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Vol. 28. Num. 1.January - February 2017Pages 1-50
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Vol. 28. Num. 1.January - February 2017Pages 1-50
Clinical Research
DOI: 10.1016/j.neucie.2017.01.002
Trends in computed tomography characteristics, intracranial pressure monitoring and surgical management in severe traumatic brain injury: Analysis of a data base of the past 25 years in a neurosurgery department
Evolución temporal en las características de la tomografía computarizada, presión intracraneal y tratamiento quirúrgico en el traumatismo craneal grave: análisis de la base de datos de los últimos 25 años en un servicio de neurocirugía
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Pedro A. Gómeza,
Corresponding author
pagolopez@gmail.com

Coresponding author.
, Ana M. Castaño-Leóna, David Lorab, Santiago Cepedaa, Alfonso Lagaresa
a Servicio de Neurocirugía, Hospital Universitario 12 de Octubre, Universidad Complutense (UCM), Madrid, Spain
b Unidad de Investigación Clínica Unit, IMAS12-CIBERESP, Hospital Universitario 12 de Octubre, Madrid, Spain
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Tables (3)
Table 1. Relation between the initial Marshall CT classification (TCDB) and type of brain injury with the 3 time periods.
Table 2. Association between the initial CT (TCDB) and the CT findings.
Table 3. Multivariate study.
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Abstract
Objective

To describe the radiological characteristics, surgical indications, procedures, and intracranial pressure monitoring of a representative cohort of severe traumatic brain injury (sTBI) cases collected over the past 25years, and to analyse the changes that have occurred by dividing the period into 3 equal time periods.

Methods

An observational cohort study was conducted on consecutive adult patients (>14years of age) with severe closed TBI (Glasgow Coma Scale score [GCS]8) who were admitted during the first 48h after injury to the Hospital 12 de Octubre from 1987 to 2012. The most relevant radiological findings, surgical procedures, and intracranial monitoring indications reported in the literature were defined and compared in 3 equal time periods (1987–1995, 1996–2004, and 2005–2014).

Results

A significant increase was observed in subdural haematomas with lesions over 25cc, and midline shift in the last period of time. The incidence of subarachnoid haemorrhage increased significantly with time. There was a progression to a worse computed tomography (CT) classification from the initial CT scan in 33% of cases.

Surgery was performed on 721 (39.4%) patients. Early surgery (<12h) was performed on 585 (81.1%) patients, with the most frequent being for extra-cerebral mass lesions (subdural and epidural haematomas), whereas delayed surgery (>12h) was most frequently performed due to an intracerebral haematoma. Surgical treatment, both early and late was significantly lower with respect to the first time period. Decompressive craniectomy with evacuation of the mass lesion was the preferred procedure in the last time period.

Intracranial pressure monitoring (ICP) was carried out on 1049 (57.3%) patients, with a significantly higher frequency in the second period of time. There was adherence to Guidelines in 64.4% of cases. Elevated/uncontrolled ICP was more significant in the first time period.

Conclusions

As a result of the epidemiological changes seen in traumatic brain injury, a different pattern of morphological injury is described, as depicted in the CT, leading to a difference in practice during this period of observation.

Keywords:
Severe traumatic brain injury
Computerized tomography
Craniotomy
Decompressive craniectomy
Intracranial pressure
Guidelines
Resumen
Objetivo

Describir las características radiológicas, quirúrgicas y manejo de la presión intracraneal (PIC) de una cohorte de pacientes con traumatismo craneal grave (TCEG) ingresados en los últimos 25años.

Métodos

Estudio observacional de una cohorte consecutiva de pacientes adultos (>14años) con TCEG cerrado (GCS8) admitidos en las primeras 48h del TCEG en el Hospital 12 de Octubre entre 1987 y 2012. Se definieron las características radiológicas, los procedimientos quirúrgicos y las indicaciones de monitorización de la PIC y se compararon en los 3 periodos de tiempo (1987-1995, 1996-2004 y 2005-2014).

Resultados

Se apreció un aumento significativo del hematoma subdural mayor de 25cc, de la desviación de la línea media y de la hemorragia subaracnoidea (HSA) en el último periodo de tiempo.

Fueron intervenidos 721 pacientes (39,4%); 585 (81,1%) en las primeras 12h (cirugía precoz). El tratamiento quirúrgico disminuyó significativamente en el último periodo de tiempo, siendo la craniectomía descompresiva (CD) con la evacuación de una masa intracraneal el procedimiento más utilizado en el este periodo.

Se monitorizó la PIC en 1.049 pacientes (57,3%), con una frecuencia significativamente mayor en el segundo periodo, con una adherencia a las Guías del 64,4%. La PIC elevada incontrolable fue significativamente mayor en el primer periodo de tiempo.

Conclusiones

Como consecuencia de los cambios epidemiológicos que se han apreciado en los pacientes con TCEG en los últimos 25años, describimos un patrón diferente de lesión morfológica, como se puede apreciar por el cambio en la TC, lo que determina un cambio en la práctica clínica durante este periodo de observación.

Palabras clave:
Trauma craneal grave
Tomografía computarizada
Craneotomía
Craniectomía descompresiva
Presión intracraneal
Guías clínicas
Full Text
Introduction

The epidemiological and clinical profile of a cohort of 1830 patients with a severe traumatic brain injury (sTBI) at the Hospital 12 de Octubre has been described in a previous publication1. In this second part, we describe the trend in the computed tomography (CT) findings, indications for intracranial pressure (ICP) monitoring and surgical treatment over the last 25years, divided into three established time periods.

