The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital
Abdelkader, A., Gad, A., Mohamed, E., Elshamy, M. (2023). The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital. EKB Journal Management System, 13(1), 43-52. doi: 10.21608/aeji.2022.174090.1269
Abeer H Abdelkader; Ahmed I Gad; Emad A Mohamed; Mustafa H Elshamy. "The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital". EKB Journal Management System, 13, 1, 2023, 43-52. doi: 10.21608/aeji.2022.174090.1269
Abdelkader, A., Gad, A., Mohamed, E., Elshamy, M. (2023). 'The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital', EKB Journal Management System, 13(1), pp. 43-52. doi: 10.21608/aeji.2022.174090.1269
Abdelkader, A., Gad, A., Mohamed, E., Elshamy, M. The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital. EKB Journal Management System, 2023; 13(1): 43-52. doi: 10.21608/aeji.2022.174090.1269

The Efficacy of Bacterial Meningitis Score in Predicting Bacterial Meningitis at Mansoura Fever Hospital

Afro-Egyptian Journal of Infectious and Endemic Diseases
Article 6, Volume 13, Issue 1, March 2023, Page 43-52  XML PDF (569.17 K)
Document Type: Original Article
DOI: 10.21608/aeji.2022.174090.1269
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Authors
Abeer H Abdelkader email orcid 1; Ahmed I Gad2; Emad A Mohamed3; Mustafa H Elshamy1
1Department of Tropical Medicine, Faculty of Medicine, Zagazig University, Egypt.
2Specialist in Infectious Diseases, Mansoura Fever Hospital, Mansora, Egypt.
3Department of Microbiology, Faculty of Medicine, Zagazig University, Zagazig, Egypt.
Abstract
Background and study aims: Despite the advances in the diagnosis and treatment of infectious diseases, the meningitis and the encephalitis are still considered to be important causes of mortality and morbidity. Early diagnosis and starting immediate empirical therapy are the key factors of decreasing morbidity and mortality. We aimed to detect the frequency of bacterial meningitis among the suspected cases and to evaluate bacterial meningitis score (BMS) for detection the bacterial meningitis cases‎‎‎.
Methods: ‎This study was a cross-sectional included 48 patients admitted to the Mansoura Fever Hospital with clinical pictures suspected of meningitis. Full medical history, clinical examination, laboratory investigations and lumber puncture with CSF examination were provided to the participant patients. They were classified according to the results of CSF culture into two groups. The first group: included 12 patients with confirmed septic meningitis. The second group: included 36 patients with aseptic meningitis. The Application of bacterial meningitis score (BMS) was applied‎‎.‎
Results: The incidence of the bacterial meningitis in our study was 25% (12 from 48 patients).
The aspect of CSF was turbid among all the patients of septic meningitis, while was turbid only in in (8.3%) of aseptic meningitis cases. The total leucocytes count, polymorphs, and protein were significantly higher in patients with septic meningitis. The bacterial meningitis score has high sensitivity (91.7%), specificity (97.2%), PPV (91.7%) and NPV (97.2%) in the diagnosis of the septic meningitis cases‎‎‎‎‎‎‎‎‎.
Conclusion: The BMS is a quick, simple score, and highly accurate, which could be used for the diagnosis of the septic meningitis ‎.

Highlights
  • Acute bacterial meningitis is common in Egypt.
  • Acute bacterial meningitis is a serious infection with high morbidity and mortality.
  • Gram positive cocci mainly strept. Pneumonia is the most causative pathogen.
  • Incidence of bacterial meningitis in our study is 25%.
  • The bacterial meningitis score has high sensitivity (91.7%), specificity (97.2%), PPV (91.7%) and NPV (97.2%) in the diagnosis of the septic meningitis cases‎‎‎‎‎‎‎‎‎.
Keywords
Meningitis; CSF; septic; Aseptic; bacterial Meningitis score
Supplementary Files
Full Text

INTRODUCTION

Bacterial meningitis is a serious illness that causes more than 300 000 deaths worldwide. It is an acute purulent infection of the meninges, subarachnoid space, and the brain parenchyma all are involved in the inflammatory reaction [1]. Symptoms may include fever, headache, stiff neck, eye discomfort, confusion, drowsiness, seizures, nausea, and vomiting [2].

