Risk factors for mortality in patients with bacterial meningitis following a neurosurgical procedure: A meta‑analysis
- Authors:
- Published online on: August 21, 2024 https://doi.org/10.3892/wasj.2024.274
- Article Number: 59
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Copyright : © Suryaningtyas et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
Abstract
Introduction
Meningitis is particularly devastating due to its potential to cause severe neurological complications (1). Despite worldwide efforts made for the prevention and treatment of meningitis, the mortality rate associated with the disease remains unacceptably high (2,3). The management and outcomes of patients with meningitis are complicated by various factors, including the post-neurosurgical condition (4,5).
Post-operative bacterial meningitis (POBM) is defined as meningitis that occurs following a neurosurgical procedure. Despite the reported rate of only 10% (6,7), POBM is associated with considerable mortality rates ranging from 20 to 50% (8). Overall, there are no substantial differences in the clinical characteristics of patients with POBM and those with community-acquired meningitis (9). While there is extensive knowledge about the factors affecting the outcomes of patients with bacterial meningitis, POBM remains relatively underexplored.
Several publications have noted that the outcomes of patients with bacterial meningitis are affected by factors, such as comorbidities, initial Glasgow coma scale (GCS) score and an advanced age (10-13). Conversely, the majority of studies addressing the mortality rates of patients with POBM have concentrated on surgical issues, such as the volume of intraoperative bleeding, the duration of surgery and post-operative care, including the use of mechanical ventilation (8,14). However, numerous other factors contribute to the complexity of the disease. Gram-negative bacteria, which are more common in POBM compared to community-acquired cases, are considered to be more resistant to treatment (11,12,15-17). Patients with underlying neurosurgical conditions may have more severe baseline health or additional comorbidities, rendering their condition more difficult to treat compared to community-acquired cases (18). Certain cerebrospinal fluid (CSF) parameters, specifically glucose and lactate levels, indicate the severity of inflammation and may thus be associated with increased mortality rates (19).
Existing knowledge about the effects of age, presenting GCS scores, comorbidities, bacterial types and CSF parameters on infectious cases prompted the authors to investigate the effects of these factors on POBM. The present meta-analysis aimed to determine whether these factors significantly contribute to the mortality rate of patients with POBM.
Data and methods
Search strategy
A comprehensive literature search was performed on the PubMed, ScienceDirect, The Cochrane Library and the Directory of Open Access Journals databases to identify relevant studies. Stringent inclusion and exclusion criteria were applied, and the processes of research selection, data extraction and quality assessment were conducted meticulously. Potential sources of heterogeneity were extensively examined using subgroup and sensitivity analyses.
Types of studies and participants
The present meta-analysis encompasses clinical trials, prospective studies, retrospective studies and case-control studies. Case series with more than two cases were also included. The included studies would have to present data on patients who had undergone neurosurgery or neurosurgical interventions. Studies involving patients who developed meningitis due to an underlying neurological or neurosurgical condition, but were treated conservatively were excluded. To be included in the analysis, studies would have to provide data on at least one of the specified factors.
Types of outcome measures. The primary objective of the present study was to measure the difference between survivors and non-survivors of POBM in terms of the following: i) Risk ratio of mortality as regards the presence of comorbidities; ii) mean difference in age; iii) mean difference of presenting GCS scores; iv) mean difference of CSF lactate levels; v) mean difference of CSF glucose levels; vi) risk ratio of mortality as regards the Gram staining status. The secondary objective of the present study was to conduct a pooled analysis to determine the mortality rate of patients with POBM.
Search methods for the identification of studies
The sampling method utilized in this research involved an online literature search following the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). Searches were conducted on the PubMed, Cochrane, the Directory of Open Access Journals and ScienceDirect databases. The detailed search strategy is outlined in Table I.
Selection of studies
The search results were initially filtered based on the relevance of their titles, followed by the relevance of their abstracts. Non-English publications were automatically excluded. Full-text articles were then evaluated by all authors to identify potentially eligible studies. The reasons for exclusion were documented and reported.
