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BMC Infect Dis
BMC Infect Dis
BMC Infectious Diseases
1471-2334
BioMed Central London

9859
10.1186/s12879-024-09859-z
Research
Diagnosis and management of bacterial meningitis in adult Sudanese patients: a six years hospital based, retrospective, cross-sectional study
http://orcid.org/0000-0003-4343-8902
Hamadalneel Yousif B. Yousefbekhet2020@gmail.com

1
Mohammed Ahmed M. 2
Ahmed Saad T. 2
Yousef Alfatih A. 2
Mohammed Mohammed T. 2
http://orcid.org/0009-0005-1398-6707
Alamin Marwa F. 3
1 https://ror.org/001mf9v16 grid.411683.9 0000 0001 0083 8856 Department of Clinical Pharmacy & Pharmacy Practice, Faculty of Pharmacy, Gezira University, Wad Medani, Gezira State Sudan
2 Department of Clinical Pharmacy & Pharmacy Practice, Pharmacy Program, Wad Medani College for Science and Technology, Wad Medani, Gezira State Sudan
3 https://ror.org/02jbayz55 grid.9763.b 0000 0001 0674 6207 Department of Molecular Biology, Institute of Endemic Disease, Khartoum University, Khartoum, Khartoum State Sudan
10 9 2024
10 9 2024
2024
24 94715 12 2023
2 9 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Purpose

To evaluate the diagnosis and management of bacterial meningitis in adult Sudanese patients in accordance with the Infectious Diseases Society of America (IDSA) guidelines for bacterial meningitis management.

Patients and methods

A cross-sectional, retrospective study design was used to recruit all patients aged > 18 years who were diagnosed with or suspected of having bacterial meningitis and admitted to Wad Medani Teaching Hospital, Gezira State, Sudan, between January 2017 and October 2022.

Results

In total, 201 patients were included in the analysis. The mean age of the participants was 44.1 ± 21.4 years, and 107 (53.2%) were male. Community-acquired bacterial meningitis accounted for 193 (96%) of the studied patients, and only 8 (4%) of the patients had healthcare-associated meningitis. Neuroimaging was utilized appropriately in 148 (73.6%) patients, blood cultures were not performed entirely, and lumbar puncture was seldom performed in 1 (0.5%) patient. Corticosteroids were appropriately administered to 65 (32.3%) patients, and antibiotics were administered appropriately to only 5 (2.5%) patients. Ceftriaxone 185 (76.1%) was the most frequently utilized antibiotic, followed by vancomycin 23 (9.5%). In terms of overall adherence, this study demonstrated that the IDSA guidelines were not followed at all in the treatment of patients with suspected bacterial meningitis.

Conclusion

The results of this study contradict the IDSA guidelines for the standard of care for bacterial meningitis. Antibiotic regimens are often incorrect, corticosteroids are administered appropriately in approximately one-third of patients, and neuroimaging is reasonably utilized. This study raises attention to several important issues regarding the diagnosis of bacterial meningitis, including the lack of confirming microbiological tests and the reliance of the diagnosis primarily on CT and clinical examination.

Keywords

Diagnosis
Management
Bacterial meningitis
Sudanese
issue-copyright-statement© BioMed Central Ltd., part of Springer Nature 2024
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pmcIntroduction

Bacterial meningitis is a potentially fatal medical emergency characterized by a broad spectrum of pathogenic microorganisms and variable clinical presentations associated with considerable death and disability [1, 2].

Bacterial meningitis continues to pose a serious public health concern in Africa today [3]. Although it affects all the countries of the world, Africa remains the most affected area, especially the “Meningitis belt”, a region that extends from Senegal on the Atlantic coast to Ethiopia and Somalia, which lie along the Red Sea and Indian Ocean coasts [4]. Sudan Province had the second-highest incidence rate in the “Meningitis belt”, with 359,434 cases recorded between 1928 and 2018 [3].

Despite the advancements and emergence of guidelines for medical treatment, earlier identification, and the availability of vaccines, meningitis remains a serious medical problem given that it has extremely high mortality and morbidity rates [5]. In fact, research has shown that the case mortality rate for individuals aged ≥ 16 years is 27% and that 9% of survivors have long-lasting neurological disorders [6].

According to the 2004 guidelines developed by the Infectious Disease Society of America (IDSA), treatment for meningitis consists of two phases: the first phase consists of empiric antibiotic therapy administered after obtaining a CSF sample through lumbar puncture, and the second phase consists of microorganism-oriented therapy that follows the determination of the causative microorganism [7].

