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ORIGINAL PAPER The relationship between basal cisterns on CT and time-linked intracranial pressure in paediatric head injury Alison J. Kouvarellis & Ursula K. Rohlwink & Vishesh Sood & Devon Van Breda & Michael J. Gowen & Anthony A. Figaji Received: 31 March 2011 /Accepted: 11 April 2011 /Published online: 3 May 2011 # Springer-Verlag 2011 Abstract Purpose Although intracranial pressure (ICP) monitoring is a cornerstone of care for severe traumatic brain injury (TBI), the indications for ICP monitoring in children are unclear. Often, decisions are based on head computed tomography (CT) scan characteristics. Arguably, the patency of the basal cisterns is the most commonly used of these signs. Although raised ICP is more likely with obliterated basal cisterns, the implications of open cisterns are less clear. We examined the association between the status of perimesencephalic cisterns and time- linked ICP values in paediatric severe TBI. Methods ICP data linked to individual head CT scans were reviewed. Basal cisterns were classified as open or closed by blinded reviewers. For the initial CT scan, we examined ICP values for the first 6 h after monitor insertion. For follow-up scans, we examined ICP values 3 h before and after scanning. Mean ICP and any episode of ICP 20 mmHg during this period were recorded. Results Data from 104 patients were examined. Basal cisterns were patent in 51.72% of scans, effaced in 34.48% and obliterated in 13.79%. Even when cisterns were open, more than 40% of scans had at least one episode of ICP 20 mmHg, and 14% of scans had a mean ICP 20 mmHg. The specificity of open cisterns in predicting ICP<20 mmHg was poor (57.9%). Age-related data were worse. Conclusion Children with severe TBI frequently may have open basal cisterns on head CT despite increased ICP. Open cisterns should not discourage ICP monitoring. Keywords Basal cisterns . Traumatic brain injury . Children . Computed tomography . Head injury . Intracranial pressure monitoring Introduction Traumatic brain injury (TBI) is a major contributor to mortality and morbidity in both adults and children worldwide [14, 20]. The poor outcome associated with severe TBI may be improved by effective medical care, a large part of which is directed at preventing or ameliorating secondary insults, including raised intracranial pressure (ICP) [9, 10, 13, 28]. Increased ICP commonly occurs following TBI and may compromise brain perfusion by reducing cerebral perfusion pressure and exerting local tissue pressure effects. It is associated with disability, poor neurological outcome and decreased survival in TBI patients [2, 3, 6, 7, 17, 20, 23, 25]; therefore, monitoring and managing ICP effectively has become a cornerstone of treatment for severe TBI [1, 3, 5]. However, when to institute ICP monitoring in paediatric severe TBI is not well defined. The evidence base for an internationally accepted published recommendation for ICP monitoring in children with severe TBI was only sufficient to state that ICP monitoring was appropriate, and only at the level of an option. There was not enough support for a standard or guideline [3]. Even for these recommendations, much evidence was extrapolated from adult studies as very few data are available from paediatric studies. Not all children with severe TBI receive ICP monitoring [18]. An evaluation of TBI management practice in the UK found that only 59% of children presenting with a GCS 8 received ICP monitoring and that ICP treatment was administered in 41% of children in whom ICP was not A. J. Kouvarellis : U. K. Rohlwink : V. Sood : D. Van Breda : M. J. Gowen : A. A. Figaji (*) Division of Neurosurgery, School of Child and Adolescent Health, Red Cross War Memorial Childrens Hospital, University of Cape Town, Cape Town, South Africa e-mail: [email protected] Childs Nerv Syst (2011) 27:11391144 DOI 10.1007/s00381-011-1464-3

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Page 1: The relationship between basal cisterns on CT and time-linked intracranial pressure in paediatric head injury

ORIGINAL PAPER

The relationship between basal cisterns on CTand time-linkedintracranial pressure in paediatric head injury

Alison J. Kouvarellis & Ursula K. Rohlwink &

Vishesh Sood & Devon Van Breda & Michael J. Gowen &

Anthony A. Figaji

Received: 31 March 2011 /Accepted: 11 April 2011 /Published online: 3 May 2011# Springer-Verlag 2011

