Intensive Care Med (2006) 32:1606–1612 DOI 10.1007/s00134-006-0285-4
Kevin P. Morris Robert J. Forsyth Roger C. Parslow Robert C. Tasker Carol A. Hawley UK Paediatric Traumatic Brain Injury Study Group Paediatric Intensive Care Society Study Group
Received: 23 July 2005 Accepted: 20 June 2006 Published online: 28 July 2006 © Springer-Verlag 2006 This study was supported by grants from the Paediatric Intensive Care Society, Birmingham Children’s Hospital Research Foundation and the Warwick University Research and Teaching Development Fund. K. P. Morris (u) Diana Princess of Wales Children’s Hospital, Steelhouse Lane, B4 6NH Birmingham, UK e-mail:
[email protected] Tel.: +44-121-3339673 Fax: +44-121-3339651 R. J. Forsyth Sir James Spence Institute of Child Health, Royal Victoria Infirmary, Child Health, School of Clinical Medical Sciences, NE1 4 lP Newcastle upon Tyne, UK R. C. Parslow Leeds Institute of Genetics, Health and Therapeutics, University of Leeds, Paediatric Epidemiology Group, Centre for Epidemiology and Biostatistics, 30 Hyde Terrace, LS2 9JT Leeds, UK R. C. Tasker Addenbrooke’s Hospital, Cambridge University Clinical School, Hills Rd, CB2 2QQ Cambridge, UK C. A. Hawley Warwick Medical School, University of Warwick, Division of Health in the Community, CV4 7AL Coventry, UK
PE D I A T R I C O R I G I N A L
Intracranial pressure complicating severe traumatic brain injury in children: monitoring and management
Abstract Objective: To identify factors associated with the use of intracranial pressure (ICP) monitoring and to establish which ICP-targetted therapies are being used in children with severe traumatic brain injury (TBI) in the United Kingdom. To evaluate current practice against recently published guidelines. Design and setting: Prospective data collection of clinical and demographic information from paediatric and adult intensive care units in the UK and Ireland admitting children (< 16 years) with TBI between February 2001 and August 2003. Results: Detailed clinical information was obtained for 501 children, with information on the use of ICP monitoring available in 445. ICP monitoring was used in only 59% (75/127) of children presenting with an emergency room Glasgow Coma Scale of 8 or below. Large between centre variation was seen in the use of ICP monitoring, independent of severity of injury. There were 86 children who received ICP-targetted therapies without ICP monitoring. Wide between centre variation was found in the use of ICP-targetted therapies and in general aspects of management, such as fluid restriction, the use of muscle relaxants and prophylactic anticonvulsants. Intraventricular catheters are rarely placed
(6% of cases); therefore cerebrospinal fluid drainage is seldom used as a first-line therapy for raised ICP. Jugular venous bulb oximetry (4%), brain microdialysis (< 1%) and brain tissue oxygen monitoring (< 1%) are rarely used in current practice. Contrary to published guidelines, moderate to severe hyperventilation is being used without monitoring for cerebral ischaemia. Conclusions: There is an urgent need for greater standardisation of practice across UK centres admitting children with severe TBI. Keywords Traumatic brain injury · Children · Intensive care · Intracranial pressure · Treatment · Monitoring
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Introduction The United Kingdom Paediatric Traumatic Brain Injury (TBI) Study Group was established in 1999 with the intention of promoting multi-centre interdisciplinary research aimed at improving the outcome of children who have suffered a head injury. As a first step it was decided to conduct a prospective data collection across the UK of children with TBI admitted to an intensive care unit. This study had three purposes. First, the exercise would test whether it is feasible to collect a large volume of data through an organisation with strong commitment but limited resources. Second, the information would provide a unique epidemiological picture of severe TBI in children and of contemporary practice across the UK, the first such database of paediatric TBI in the UK. Third, the results would be invaluable for informing future clinical trials. The need to prevent raised intracranial pressure (ICP) is recognised as central to current intensive care practice. Previous questionnaire surveys of both adult and paediatric physicians have highlighted wide variation in the use of ICP monitoring and in the management of raised ICP [1, 2], but questionnaire surveys are based on physician recall and do not necessarily provide a true reflection of actual practice. Prospective studies in adults with TBI have confirmed considerable centre to centre variation [3]. We analysed data from the national database with the aim of identifying factors that are associated with the use of ICP monitoring and the secondary aim of establishing which ICP-targetted therapies are being used in children with severe TBI. We have related our findings to the recommendations made in the recently published ‘Guidelines for the acute medical management of severe traumatic brain injury in infants, children, and adolescents’ [4].
