Scientific Papers

Burden, risk factors, neurosurgical evacuation outcomes, and predictors of mortality among traumatic brain injury patients with expansive intracranial hematomas in Uganda: a mixed methods study design | BMC Surgery

There is a significant deficit of reliable data and research on the extent of the effect of EIH on neurosurgical outcomes, particularly from the prevalence, risk factors, predictors of mortality, QOLIBRI, and functional outcomes perspectives in Uganda and related low-and-middle-income countries (LMIC). Consequently, this study set out to assess the burden, risk factors, surgical evacuation outcomes, and predictor of mortality for EIH following traumatic brain injury (TBI). Through the fitness of our study design, we were able to collect adequate information and data regarding TBI patients, factors contributing to EIH, predictors of mortality, and related surgical outcomes to further inform community-based interventions. This study found that the prevalence of EIH was 59.3% in adult TBI patients and risk factors for EIH for adult TBI patients included increased age above 39 years, smoking, having severe systemic disease, and the presence of swirl sign (Tables 1, 2 and 3).

In addition, the 16 months Kaplan Meier mortality was 53.4% (95% CI = 28.1 to 85.0) and predictors of mortality were age, MAP values above 95 mmHg, low GCS, a complication such infection, spasticity, wound dehiscence, CSF leaks, having GOS < 3, QOLIBRI of less than 50, ASDH, contusion, and EIH (Fig. 3 and Table 6). Furthermore, the Kaplan–Meier curve displayed increased mortality between the 5th and 8th month after traumatic brain injury. This indicates a critical period during which individuals are at higher risk of death. There could be several factors contributing to this observation including delayed complications, rehabilitation challenges, and long-term consequences. Some complications or health issues related to TBI may take time to manifest and become more severe. These complications could include infections, neurological deterioration, or secondary injuries that lead to increased mortality during this specific time frame. The 5th to 8th month after TBI is a crucial phase of rehabilitation for many patients. It is a period when individuals may face challenges in their recovery, such as motor and cognitive impairments, emotional and psychological difficulties, or difficulties adapting to daily activities. These challenges can indirectly contribute to an increased risk of mortality. TBI can have long-lasting effects on an individual’s overall health and well-being. The 5th to 8th-month post-injury may be a critical time when some individuals experience progressive deterioration in their condition or encounter complications related to TBI, leading to higher mortality rates.

Sociodemographic characteristics and injury factors of patients with EIH

Demographic characteristics in this study showed that the mean age of the study participants was 37.5 ± 17.4 years. Majority of the participants were male (80.6%). Almost half of the study participants were bodaboda riders(46.9%), the majority of patients were coming from rural areas and 60.8% of patients were married (Table 1). Bodaboda riders are the main contributor of TBI, hence expansive hematoma. These findings agree with previous studies in Uganda and elsewhere [28]. Given the high rate and early time course of this phenomenon, participants of different socio-demographic and other characteristics were assessed for the articulated result. In the univariate model, 43.5% of the participants were between 18 and 28 years. This finding concurs with a study conducted by Maas et al. [1] which revealed that TBI affects the more productive age groups, which can put additional pressure on existing economic and healthcare burdens [1]. In addition, 56.2% of TBI occurred in rural areas in Uganda. This result is consistent with a study conducted by LaGrone et al. [29], which showed that the high incidence of TBI in developing regions may be partly due to an increased number of individuals with a high demand for unsafe movement and partly due to poor infrastructure. Other contributing factors include inadequate enforcement of traffic laws, alcohol abuse, and inefficient response from an already weak healthcare system [29].

According to this study, the mean age (SD) of patients with EIH was statistically different from that of patients without EIH (42.3 ± 17.9 vs. 30.5 ± 14.0 years, p = 0.000). It is consistently demonstrated that increased age is associated with intracranial hematoma progression and age-related structural deficiencies in the microvasculature, endothelial loss, and lower resting CBF making people more susceptible to developing EIH [2, 13, 30, 31].