AbstractPurpose Although intracranial pressure (ICP) monitoring is acornerstone of care for severe traumatic brain injury (TBI), theindications for ICP monitoring in children are unclear. Often,decisions are based on head computed tomography (CT) scancharacteristics. Arguably, the patency of the basal cisterns isthe most commonly used of these signs. Although raised ICPis more likely with obliterated basal cisterns, the implicationsof open cisterns are less clear. We examined the associationbetween the status of perimesencephalic cisterns and time-linked ICP values in paediatric severe TBI.Methods ICP data linked to individual head CT scans werereviewed. Basal cisterns were classified as open or closedby blinded reviewers. For the initial CT scan, we examinedICP values for the first 6 h after monitor insertion. Forfollow-up scans, we examined ICP values 3 h before andafter scanning. Mean ICP and any episode of ICP≥20 mmHg during this period were recorded.Results Data from 104 patients were examined. Basal cisternswere patent in 51.72% of scans, effaced in 34.48% andobliterated in 13.79%. Even when cisterns were open, morethan 40% of scans had at least one episode of ICP≥20mmHg,and 14% of scans had a mean ICP≥20 mmHg. The specificityof open cisterns in predicting ICP<20 mmHg was poor(57.9%). Age-related data were worse.Conclusion Children with severe TBI frequently may haveopen basal cisterns on head CT despite increased ICP. Opencisterns should not discourage ICP monitoring.

Keywords Basal cisterns . Traumatic brain injury .

Children . Computed tomography . Head injury . Intracranialpressure monitoring

Introduction

Traumatic brain injury (TBI) is a major contributor tomortality and morbidity in both adults and childrenworldwide [14, 20]. The poor outcome associated withsevere TBI may be improved by effective medical care, alarge part of which is directed at preventing or amelioratingsecondary insults, including raised intracranial pressure(ICP) [9, 10, 13, 28]. Increased ICP commonly occursfollowing TBI and may compromise brain perfusion byreducing cerebral perfusion pressure and exerting localtissue pressure effects. It is associated with disability, poorneurological outcome and decreased survival in TBIpatients [2, 3, 6, 7, 17, 20, 23, 25]; therefore, monitoringand managing ICP effectively has become a cornerstone oftreatment for severe TBI [1, 3, 5].

However, when to institute ICP monitoring in paediatricsevere TBI is not well defined. The evidence base for aninternationally accepted published recommendation for ICPmonitoring in children with severe TBI was only sufficientto state that ICP monitoring was appropriate, and only atthe level of an option. There was not enough support for astandard or guideline [3]. Even for these recommendations,much evidence was extrapolated from adult studies as veryfew data are available from paediatric studies.

Not all children with severe TBI receive ICP monitoring[18]. An evaluation of TBI management practice in the UKfound that only 59% of children presenting with a GCS≤8 received ICP monitoring and that ICP treatment wasadministered in 41% of children in whom ICP was not

A. J. Kouvarellis :U. K. Rohlwink :V. Sood :D. Van Breda :M. J. Gowen :A. A. Figaji (*)Division of Neurosurgery, School of Child and Adolescent Health,Red Cross War Memorial Children’s Hospital,University of Cape Town,Cape Town, South Africae-mail: [email protected]