Methods and materials Detailed methods have been reported elsewhere [5]. In summary, a clinician or nurse at each participating centre provided anonymised data for each child under 16 years of age admitted primarily for the management of a traumatic brain injury to one of 28 participating paediatric intensive care units (PICUs) in England, Wales, Scotland, Northern Ireland and the Republic of Ireland over a rolling 12-month period. In most centres this was 1 April 2001–31 March 2002. A total of 721 children were identified across the data collection period. Detailed clinical abstracts were returned on 501 children (69%), who form the basis for this analysis. As a result of unknown data items, missing data items and subgroup analysis the precise denominator varied for individual analyses.
Two clinical abstracts were prepared prospectively for each child. The first detailed information available within 24 h of admission including demographics, mechanism of injury, pre-admission management, Glasgow Coma Score (GCS), surgical procedures and computed tomography (CT) findings. A second abstract was prepared at discharge from the intensive care unit and included data on monitoring modalities, medical interventions, any further surgical procedures and subsequent CT findings. In addition we asked whether a patient was enrolled into a trial and whether inclusion in the trial could affect the data items being collected. We identified 44 children (9%) as being enrolled in a research trial but in only 13 (3%) was it felt that the responses given for this study could be affected by inclusion in the trial. These cases were therefore included in the analysis. Ethical approval for data collection was obtained from the West Midlands Multicentre Research Ethics Committee; approval was additionally gained from the Local Research Ethics Committee for each participating ICU. In addition limited data on children under 16 years admitted with TBI as the primary reason for admission to 48 adult ICUs were obtained from the Intensive Care National Audit Research Centre (ICNARC) for the period 1 April 2001–31 March 2002. A cross-check identified children who were transferred from an adult ICU to a PICU to avoid double-counting. No data relating to the use of ICP monitoring or use of ICP-targetted therapies was available for the group of children who were managed exclusively in an adult ICU. Data items used for this report were use of ICP monitoring, mode of ICP monitoring, presence of raised ICP, use of other modalities of brain monitoring (microdialysis, jugular venous oximetry, brain tissue oxygenation), use of invasive haemodynamic monitoring (arterial line, central line) and the use of different therapies. Raised ICP was defined as a level higher than 20 mmHg on more than 1 hourly recording at any point during ICU stay. This threshold is consistent with the United States guidelines [4]. ICP-targetted therapies were classified as first- or second-tier therapies [4]. First-tier therapies were mannitol, hypertonic saline, mild hyperventilation (PaCO2 4.0–4.5 kPa) and cerebrospinal fluid (CSF) drainage. Second-tier therapies were barbiturates, hypothermia, moderate (3.5–3.9 kPa) or severe hyperventilation (< 3.5 kPa). In addition we looked separately at children undergoing decompressive craniectomy. General therapeutic approaches were also included such as the use of fluid restriction, artificial ventilation, muscle relaxants, steroids, prophylactic anticonvulsants and inotropes or vasopressors. Findings on cerebral CT were noted. CT findings were defined as abnormal if they demonstrated intracranial haemorrhage (extradural, subdural, subarachnoid, intracerebral), diffuse axonal injury, or features of
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cerebral oedema (reduced grey/white differentiation, compressed lateral ventricles or basal cisterns, midline shift). In order to contrast the use of ICP targetted therapies across different centres in comparable patients we defined a ‘severe TBI’ group to include children with GCS of 8 or below in the accident and emergency department and those children requiring intubation and ventilation pre-hospital or in the accident and emergency department in whom no GCS was recordable. For statistical analysis, ICP monitoring (yes/no) was entered as the dependent variable in a random effects logistic regression analysis with the following independent variables: age, sex, emergency department GCS score, pupil reactivity, CT abnormality, admitting centre, and the need for a neurosurgical procedure within 24 h of injury. A random effects model was used to allow for variability between admitting centres. In a separate multiple regression analysis ICU length of stay was the dependent variable with the following independent factors: emergency department GCS, age, sex, mechanism of injury, pupil reactivity, CT abnormality, need for a neurosurgical procedure within 24 h of injury, ICP monitoring and development of raised ICP. Kaplan-Meier ‘survival’ plots were produced for ICU length of stay, with Cox regression used to derive length of stay hazard ratios for the groups: (a) ICP monitored and raised, (b) ICP monitored but normal and (c) ICP not monitored. All statistical analyses were performed using Stata version 8.2.