In the United States of America (USA), a one-year retrospective cross-sectional study was carried out to evaluate treatment compliance with the standard of care for suspected bacterial meningitis. The results showed that overall compliance with the IDSA guidelines was only 0.6%, and antibiotics and steroids were appropriately utilized in only 5.6% and 7.5%, respectively, of patients [8]. A different study with the same goal carried out in Lebanon revealed that 30.8% of the patients received treatment that was deemed to comply with the IDSA guidelines [9]. In addition to a study conducted in Ethiopia, most patients treated for bacterial meningitis did not receive proper diagnostic workup therapeutic strategies [10]. No research has been conducted or published on the assessment of adult bacterial meningitis care in Sudan. This study is the first of its kind to assess the diagnosis and management of bacterial meningitis in adult Sudanese patients. Therefore, this study aimed to evaluate the diagnosis and management of bacterial meningitis in adult Sudanese patients in compliance to the IDSA guidelines for bacterial meningitis management; including the appropriate use of neuroimaging, lumbar puncture (LP), corticosteroids, blood culture, and antibiotics.

Materials and methods

Study site

The study was conducted at Wad Medani Teaching Hospital, Gezira State, Sudan. Wad Medani is the capital city of Gezira State and is located in the center of Sudan. This makes Wad Medani Teaching Hospital a reference hospital for several neighboring states. Wad Medani Teaching Hospital is covered by eight medical units, each unit is made up of one consultant, two specialists, four registrars, and eight medical officers.

Study design

This was a cross-sectional, retrospective study.

Sample size and data collection

The minimum sample size required was 186 patients, used Epi Info™, 95% confidence interval; 359.434 population size [3]; expected frequency 50%; acceptable margin of error 5%; design effect 1; and cluster 1.

All patients aged > 18 years who were diagnosed with or suspected of having bacterial meningitis and admitted to Wad Medani Teaching Hospital between January 2017 and October 2022 were evaluated for potential participation in the study, and they were included. Bacterial meningitis cases or suspected cases were identified and included in this study based on the documented medical diagnosis provided by the consultant in the patient medical records and incomplete file data were excluded.

The data were collected from patient medical records at the Health Information Center, Wad Medani Teaching Hospital. Patient’s medical records are kept on paper, with a signed number for each patient record and their diagnosis recorded in the records book. The procedure for searching the data involved first looking up the file numbers in the records book containing the patients’ diagnoses of bacterial meningitis and then accessing the particular file and extracting the data. This process was conducted by the study authors.

Outcome measures

The patient’s adherence to neuroimaging was assessed based on two factors: whether head computed tomography (CT) was performed prior to LP and whether the patient met the appropriate criteria for CT (new-onset seizure within a week, immune-compromised patient, new focal neurological deficit, and central nervous system disease).

Corticosteroid adherence was evaluated according to whether the drugs were given, if they were given, whether they were utilized before or at the same time with antibiotics, and in the correct duration of treatment (4 days).

The following factors were used to assess antibiotic adherence: whether or not antibiotics were administered; if so, whether the correct regimen, duration (between 7 and 21 days), dose, and dose interval were prescribed in compliance with IDSA guidelines; and whether or not the antibiotics were administered prior to head CT (if CT was performed) or following LP (if CT was not performed).

Blood culture adherence was assessed on the basis of whether blood cultures were performed and whether cultures were obtained before the administration of antibiotics.

LP adherence was assessed on the basis of whether LP was performed and whether LP was performed before CT.

Total adherence to blood culture, corticosteroids, antibiotics, LP, and neuroimaging was used to measure overall adherence.

Statistical analysis

The Statistical Package for the Social Sciences (SPSS), version 27.0 was used to analyze the data. The mean and standard deviation (SD) were used to present quantitative and qualitative data as frequencies (percentages).

Results

Throughout the six-year study period, 267 patients were suspected of having bacterial meningitis, 201 of whom met the inclusion criteria and underwent analysis.

The mean age of the participants was 44.1 ± 21.4 years, and 107 (53.2%) were male. Community-acquired meningitis accounted for 193 (96%) of the studied patients, and only 8 (4%) of the patients had healthcare-associated meningitis.

In terms of coexisting conditions, 57 patients (28.4%) were immunocompromised, 1 patient (1.75%) was HIV positive, 1 patient (1.75%) had a known cancer, 54 patients (94.7%) had diabetes, and 1 patient (1.75%) had a history of alcohol use. Upon admission, the mean Glasgow coma score (GCS) of the patients under investigation was 10.19 ± 2.60, and following management, it was 11.14 ± 3.33. The mean length of stay (LOS) was 9.29 ± 4.2 days, and the other clinical presentations are summarized in Table 1.