Data extraction and management
The present meta-analysis aimed to examine the clinical, laboratory and microbiological factors affecting the mortality rates of patients with POBM. The clinical factors considered include age, comorbidities and the presenting GCS scores. Laboratory factors encompassed CSF lactate and glucose levels, while microbiological factors involved the Gram staining status of the CSF. Data were extracted and presented in a table. In the case that studies reported the median and range or median and interquartile range for age, GCS, CSF lactate and CSF glucose, these data were converted to the mean and standard deviation using the mathematical methods described in the study by Wan et al (20).
Assessment of risk of bias
All authors evaluated the risk of bias. The biases assessed were those outlined in the Cochrane Collaboration Tool for Assessing Risk of Bias in Randomized Trials, published in 2011(21). Studies that were not clinical trials were evaluated using Cochrane's ROBINS-I tool (22).
Statistical analysis
Statistical analysis was performed using Review Manager (RevMan) 5.4 and STATA, with the results presented as forest plots. Confidence intervals (CI) and odds ratios (ORs) were calculated automatically using the same software. The assessment of heterogeneity was performed using the I2 value during the construction of forest plots with RevMan 5.4 and STATA. In the case that the I2 value was ≥50%, indicating significant heterogeneity, the statistical model was adjusted to a random effects model (21).
Results
Results of the search
The exclusion process, following the PRISMA guidelines, is illustrated in Fig. 1.
Included studies
A total of 80 studies (14,23-101) were incorporated into at least one analysis within the present meta-analysis. Among these, 79 were non-randomized studies, consisting of 61 retrospective studies, nine prospective studies, one propensity-matched cohort, seven case series and three cross-sectional studies. Additionally, there was one clinical trial. The detailed data from each of the included studies are provided in Table II.
Risk of bias of clinical trial
Of note, one study (100) was a clinical trial, and its risk of bias was evaluated using Cochrane's ROBINS II tool. The blinding of outcome assessment was judged to be high-risk due to the failure of that study to adequately address this bias domain (Table III).
The bias of the remaining studies was evaluated using the ROBINS-I tool. Several studies were identified as having a high risk of confounding bias, primarily as they presented data in median form rather than as the mean (14,23,26-29,33-35,38,45,47,53,55,59,61,62,64,65,70,72,74,77,80,81,88-90). As aforementioned, these data were mathematically transformed into mean values, which introduced a potential source of bias (20). Case series were inherently considered to carry a high risk. Of note, three studies were judged to have a high risk in the outcome domain due to incomplete data on the non-survivors (57), unusually large standard deviation (31), and incomplete reporting of GCS scores (58). Studies that presented a high risk in the selection domain typically focused solely on a specific bacterial species or procedure. This approach may not accurately represent the actual number of cases at the respective institutions of the authors (Table IV).
Mortality rate of patients with POBM
A total of 70 studies reported the number of non-survivors, allowing for a pooled analysis of the mortality rates of patients with POBM. These studies cumulatively included 3,235 POBM cases with 853 fatalities. The pooled analysis indicated a median mortality rate of 28% (95% CI, 23-32%). This analysis was considered homogenous (I²=36.19%) (Fig. 2).
Comorbidity and mortality
A total of 19 studies presented data on the presence of comorbidities in both survivors and non-survivors. These studies included 97 fatalities out of 235 cases with comorbidities and 129 fatalities out of 648 cases without comorbidities. The meta-analysis indicated a risk ratio of 1.97 (95% CI, 1.58-2.46), suggesting that patients with comorbidities have a higher risk of mortality (Fig. 3).
Age and mortality
A total of 32 studies reported the mean age of the patients with POBM who survived and those who did not, encompassing a total of 1,705 cases with 497 fatalities. The meta-analysis revealed a small mean age difference of 4.65 years (95% CI, 1.78-7.52) between survivors and non-survivors (Fig. 4). This analysis was deemed heterogeneous with an I² of 71% (Fig. 4).
