Department of Neuroscience, Section of Neurosurgery, Uppsala university, Uppsala, Sweden
Published Date: 20/08/2021.
*Corresponding author: Per Enblad, Department of Neuroscience, Section of Neurosurgery, Uppsala University Hospital, SE-751 85 Uppsala, Sweden
The aim of this investigation was to study patient characteristics and long and short-term results specifically in patients primarily admitted to a neurosurgical department and operated acutely for acute subdural hematoma (ASDH) or epidural hematoma (EDH). Forty-five patients operated at Uppsala university hospital 2008-2019 were included (ASDH=39 and EDH=6): 28 men and 17 women, mean age 61 years (range 8-93), 76% >1 co-morbidity, 44% on anticoagulants/antiplatelets, mean hematoma width 20mm (range 7-37) and mean midline shift 9mm (range 0-26). Seventy-three percent had >3 characteristics indicating vital surgical indication, i.e preoperative unconsciousness (GCSM <5), pupillary dilation (one or both eyes), lucid interval, hematoma width >10 mm, midline shift >5 mm. Postoperative CT was improved in all cases. Proportion of patients responding on commands increased from 36% at admission to 69% at discharge. Favorable outcome was seen in 36% and 31% died (all ASDH, mean width 21mm, range 12-35, mean shift 13mm, range 4-26; mean age 70 years, range 43-87; 64% not responding to commands and 57% abnormal pupils on admission). In conclusion, substantial mortality and morbidity were found in patients operated for ASDH and EDH even if primarily admitted to a university hospital and operated by a neurosurgeon. Taking into consideration the substantial presence of negative pre-operative prognostic characteristics, the results may afterall be interpreted as relatively favorable. An important observation was that also patients with poor prognostic factors may sometimes have favorable outcome when operated without delay. The proportion of favorable outcome achived despite that many patients displayed features related to poor prognosis, indicates that the decision making to operate was appropriate, accepting also patients indicative of having relatively poor prognosis.
Keywords: Traumatic brain injury; Acute subdural hematoma; Epidural haematoma; Acute neurosurgery
Acute subdural hematoma (ASDH) and epidural hematoma (EDH) are common types of traumatic brain injury (TBI). ASDH comprised 30% and EDH 22.5% of 13,962 TBI patients registered in an European database 2001-2008 [1]. The corresponding figures for Sweden were 46% and 6%, respectively, among in-hospital treated patients 1987-2000 [2]. A review of the literature made for the Brain trauma foundation found mortality rates between 40-60% for ASDH [3] and around 10% for EDH [4]. It is well known that a delay of surgical evacuation may be detrimental both in ASDH and EDH, especially in patients losing consciousness [5-9]. In Sweden, as well as in many other countries, there may be long distances to the nearest neurosurgical department and many patients are primarily admitted to local hospitals and transferred secondarily to neurosurgical departments. When patients are admitted primarily to a university hospital with neurosurgery the time factor is usually limited and one are probably more inclined to take the chance to operate even patients with less favourble prognostic factors. It would be of interest to particularly study this group of patients. The aim of this investigation was therefore to study patient characteristics and long- and short-term results specifically in patients primarily admitted to a neurosurgical department and operated acutely for EDH or ASDH.
The Department of Neurosurgery at Uppsala University Hospital (UUH) provides neurosurgical care for 6 counties with one another university hospital, 5 county hospital and various smaller local hosptals. The total catchment area includes around 2 milj inhabitants of which 200,000 live in the Uppsala county region and are referred primarily to UUH. The longest distance from the most distant local hospital within the catchment area is 300 km. TBI patients treated between 2008 and 2019 at the Department of Neurosurgery, UUH, were selected from the Uppsala TBI register [10]. Inclusion criterion were: 1. ASDH or EDH (dominating injury); 2. acute admittance primarily to UUH and 3. acute neurosurgery performed at UUH. During this time 1102 TBI patients treated in Uppsala were included in the TBI registry. From this population, 391 patients were identified with ASDH or EDH as the dominating injury. Three-hundred-forty-six patients were primarily admitted to a local hospital and therefore excluded from further analysis, leaving us with 45 patients in the final study population. The following parameters were analyzed: age, gender, former and ongoing diseases, use of anticoagulants/antiplatelets, type of trauma, intoxication, lucid interval, major extracranial injury (requiring hospital care itself), global ischemia (circulatory or respiratory); and neurological reaction grade based on the Reaction Level Scale 85 (RLS) [11,12], presence of pupillary dilatation and paresis, at admission and at discharge from the neurointensive care (NIC) unit or step down unit, respectively. The correspondence between RLS and Glasgow coma scale motor score (GCS M) is described in Table 1.