Childs Nerv Syst (2011) 27:1139–1144DOI 10.1007/s00381-011-1464-3

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monitored. However, the study found that ICP monitoringwas more common in patients with an abnormal admissionCT scan (56%) than in those for whom it was normal (26%)[26]. This would be expected as most clinicians assess headCT signs to predict the likelihood of increased ICP andtherefore the benefit of ICP monitoring. Of these signs, thebasal cisterns of the midbrain are arguably the mostcommonly used measure of the degree of brain swelling,being an indicator of the available perimesencephalic spaceat the tentorial incisura. Often the assumption is made thatif the cisterns are not effaced, ICP is unlikely to besignificantly elevated, and ICP monitoring may not berequired. Although support for this is found in a number ofstudies [11, 19, 29], these studies focussed largely on theassociation between abnormal scans and ICP and reviewedonly a limited number of scans with patent cisterns. Thereis evidence to suggest, however, that patients with patentbasal cisterns are still at risk of raised ICP and pooroutcome [12, 16, 22], but the risk of increased ICP in thisgroup is poorly quantified, and so, patent cisterns likely arestill used to indicate a lower risk of increased ICP. Todetermine whether patent basal cisterns are a useful sign ofICP that is not significantly increased, in this study, weaimed to examine the association between the status of theperimesencephalic cisterns and time-linked ICP values in alarge cohort of children with severe TBI. We chose toexamine the association of basal cisternal status and ICPbecause (1) cisterns are most commonly used to estimatethe likelihood of elevated ICP, (2) basal cisterns are easilyidentifiable to most clinicians, including those with littleexperience in reviewing paediatric CT scans, and (3) basalcisterns are probably one of the least age-dependent signson a paediatric head CT, and the distinction between open,effaced and obliterated cisterns is usually straightforward.

Methods

Patient selection

Approval for this study was obtained from the institutionalreview boards of the University of Cape Town and RedCross War Memorial Children's Hospital. This studyretrospectively examined medical records of consecutivepatients <15 years old admitted to the Red Cross WarMemorial Children's Hospital, Cape Town, with severe TBI(GCS score≤8).

Head CT scan evaluation

On admission, all patients underwent a head CT scan assoon as they were stable post-resuscitation. In general,follow-up CT scans were performed 2–3 days after the

initial scan or when clinically indicated for neurologicaldeterioration or worsening ICP control. For this study, allinitial and subsequent scans with ICP monitors in situ wereevaluated. Head CT scans were classified according to theMarshall criteria. We selected only patients with head CTscans meeting grade I, II or III of these criteria, in whomICP monitoring was instituted, i.e. we excluded patientswith a midline shift greater than 5 mm, mass lesions greaterthan 25 cc and/or hydrocephalus. We also excluded thefollowing: any scans in which there was a delay betweenthe CT scan and starting ICP monitoring greater than 6 h, ifthere was any medical or surgical intervention between thehead CT scan and the start of ICP monitoring, and if thepatient was brain dead at the time of the scan. Twoexperienced neurosurgeons (AAF, MJG), blinded to patientname and ICP data, evaluated the CT scans. The state of theperimesencephalic cisterns was classified as: ‘patent’, ifboth sides were open; ‘effaced’, if one or both sides werethought to be narrowed; or ‘obliterated’, if one or both sideswere not visible. Figure 1 shows typical examples of openand obliterated cisterns. For analysis, the cistern categorieseffaced and obliterated were collapsed into one categorydefined as ‘closed’.

ICP monitoring

ICP was measured with an intraparenchymal monitor(Codman ICP Express, Codman, Raynham, MA, USA; orCamino, Integra Neurosciences, Plainsboro, NJ, USA). ICPprobes were placed conventionally in right frontal paren-chyma in a diffuse injury or in the hemisphere with greaterswelling or focal lesions. ICP monitors were inserted assoon as possible after the initial CT scan. In general,patients did not receive treatment for raised ICP without anICP monitor in situ. Intracranial monitoring continued untilICP was stable for >24–48 h or until the patient died. In

Fig. 1 Head CT scans of two patients showing the typical appearanceof open basal cisterns (a) and obliterated cisterns (b). In a, thequadrigeminal cisterns are easily visible, while in b, the quadrigeminaland ambient cisterns are completely obliterated

1140 Childs Nerv Syst (2011) 27:1139–1144

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accordance with current treatment guidelines [4], increasedICP was defined as ICP≥20 mmHg for more than 5 min;treatment was directed at maintaining ICP<20 mmHg. ICPdata were recorded hourly as per ICU protocol, and the ICUnursing records were used to collect these data.

Data collection

We compared time-linked data from ICP recordings and CTscans (initial and subsequent) by pairing each CT scan withthe closest available ICP data as follows: initial scans werecompared with the first 6 h of ICP monitoring data available ifthe intervening period between the initial scan and thecommencement of ICP monitoring was ≤6 h; each subsequentCTscan performedwith the ICPmonitor in situ was comparedwith the ICP data of 3 h before the scan and 3 h thereafter.Data were excluded from analyses if CT scans or ICP datawere missing or if the ICP probe malfunctioned.