Fig. 1 Illustration of the variation in use of ICP monitoring, ICP therapies and general therapies across 12 centres admitting more than ten cases of severe TBI (n = 168). For each centre the percentage of patients in whom each intervention was used is calculated. The data are shown as box plots, with the median value representing practice at the centre with the median use of each intervention, and low and high outliers representing practice at centres with the lowest and greatest use of each intervention, respectively
Results Monitoring ICP monitoring Information relating to the use of ICP monitoring was recorded in 445 cases. ICP monitoring was undertaken in 45% of cases (199/445). ICP monitoring was more common in those with an emergency room GCS of 8 or below (59%, 75/127) than in those with GCS 9–12 (38%, 30/80) or GCS 13–15 (22%, 22/98). The US guidelines recommend that ICP monitoring be undertaken in all children with an admission GCS of 8 or below. ICP monitoring was also more common in the group of children in whom GCS could not be assessed accurately in accident and emergency departments (51%, 72/140). This group comprised children who were intubated or had received sedation or muscle relaxants. ICP monitoring was more common in those with an abnormal admission CT (56%, 156/282) than in those with a normal initial CT (26%, 43/163). We found large between centre variation in the proportion of cases undergoing ICP monitoring (7–100% of cases within each centre). This persisted when only the 212 cases meeting the definition of ‘severe TBI’ cases were analysed (7–100% of cases within each centre; Fig. 1). The random effects logistic model confirmed a strong admitting centre effect on ICP monitoring rates (lr test χ2 = 37.8, 1 df,
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Table 1 Random effects model for use of ICP monitoring (n = 331). Glasgow Coma Score (GCS) refers to that measured in the accident and emergency department. Baseline categories for the analysis were GCS 13–15 and age 10–14 years. In addition to the significance of GCS, age and CT abnormality, a strong admitting centre effect was found (ρ = 0.293, likelihood ratio test p < 0.001, χ 2 = 37.8) (OR odds ratio, CI confidence interval)
GCS ≤ 8 GCS 9–12 GCS unrecordable Age ≤ 1 year Age 1–4 years Age 5–10 years Age > 14 years CT abnormality Neurosurgical procedure first 24 h Pupil(s) unreactive first 24 h
OR
p
95% CI
4.67 2.20 4.13 0.08 1.27 0.99 0.62 3.89 1.05
0.000 0.09 0.001 0.001 0.53 0.97 0.47 0.000 0.90
2.00–10.86 0.88–5.49 1.77–9.67 0.02–0.36 0.60–2.72 0.51–1.92 0.17–2.24 1.98–7.64 0.50–2.21
1.60
0.21
0.77–3.31
p < 0.001). Inter-centre variation accounted for 29% of the overall variance in the model. In addition the model confirmed greater use of ICP monitoring in the group with an emergency department GCS of 8 or below in those in whom GCS could not be assessed in the emergency department, and those with abnormalities on CT. ICP monitoring was used less in children below the age of 1 year (Table 1). There was considerable variation in the mode of ICP monitoring reported, with the most common being parenchymal catheter placement (50%, 100/198), followed by subdural (29%, 57/198), extradural (15%, 30/198) and intraventricular (6%, 11/198). Only two centres reported use of intraventricular monitoring. Multi-modality brain monitoring Additional brain monitoring was undertaken infrequently; jugular venous oximetry in 4% of cases (n = 20) in seven centres, microdialysis in only two cases in one centre, and brain tissue oxygenation monitoring in two cases in two centres. Invasive haemodynamic monitoring Accurate assessment of cerebral perfusion pressure requires invasive arterial pressure monitoring as well as ICP monitoring. Invasive arterial pressure monitoring was undertaken in 87% (390/450) of total cases and 94% (200/212) of cases classified as severe TBI. A central venous line was placed in 52% (232/444) of total cases and 66% (139/212) of severe TBI cases.