Table 1 Correspondence between Reaction Level Scale 85 grades (RLS) and Glasgow Coma Scale motor scores (GCS M).
Factors indicating vital indication for surgery were evaluated [13]: 1. Preoperative unconsciousness (RLS 4-8), 2. Pupillary dilation (one or both eyes), 3. Lucid interval, 4. Hematoma width >10 mm, 5. Midline shift >5 mm. Lucid interval was defined as when the patient was awake after the injury and later became unconscious. ICP monitoring, type of ICP monitoring, re-operation <24h and additional surgery during NIC (>24h) were investigated. The hematomas were analyzed regarding type, width, and midline shift on the CT-scans. The radiological outcome of surgery was assessed as improved, unchanged, or worsened by comparing the midline shift and the width of the hematoma between the latest preoperative and first postoperative CT-scan.
Clinical outcome was measured using the Glasgow Outcome Scale Extended (GOSE) after around six months [14]. GOSE categories between 8-5 were assessed as favorable outcome and categories between 4-1 as unfavorable. Unknown or missing data were reported as unknown.
The statistical methods were mainly descriptive. The data analysis was done in Prism Graph Pad 8. Fisher´s exact test was used for a significance assessment of the difference between groups. P-values <0.05 was considered statistically significant.
Demographics
The demographics are presented in Table 2. There were 28 men (62%) and 17 women (38%), and the mean age was 61 years (range 8-93 years). Twenty-seven (60%) of the patients were >60 years. Thirty-four (76%) of the patients had one or more co-morbidity: hypertension or cardiac disease in 49% of all cases, past brain trauma or brain disease in 27%, history of alcohol abuse in 11%. Intoxication at the time of trauma was confirmed in 6 of the cases (13%). Twenty patients (44%) were on anticoagulants/antiplatelets.
The dominating types of trauma were fall accidents (71%) and traffic accidents (20%) (Table 2). Seven of the patients (16%) had one or more major extracranial injury (Table 2), i.e. extremity injury (n=3), facial fractures (n=2), spinal injury (n=2), thoracic injury (n=2), pelvic fractures (n=2), and extensive hemorrhage (n=1).
Preoperative CT-scan findings
The dominant finding on the preoperative CT scan was ASDH in 39 cases (87%) and EDH in 6 cases (13%). The mean hematoma width was 20 mm (range 7-37) and the mean midline shift was 9 mm (range 0-26).
Preoperative neurological status
Preoperatively, 29 patients (64%) did not respond to commands (RLS 3B-8/GCS M 5-1) (Figure 1), 17 patients had pupillary dilatation (38%; 1 unknown) (Figure 2) and 13 patients had paresis (29%; 2 unknown; > RLS 6/flexion not evaluated) (Figure 3).
Table 2: Demographics of the study cohort.
* Individual patients may have > 1 condition.
Figure 1: RLS at admission and discharge Fisher’s exact test, conscious (RLS 1-3a) vs. unconscious and dead (RLS 3b–8), p= 0.0029 (n=45).
Figure 2: Pupillary dilatation at admission and discharge.
Figure 3: Paresis at admission and discharge Patients with RLS >5 excluded.
Presence of vital indication
Preoperative unconsciousness (RLS 4-8/GCS M 5-1) existed in 20 patients (44%), pupillary dilation (uni- or bilateral) in 17 (38%; 1 unknown), lucid interval in 11 (24%; 6 unknown), hematoma width >10 mm in 39 (87%), midline shift >5 mm in 37 (82%) (Table 3). One factor indicating vital indication for surgery was present in 7 patients (16%), 2 factors in 17 (38%), 3 factors in 4 (9%), 4 factors in 15 (33%) and 5 factors in 2 (4%) (Table 3).