Bacterial meningitis is predominately caused by three pathogens, Streptococcus pneumoniae, Neisseria meningitides and Haemophilus influenza type B. Additionally, Listeria monocytogenes, Group B Streptococci, and Gram-negative bacteria such as Escherichia coli and Klebsiella pneumoniae, cause meningitis in specific groups, including neonates, pregnant women, transplant recipients and older adults [3].

In Egypt, meningitis is endemic and occasional instances can be seen at any time of the year. The winter and spring months of January to April have the highest prevalence of bacterial meningitis [4]. Streptococcus pneumonia is a leading causative agent of bacterial meningitis infections In Egypt [5].  It affects males slightly more than females. The incidence and the proportion of deaths among diagnosed cases of bacterial meningitis are dependent on area and Country, the causative micro-organism and age. [6].

Positive Kerning’s and Brudzinski's signs of meningeal irritation are seen in many of patients. A meta-analysis of several studies revealed sensitivities of 51% for neck stiffness, 53% for Kernig sign and 66% for Brudzinski sign for the diagnosis of bacterial meningitis, as well as poor test characteristics of other common signs and symptoms in the differentiation between bacterial and viral/aseptic or no meningitis [7].These data indicate that clinical characteristics cannot be used to rule out bacterial meningitis [8]. With progression of the disease other symptoms develop such as cardiorespiratory arrest, focal CNS signs, and seizures may frequently occur [9].

Many guidelines recommend early diagnosis and starting immediate empiric antibiotics for cases suspected to be bacterial meningitis based on age and type of microorganism and can be modified once the results are available [10]. The bacterial meningitis score (BMS) is a validated clinical score to detect high-risk patients with bacterial meningitis for better diagnosis and to start early empirical antibiotics which leads to improved outcome. BMS consists of positive Gram-stain of Cerebrospinal Fluid (CSF), CSF protein >80mg/dl, peripheral absolute neutrophil count >10,000 cells/mm3, CSF neutrophil count >1000cells / mm3 and seizure before or at time of presentation [11, 12].

This study aimed to detect the frequency of bacterial meningitis among suspected cases and to evaluate bacterial meningitis score in detecting bacterial meningitis cases.

PATIENTS AND METHODS

Study design and Participants

This cross-sectional study included 48 patients with acute meningitis admitted to the Mansoura Fever Hospital, Dakahlia Governorate, Egypt in the period from October 2018 to March 2019. Patients with clinical pictures suspected of meningitis (fever, headache, projectile vomiting, neck rigidity, positive Kernig’s and Brudzinski’s signs) at any age, gender, and acute onset in equal or less than 10 days were included.

Exclusion criteria: onset of symptoms in more than 10 days prior to presentation, post neurosurgery, post- traumatic, cerebrovascular accidents, and patient refusing to share in the study

Patients’ assessments:All patients in the current study were subjected to full medical history and complete clinical examination. Routine laboratory investigations including complete blood count (CBC), erythrocyte sedimentation rate (ESR), C-reactive protein, Kidney function tests (Serum creatinine, blood urea), liver biochemistry (ALT, AST albumin, prothrombin time), and blood glucose level.

All patients suspected of acute meningitis underwent lumber puncture for CSF analysis for confirmation of diagnosis once the patients admitted to the hospital and no contraindication for lumber puncture.

Bacterial meningitis was defined for patients who had a lumbar puncture with CSF leucocytosis and positive bacterial culture of CSF [13].

The technique of Lumbar puncture:Lumber puncture was done for all patients by expertise once the patients came to the hospital with clinical picture suggestive of acute meningitis. The patient assumed either the lateral recumbent position or a sitting position. The needle under complete aseptic technique was inserted in the interspace between L3 and L4 or L4 and L5, in the midline, approximately 15 degrees cephalic. The amount of CSF withdrawn was 3 to 5 ml enough for analysis [14, 15].

CSF analysis

We examined CSF for Physical appearance (color, aspect,), chemical (glucose, protein), cell count, gram's stain and culture. According to the results of the CSF examination, meningitis cases were divided into:

Septic meningitis (positive CSF culture) and aseptic meningitis (negative CSF culture)

Application of bacterial meningitis score

Bacterial meningitis score predictors

 criteria

 CSF gram stain

Positive  (2 points)

CSF protein

≥  80 mg/dl (1 point)

CSF absolute neutrophil count

≥ 1000 cells/ mm3   (1 point)

Peripheral blood neutrophil count

≥ 10 000 cells / mm3  (1 point )

Seizure

Before or at  the time of presentation  (1 point)

If the score 2-6 points, the bacterial meningitis is  most likely [16].