Table 1 Clinical presentation of patients with suspected bacterial meningitis

Clinical symptoms	N (%)	
Headache	149 (74.1)	
Fever	195 (97)	
Neck stiffness	162 (80.6)	
Seizer	92 (45.8)	
Sensory complication	35 (17.4)	
Nausea	39 (19.4)	

Neuroimaging was utilized appropriately for 148 (73.6%) patients, blood cultures were not performed entirely, and LP was seldom performed for 1 (0.5%) patient, as shown in Table 2.

Table 2 Adherence to the IDSA guidelines

Measured outcome	Percentage	Adherence to IDSA guidelines	
Head CT scan:		 73.6% (148/201)	
Head CT indicated	74.1% (149/201)		
Head CT performed	69.2% (139/201)		
Blood culture		0	
Blood culture obtained	0		
Blood culture obtained before antibiotics	0		
Corticosteroid		32.3% (65/201)	
Administered	49.8% (100/201)		
Administered with/before antibiotics	71% (71/100)		
Correct duration	85% (85/100)		
Antibiotics		 2.5% (5/201)	
Antibiotics administered	100% (201/201)		
Antibiotics administered before head CT	100% (139/139)		
Correct antibiotic regimen	8% (16/201)		
Correct antibiotic dose	75.1% (151/201)		
Correct antibiotic dose interval	92% (185/201)		
Correct antibiotic duration	75.6% (152/201)		
Lumbar puncture			
Lumbar puncture performed	0.5% (1/201)		
Lumbar puncture performed before CT	0		
Overall IDSA guideline		0%	
Abbreviations CT, computed tomography; IDSA, Infectious Diseases Society of America

Antibiotics and corticosteroids are rarely used appropriately in terms of regimen, dose, dose interval, duration, and timing. The most common cause of inappropriate antibiotic use was incorrect antibiotic selection, and failure to administer corticosteroids resulted in noncompliance with the IDSA guidelines, as shown in Table 2.

Ceftriaxone 185 (76.1%) was the most frequently utilized antibiotic, followed by vancomycin 23 (9.5), meropenem 17 (7%), cefepime 7 (2.9%), cefotaxime 6 (2.5%) and the least common antibiotic was benzyl penicillin 5 (2.1%).

Among the patients under investigation, 136 (67.7%) needed ICU admission, 24 (11.9%) experienced sepsis or septic shock, and 30 (14.9%) died.

Discussion

The current study demonstrated that the IDSA guidelines were not followed for the treatment of patients with suspected bacterial meningitis. The antibiotic regimen, dose, dose interval, and duration were mostly incorrect, and corticosteroids were appropriately administered to approximately one-third of the patients. Blood cultures were not performed entirely, and the infrequent use of LP resulted in delays in receiving definitive treatment, which increased the rate of mortality and LOS. However, neuroimaging is also frequently performed.

Few studies have assessed the standard of care for bacterial meningitis with respect to the IDSA guidelines, most of which did not follow the IDSA recommendations for bacterial meningitis management.

The results of this study, which were corroborated by Chia et al., showed that 0.6% of patients with bacterial meningitis hospitalized in the emergency department in the USA followed the IDSA guidelines [8]; in contrast, 35% of patients in another study carried out in the same country did not adhere to the IDSA guidelines [11]. Furthermore, another study conducted in Lebanon to assess treatment adherence for bacterial meningitis according to the IDSA guidelines revealed that 30.8% of patients received management incompatible with the IDSA guidelines [9]. This variation may be related to the different inquiry methods used in this study.

In this study, the adherence to neuroimaging was assessed based on two factors: “whether CT was performed prior to LP and whether the patient met the appropriate criteria for CT. The other CT details were not included in the study objectives, because we included patients based on the consultant’s medical diagnosis. Our findings revealed that neuroimaging was utilized appropriately for 73.6% of the studied patients, which was greater than that reported by the study conducted in the USA (54.3%), which evaluated the appropriateness of neuroimaging based on these two factors [8]. This variation might be related to that in our study the reliance of the diagnosis primarily on CT and clinical examination.

In this study, there was a total absence of blood culture and LP was performed in only one patient, while the IDSA guidelines state that blood samples for culture and LP must be taken immediately if there is suspicion of acute bacterial meningitis to confirm the diagnosis [7]. This might be explained by the absence of a local protocol for bacterial meningitis management, which made the diagnosis depend mainly on the knowledge and experience of the consultant. Furthermore, numerous logistical concerns were raised, including the patient’s financial difficulties and the lengthy turnaround time of our hospital laboratory, which required approximately five days to obtain culture results.