ICP monitoring
ICP was monitored in 32 patients (71%); 29 received an intraparenchymal pressure device, one received an external ventricular drain, and two received both.
Radiological outcome
Postoperative CT showed improvement in all patients who performed a postoperative scan CT examination (2 patients deteriorated and died before this was done).
Reoperation
A reoperation < 24 h was performed in one patient with removal av remaining hematoma and 5 patients had additional surgery later during NIC.
Short term neurological outcome
The mean duration from admission to discharge from the NIC unit or step down unit was 19 days (range 1-93). The proportion of patients responding on commands (RLS 1-3A/GCS M 6) increased from 36% (16/45) to 69% (31/45) at discharge (p=0.0029) (Figure 1). There were no obvious improvements regarding presence of pupillary abnormality (Figure 2) and presence of paresis (Figure 3).
Long term neurological outcome
Clinical outcome was assessed in mean after 7 months (range 5-10). Fifteen patients (33%) had good recovery, 1 (2%) moderate disability, 12 (27%) severe disability, 1 (2%) vegetative state, 14 (31%) had died and 2 patients (4%) were lost to follow-up (Figure 4). The outcome was classified as favorable (good recovery and moderate disability) in 16 patients (36%) and unfavorable (severe, vegetative, and dead) in 27 (60%). The 14 patients who died, had all ASDH and they died within 21 days after the trauma, 8 before discharge from NIC and 6 after discharge. When different potential prognostic factors were related to outcome (favorable and unfavorable), age >65 years and ASDH were significant negative prognostic factors and use of anticoagulants/antiplateles showed a tendency to be related to unfavorable outcome (Table 3). The patients who died had a mean age of 70 years (range 43-87), 36% (5/14) were RLS 7-8, 57% (8/14) had abnormal pupils, and the mean width of the hematomas was 21 mm (range 12-35) and the mean midline shift was 13mm (range 4-26) on CT (Table 4).
Table 3: Patient’s characteristics and clinical outcome.
* Fisher’s exact test, unknown excluded (n=45).
Table 4: Characteristics of the patients who died.
Figure 4: Clinical outcome according to Glasgow outcome scale extended (GOSE). GR: good recovery, MD: moderate recovery, SD: severe disability, VS: vegetative state, D: dead. H/L: higher/lower (n=45).
In this study of patients primarily admitted to a neurosurgical department and operated acutely for an EDH or ASDH, we found that ASDH was more common than EDH and associated with a significantly worse outcome. We also found that males were overrepresented and that traffic accidents and falls were the most common causes of trauma. Hence, our cohort was similar to those in other comparable studies with regard to these results [1,15,16]. However, our patient cohort showed a high prevalence of unfavorable prognostic factors. The prognostic factor that most clearly differed from other studies [1,15,16] was age; the median age in our cohort was 68 years, and 60% of the patients were older than 60 years and 55% were older than 65 years. Furthermore, 76% had a previous disease/comorbidity, and 44% used anticoagulants/antiplatelets. Since age, history of prior disease, and use of anticoagulants/antiplatelets contribute to poor clinical outcome [1,15,17,18], our cohort was more likely to have less favorable outcome.
Overall, 37% (16/43; 2 unknown) of the patients showed favorable outcome in the particular group of patients studied (EDH: 5/5, one unknown; ASDH: 11/38, 29%, one unknown), which is within the ranges reported by others [7,14,15,19-24]. It is important to analyse the outcome results in detail in order to evaluate whether the decision to operate appears to be reasonable or too optimistic in acute patients admitted primarily to our hospital and if one can identify reliable prognostic predictors. The proportion of favorable outcome achived, despite that many patients displayed features related to poor prognosis, indicates that the decision making to to operate were indeed appropriate. When different potential prognostic factors were related to outcome, we found that age >65 years and ASDH were significant negative prognostic factors, and use of anticoagulants/antiplateles showed a tendency to be related to unfavorable outcome (Table 3). However, the predictive value of those factors were low because a considerable number of patients with age >65 years, ASDH and anticoagulants/antiplatelses had favorable outcome. This finding underline that a judgement that surgery are without chances should be based on a multifactorial analysis.