CSF glucose and mortality
In total, 15 studies provided data on CSF glucose levels for both survivors and non-survivors, comprising a total of 164 non-survivors and 325 survivors. The meta-analysis indicated that the mean CSF glucose level in survivors is 13.55 mg/dl lower than that of non-survivors (95% CI, -20.95 to -6.15). This analysis revealed heterogeneity (I²=67%). The pooled analysis revealed that the mean CSF glucose level in survivors was 34.78 mg/dl (95% CI, 24.03-45.52 mg/dl) (I²=0%), while in non-survivors it was 27.29 mg/dl (95% CI, 12.96-41.63) (Fig. 5).
CSF lactate and mortality
A total of 15 studies provided information on CSF lactate levels, although none differentiated between survivors and non-survivors. Consequently, a mean difference analysis could not be conducted between these groups. Instead, a pooled analysis was performed to determine the average CSF lactate level in POBM cases, resulting in an average of 52.88 mg/dl (95% CI, 38.14-67.62) (Fig. 6).
Gram staining status and mortality
Only seven studies provided data on the Gram staining status of both survivors and non-survivors. These studies included 245 Gram-negative cases and 257 Gram-positive cases. The meta-analysis produced a risk ratio of 1.42 (95% CI, 0.96-2.10; I²=18%), indicating no significant difference in mortality risk between the two groups (Fig. 7).
GCS and mortality
Of note, 10 studies provided data on the presenting GCS scores of both survivors and non-survivors. These studies included a total of 442 survivors and 160 non-survivors. The meta-analysis revealed no significant difference between the two groups (mean difference, -1.69 years; 95% CI, -2.51 to -0.86) (Fig. 8).
Discussion
There is a lack of sufficient studies on the mortality rate of POBM. The present meta-analysis determined that more than one quarter of POBM cases result in mortality (28%; 95% CI, 23-32%). Chouhdari et al (8) reported mortality rate of 50% in their study, while others have reported a considerably lower number (0.3-10%) (4,102,103). This discrepancy may be attributed to the sometimes non-specific clinical presentation and CSF parameters of patients with POBM (104,105), which may cause underreporting.
The present meta-analysis determined that, on average, POBM non-survivors tend to be older. A similar pattern is evident in community-acquired meningitis, where the mortality rate is generally higher among elderly patients (106). In a previous retrospective study on bacterial meningitis, Sunwoo et al (107) discovered that the mortality risk for elderly patients did not differ significantly from that of younger individuals (odds ratio, 1.03; 95% CI, 1.0-1.06). This outcome contradicts the fundamental concept of aging and immunology. It is well-established that aging is associated with immunosenescence, particularly in individuals >60 years of age. Immunosenescence weakens both innate and adaptive immune responses, leading to more severe infections (108).
To the best of our knowledge, Shi et al (42) are the only researchers who have examined the impact of comorbidities on mortality risk in POBM cases. They discovered that patients with POBM with comorbidities were more susceptible to poor outcomes (42). Conversely, studies focusing on comorbidity and mortality in bacterial meningitis are more prevalent. Some of these studies have indicated that patients with comorbidities are >3-fold more likely to experience adverse outcomes (14,109). In a prospective cohort study, van Veen et al (11) concluded that individuals with diabetes had a higher likelihood of developing bacterial meningitis. The prognosis of patients with comorbidities is closely linked to their immune function. Patients with diabetes typically have elevated levels of circulating inflammatory cytokines, and hyperglycemia hinders the normal response of leukocytes to pathogens (110). Chronic kidney disease is known to elevate inflammatory factors in the bloodstream and impair leukocyte function (111).