The Glasgow Coma Scale (GCS) is now essential for classifying patients with a sTBI, but it has become increasingly unreliable when assessing the severity of the injury, primarily due to the ever-increasing early use of sedation, intubation and ventilation in patients with sTBI.2 CT scans provide essential diagnostic information about the structural injury caused after a sTBI and the need to perform surgery or ICP monitoring. As a result, they have been gaining greater importance when it comes to the classification and prognosis of these patients.

In 1991, Marshall et al.3 introduced a CT classification based on the experience of the Traumatic Coma Data Bank (TCDB), grouping patients with sTBI according to certain CT characteristics. The purpose of this classification was descriptive, and it has since become the standard used for assessing and giving the final prognosis for these patients. It is now the most used sTBI test, since it adequately describes the structural injury; nevertheless, there are some constraints to its interpretation: it does not describe the type of injury, it does not assess subarachnoid haemorrhage (SAH), nor does it provide clear criteria for indicating surgery.2,4–12 Moreover, this classification has no physiopathological basis. Maas9 showed that it may be preferable to use the individual CT findings over the Marshall classification for prognostic purposes or a combination of both.10

One of the most important sTBI complications is the development of an intracranial haematoma, which occurs in a large proportion of patients.13,14 Despite this, there is no clear indication of the time of surgery,15 nor the procedure to be performed to evacuate the haematoma. Interest in decompressive craniectomy (DC) has made a comeback in recent years, although it is still not considered to be the standard protocol.16

Although the indications for ICP monitoring have been well specified for decades and recommended in the Brain Trauma Foundation (BTF) Guidelines,17,18 there are not enough prospective, randomised studies showing better progress in monitored patients who receive a standard treatment to control ICP elevation, therefore there is still wide variability in the indication for ICP monitoring, even within the same hospital. Recently, a randomised study found no significant differences in the final outcome between monitored and unmonitored patients,19 which resulted in much debate.20 Another study comparing two patient cohorts treated in different hospitals,21 one with monitoring and the other without, showed no improvement in the final outcome in the patients who survived more than 24h. The study by the European Brain Injury Consortium (EBIC)2,22 showed that the frequency of ICP monitoring in Europe was 37% (5–53%), and it was more common in the United States.23

Objective

To describe the trend in CT characteristics, surgical treatment, frequency and adherence to the ICP monitoring guidelines in a representative cohort of sTBI patients admitted to a single centre in the last 25years, divided into three time periods (1987–1995, 1996–2004 and 2005–2012).

Methods

The admission criteria and epidemiological and clinical characteristics of this population have already been published.1 In brief, the Hospital 12 de Octubre database contains adult patients (≥15 years) with a closed sTBI admitted during the first 48h after injury (GCS8 after non-surgical resuscitation or decline in this score in 48h). The excluded patients included those with great haemodynamic instability, which impeded transfer to the radiology unit and who died prematurely, or those who were admitted under intubation with a normal CT or with minimal injury and who obeyed orders upon withdrawing sedation in the early hours.

Radiological characteristics (structural damage)

All patients had a CT performed immediately after resuscitation and stabilisation. On rare occasions, the initial CT was performed in the referral hospital. The findings were classified as follows:

  • 1.

    Marshall Classification (Traumatic Coma Data Bank [TCDB])3: CT I (normal), CT II (diffuse), CT III (swelling), CT IV (swelling with shift), CT V (evacuated mass lesion), and CT VI (non-evacuated mass lesion).

  • 2.

    Type of injury on the CT4,6,7,9,10:

    • a.

      Traumatic subarachnoid haemorrhage (SAH). Defined as the presence of blood in any amount in the subarachnoid space of the convexity or the base.

    • b.

      Intraventricular haemorrhage (IVH). Any amount of intraventricular blood.

    • c.

      Basal cisterns. Categorised into 2 groups: normal and compressed or absent.

    • d.

      Midline shift in mm. Also categorised as ≤5mm versus >5mm.

    • e.

      Presence, type, multiplicity and associations with mass lesions. Epidural haematoma (EDH), subdural haematoma (SDH) and intracerebral haematoma (ICH), with the latter grouping contusions and pure haematomas. The individual volume of the lesion was calculated using the formula (A×B×C/2),24,25 and the total volume was categorised into 2 groups: ≤25cc and >25cc.

Control computed tomography scan

This was performed in all patients, except in those who died prematurely due to the severity of the initial injury (338 patients [18.5%]). Therefore 1492 patients underwent a control CT. If the patients had a stable respiratory and haemodynamic status, the controls were performed between 6 and 48h after injury depending on the admission time, injury type and surgical procedure performed. All patients who underwent surgery had a CT performed immediately after the procedure. A CT was also performed whenever the ICP rose or the patient declined clinically. To define the change in the intracranial pathology, if any, we defined the “worst CT” as that with the worst prognosis according to the TCDB classification, considering it the “final CT” in the last 10 days.8,26

Medical treatment

This study is not designed to assess the efficacy of the medical treatment on the final outcome or on the ICP, therefore we did not include therapeutic variables in our study. As a general rule, all the patients were directly admitted to an ICU dedicated exclusively to treating injured patients and were treated uniformly according to international protocols,17,27 including ventilation, haemodynamic and ICP monitoring, with ICP reduction if it exceeded 20–25mmHg, and adequate perfusion pressure was maintained. This medical treatment was maintained until the ICP levels normalised for 24/48h and the absence of mass effect on the control CT.