Strong recommendation made by the IDSA guidelines for the use of adjunctive dexamethasone 0.15 mg/kg q6h for 2–4 days in adults with pneumococcal meningitis should be given 10–20 min prior to, or at least concurrently with, the first dose of antimicrobial (A-1), and moderate recommendation for use in all adults, as the cause of meningitis is not often known at the time of initial assessment (B-III) [7]. In Africa, including Sudan, Streptococcus pneumoniae and Haemophilus influenzae accounted for up to 80 to 85% of bacterial meningitis cases [3], which highlights the importance of adjunctive corticosteroid use. In this study, only half of the patients received adjunctive corticosteroids, this might be explained by that, most of the patients were referred from other hospitals/clinics and received antibiotics before arriving at Wad Medani Teaching Hospital, in addition to the lack of a local protocol for the management of bacterial meningitis.

While the IDSA guidelines recommend a vancomycin-based antibiotic regimen for adult bacterial meningitis, most of the studied patients seldom used this regimen, in accordance with the findings of two studies conducted in the USA, which revealed that the majority of patients did not use vancomycin [8, 11]. Furthermore, we observed the empirical use of anti-Pseudomonas antibiotics for community-acquired bacterial meningitis, despite the IDSA guidelines recommending them for healthcare meningitis.

According to the present study, an incorrect antibiotic regimen was the most common reason for treatment incompatibility. This result was corroborated by a study conducted in Lebanon to assess treatment adherence to the IDSA guidelines for bacterial meningitis, which showed that antibiotic selection was the most frequent reason for inappropriate treatment [9].

Ceftriaxone is the most commonly prescribed antibiotic. This conclusion was strengthened by a study conducted in Ethiopia to assess the current approaches for diagnosing and treating suspected bacterial meningitis patients [10]. However, a study conducted in the USA revealed that cefotaxime was the most frequently used antibiotic, followed by ceftriaxone [11].

This study revealed a significant increase in the mortality rate, an increase in the GCS score from baseline, and a considerable increase in the number of patients who developed sepsis/septic shock while all patients were receiving antibiotic treatment. These findings may be explained by inappropriate management, and further investigations should be conducted to evaluate these associations. This mortality rate is supported by a study conducted in Lebanon to assess treatment adherence of bacterial meningitis to the IDSA guidelines, which reported a mortality rate of 13.5% [9], and by a study conducted in the USA to assess treatment adherence to the IDSA guidelines for bacterial meningitis, which reported mortality rates of 5% and 16.7% in patients who used appropriate and inappropriate antibiotics, respectively [12].

Strengths and limitations

The strength of this study is that the method of inquiry used revealed data that precisely reflected clinical practice in actual situations and adherence to guidelines. Clinicians must follow all steps listed in the IDSA guidelines to be considered compliant.

The limitations of this study include its retrospective design and reliance on the accuracy and preservation of patient files, in which the majority of patients’ weight data were missing, making it challenging to assess the corticosteroid dose. In addition, the absence of national and local protocols for the diagnosis and management of bacterial meningitis makes comparisons with relevant international guidelines the sole way to evaluate our practice. Numerous studies have shown no differences in pathogenic organisms between Africa, especially the “Meningitis belt”, which includes Sudan, and the USA [3, 7].

Conclusion

In conclusion, the results of this study contradict the IDSA guidelines for the standard of care for bacterial meningitis. Antibiotic regimens were often incorrect, corticosteroids were administered correctly in approximately one-third of patients, and neuroimaging was reasonably utilized. This study raises attention to several important issues regarding the diagnosis of bacterial meningitis, including the lack of confirming microbiological tests and the reliance of the diagnosis primarily on CT and clinical examination. Therefore, a local protocol for the diagnosis and management of bacterial meningitis should be established at the hospital. However, further studies are needed to analyze the etiologic agents of bacterial meningitis and antimicrobial resistance to guide antibiotic use. Moreover, we recommend future research to assess the CT findings of bacterial meningitis patients and the factors that affect them.

Acknowledgements

None.

Author contributions

YBH: Conception, study design, execution, acquisition of data, analysis, interpretation and drafting of the main manuscript. AMM: Acquisition of the data and analysis, interpretation and drafting of the manuscript STA: Acquisition of the data and analysis, interpretation and drafting of the manuscript. AAY: Acquisition of the data and analysis, interpretation and drafting of the manuscript. MTM: Acquisition of the data and analysis, interpretation and drafting of the manuscript. MFA: Contributed to the revision, study design, analysis, interpretation of the data, editing and critical revision of the manuscript.

Funding

This study did not receive any specific grants from funding agencies in the.

public, commercial, or not-for-profit sectors.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Declarations

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of the Ministry of Health, Gezira State, Sudan. N: 44/T/Kh/1, (21/11/2022). Which waived the requirement for informed consent due to the retrospective nature of the study, and permission to access patient records was obtained from the administration of the Wad Medani Teaching Hospital to ensure confidentiality. We confirm that all methods were carried out in accordance with the Declaration of Helsinki.

Consent of publications

Not applicable.

Competing interests

The authors declare no competing interests.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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