Statistical analysis

The collected data was revised, coded, and tabulated using the Statistical package for Social Science (SPSS Statistics for Windows, Version 25.0.). Data were presented and a suitable analysis was done according to the type of data obtained for each parameter. Shapiro test was done to test the normality of data distribution. Mean, Standard deviation (± SD) were used for numerical data. Frequency and percentage of non-numerical (qualitative) data. Student T test was used to assess the statistical significance of the difference between the two study group means. The Chi-Square test was used to examine the relationship between two qualitative variables. Sensitivity, specificity, PPV, NPV, and accuracy to differentiate the patient and healthy cases correctly. P values is significant if

RESULTS

Patient characteristics

This cross-sectional study recruited patients with symptoms suggestive of acute meningitis, their ages ranged from 4 to 73 years, 47.9% were less than 18 years, and predominantly there were males (n=  32, 66.7%).

Their residence was predominantly rural 52.1%, 66.7% had low socioeconomic status. All cases presented with fever, 91.7% with headache and in 75% neck rigidity was evident (Table 1- Figure 1).

Results of CSF examination and culture

According to the results of CSF culture, cases were classified into septic (positive culture growth) and aseptic (negative bacterial growth) (Figure 2).  Septic cases were significantly associated with urban residence, low socioeconomic status, and family history of smoking (Table 1). There were no significant differences in the clinical presentation between septic and aseptic cases.

According to physical appearance of CSF sample, septic group was significantly associated with whitish color, turbid aspect, and high pressure (p(Table 3). Total leucocytes count, neutrophil, lymphocytes, protein, ESR, and CRP were significantly higher in CSF of septic cases, while CSF glucose was significantly low (Table 2).

One-quarter of patients show bacterial growth (12 patients), 8 of them (66.7%) were Gram-positive cocci (Streptococcus pneumoniae), while 4 cases (33.3%) were Gram-negative bacilli (3 cases of H Influenza and one case was Pseudomonas) (Figure 3).

Bacterial meningitis score:

We calculate bacterial Meningitis Scores for all cases. Gram stain was positive in 12 samples, 31.3% of cases had CSF protein >80 mg/d1, 20.8% had peripheral absolute neutrophils count ≥ 10000/ mm3, 18.8% had CSF neutrophils ≥ 1000 cells/mm3, 16.7% had seizure at or before the presentation. The total score in all studied cases was 1.7, with range from 0 to 6 (Table 4).

BMS was significantly higher in septic cases, it ranged from 3 to 6, comparing to that of aseptic cases which ranged from 0 to 2. (Table 4)

Bacterial meningitis score detected 11 out of the 12 cases diagnosed with bacterial meningitis with PPV of 91.7% and only missed one case which has a score of less than 2. Moreover, 35 cases from the 36 aseptic meningitis cases had a score ≤ 2 with a NPV of 97.2%. Sensitivity was 91.7%, and specificity was 97.2%. The overall accuracy of the test is 95.8% (Table 5).

Table (1): Sociodemographic data of all septic and aseptic cases.

Parameter

Aseptic n=36

N      %

Septic n= 12

N    %

P value

Ages in years

                Mean±SD

 

25.3±3.4

 

19.1±4.4

 

0.397

Ages in groups

                ≤ 18 years

                19-40

                >40

 

17          47.2%

11         30.6%

8          22.2%

 

6         50%

5        41%

1        8.3%

 

0.558

Gender:

                Male

                female

 

23          63.9%

13          36.1%

 

9          75%

3          25%

 

0.725

Resident

                Urban

                Rural

 

13        36.1%

23        63.9%

 

10     83.3%

2      16.7%

 

0.005

Socioeconomic status

                Low

                high

 

21      58.3 %

15      41.7%

 

11     91.7 %

1       8.3 %

 

 

0.04

Smoker in the family

                Yes

                No

 

12     33.3 %

14      66.7 %

 

9        75 %

3       25 %

 

 

0.012

 

Table (2): Comparison of blood laboratory data between septic and aseptic cases.