Surgical treatment

Surgery was performed after haemodynamic stabilisation with a suitable coagulation test. Surgery was considered to be early if performed in the first 12h after injury and late if performed afterwards, although there may be patients who underwent surgery in both periods. The general indications for the surgery were similar to those recommended in the guidelines14,24: (a) clinical decline; (b) haematoma (>25–30cc) with midline shift >5mm and effacement of the basal cisterns or iii ventricle, and (c) elevated or medically uncontrolled ICP.

We classified the surgical procedure performed into 3 groups: (a) craniotomy with haematoma evacuation; (b) DC with bone removal and haematoma evacuation, for the purpose of increasing the volume of the cranial cavity, a procedure that was performed both for primary haematoma evacuation (primary DC) as well as to control ICP elevation that did not respond to medical treatment (secondary DC); and (c) other procedures such as trepanning, elevations of sunken skull fragments and cerebrospinal fluid bypasses, etc. It was not considered a surgical treatment if only the ICP sensor was placed.

Intracranial pressure monitoring

In the first years (1987–1991), an intraventricular catheter was used; after the introduction of intraparenchymal pressure transducers (Camino Laboratories, Integra, USA), most patients were monitored with this device. One thousand and forty-nine patients (1049) were monitored (57.3%); the unmonitored patients (781 [42.7%]) were generally those with a severe lesion on the initial CT and a poor neurological situation (bilateral mydriasis or absence of motor response after resuscitation) who were considered “unsalvageable”. Furthermore, patients with a diffuse lesion on the initial CT, with no mass effect on either the first CT or on the control CT, or with pure EDH with no significant midline shift who underwent surgery, were also not monitored.

The ICP sensor was placed in the most affected hemisphere within the first 24h in all patients and always after a suitable coagulation test. For the ICP analysis, we classified it into 3 groups: (a) no ICP monitoring; (b) low/controlled (normal ICP<20mmHg or controlled with medical or surgical treatment); and (c) high, uncontrollable ICP despite medical or surgical treatment.

Adherence to the Guidelines17

Following the BTF Guidelines, ICP should be monitored in all “salvageable” sTBI patients (GCS8 after non-surgical resuscitation within a period of 6h after injury) with an abnormal CT. If the CT was normal, ICP monitoring would be indicated if two or more premises are met: age>40 years, unilateral or bilateral motor score 2–3, or systolic blood pressure ≤90mmHg. We define adherence to the Guidelines to be when these criteria were met.

There is no standard criteria to define “salvageable” patients, therefore we used the score obtained in a previous study to predict early mortality (48h).28 The patients with a more than 80% chance of dying in the first two days were excluded, therefore 1622 patients were eligible for this analysis.

Statistical analysis

Continuous variables are presented as mean±standard deviation (SD) and categorical variables as absolute and relative frequencies. The statistical significance from comparing proportions was determined using the Chi-squared test or Fisher's test. The Cochran–Mantel–Haenszel test was used for ordinal variables; for example, age or time periods. The distribution of continuous values (age, CT time, volume) were compared using analysis of variance (ANOVA), with the p-value for multiple tests (Bonferroni).

A multivariate logistic regression study was performed using the backwards method of elimination by selecting p=0.05 to estimate the association between the predictors (age, period of time, motor score, clinical decline, cistern status, midline shift, SAH, IVH, type and volume of intracranial mass) and the endpoints (surgery, ICP monitoring and ICP levels). The results are shown as OR with a 95% confidence interval (CI) and the p-values of the predictors.

The independent variables included in the selection process had correlations under 0.5. No interactions were included in the selection process. To quantify the discrimination, we used the area under the curve (AUC).29

All the data were generated using SPSS, version 16.0 (SPSS, Inc., Chicago, IL, USA).

ResultsRadiological data

In 95% of the patients, the CT was performed within the first 7h and 45min. The time between the injury and performing the first CT was reduced from 4.1h in the first period to 2.5h in the second and to 2.4h in the last (p<0.001), showing a significant difference between the first period and the other two (p<0.001).

Table 1 shows the findings from the initial CT (TCDB and injury type) in the 3 periods. The CT was normal (TCDB type i) in only 45 patients (2.5%). A significant increase in diffuse injuries was observed (TCDB type ii), p=0.001, and injuries with swelling occurred significantly less frequently (TCDB type iii and iv, p<0.001). Evacuated mass lesions showed a significant reduction (TCDB type v, p<0.001), but with a significant increase in the non-evacuated lesions (TCDB type vi, p<0.001).

Table 1.

Relation between the initial Marshall CT classification (TCDB) and type of brain injury with the 3 time periods.