Between centre variation in management of ICP and general management To allow for between-centre variation in the GCS threshold for ICU admission this analysis was confined to ‘severe TBI’ cases in 12 centres admitting ten or more ‘severe’ cases and includes cases with and without ICP monitoring (n = 168). Wide variation in every aspect of practice was evident (Fig. 1). Use of mannitol was recorded in 43% (73/168) of cases, with considerable variation across centres (range 7–77% of cases within each centre). Of these, 92% (155/168) were managed with some degree of hyperventilation (range 50–100% of cases within each centre), and 14% (24/168) barbiturate therapy (range 0–27% of cases within each centre). Fluid restriction was used in 58% (98/168) of severe TBI cases, with considerable variation across centres (0–100% of cases within each centre). The restriction was moderate (51–75% of normal fluids) in 70% of these cases and severe (< 50% of normal fluids) in 30% of cases. Management of raised ICP Of the 199 children in whom ICP was monitored 98 (49%) developed raised ICP. Complete data relating to ICP therapies was available for 90 of the 98 cases. First-tier therapies were used in 99% (89/90) of cases. Figure 2a shows the frequency with which individual therapies and combinations of therapies were used. We did not specifically collect data relating to the order with which therapies were used. The US guidelines suggest that the initial ICP specific therapeutic intervention be CSF drainage when ventricular access is available. CSF drainage was used in only 16% (14/90) of UK cases, and all cases received at least one other first-tier therapy, suggesting that CSF drainage is not being employed as a first-line therapy. Hyperosmolar therapy is recommended as the next line therapy in the US guidelines, with the choice between mannitol and hypertonic saline left to the clinician. Hyperosmolar therapy was used in 87% (78/90) of cases, with mannitol use (78%, 70/90) exceeding hypertonic saline use (36%, 32/90). Mild hyperventilation was used in 83% (75/90) of cases, frequently in combination with hyperosmolar therapy (72%, 65/90). Figure 2a suggests that there is no consistency of practice with respect to whether hyperosmolar therapy or mild hyperventilation is employed as the first intervention. Second-tier therapies were used in 54% (49/90) of children with raised ICP (Table 2). The US guidelines do not make recommendations concerning the order with which these therapies should be employed. Barbiturates were used in 36% (32/90) of cases, moderate or severe hyperventilation in 27% (24/90), hypothermia in 24% (22/90) and decompressive craniectomy in 10% (9/90). Figure 2b shows the frequency with which individual
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therapies and combinations of therapies were used and suggests a lack of consistency of practice in terms of the order in which they are employed. Therapeutic hypothermia was employed in only six centres, most frequently mild hypothermia (34–36 °C; 77%, 17/22) rather than moderate hypothermia (32–34 °C; 23%, 5/22). Eight of nine cases undergoing decompressive craniectomy received at least one other second-tier therapy, suggesting that decompressive craniectomy is being undertaken once other therapies have been used. For the purposes of this study raised ICP was recorded when ICP was higher than 20 mmHg on more than 1 hourly recording at any point during ICU stay. There were 101 children in whom ICP was monitored who did not fulfil this definition. Complete data relating to ICP therapies were available for 87 of these 101 cases. Firsttier therapies were used in 51% (44/87) of cases in this group and second-tier therapies in 12% (10/87; Table 2), suggesting that a proportion of these children may have experienced raised ICP of insufficient duration to meet the definition. Alternatively centres may be employing these therapies at an ICP threshold below 20 mmHg, as suggested by an earlier survey [2].
Use of ICP-targetted therapies without ICP monitoring ICP was not monitored in 246 children. Despite this firsttier therapies were used in 86 children (35%) and secondtier in 21 (9%; Table 2).