The proportion of traumatic brain injury patients presenting with expansive hematomas

The prevalence of EIH among TBI patients presenting at the Accident and emergency unit at MNRH was 59.3% among adult TBI patients. These findings were consistent with previous studies which showed that the rate of EIH following TBI ranged from 38 to 59% of cerebral hemorrhages [6, 11, 32,33,34], but was lower than a study by Adatia and colleagues who reported it to be as high as 75% [13]. These variations may, in part, have resulted from the absence of a common definition of EH in the literature [35,36,37]. The timing between baseline (first scan at the initial presentation at the Accident and emergency unit) and follow-up scans, research inclusion criteria, and various hematoma volume measuring techniques, on the other hand, could all contribute to this variation in proportion among studies [13]. In addition, lack of standardized protocol on EIH case definition and hence timely management of the case often leads to unfavorable outcomes and poor survival rate long term, therefore there is need to continuously monitor TBI patients with intracranial hematoma with evidence on initial CT scan for any progression of EIH and thus instituting appropriate case management plan including surgical evacuation. From the findings, a protocol could be put in place for risk stratifying those patients to determine how large of an EIH would lead to specific surgical or medical interventions. The study also determined that among TBI patients admitted to MNRH, following 2 CT scans with evidence of increased hematoma volume of over 33% or absolute hematoma growth over 6 mL from the initial scan, EIH was common in all subgroups of intracranial hematomas. The likelihood of EIH for a given lesion was 51.5% for EDH, 51.1 for SDH, 47.6% for ICH, 37.5% for contusions, and 40% for SAH. This result correlates with reports from several series, which demonstrated that the rate of EIH after TBI ranged from 38 to 59% of intracranial hemorrhages [6, 11, 32,33,34], but presented a lower prevalence compared to results from a study conducted by Adatia and colleagues, who indicated the rate of EIH to be 75% [13]. These differences, in part, may have been due to a lack of standardized definitions of EIH across the literature [35,36,37]. However, different methods of hematoma volume assessment, study inclusion criteria, and timing between baseline and follow-up scans may explain this discrepancy in proportion across studies [13]. In addition, the findings from the study showed that intracranial hematomas enlarged over time and there were 43.2% of patients developed EIH over 72 h. The findings differ from the findings of the study conducted by Adena et al.(2012), which reported that over 75% of intracranial bleeding occurred within 2 h from the time of the initial head CT scan [4] (Table 4). Therefore, there is variation in the time of EIH occurrence on the initial first CT scan.

Risk factors leading to expansive intracranial hematoma development following TBI

According to this study, TBI patients aged 48 years and above were 1.56 times more likely to be at risk for EIH than their counterparts. Similarly, TBI patients aged between 39 to 48 years were 1.54 times more likely to be at risk for EIH than TBI patients in other age groups, which is consistent with previous studies [8, 31, 36, 38]. In addition, the prevalence risk of developing EIH in adult TBI patients was 1.21 times more likely in patients with smoking behavior which is lower compared with a study conducted in Korea (sixfold) [39]. The possible explanation for increased likelihood of EIH in smokers may be due to reduced cerebral blood flow within the penumbral zone and greater fragility of vessels [13, 40].

In the present study, TBI patients with severe systemic disease, on the other hand, were 1.36 times more likely to develop EIH than their counterparts. This finding aligns with previous studies where severe systemic diseases like hypertension and diabetes were associated with EIH [5]. Systolic blood pressure (SBP) is correlated with EIH [5, 41], and patients with post-admission SBP more than 160 mmHg are at a considerably higher risk for expanding hematomas [41, 42]. This may be partially explained by the ongoing rupture and bleeding of small blood vessels, making early blood pressure a potential therapy target. This study found that having a background of hypertension was positively related to hematoma enlargement. In addition, patients with a history of hypertension are four times more likely to experience intracranial hematoma expansion than those without a past of hypertension. Endovascular malfunction and cerebrovascular remodeling were seen among patients with chronic hypertension. These changes may be associated with raised blood–brain barrier permeability [13, 43].