  1987–1995 (n=746)  1996–2004 (n=587)  2005–2012 (n=497)  Total (n=1830) 
Admission CT (Marshall)
Normal – type I  18 (2.4)  17 (2.9)  10 (2.0)  45 (2.5)  NS 
Diffuse – type II  259 (34.7)  251 (42.8)  219 (44.1)  729 (39.8)  0.001 
“Swelling” – type III  146 (19.6)  115 (19.6)  57 (11.5)  318 (17.4)  <0.001 
Swelling&Mass Effect- type IV  29 (3.9)  30 (5.1)  19 (3.8)  78 (4.3)  NS 
Evacuated Mass Lesion – type V  272 (36.5)  146 (24.9)  117 (23.5)  535 (29.2)  <0.001 
Non-Evacuated Mass Lesion – type VI  22 (2.9)  28 (4.8)  75 (15.1)  125 (6.8)  <0.001 
CT findings
Petechiae  311 (41.7)  245 (41.7)  196 (39.4)  752 (41.1)  NS 
IVH  221 (29.6)  206 (35.10)  210 (42.3)  637 (34.8)  <0.001 
tSAH  483 (64.7)  447 (76.1)  424 (85.3)  1354 (74.0)  <0.001 
Cistern compression  449 (60.2)  294 (50.1)  249 (50.1)  992 (54.2)  <0.001 
Midline shift>5mm
Mean (mm) 
222 (29.8)
3.6 
139 (23.7)
3.0 
145 (29.2)
4.1 
506 (27.7)
3.5 
0.032
0.003 
Total volume>25cc  226 (30.3)  135 (23)  181 (36.4)  542 (29.6)  <0.001 
Mean (cc)  18.4  15.8  23.9  19.5  <0.001 
ICH  290 (38.9)  248 (42.2)  216 (43.5)  754 (41.2)  NS 
Focal contusion  186 (24.9)  138 (23.5)  103 (20.7)  427 (23.3)  NS 
Unilateral multiple contusion  28 (3.8)  23 (3.9)  25 (5.0)  76 (4.2)  NS 
Bilateral multiple contusion  76 (10.2)  87 (14.8)  88 (17.7)  251 (13.7)  0.001 
EDH  107 (14.3)  95 (16.2)  89 (17.9)  291 (15.9)  NS 
SDH  284 (38.1)  216 (36.8)  262 (52.7)  762 (41.6)  <0.001 
Total  746 (40.8)  587 (32.1)  497 (27.2)  1830   

EDH, epidural haematoma; ICH, intracerebral haematoma; IVH, intraventricular haemorrhage; SAH, subarachnoid haemorrhage; SDH, subdural haematoma; NS, not significant.

The frequency of SAH and IVH, common in type ii injuries, increased significantly (p<0.001), although the frequency of petechiae was constant. Cistern compression decreased significantly (p<0.001), although midline shift (p=0.03) and injury volume over 25cc increased (p<0.001). The frequency of EDH and focal contusions remained stable, but the frequency of SDH (p<0.001) and multiple bilateral multiple contusions increased (p=0.001).

Fig. 1 shows the frequency of single and combination intracranial haematomas that appeared on the initial CT. There were no haematomas in 545 (29.8%) of the patients. The most common single intracranial haematoma was SDH, in 375 cases (20.5%), followed by contusions (ICH) in 309 cases (17%), and lastly EDH in 135 cases (7.4%). A combination of injuries was observed in 466 cases; the most common was a combination of SDH with ICH in 310 (16.9%) patients. Other combinations were less common.

Fig. 1.
(0.09MB).

Frequency of pure and combination brain injuries on the initial CT.

Table 2 shows the findings from the CT combined with the Marshall classification and the individual CT characteristics. Of the 535 patients with TCDB type v, 118 (22.1%) had masses <25cc and 417 (77%) had larger masses. A high incidence of SAH was found (74%), most frequently associated with patients with TCDB type iii (87.7%) or TCDB type iv (89.7%).

Table 2.

Association between the initial CT (TCDB) and the CT findings.

CT Findings  CT classification (TCDB)
  I, n (%)  II, n (%)  III, n (%)  IV, n (%)  V, n (%)  VI, n (%)  Total, n (%) 
IVH
Absent  45 (3.8)  435 (36.5)  183 (15.3)  49 (4.1)  413 (34.6)  68 (5.7)  1193 (65.2) 
Present  294 (46.2)  135 (21.2)  29 (4.6)  122 (19.2)  57 (8.9)  637 (34.8) 
Cisterns
Normal  45 (5.4)  729 (87)  51 (6.1)  13 (1.6)  838 (45.8) 
Abnormal  318 (32.1)  78 (7.9)  484 (48.8)  112 (11.3)  992 (54.2) 
Midline shift>5mm
Absent  45 (3.4)  729 (55.1)  318 (24.0)  194 (14.7)  38 (2.9)  1324 (72.3) 
Present  78 (15.4)  341 (67.4)  87 (17.2)  506 (27.7) 
SAH
Absent  45 (9.5)  203 (42.6)  39 (8.2)  8 (1.7)  161 (33.8)  20 (4.2)  476 (26) 
Present  526 (38.8)  279 (20.6)  70 (5.2)  374 (27.6)  105 (7.8)  1354 (74) 
Mass volume
≤25cc  45 (3.5)  729 (56.6)  318 (24.7)  78 (6.1)  118 (9.2)  1288 (70.4) 
>25cc  417 (76.9)  125 (23.1)  542 (29.6) 
Total  45 (2.5)  729 (39.8)  318 (17.4)  78 (4.3)  535 (29.2)  125 (6.8)  1830 (100) 

IVH, intraventricular haemorrhage; SAH, subarachnoid haemorrhage.

No control CT was performed in 338 patients (18.5%). At least one control CT was performed in the remaining 1492 patients within the first hours of admission. A worsening in the Marshall classification was observed in 492 patients (33%). This change was observed in 37.4% in the first time period, 28.8% in the second and 30.9% in the third (p=0.006). Fig. 2 shows how the initial CT worsened. Of the 45 patients with an initial normal CT (type i), 2 (4.4%) developed swelling and one (2.2%) an evacuated mass lesion. Of the 729 patients with TCDB type ii, 32 (4.4%) developed swelling and 106 (14.5%) a mass lesion. Of the 318 patients with TCDB type iii, in 14 (4.4%) the swelling increased with midline shift and 78 (24.5%) developed a mass lesion. Of the 78 patients with TCDB type iv, 14 (17.9%) developed a mass lesion. Of the 535 with a TCDB type v, 71 (13.3%) developed swelling and 164 (30.7%), a new mass lesion. Of the 125 patients with TCDB type vi, 10 (8%) underwent surgery due to an increase in the mass lesion. Therefore, in total 119 patients (6.5%) developed swelling with or without midline shift and 373 (20.4%) a new/increased intracranial mass. Of the latter, 260 (69.7%) were evacuated and 113 (30.3%) were not.