variables

Aseptic  group n= 36

Mean ± SD

Septic group n= 12

Mean ± SD

P value

WBCs  (109/L)

9.6 ± 0.6

14.6 ±  2

0.003

Neutrophiles (X109/L)

3.4 ± 0.5

10.9 ±  1.5

0.001

Lumphocytes (X109 /L)

6.2  ±  2

3.5 ±  1.1

0.001

Hemoglobin (g/dl)

11.1±   0.2

10.4 ±  0.4

0.177

Plateletes (X109/L)

258.5 ±  15.5

296.4 ±  40.5

0.290

ESR at second hour (mm/h)

37.8  ±  2.3

75.7 ±  8.2

0.001

CRP (mg/dl)

14.9  ±  1.7

111.6  ±   28.5

0.001

Blood glucose  (mg/dl)

152.2  ±   6.9

151.5  ±   17.5

0.915

 CRP: C reactive protein.

Table (3): Comparison of CSF examination between septic and aseptic cases.

P value

Septic group n= 12

N       %

Aseptic group n= 36

N          %

Physical apperance

 

<0.001

 

0

12     100 %

0

 

33       91.7 %

0

3          8.3%

Color:

Watery (colorless, clear)

Whitish(purulent)

Reddish

 

<0.001

 

0

12     100 %

 

33       91.7 %

3         8.3%

Aspect :

Clear

Turbid

 

 

<0.001

 

0

12        100%

 

31      86.1 %

5       13.9 %

Pressure:

Normal

High

 

Mean ± SD

Mean ± SD

Laboratory data

 

<0.001

11258.3 ± 4262.9

30.1 ± 6.6

TLC (cells/mm3)

<0.001

9179.5  ± 3453.3

9.9 ± 4.5

Neutrophils  (cells/mm3)

<0.001

2078.5 ± 647.3

20.2  ± 5.4

lymphocytes (cells/mm3)

<0.001

40.3 ± 3.3

72 ±  3.2

Glucose (mg/dL)

<0.001

211.4 ± 24.8

47.9 ± 11

Protein (mg/dL)

TLC: total leucocytes count.

Table (4). Comparison of total score between septic and aseptic cases.

Bacterial meningitis score

Aseptic

N=36

Septic

N=12

P
 

Mean±SD

0.4

±

0.1

4.3

±

0.3

<0.001

 

range

0

-

2

3

-

6

 

≤2

      35

 

 

1

 

 
 

>2

1

 

 

 

11

 

Table (5): Bacterial meningitis score items and efficacy.

Items

Absent

Present

Positive Gram stain

36       75%

12       25 %

CSF protein >80 mg/d1

33    68.8%

15     31.3 %

 blood neutrophils count ≥ 10000 cells/ mm3   

38    79.2%

10      20.8 %

CSF neutophils counts ≥  1000 cells/mm3

39     83.3 %

9      18.8 %

Seizure at or before presentation

40      83.3 %

8     16.7 %

Total score:

Means± SD

Range

1.7±0.3

0 – 6

Sensitivity

91.7%

Specificity

97.2%

PPV

91.7%

NPV

97.2%

Accuracy

95.8%

PPV: positive predictive value, NPV: negative predictive value.

DISCUSSION

Bacterial meningitis is life-threatening inflammation of the meninges and cerebrospinal fluid (CSF) that surrounds and protects the brain and spinal cord. Some people with the infection die and death can occur in a few hours. Patients who do recover can have permanent disabilities, such as brain damage, hearing loss, and learning disabilities [17-19]. The incidence and fatality rates for bacterial meningitis vary by region, country, pathogen, and age group. Without treatment, the fatality rate can be as high as 70 percent [20].

Meningitis can affect any age and gender, affecting more children and the elderly. The association seems to be related to poor immunity in younger children and a combination of other diseases and immunosuppression in the elderly. [21].

The current study was designed to determine the frequency of acute bacterial meningitis and identify some risk factors and for evaluation of bacterial meningitis score to detect high risk patients with acute bacterial meningitis.

In this study, we recruited 48 patients (32 male and 16 female). Males account for 66.7% of patients, with no significant difference between patients with septic meningitis and aseptic meningitis. These results less than with those of Abro et al. [22]who found that males predominance (84%). However, these results are close to that reported by Alkholiet al., and Moradi et al. [23, 24] who found that 57.5%  and 59.6% of patients with meningitis were men, respectively. There were no variations in terms of gender, age groupings, or age. These findings support other research findings [25, 26].