Data analysis

Data analysis was conducted in four stages: (1) CT scanswere classified as ‘open’ or ‘closed’ based on the patencyof the basal cisterns. (2) For each scan, corresponding ICPdata were analysed in two ways: first, the number ofindividual ICP values ≥20 mmHg over the period wasidentified; second, an average ICP value for the period wascalculated, and averages ≥20 mmHg were identified. (3) Weused the ICP threshold of 20 mmHg as it is therecommended treatment threshold outlined in the paediatrictreatment guidelines [4]. However, since children varysubstantially in physiology from infancy to adolescence,age may influence the ICP threshold for optimal treatment;therefore, we repeated our analysis using age-relatedthresholds. Based on a study by Chambers et al. [8] whichexamined the relationship between ICP and outcome, wecategorised our patients into the following age bands withrecommended age-related ICP thresholds: 2–6 years (ICP<6 mmHg), 7–10 years (ICP<9 mmHg) and 11–15 years(ICP<13 mmHg). The number of individual or averagedICP values greater than the age-related threshold wasidentified. (4) Probability, sensitivity, specificity, odds ratioand positive and negative predictive values for increasedICP were then calculated for open and closed cisterns.

Results

Data from 141 patients between June 2003 and January2010 were collected and analysed. A total of 298 head CTscans were reviewed; the mean number of scans per patientwas two. Thirty-seven patients and their scans (n=68) wereexcluded based on the CT scan criteria mentioned above.

Of the remaining 104 patients, a further 56 scans wereexcluded. Reasons for exclusions are summarised inTable 1. This left 174 scans in 104 patients that wereanalysed. Basic demographic data for the patients areprovided in Table 2.

Of the scans that were analysed (n=174), cisterns werepatent in 51.72%, effaced in 34.48% and obliterated in13.79%. Even when cisterns were open (n=90 scans in 57patients), more than 40% of scans were associated with anepisode of ICP≥20 mmHg, and almost 15% of these scanswere associated with an average ICP≥20 mmHg. When thedata were analysed according to the age-related thresholdssuggested by Chambers et al., 80% of scans (n=65 scans in43 patients) were associated with an average ICP valueabove the age threshold of the patient when cisterns wereopen. These age thresholds were considerably lower than thecurrently accepted treatment threshold of 20 mmHg. How-ever, analyses showed that even if the ICP threshold wasonly reduced to 15 mmHg for all patients, when cisternswere open, almost 40% of scans had an average ICP greaterthan 15 mmHg, and almost 65% had individual ICP valuesabove this threshold. These results are summarised inTables 3 and 4.

The probability of all ICP values being <20 mmHg in thecontext of open cisterns was 59%. The probability of thesepatients having an episode of ICP≥20 mmHg was 60% ifcisterns were closed (effaced or obliterated) and 75% if theywere obliterated. The specificity of open cisterns in detectingICP<20 mmHg was 57.9%, and the positive predictive valuewas 59%. Statistics for open cisterns in predicting ICP belowthe various thresholds are summarised in Table 5. The oddsratio of ICP≥20 mmHg when cisterns were closed versusopen was 2.2 (CI, 1.21–4.06).

Discussion

In this study, we examined the relationship between thestatus of the perimesencephalic cisterns (classified as open

Table 1 Reasons for CT scan/patient exclusion

Intervening period between initial scanand ICP monitoring was >6 h long

18 (14.5)

Patient underwent intervening surgery 15 (12.1)

ICP data were missing 8 (6.4)

ICP probe malfunction 3 (2.4)

Other 80 (64.5)

Data are presented as a number (percentage of the total scansexcluded). ‘Intervening surgery’ indicates any surgery other thaninsertion of an ICP monitor between the time of the scan and the firstICP recordings. ‘Other’ exclusions include scans that could not beretrieved, scans that were performed at referring hospitals and scansexcluded based on the Marshall Criteria as outlined in the text

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or closed) and time-linked ICP values corresponding witheach head CT scan in a large group of children with severediffuse TBI who underwent ICP monitoring. The studyfound that these children frequently have patent basalcisterns on head CT and that increased ICP (≥20 mmHg) iscommon despite these open cisterns: 40% of scans withopen cisterns had episodes of ICP≥20 mmHg. These datasuggest that open cisterns do not necessarily indicate anormal ICP.