Fig. 2.
(0.1MB).

Change on the Control CT (TCDB) Increase in swelling and haematoma volume.

Surgical treatment

The surgical treatment breakdown is shown in Fig. 3. In total, 721 patients (34.8%) underwent surgery: 352 (47.2%) between 1987 and 1995, 204 (34.8%) between 1996 and 2004 and 165 (33.2%) between 2005 and 2012. In total, 851 surgeries were performed: 597 patients (82.8%) had one operation, 118 (16.4%) two and 6 (0.8%) three. The frequency of surgical interventions decreased significantly for both early and late surgeries versus the first time period (1987–1995). Early surgery (within the first 12h) was performed in 585 patients (81.1%): 280 (37.5%) in the first time period, 164 (27.9%) in the second and 141 (28.4%) in the last. Surgery was performed earliest in the last time period (4.4, 4.2 and 3.5h, p=0.003). In 136 patients (18.9%), surgery was performed after 12h (late surgery); 72 (9.7%) in the first period, 40 (6.8%) in the second and only 24 (4.8%) in the third.

Fig. 3.
(0.13MB).

Time and number of surgical procedures in the 3 time periods.

Fig. 4 shows the variation in the surgical procedures performed. DC was performed in 88 patients (25.0%) in the first period, 124 (61%) in the second and 119 (72%) in the third (p<0.001). In total, DC was performed as the first or second procedure in 331 patients (45.9%): 266 (36.9%) within the first 12h and 65 (9.0%) after 12h. In 36 patients (10.9%), two DCs were performed. Of the 721 patients who underwent surgery, 218 did so for an EDH, 259 for an ICH and 418 for an SDH (more than one injury could have been evacuated during the surgery or, in the case of a reaccumulated lesion, the same lesion could have been evacuated more than once). Early surgery was performed in 195 patients (89.4%) with EDH, in 366 (87.5%) with SDH and in 182 (70.3%) with contusions. A DC was performed in 78 (35.8%) of the patients with EDH, in 214 patients (51.2%) with an SDH and in 167 (64.5%) with contusions.

Fig. 4.
(0.11MB).

Surgical procedures performed in the 3 time periods by type of haematoma evacuated.

Between 1987 and 2012, a progressive decrease was observed in patients undergoing surgery for an extracerebral injury (EDH and SDH). This trend is shown in Fig. 5.

Fig. 5.
(0.24MB).

Surgery trend over time in evacuating an extracerebral haematoma.

Intracranial pressure monitoring

Fig. 6 shows the frequency of ICP monitoring and its response to treatment in the 3 time periods. One thousand and forty-nine (1049) patients (57.3%) were monitored. In the first time period, 399 (53.5%) were monitored vs 347 (46.5%) who were not; in the second period, 384 (65.4%) vs 203 (34.6%) and in the third period, 266 (53.5%) vs 231 (46.5%). Significantly more patients were monitored in the second time period (p<0.001). The proportion of patients with high/uncontrollable ICP was 157 patients (21%) in the first period versus 81 (13.3%) in the second and 29 (5.8%) in the third.

Fig. 6.
(0.07MB).

Monitoring frequency and ICP levels.

The main reasons for not monitoring 781 patients (42.7%) were: (a) age: unmonitored patients were older (p<0.001); only 25/156 patients (16%) over 70 were monitored; (b) patients considered unsalvageable (death in 48h): of the 781 unmonitored patients, 284 (32.5%) died within the first 2 days; and (c) diffuse injuries with no mass effect on the initial CT with no changes on the control CT; only 53.2% of the patients with TCDB i or ii were monitored.

Of the 1035 monitored patients with an abnormal CT, 557 (54%) had high ICP. Fig. 7 shows the correlation between the final CT and the ICP response and, as can be observed, the higher incidence of unmonitored patients belonging to categories i, iv and vi. TCDB type iv was the most correlated with high/uncontrolled ICP.

Fig. 7.
(0.09MB).

Relation between the final CT and ICP levels.

Fig. 8 shows the frequency of monitoring by year and adherence to the BTF Guidelines. If we exclude the “unsalvageable” cases who had a >80% chance of dying prematurely within 48h (1622 patients), adherence to the BTF Guidelines was 63.4%.

Fig. 8.
(0.19MB).

ICP monitoring frequency trend and adherence to the BTF Guidelines.

Multivariate study

Table 3 and Fig. 9 show the results from these studies.

Table 3.

Multivariate study.