A low socioeconomic state has an important role in the increased incidence of bacterial meningitis. These factors include poverty, household crowding, limited access to health care, and lower educational level [27]. Overcrowding and poor households, facilitate the transmission of respiratory droplets from the carrier or symptomatic patients to healthy individuals [28]. Tobacco seems to increase the risk of bacterial meningitis among both active and passive smokers [29-31].The results of the current study as shown above are in agreement with these demographic variables.

All cases with bacterial meningitis in the current study presented with fever. It is clear from the available literature that fever is the most commonly reported symptom in bacterial meningitis, with an occurrence rate of 92–93%. Vomiting is reported in 55–67% of children with bacterial meningitis [32- 34], figures emphasized by the current study.

Regarding symptoms and signs of septic and aseptic meningitis, there is no statistically significant difference between both groups.Our results are matched with Singhi& Bansal [35]. On the other hand Zhang et al.,found that headache was statistically significantly higher in bacterial meningitis [26].

The diagnosis of bacterial meningitis cannot be proven without CSF examination. A positive CSF culture is diagnostic for bacterial meningitis and enables testing of the antimicrobial susceptibility patterns, after which antibiotic treatment can be optimized [36], and this was followed in the current study.

In our study, CSF was turbid among all patients with septic meningitis and in 8.3% among patients with aseptic meningitis, due to excessive cells (pus, inflammatory cells, WBCs; mainly neutrophils, and RBCs) and proteins. As usual WBCs, neutrophils, and protein were significantly higher in CSF samples of septic cases when compared to samples of aseptic cases. These results are in agreement with many studies [25, 26, 37, 38]. The white blood cell count in bacterial meningitis is typically greater than 1000 cells/mL; mainly neutrophils predominate, but about 10% of patients present with lymphocyte predominance [39-42]. The CSF glucose concentration is < 40 mg/dL In more than half of BM patients. Low CSF glucose concentration virtually excludes viral meningitis. In BM, the CSF protein concentration is elevated usually to 1,000 to 5,000 mg/L [43, 44].

According to CSF culture, 8 cases out of the 12 were gram positive cocci (Strept. Pneumonia), while Gram negative bacilli (H influenza) were isolated in 3 cases and one isolate was due to Pseudomonas. These results are in agreement with many reports in the literature [45-47]. These reports stated that S. pneumonia was the leading cause of bacterial meningitis among adults in Egypt and Neisseria meningitides was described as the second or third leading cause. Reflecting a change in the epidemiology of the disease where N. meningitides was for a long time the main etiological agent [48]. The decrease in the number of meningococcal meningitis may be due to the introduction of school-based vaccination program, vaccination for all persons before travelling to the Hajj in addition to the immunization programs of military recruits [49].

While in a large European study conducted on children presented with sepsis and admitted to ICU, the common clinical illnesses were meningitis/encephalitis. Neisseria meningitides was the most commonly identified pathogen (n = 131, 31%) followed by S. pneumonia (n = 78, 18%) [50].

CSF sterility is achieved rapidly after IV antibiotics, within 15 minutes to 2 hours for meningococcal, 4–6 hours for pneumococcal and 8 hours for neonatal GBS infection [51, 52].  

This study determines high-risk patients of bacterial meningitis for recognition and immediate antibiotic administration and hospitalization, and therefore better outcomes and improved morbidity and mortality in this serious disease. Patients with a bacterial meningitis score of less than 2 can be considered to be at very low risk of bacterial meningitis. Bacterial meningitis score in our study detected 11 cases from 12 cases with proven bacterial meningitis in whom medicines were appropriately commenced, with PPV; 91.7%., NPV; 97.2%, and the accuracy of the test was 95.8%. These results are in agreement with many studies [53-55]. Furthermore, one large European multicenter study showed BMS NPV was 100% (95% CI, 98.8-100%) [56].

This study had its own limitation; which is not only small number of the patients recruited, but also and being single center study which consequently don’t allow for better recognition of microbiological patterns of acute meningitis.

Funding:  None.

Conflicts of interest: None.