When evaluating the results, it is also important to look on the degree of vital indication, i.e. how urgent surgery was. With this purpose, five characteristics indicating vital indication were evaluated [13]. It was found that all patients included in the study had at least one parameter that indicated vital indication and a large majority (73%) had three or more (Table 3). Neither any specific characteristic of vital indication nor the number of vital indications showed significant relation to outcome, which was expected since precence of characteristics indicating vital indication was so common. It is, however, notable that also patients with 4-5 characteristics of vital indications had favorable outcome, which shows that such patients may have favorable outcome if acute surgery can be performed without delay. Furthermore, the outcome in relation to presence of vital indications further support that the decision making to operate was appropriate.
The overall mortality rate in this study was 33% (14/43; 2 unknown), all due to ASDH (14/37, 36%; one unknown), which can be compared with the mortality rates of 40-60% in ASDH [3] and around 10% in EDH (4) reported by the Brain trauma foundation. Detailed analysis of patients who died in our study showed a mean age of 70 years and large proportions of patients in RLS 7-8 with abnormal pupils and large hematomas with extensive midline shift on CT (Table 4). Overall, the characteristics of the patients who died indicate that they all had very poor chances to survive, except one 43-year-old man in RLS 3B on admission, although he had abnormal pupil reactions (Table 4). Thus, no obvious potentially avoidable deaths were observed.
When the distances from local hospitals to university hospitals with neurosurgery are long, there has been a tradition in some countries, including e.g. Sweden and Norway, that life-saving evacuations of ASDHs and EDHs may be performed by general surgeons at local hospitals. An earlier regional study in Norway, indicated that the clinical outcome was suboptimal for patients operated at regional hospitals, suggesting that perhaps all patients should be transferred to a university hospital for surgery despite the time delay [25]. In the region where we provide neurosurgical service, we have had a long-standing working routine that a general surgeon with neurosurgical training may perform an acute evacuation of an ASDH or EDH at a local hospital, after consultation of the neurosurgeon on call in Uppsala, if the operation is life-saving and the patient judget not to survive a delay of surgery [13]. The policy includes also that the patient after surgery should be referred to Uppsala for NIC [13]. When we evaluated the results 2005-2010 we found, on the contrary to the Norwegian study [25], relatively favorable results after acute evacuations of extracerebral hematomas performed in the local hospitals [13]. The results of the present study shows that the rate of favorable clinical outcome was even higher (51%) and mortality rate lower (18%) in the local hospitals. It is however important to highlight the differences with younger patients, more cases of EDH, less co-morbidity and less use of anticoagulants/antiplatelets in the local hospital series [13]. Even if the patient materials differ and are difficult to compare, we do think the results of this study concerning patients primarily admitted to a neurosurgical department not in any way contradict continuing the practice of acute evacuation in local hospitals when there is a clear vital indication in our health care reagion. It is however important to underline that the patient should be transferred for NIC after a life saving operation in a local hospital.
There are some methodolocical issues of this study which need to be considered. There were a limited number of patients studied and therefore multivariate statistical analysis or applying statistical model grading systems for outcome prediction was not possible. Detailed information about time courses, e.g. time from detoriation to surgery, was lacking. On the other hand, a strength was that a large proportion of patients with a considerable number of negative prognostic factors were operated, included and analysed, which provided the valuable information that relatively favourable results may be obtained also despite these conditions.
In conclusion, substantial mortality and morbidity were found overall in patients with ASDH and EDH even if they were primarily admitted to a university hospital and operated by a neurosurgeon. Poor results could to a large extent be explained by considerable presence of negative prognostic characteristics, e.g. poor neurological grade, high age, co-morbidity, anticoagulants, and preoperative indications of a clear need for instant surgical evacuation on vital indication. Taking these conditions into consideration, the results may afterall be interpreted as relatively favorable. An important observation was that also patients with poor prognostic factors may sometimes have favorable outcome when operated without delay. The proportion of favorable outcome achived (37%) despite that many patients displayed features related to poor prognosis, indicates that the decision making to to operate was appropriate accepting also patients indicative of having relatively poor prognosis.
Funding
No funding was received for this research.
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethics: The ethical principles for medical research involving human subjects outlined in the Deklaration of Helsinki were followed. Ethical committee approval was obtained and informed consent was obtained from the next of kin.
Declaration of interest: None.