CSF lactate levels in meningitis cases have been previously studied, with outcomes highlighting their diagnostic value (112,113). Lotfi et al (45) identified a threshold value of 4 mmol/l (equivalent to 36.04 mg/dl) for the diagnosis of POBM. In a previous study on tuberculous meningitis, Nuwagira et al (114) determined that CSF lactate was a crucial diagnostic test. However, it did not provide any predictive value for mortality within the first 2 weeks (114). There is a lack of studies comparing CSF lactate levels between POBM survivors and non-survivors, preventing any comparisons in the present meta-analysis. However, the pooled analysis performed herein indicated a CSF lactate value of 52.88 mg/dl (95% CI, 38.14-67.62).
CSF glucose levels in POBM cases have not been extensively studied; yet, they are frequently used as a diagnostic tool for bacterial meningitis. The present meta-analysis revealed that non-survivors tend to have lower average CSF glucose levels. Baud et al (19) found that higher levels of CSF inflammation were linked to low CSF glucose in bacterial meningitis. The notion of using CSF glucose as a prognostic marker is based on the understanding that microbes consume glucose for metabolism. Consequently, severe inflammation, which demands higher levels of glucose, would lead to more severe clinical symptoms and a poorer prognosis (19). The present meta-analysis revealed that non-survivors had reduced levels of CSF glucose.
Despite the established knowledge that Gram-negative bacteria are more virulent and resistant to antibiotics, the present study did not identify a higher risk of mortality for infections caused by Gram-negative bacteria compared to those caused by Gram-positive bacteria. This outcome contradicts previous concepts, which suggest that meningitis from Gram-negative bacteria typically results in higher mortality rates (12). Additionally, patients with POBM with Gram-negative infections are generally considered to be at a greater risk of treatment failure and adverse outcomes (32). In theory, Gram-negative bacteria are more difficult to treat due to their distinct characteristics, such as the presence of an outer membrane and several unique enzymes that aid in antibiotic resistance (115). The discrepancy between the outcomes of the present meta-analysis and previous knowledge of Gram-negative bacteria may stem from some studies reporting only specific types of bacteria (28,30-33,35-37,39,41-43,47,51,57,69,71,72,75-77,79,81,83-85,87,88,93,96-100). This selective reporting could lead to an unfair comparison between meningitis caused by Gram-negative and Gram-positive bacteria.
In summary, the present study has several limitations which should be mentioned: i) It did not include subgroup analyses for different types of comorbidities; ii) it lacks subgroup analyses for antibiotic usage; and iii) it did not categorize patients based on the type of surgical intervention. Thus, further research addressing these aspects is required in order to provide a clearer understanding of the prognostic factors for POBM.
In conclusion, the present meta-analysis provided critical insight into the factors affecting mortality in patients with POBM. The results presented herein can assist in clinical decision-making and direct future research in the field of surgical infectious complications. Based on these outcomes, the following conclusions can be drawn: i) There is no marked difference between POBM non-survivors and survivors in terms of age; ii) there is no marked difference between POBM non-survivors and survivors in terms of presenting GCS scores; iii) POBM non-survivors have an average CSF glucose of <30 mg/dl; iv) patients with POBM with comorbidities are at a higher risk of mortality; and v) more than one quarter of patients with POBM do not survive.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
WS constructed the basic concept of the study, and was also involved in the editing and reviewing of the manuscript, as well as in data extraction and study supervision. RM constructed the basic concept of the study, and was also involved in the editing of the manuscript, in the literature search, data extraction and statistical analysis. MAP was involved in the reviewing and editing of the manuscript, in the conception of the study, in the literature search and in study supervision. BU was involved in data extraction, in the literature search and in the statistical analysis. AAF was involved in the reviewing of the manuscript, in the literature search, in the statistical analysis, and in study supervision. AHB was involved in the conception of the study, in the reviewing and editing of the manuscript and in study supervision. All authors have read and approved the final manuscript. WS and RM confirm the authenticity of all the raw data.
Ethics approval and consent to participate
Not applicable.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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