ICU length of stay
Fig. 2 Venn diagrams showing the use of first-tier ICP-targetted therapies in 89 children with raised ICP and complete data relating to use of first-tier therapies (a) and the use of second-tier ICP-targetted therapies in 49 children with raised ICP and complete data relating to use of second-tier therapies (b) Table 2 Use of ICP-targetted therapies in children undergoing ICP monitoring, with and without raised ICP, and in children in whom ICP monitoring was not instituted. Only cases with complete data relating to ICP therapies have been included
Independent risk factors for longer length of stay were GCS score below 8 (p = 0.005) or unrecordable GCS (p = 0.001), abnormal CT (p < 0.001), fixed pupil(s) (p < 0.001), and raised ICP (p < 0.001). In addition patients with a normal ICP on monitoring also had a longer length of stay than those in whom ICP was not monitored ICP monitoring
First-tier ICP therapies CSF drainage Mannitol Hypertonic saline Mild hyperventilation Second-tier ICP therapies Barbiturates Hypothermia Moderate, severe hyperventilation
No ICP monitoring (n = 246)
ICP raised (n = 90) n %
ICP not raised (n = 87) n %
n
%
14 70 32 75
16 78 36 83
2 21 4 28
2 24 5 32
1 35 13 64
0.4 14 5 26
32 22 24
36 24 27
1 2 7
1 2 8
2 2 17
1 1 7
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Fig. 3 Kaplan Meier plots for time to discharge from ICU by ICP monitoring status and whether or not ICP was raised. Deaths are excluded. Using Cox regression both the high-ICP group (hazard ratio 0.26, p < 0.001) and the normal-ICP group (hazard ratio 0.60, p < 0.001) had a longer length of ICU stay than the unmonitored group
(p = 0.001; Fig. 3). Fall as the mechanism of injury was associated with a shorter length of stay (p = 0.04).
Discussion This study highlights the large variation in practice that exists across UK units admitting children with severe TBI. Variation is evident with respect to ICP monitoring, use of ICP-targetted therapies and areas of general management. Of particular concern is the use of ICP-targetted therapies in 86 children without ICP monitoring. The data were collected before publication of the US guidelines [4], the first published paediatric TBI guidelines. It is possible that publication of the guidelines will have resulted in a greater standardisation of approach, although certain areas of management such as fluid restriction and use of prophylactic anticonvulsants are not covered within the guidelines. Previous studies have shown that institutional variations in practice can have an effect on outcome of patients with severe TBI. Bulger et al. [6] compared the management and outcomes of 182 adult patients with severe TBI admitted to 33 US trauma centres. They defined ‘aggressive’ centres as those who instituted ICP monitoring in more than 50% of patients with a GCS below 8 and abnormal CT findings. Management at an aggressive centre was associated with a significant reduction in the risk of mortality and a shorter hospital length of stay for survivors. Tilford et al. [7] compared management and outcomes of 477 children with an admitting diagnosis of head trauma admitted to three US paediatric trauma centres. They found significant variation in the use of muscle relaxants, anticonvulsants, induced hypothermia, and ICP monitoring across
the three centres, with the use of anticonvulsants associated with a reduced risk of mortality. Just over one-half of children with severe TBI underwent ICP monitoring, with large between centre differences. TBI guidelines recommend intra-ventricular catheter placement as the most accurate, low cost, reliable method of ICP monitoring, with the additional benefit of allowing CSF drainage [4, 8]. We found a very low reported use of ventricular catheters and a higher than expected reported use of subdural and extradural catheter positions, methods that have been shown to be less accurate than parenchymal or ventricular placement [9, 10]. It was not possible to check the accuracy of reporting, and therefore we cannot rule out the possibility that parenchymal devices were in some cases described as subdural. The greater ICU length of stay associated with ICP monitoring could reflect the selective use of ICP monitoring in more severely injured children. However, the relationship between ICP monitor use and ICU length of stay persists after controlling for markers of injury severity and the presence of raised ICP. This suggests that ICP monitoring in less severely injured children may at times be unnecessarily delaying discharge from ICU. Robust criteria are needed for the prospective identification of children at significant risk of developing raised ICP. The management of raised ICP was found to be broadly consistent with US guidelines, although it is not possible to be confident about the order with which therapies are being used. The data would support the survey findings of Segal et