Variable  OR (Wald 95% CI) 
Logistic regression study for predicting surgery
Age  0.97 (0.96–0.98)  <0.0001 
1996–2004  0.66 (0.48–0.89)  0.0081 
2005–2012  0.37 (0.26–0.52)  <0.0001 
Clinical decline  2.92 (2.23–3.81)  <0.0001 
Motor score (1–4 vs 5–6)  1.65 (1.21–2.25)  0.0017 
Cistern compression  2.72 (2.01–3.70)  <0.0001 
Mass volume (25 cc)  7.45 (5.34–10.40)  <0.0001 
ICH  2.00 (1.54–2.60)  <0.0001 
EDH  5.31 (3.62–7.79)  <0.0001 
SDH  2.94 (2.17–3.98)  <0.0001 
Multivariate logistic regression model for predicting ICP monitoring
Age  0.97 (0.96–0.97)  <0.0001 
1996–2004  2.21 (1.71–2.85)  <0.0001 
2005–2012  1.36 (1.04–1.78)  0.0229 
ICH  2.15 (1.72–2.68)  <0.0001 
SAH  1.80 (1.41–2.31)  <0.0001 
Surgery  5.95 (4.58–7.73)  <0.0001 
Logistic regression study for predicting high intracranial pressure
1996–2004  0.68 (0.46–1.00)  0.0537 
2005–2012  0.30 (0.18–0.49)  <0.0001 
Clinical decline  2.42 (1.60–3.65)  <0.0001 
Cistern compression  3.36 (2.23–5.07)  <0.0001 
IVH  2.22 (1.50–3.28)  <0.0001 
SAH  2.05 (1.30–3.24)  0.0020 

CI, confidence interval; EDH, epidural haematoma; ICH, intracerebral haematoma; IVH, intraventricular haemorrhage; OR, odds ratio; SAH, subarachnoid haemorrhage; SDH, subdural haematoma.

Fig. 9.
(0.2MB).

Area under the curve: (a) surgery prediction; (b) ICP monitoring prediction; (c) high ICP prediction.

Factors that influenced the surgical treatment

The variables included are those usually used in the Guidelines,24 as all are relevant when deciding the need for surgery. The age and number of patients undergoing surgery have an inverse relation with the surgery; i.e., older patients underwent surgery less frequently, and the frequency of the surgery decreased significantly versus the first time period (1987–1995). The most important surgery-related prognostic factor is injury volume >25cc. Other independent surgery-related predictive factors are clinical decline, a low motor score, cistern compression and the presence of any type of intracranial haematoma (EDH, SDH, and ICH). The AUC for this model was 0.8876.

Intracranial pressure monitoring

The predictive factors associated with placing a sensor to measure ICP (monitoring vs no monitoring as an endpoint) are: (a) there is a significant difference in monitoring admitted patients in the second and third time periods versus the first period (1987–1995); (b) surgery was strongly correlated with monitoring; (c) other related factors were the presence of SAH and ICH. Age is an inverse predictor (older patients were monitored less). The AUC for this model was 0.7615.

High/uncontrollable intracranial pressure

The predictive factors independently associated with the presence of a high ICP were: (a) time periods: in the first time period (1987–1995), there was a significantly higher incidence of high ICP; (b) clinical decline; (c) cistern compression; and (d) presence of SAH and IVH. The AUC for this model was 0.8012.

Discussion

As we have already seen in previous studies,1,30 a change in the epidemiological and clinical characteristics of sTBI patients has occurred. This trend has also been observed in other Western countries31,32; this new scenario is due to a drop in the sTBIs caused by road traffic accidents. However, the incidence of non-road traffic accident-related sTBIs (falls) in elderly patients has dramatically increased. In this new study, a continuation of the previous one, we found a different sTBI patient profile, with different structural patterns, showing significant changes in the CT findings, surgical procedures and ICP monitoring over the study time period, prompting a change in how these patients are managed in recent years.

Characteristics of the initial computed tomography

The Marshall classification is a valid instrument for descriptive and prognostic purposes and it is routinely used to stratify patients according to morphological criteria, presenting a high degree of agreement among observers.12 Moreover, its relevance has increased over the years due to the progressive difficulty in Glasgow Scale assessments and due to the intubation and early sedation policies more frequently practiced in sTBI today. Although this classification is the most used at present, it also has disadvantages, such as not taking into account the presence of SAH or IVH. Adding these findings to the Marshall classification increases sTBI predictive power, improving patient stratification in randomised studies.9–12 Maas9,10 observed a 30–35% discrepancy when using CT to classify these patients, due to interobserver variability in coding these cases. He therefore recommended using this classification jointly with the individual findings to improve prognostic reliability.

Normal or diffuse CT scans (TCDB I and II) accounted for 42.3% in our study and ranges between 25% and 55% in other studies,33–36 reflecting the different inclusion criteria of the IMPACT10,37 and CRASH38 studies. Our work brings to light an upward trend over time in type ii injuries (34.7% to 44.1%), with SAH and IVH also increasing significantly.

Type iii and iv injuries accounted for 21.7% of the patients in our study, and range between 11% and 25% in other studies.2,3,33–38 A decrease in TCDB type iii and iv was observed from 23.5% in 1987–1995 to 15.3% in the last period.

Mass lesions, whether or not they were operated on (type v and vi) accounted for 36% of the patients in our study. This proportion varies between 30% and 48%,2,3,33,36–38 or between 55% and 63% in the studies conducted in the United Kingdom.34,35 This figure depends on the different indications for surgery and the type of mass lesions. In our study the frequency of non-evacuated mass lesion was 6.8%, varying from that found in other studies2,3,33–36 between 5% and 27%. The frequency of mass lesions had a uniform distribution across the 3 time periods; however, this frequency is off-set by a significant increase in the incidence of non-evacuated mass lesions (CT type vi). These differences are in relation to the epidemiological change described in our patients. Despite the lack of studies such as ours that describe the change over time in the CT category, it is certain that older studies describe a higher frequency of evacuated mass lesion3,34 than more recent studies.33 In addition, not many studies have been published that take into account combinations of intracranial mass lesions.39 We found an incidence of 16% for EDH (single and combined), within the range of other studies which place it between 9%3 and 21%.39 The incidence of SDH was 41.6%, similar to that of an Austrian study39 or the series by Bullock24 (49%), but clearly higher than that of the TCDB (29%).3 The incidence of ICH (isolated or combined) was 41.2%, varying in other studies between 35%24 and 69%.39 The most common combination was SDH and contusion, which was observed in 16%, and the least common were a combination of EDH+SDH+ICH (3.1%) and EDH+SDH (1%), both similar to the Austrian study.39

