severe head injury, and the value of the test was assessed by comparing its result with the individual's clinical condition (Glasgow Coma Scale [GCS] score), cerebral perfusion pressure (CPP), transcranial Doppler wave form—derived index for cerebral autoregulation (relationship between the CPP and the middle cerebral artery flow velocity), and outcome (Glasgow Outcome Scale [GOS] score).

Forty-seven patients, aged 16 to 63 years, with head injuries were included in the study. Signals of intracranial pressure, arterial blood pressure, flow velocity, and cortical microcirculatory flux were digitized and recorded for a period of 30 minutes using special computer software. Two carotid compressions were performed at the beginning of each recording. The transient hyperemic response ratio (THRR: the ratio of the hyperemic flow velocity recorded after carotid release and the precompression baseline flow velocity) was calculated, as was the correlation coefficient Sx used to describe the relationship between slow fluctuations in the systolic flow velocity and CPP throughout the period of recording.

No significant changes in CPP were found during compression. There was a significant correlation between the THRR and the Sx (r = 0.49, p < 0.0001). The hyperemic response proved to be lower in patients who exhibited a poor clinical grade at presentation (GCS scores < 6, p = 0.01) and lower in patients achieving a poor outcome (GOS scores of 3, 4, and 5, p = 0.003). Loss of postcompression hyperemia occurred when the CPP fell below 50 mm Hg.

The carotid compression test provides a simple index of cerebral autoregulation that is relevant to the clinical condition and outcome of the severely head injured patient.

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Peter J. Kirkpatrick, Joseph Lam, Pippa Al-Rawi, Piotr Smielewski, and Marek Czosnyka

Object. Signal changes in adult extracranial tissues may have a profound effect on cerebral near-infrared spectroscopy (NIRS) measurements. During carotid surgery NIRS signals provide the opportunity to determine the relative contributions from the intra- and extracranial vascular territories, allowing for a more accurate quantification. In this study the authors applied multimodal monitoring methods to patients undergoing carotid endarterectomy and explored the hypothesis that NIRS can define thresholds for cerebral ischemia, provided extracranial NIRS signal changes are identified and removed. Relative criteria for intraoperative severe cerebral ischemia (SCI) were applied to 103 patients undergoing carotid endarterectomy.

Methods. One hundred three patients underwent carotid endarterectomy. An intraoperative fall in transcranial Doppler—detected middle cerebral artery flow velocity (%ΔFV) of greater than 60% accompanied by a sustained fall in cortical electrical activity were adopted as criteria for SCI. Ipsilateral frontal NIRS recorded the total difference in concentrations of oxyhemoglobin and deoxyhemoglobin (Total ΔHbdiff). Interrupted time series analysis following clamping of the external carotid artery (ECA) and the internal carotid artery (ICA) allowed the different vascular components of Total ΔHbdiff (ECA ΔHbdiff and ICA ΔHbdiff) to be identified.

Data obtained in 76 patients were deemed suitable. A good correlation between %ΔFV and ICA ΔHbdiff (r = 0.73, p < 0.0001) was evident. Sixteen patients (21%) fulfilled the criteria for SCI. All patients who demonstrated an ICA ΔHbdiff of greater than 6.8 µmol/L showed SCI, and in two patients within this group nondisabling watershed infarction developed, as seen on postoperative computerized tomography scans. No patient with an ICA ΔHbdiff less than 5 µmol/L exhibited SCI or suffered a stroke. Within the resolution of the criteria used an ICA ΔHbdiff threshold of 6.8 µmol/L provided 100% specificity for SCI, whereas an ICA ΔHbdiff less than 5 µmol/L was 100% sensitive for excluding SCI. When Total ΔHbdiff was used without removing the ECA component, no thresholds for SCI were apparent.

Conclusions. Carotid endarterectomy provides a stable environment for exploring NIRS-quantified thresholds for SCI in the adult head.