al. [2], with hyperventilation used in some units as first line therapy ahead of hyperosmolar therapy. As a result of the infrequent use of ventricular catheters CSF drainage was rarely used and was never used as the sole ICP therapy. This suggests that some centres selectively place ventricular catheters in patients who demonstrate refractory intracranial hypertension. The US guidelines recommend that monitoring for cerebral ischaemia, such as jugular venous bulb oximetry, be used if ‘aggressive’ hyperventilation is employed to lower ICP; 75% of UK cases underwent moderate or severe hyperventilation without such monitoring. A small randomised controlled trial has suggested benefit for early decompressive craniectomy in children with raised ICP following TBI [11]. Decompressive craniectomy was undertaken only on nine occasions across the UK over the 1-year period of this study and appeared to be used later in patients with raised ICP despite first- and second-tier therapies. This study shows that it is feasible to collect a large volume of data through an organisation with strong commitment but limited resources. The study was inexpensive, as centres were offered minimal funding, and its success depended upon the commitment of the participants. Nevertheless the data returned were generally of high quality with regard to completeness of information. More than 90% of potential observations were completed, and data checking revealed few recordings outside specified ranges
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or showing obvious inconsistencies requiring referral back to the investigator for clarification. A limitation of the study was that no attempt could be made to confirm the accuracy of the data by comparison with original case records, as this process is extremely expensive in time and personnel. In addition our findings relate to those cases in which a detailed clinical abstract was completed, representing only 69% of the total cases admitted to participating units. Only two PICUs that admit children with TBI did not participate in the study. We think it unlikely that inclusion of additional cases from these centres would have altered the key conclusions of the study. A further limitation of the study was the reliance on intermittent hourly recording of ICP to define a group with raised ICP. It is conceivable that a number of additional children experienced ICP readings above 20 mmHg that were not captured on the hourly chart recordings.
Conclusions There is a need for greater standardisation of practice across UK centres admitting children with severe TBI. Less variation in management could have a beneficial effect on outcomes and would be essential, to reduce between centre heterogeneity, before embarking on multicentre trials.
Acknowledgements. We are grateful to all the staff of PICUs who completed data collection forms, to Dr. Kathy Rowan of ICNARC for supplying data on paediatric admissions to adult ICUs, and to Naveed Hussain, Helen Sherry and Neil Hallworth for database design, data entry and preliminary data processing. The UK Paediatric Traumatic Brain Injury Study Steering Group consists of: K. Morris (Chair), R. Appleton, M. Crouchman, R. Forsyth, C. Hawley, M. Marsh, P. May, P. McKinney, J. Middleton, R. Parslow, J. Punt, T. Ralph and R. Tasker. Participating centres and investigators were: Addenbrooke’s Hospital (R. Tasker), Alder Hey Children’s Hospital (R. Sarginson), Antrim Hospital (A. Ferguson), Beaumont Hospital, Dublin (E. Keane), Birmingham Children’s Hospital (K. Morris), Bristol Children’s Hospital (J. Fraser), City General Hospital, Stoke (J. Alexander), Derriford Hospital, Plymouth (S. Ferguson), Great Ormond St. Hospital (M. Kenny, D. Lutman), Guy’s Hospital (A. Durward), Hull Royal Infirmary (H. Klonin), John Radcliffe Hospital (A. Shefler, C. Killick), King’s College Hospital (D. Prior, l. Edwards, Y. Egberongbe), Leeds General Infirmary (T. Chater, M. Darowski), Leicester Royal Infirmary (P. Barry), Queen’s Medical Centre, Nottingham (P. Khandelwal), James Cook University Hospital (A. Robinson), Newcastle General Hospital (R. Forsyth), Royal Belfast Hospital for Sick Children (B. Taylor), Royal Berkshire Hospital (A. Maunganidze), Royal Devon & Exeter Hospital (J. Purday), Royal Hospital for Sick Children, Edinburgh (M. Lo, D. Simpson), Royal Hospital for Sick Children, Glasgow (P. Cullen), Royal London Hospital (P. Withington), Royal Manchester Children’s Hospital (D. Stewart, M. Samuels), Royal Preston Hospital (P. Tomlin), Sandwell Hospital (J. Bellin), Sheffield Children’s Hospital (T. Ralph), Southampton General Hospital (C. Boyles), Southern General Hospital, Glasgow (D. Snaddon, A. Wagstaff), St. Georges Hospital (S. Skellett), University Hospital of Wales (M. Gajraj), Walsgrave Hospital (M. Christie), Walton Centre for Neurosurgery (E. Wright).
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