Obliterated cisterns have been associated with raised ICPand poor outcomes [11, 19, 29], but the relationshipbetween patent cisterns and ICP is less well defined. Mostof the studies which have examined this topic have been

limited by small sample sizes and a focus on a predomi-nantly adult population. Colquhoun et al. [11] demonstratedthat patients with compression or obliteration of the thirdventricle or basal cisterns were likely to have elevated ICP,and the authors suggest that if both the third ventricle andbasal cisterns outline normally, ICP is unlikely to beelevated [11]. However, this small (n=13) study excludedall normal-appearing scans thereby preventing a completeassessment of the relationship between open cisterns andICP. Similarly, Teasdale et al. [29] found a significantassociation between cistern appearance and ICP andadvocated that normal ventricles and cisterns are unlikelyto indicate future elevation in ICP and the need for ICPmonitoring. This study related cistern status to modal ICPover a 24-h period; however, ICP is a highly dynamicphenomenon, and evaluation over a long time period couldmask significant individual episodes of increased ICP.Furthermore, modal ICP may not reflect the ICP status atthe time of scanning. A study by Sadhu et al. [24] did not

Table 3 Individual ICP data

Status of cisterns ICP categories Totals

ICP<age threshold ICP≥age threshold

Cisterns open 6 (7.4) 75 (92.6) 81

Cisterns closed 6 (8.1) 68 (91.9) 74

ICP<15 ICP≥15Cisterns open 32 (35.6) 58 (64.4) 90

Cisterns closed 20 (23.8) 64 (76.2) 84

ICP<20 ICP≥20Cisterns open 53 (58.9) 37 (41.1) 90

Cisterns closed 33 (39.3) 51 (60.7) 84

ICP<25 ICP≥25Cisterns open 66 (73.3) 24 (26.7) 90

Cisterns closed 48 (57.1) 36 (42.9) 84

Description of cisternal status and individual ICP values that wereabove or below the designated thresholds corresponding with eachscan. ICP values designated as greater than threshold imply that one ormore ICP values during the analysed period were greater than thecorresponding threshold. Data are presented as a number (percentage).Scans (n=19) for children under 2 years were excluded in the agethreshold analysis

Table 2 Demographic data (n=104)

Age Mdn, 6 years (5 months–14 years)

Male 65 (63)

Female 39 (37)

Mechanism of injury

MVA pedestrian 66 (63.5)

MVA passenger 19 (18.3)

Penetrating injury 7 (6.7)

Crush injury 4 (3.8)

Blunt assault 3 (2.9)

Fall from a height 3 (2.9)

Non-accidental injury 2 (1.9)

Data are presented as median (Mdn) and range, number and(percentage)

Table 4 Average ICP data

Cistern status ICP categories Totals

ICP<age threshold ICP≥age threshold

Cisterns open 16 (19.8) 65 (80.2) 81

Cisterns closed 12 (16.2) 62 (83.8) 74

ICP<15 ICP≥15Cisterns open 55 (61.1) 35 (38.9) 90

Cisterns closed 34 (40.5) 50 (59.5) 84

ICP<20 ICP≥20Cisterns open 77 (85.6) 13 (14.4) 90

Cisterns closed 58 (69.0) 26 (31.0) 84

ICP<25 ICP≥25Cisterns open 85 (94.4) 5 (5.6) 90

Cisterns closed 70 (83.3) 14 (16.7) 84

Description of cisternal status and average ICP values for the 6-h analysed period that were above or below the designated thresholdscorresponding with each scan. Data are presented as a number(percentage). Scans (n=19) for children under 2 years were excludedin the age threshold analysis

Table 5 Statistical characteristics of open cisterns in relation to ICPbelow thresholds