Lastly, TBI patients with the presence of a swirl sign have a 2.26-times higher risk of developing an EIH when compared to patients who had no swirl sign. This result was supported by a recent meta-analysis study which revealed that swirl sign has a high specificity for predicting EIH with a pooled positive likelihood ratio of 2.2 (95%CI 1.8–2.5) in intracerebral hemorrhage [44]. In other studies, this imaging marker was associated with EIH and overall poor outcomes [45,46,47,48,49,50]. This result, however, is inconsistent with research conducted by Boulouis et al., where the Swirl sign was not related to EIH, as revealed by the multivariate analysis [46]. Although our study suggests that the presence of swirl signs is a risk factor for developing EIH, further exploration is required to confirm the role of this factor in EIH prevalence.

Treatment modalities, evolution, type, timing of surgery, complications, baseline quality of life, and predictors of mortality of intracranial hematoma patients following TBI

In this cohort of EIH patients following TBI, 33 (10.2%) died between the 16th of June 2021 to the 17th of December 2022 with increased age (> 31 years), increased MAP (> 95 mmHg), decreased GCS (< 12), decreased GOS (< 3), decreased QOL (< 50%), SDH, contusions, infection source from GIT, URT, perinephric abscess, fever, platelet dysfunction, skin abscess, wound dehiscence, spasticity, and CSF leakage all contributing to increased risk of death. Older age is generally associated with a higher risk of mortality in various medical conditions, including traumatic brain injuries. Advanced age may lead to reduced physiological reserves and increased vulnerability to severe injuries. Elevated MAP values (> 95 mmHg) can indicate systemic hypertension, which may exacerbate intracranial bleeding and increase the risk of mortality. These findings concur with a study that reported that the survival of TBI patients were low and that elevated blood pressure and nonreactive pupils were predictors of mortality [51]. A lower GCS (< 12) score suggests more severe brain injury and impaired consciousness. Therefore, patients with a decreased GCS were found to be at higher risk of death due to the severity of their brain trauma. Furthermore, the mortality rate among severe TBI (GCS ≤ 8) patients with intracranial hematomas was 63.6%, which is higher compared with a study conducted in Ethiopia where the cumulative incidence of death was 49.71% [51], but slightly lower compared with a prospective study in Uganda where the mortality among severe TBI patients with hyperglycemia at MNRH was 68.8% [52]. A GOS (< 3) score below 3 indicates a poor outcome and increased mortality risk. A low QOL (< 50%) score indicates compromised well-being and may be associated with more severe injuries and an increased risk of death. In addition, the present findings differ from a retrospective study where the mortality rate observed among severe TBI patients was 21.8% [53]. This observed difference in mortality rate can be explained by the sample size, changes in the treatment protocols, and accessibility to intensive care units.

The present study had limitations including, missing values and recall bias on some of the information during the follow-up period. This was expected and the research team increased 10% of possible dropout or missing data. The prospective nature of the study required that patients be followed up for periods including after discharge. This carries with it the risk of loss to follow-up, which has partly been addressed by adjusting the sample size for loss to follow-up. Phone calls were used to help in addressing the loss of follow-up. Patients had CT scans when their neurological condition deteriorated. Even in the absence of neurological decline, changes in serial CT scans may be seen. However, previous studies have not found any abnormalities on serial CT scans in the absence of neurological deterioration that results in therapeutic decision-making. Therefore, the rate of hematoma enlargement may have been underestimated in this analysis. Most of such undetected enlargements, however, are most likely asymptomatic and do not require any therapeutic interventions. Neurological examination was performed by the attending neurosurgeons, senior neurosurgery residents, or the trained research assistants in the Neurosurgery Department. The date, time, and results of the initial and all subsequent scans were recorded. Therefore, interobserver variation can be expected among the different neurological examinations. Nevertheless, this is one of the largest studies to date on EIH, which allows our team to contribute to the broader conversation on TBI in low-resource settings. The current study highlights the burden of EIH, the associated risk factors, the surgical outcomes, and predictors of mortality among TBI patients admitted to the MNRH emergency unit as well as country-wide in Uganda following RTA, assaults, and falls. Future studies must continue to assess (1) the effect of timing on surgery and patient outcomes among adult patients with EIH; (2) survival trends and predictors of mortality among adult patients with EIH; (3) long-term health-related quality of life changes for adult patients in Uganda with or without traumatic EIH.

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