The association between SAH and advanced age in autopsies of sTBI patients is a well-known finding. In our study, we found a 74% incidence of SAH, significantly higher than that found in other studies, especially in combination with TCDB III and IV (87.7% and 89.7%, respectively). The IMPACT analysis, conducted by Maas,9,10 found that SAH varied between 28% and 79%, with a mean of 46%. There was a greater association of SAH in patients with TCDB type iii (58%) or type iv (71%), than in TCDB type ii (44%) or TCDB type v/vi (49%). In the more recent studies by Selfotel and Bradykor, the incidence of SAH was similar to that of our study. In the EBIC,2 this incidence varied between 33% and 57%, and in other more recent studies, between 43%33 and 56%.39 The variations in the frequency of SAH between the published series likely reflect the variability of the populations included in the studies: patients with less severe injuries would have a lower incidence of SAH. In our study, we observed an upward trend in the frequency of SAH over time; in addition, in another study (Gómez: unpublished data), we found a clear correlation of SAH with advanced age and TCDB type iii and iv, which could be related to the greater fragility of the arteries in elderly patients. Servadei11 demonstrated that the presence of SAH was correlated with advanced age and a poor motor response.

Control computed tomography scan

sTBI is a dynamic process in which the injuries can evolve, which makes the control CT essential. Lobato8 found a variation in around 50% of the initial CT classifications in sTBI patients (GCS8), with the best predictor of the final outcome being the control CT. Servadei40 published a radiological progression in the Marshall classification of 16% of patients with moderate sTBI (GCS 3–12). Recent studies demonstrate that the injury generally progresses between 6 and 9h after the injury and it is greater if the initial CT is performed within the first 2h. ICH can grow in 25–45% of cases,41–44 therefore the control CT is always indicated if there is clinical decline or an increase in the ICP.8,45

The drop in the incidence of decline from the initial CT in the last two time periods versus that observed in 1987–1995, together with the decrease in clinical decline and hypoxia that we saw in the first study,1 may reflect the improved pre-hospital care these patients receive, with a faster transfer to the hospital and better monitoring versus the first time period.

Surgical treatment

In total, 721 patients (39.4%) underwent surgery, most (585) in the first 12h, a similar figure to that from the EBIC,2 although there is wide variability in the published series (23–69%14,33,34,39). The reasons for these differences are unclear, but they may be due to a different case-mix. The haematoma type is an important factor when issuing the prognosis. It is therefore an aspect that should be considered when describing these sTBI patients.

The treatment for haematomas after an sTBI is not yet fully determined. The technique used and the appropriate time for the surgery are disputed. The published surgical guidelines do not have a robust scientific basis.24 Our indications for surgery are similar to these. We found in our multivariate study that a volume above 25cc is the strongest independent factor associated with surgical treatment, similar to that published by other authors.24,46

The indications for surgery for a significantly sized EDH and SDH are unquestionable; all the authors agree that they should be operated on as soon as possible to prevent brain herniation.24 In our study, early surgery was performed for these injuries in 89.4% and 87.5% of cases, respectively; however, evacuating ICH presents greater variability. The mean reason for performing early surgery in these cases is to prevent the development of secondary brain injuries.14,24 In a randomised, prospective study, Mendelow (STITCH [Trauma])15 found better outcome in cases that underwent surgery before a decline occurred than in patients who underwent surgery after that happened. STITCH had to be stopped due to a lack of resources. A larger trial is needed to confirm this trend towards early surgery. In our study, early ICH surgery fell to 70.3%, which reflects this discrepancy.

Haematomas do not always have to be evacuated; select cases have been found with a small or moderate volume and a discrete mass effect in which the evolution can be followed with adequate clinical surveillance via serial control CTs and ICP monitoring until the injury is resorbed. In our cases, 418 (54.8%) of the 762 total SDHs underwent surgery, although this percentage is lowered by including patients who did not undergo surgery because of old age and unsalvageable patients with a poor clinical situation. An important finding in our study is demonstrating a drop in the surgical treatment of extra-axial injuries (EDH and SDH) between 1996 and 2012, versus the first time period (1987–1995), comparable to a recent U.S. study.47 The reasons for this finding are difficult to explain, but it may be due to a change in clinical practice (less surgery in patients with subdural haematomas and advanced age), as may be deduced by the increase in CT type vi in the last period or to a different case-mix. The frequency of EDH remained stabled over the three periods, but the frequency of SDH increased from 38.1% to 52.7% in the last period.

The standard treatment for evacuating space-occupying lesions with a mass effect is craniotomy, with the aim of decreasing the pressure on the brain.24 Primary DC can be performed for the same reasons, or afterwards to decrease medical treatment-resistant intracranial hypertension (secondary DC). The DECRA study48 did not demonstrate any improvement in the final outcome of patients in whom a secondary DC was performed, and a systematic Cochrane study16 did not find evidence to recommend the routine use of DC in these patients. One study has shown an increase in neurosurgeons using this technique; nevertheless, the surgical criteria have not been firmly established.49,50 In general, the literature suggests, but does not prove, that DC is the intervention of choice. In our practice, a trend towards performing this procedure is shown, especially after evacuating an ICH, which is the most commonly used procedure at present. At this time, there is an on-going study to try to assess the efficacy of this RESCUEicp treatment (www.rescueicp.com).