ICP <Agethreshold

<15 mmHg <20 mmHg <25 mmHg

Sensitivity 50 (21–78) 61.5 (47–74) 61.6 (50–71) 57.9 (48–67)

Specificity 47.2 (38–55) 52.5 (43–61) 57.9 (46–68) 59.3 (45–71)

Positive predictivevalue

7.4 (2–15) 35.6 (25–46) 59 (48–69) 73.3 (62–82)

Statistics presented with 95% confidence interval. The categoriesimply that all values were below the stated threshold

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find an association between abnormal scans and ICP, andthese authors also proposed that normal scans suggestnormal ICP, although this was based on only four normalscans. Hirsch et al. [15] examined several characteristicsvisible on head CT in children and compared thepredictions of radiologists to actual measured ICP. Theseauthors showed a good predictive value for recognisingincreased ICP; however, the study does not mention howICP values were analysed, whether individual, peak oraverage. By contrast to these studies, O'Sullivan et al. [22]examined eight patients with normal scans, and Holliday etal. [16] investigated 17 patients with normal scans, andfound that these patients were still at risk of substantiallyelevated ICP and poor outcomes and that a normal scan didnot preclude the need for ICP monitoring. These findingswere mirrored in another larger study using data from theNational Institute of Health's Traumatic Coma Data Bankwhich indicated that although the risk of intracranialhypertension and death was higher with an abnormaladmission CT scan, the risk associated with normal scanswas not negligible [12]. However, none of these studiesspecifically examined the CT scan with time-linked ICPdata.

The present study was limited to children and included alarge cohort (n=104) of patients with diffuse head injuryand examined head CT scans with corresponding time-linked ICP data. Our results indicate that increased ICPoccurs frequently even when cisterns are open; therefore,the status of cisterns alone should not be used as anindication for ICP monitoring. Furthermore, a decision toinstitute ICP monitoring (or not) based on the initial CTscan overlooks the possibility that patients may developdelayed raised ICP, which commonly may occur followingTBI [21, 27, 30]. TBI is highly heterogeneous in itspathophysiology and temporal course and may exhibitsubstantial inter-individual variability. This makes it diffi-cult to predict intracerebral physiology in patients withdiffering mechanisms and severity of injury using a CTscan which offers only one snapshot in time of the state ofthe injured brain.

There are a number of possible limitations to this study.First, hourly recordings from the ICU charts were used;however, because ICP is a dynamic variable, higherfrequency data collection may have identified moreepisodes of increased ICP. Therefore, this report mayunderestimate the number of patients with clinicallysignificant elevations of ICP. Second, the scans of patientsover several years were reviewed. Earlier in the series,patients presumably were more likely to have ICPmonitoring instituted only if the cisterns were effaced orobliterated, whereas the current threshold for ICP monitor-ing at our institution is lower, i.e. it is standard treatment forall patients who present with severe TBI to receive an ICP

monitor. However, this is expected to affect the relativeproportions of patients with patent versus obliteratedcisterns, but not the relationship between cisterns and ICP.Similarly, the proportional results cannot be generalized tothe whole paediatric TBI population, as patients who werelikely to be extubated early, and patients with imminentbrain death, may not have been monitored. Third, treatmentfor increased ICP was not taken into account. Again, thismay underestimate the true proportion of patients withelevated ICP. Fourth, the transport of patients from the ICUto the CT scanner may be associated with elevations of ICPwhich may have affected the ICP results on returning fromthe scanner. However, ICP values during transport were notconsidered; the first ICP values after the return from theICU were recorded usually once the patient had been stablefor at least 15 min, and there were no significant differences(p=0.9) in the ICP readings before and after transport to thescanner.

Conclusion

This study examined the question of whether patent basalcisterns predict normal ICP in children with severe TBI, themain finding being that ICP is frequently increased despiteopen basal cisterns. Although effaced or obliterated cisternsare indeed associated with a greater likelihood of increasedICP, open cisterns do not indicate the absence of increasedICP. Based on these data, the status of basal cisterns shouldnot be used as a sole criterion for deciding whether ICPmonitoring is indicated.

Disclosure The authors have no conflicts of interest to disclose.

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