Intracranial pressure monitoring

Marshall51,52 and Miller18 were the first to demonstrate the relationship between ICP and the final outcome of sTBI patients. Monitoring this parameter has been demonstrated to be of great help when detecting incipient secondary damage or the development of a haematoma,45,53 as high ICP levels are correlated with mortality. In the eighties, many authors predicted the use of ICP-targeted therapies, comparing the mortality obtained in their cases with a systematic ICP treatment (28–36%)18,52 with the mortality observed in a previous study by Jennett et al.34 (50%). The BTF Guidelines were published in 1996 and recommended that ICP should be used to monitor all “salvageable” sTBI patients (GCS 3–8 after resuscitation) and an abnormal CT.17 In these patients, the probability of having high ICP was around 50%, a similar figure to that reported in this study.

Although monitoring and intensive ICP treatment have since become standard today, there is no robust evidence that demonstrates an improvement in the final outcome. The only randomised, prospective study conducted to date has not found a benefit to monitoring patients over a symptom-based protocol and the CT findings. The evidence for using ICP monitoring was not conclusive19; however, these results were debated at a meeting of experts, who recommended continuing with the ICP monitoring policy.20 Other European studies and a recent systematic review21,54 also found no benefit in the use of monitoring. One study conducted in the United Kingdom demonstrated the wide variability that still exists in the use of this technique, which shows a lack of consensus on how to manage these patients.55

In our work, ICP was monitored in 57% of the patients, and was more commonly used in the second time period, perhaps due to the coincidence that our department was participating in several international clinical trials. The concept of “salvageable” is a vague term used differently by authors. In our case, it was defined as those patients who had a greater than 80% chance of premature death (48h)28. If we exclude these cases, we have a 63.4% adherence to the BTF Guidelines, comparable to that recently published at European sites (38–67%).20,22,33,56 In the initial surveys conducted in the United States57,58 after the BTF Guidelines were introduced, it was demonstrated that there was wide institutional variability in how sTBI patients were managed. Hesdorffer and Ghajar59 demonstrated that, although adherence to the Guidelines improved between 1990 and 2006, non-compliance continued to be 34.5% among the 413 participating sites in the study.

In our multivariate analysis, we found that patients with SAH, ICH and those who underwent surgery had a significant correlation with monitoring. Furthermore, we showed that it has been used more diligently since 1995. Age showed an inverse relationship, i.e., older patients were rarely monitored. According to our multivariate study, high ICP correlates with cistern compression and with the presence of SAH or IVH. Age was not a prognostic factor for high ICP, although this finding could be biased by the presence of atrophy in elderly patients. The limited predictive value of the midline shift observed in the initial CT may be because the mass lesions with shift undergo surgery before ICP monitoring.

Does the final outcome improve by using therapies aimed at controlling ICP? This is a difficult question to answer as the patients are screened for monitoring. Although in this paper we did not discuss the final outcome, which will be the subject of a later study, we did not find any significant differences between the monitored and unmonitored patients in terms of the final outcome by year, but in the multivariate study a very significant drop was found in high ICP. This drop could be due to implementing the BTF Guidelines in 1996, although it may also be due to a different case-mix.

In more recent U.S. studies,60 which grouped the patients treated without monitoring and those treated with monitoring and a targeted ICP-lowering therapy, a 12% drop in mortality was found and a 6% increase in favourable outcomes, which suggests that monitoring has a positive impact on the final outcome. Gerber et al.23 demonstrated a marked reduction in mortality over 9 years, which could be associated with an increase in the incidence of monitoring. Farahvar et al.61 demonstrated a 64% drop in 2-week mortality in those patients who responded to the ICP-targeted therapy, after adjusting for the predictive factors for mortality. The only demographic factor correlated with treatment response was age, which is in contradiction with our findings, in which age is not an independent factor of high ICP. In a recent study in which compliance with the BTF Guidelines was 46.8%, Talving et al.62 demonstrated a significant improvement in survival, although, like in our study, elderly patients were monitored less frequently.

Limitations

Similar to the EBIC study, ours is an observational study, which implies certain problems inherent to this type of study, such as the lack of a central evaluation committee and external auditing, which may bring into doubt the quality of the collected cases. There was also no centralised CT interpretation, although this was performed by the senior authors with extensive experience in handling these cases (PAG, AL). Despite these disadvantages, the data quality has been satisfactory, given that little data was lost and the data obtained is consistent and tested by an internal validation process.

Conclusions

As a consequence of the epidemiological changes observed in sTBI patients over the last 25 years, a different morphological injury pattern is described, reflected in the CT, which involves a different clinical practice during this time period.

Conflicts of interest

The authors declare that they have no conflicts of interest.

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Please cite this article as: Gómez PA, Castaño-León AM, Lora D, Cepeda S, Lagares A. Evolución temporal en las características de la tomografía computarizada, presión intracraneal y tratamiento quirúrgico en el traumatismo craneal grave: análisis de la base de datos de los últimos 25 años en un servicio de neurocirugía. Neurocirugia. 2017;28:1–14.

Copyright © 2016. Sociedad Española de Neurocirugía
Neurocirugía (English edition)

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