Informed consent and ethical approval :

The study was carried out following the ethical principles of the Declaration of Helsinki, and it was approved by the Institutional Review Board (IRB) of the Faculty of Medicine, Zagazig University, Egypt (approval no. 4086). Informed consent has been obtained from every participant, verbal explanations were done to all children in front of their parents and misunderstanding was clarified and written consent was then signed by the parents. 

References
  1. Roos KL. Acute bacterial meningitis. Semin Neurol. 2000; 20(3):293-306.
  2. Marcus R, Walter K. Bacterial Meningitis. JAMA. 2022; 328(21):2170.
  3. GBD 2016 Meningitis Collaborators. Global, regional, and national burden of meningitis, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2018 Dec; 17(12):1061-1082.
  4. Zaky S., Baki A., Farouk S., Sabry S., Saad Deraz, A., & Sanad, M   "Presentation, prognostic factors and outcome of acute septic meningitis in an egyptian fever hospital."Ind J Sci Res and Tech 2 (2014): 112-8.
  5. Afifi S, Wasfy MO, Azab MA, Youssef FG, Pimentel G, Graham TW, et al. Laboratory-based surveillance of patients with bacterial meningitis in Egypt (1998-2004). Eur J Clin Microbiol Infect Dis. 2007 May; 26(5):331-340.
  6. Al Bekairy AM, Al Harbi S,  Alkatheri AM, Al Dekhail S, Al Swaidan L,  Khalidi N. Bacterial meningitis: an update review. African Journal of Pharmacy and Pharmacology, 2014; 8(18), 469–478.
  7. Curtis S, Stobart K, Vandermeer B, Simel DL, Klassen T. Clinical features suggestive of meningitis in children: a systematic review of prospective data. Pediatrics. 2010 Nov; 126(5):952-60.
  8. Brouwer MC, Thwaites GE, Tunkel AR, van de Beek D. Dilemmas in the diagnosis of acute community-acquired bacterial meningitis. Lancet. 2012 Nov 10; 380(9854):1684-92.
  9. Kim KS. Acute bacterial meningitis in infants and children. Lancet Infect Dis. 2010 Jan; 10(1):32-42.
  10.  Griffiths MJ, McGill F, Solomon T. Management of acute meningitis. Clin Med (Lond). 2018 Mar; 18(2):164-169.
  11. Nigrovic LE, Kuppermann N, Malley R. Development and validation of a multivariable predictive model to distinguish bacterial from aseptic meningitis in children in the post-Haemophilus influenzae era. Pediatrics. 2002 Oct; 110(4):712-9.
  12. Nigrovic LE, Kuppermann N, Macias CG, Cannavino CR, Moro-Sutherland DM, Schremmer et al. Pediatric Emergency Medicine Collaborative Research Committee of the American Academy of Pediatrics. Clinical prediction rule for identifying children with cerebrospinal fluid pleocytosis at very low risk of bacterial meningitis. JAMA. 2007; 297(1):52–60.
  13. Delannoy Q, Pean-de-Ponfilly G, Mesnil C, Severin C, Robert J, Plaisance P, Freund Y, Hausfater P, Cambau E, Jacquier H, Chauvin A. Validation of the Bacterial Meningitis Score in adults consulting at an emergency department: a retrospective multicentric study. Eur J Emerg Med. 2020 Dec; 27(6):447-453.
  14. Sternbach G. Lumbar puncture. J Emerg Med 1985; 2:199.
  15.  Chakraverty R, Pynsent P, Isaacs K. Which spinal levels are identified by palpation of the iliac crests and the posterior superior iliac spines? J Anatomy. 2007; 210:232.
  16. Nigrovic LE, Malley R, Kuppermann N. Meta-analysis of bacterial meningitis score validation studies. Arch Dis Child. 2012; 97:799–805.
  17. CDC. Bacterial meningitis. https://www.cdc.gov/ meningitis/bacterial.html. acessed 9 december.2022]
  18. Wall EC, Chan JM, Gil E, Heyderman RS. Acute bacterial meningitis. Curr Opin Neurol. 2021 Jun 1; 34(3):386-395.
  19. Hasbun R. Progress and Challenges in Bacterial Meningitis: A Review. JAMA. 2022 Dec 6; 328(21): 2147-2154.
  20. Rosenstein, N. E., B. A. Perkins, D. S. Stephens, T. Popovic, and J. M. Hughes. Meningococcal Disease. NEJM. 2001; 344:1378-1388.
  21. van de Beek D, de Gans J, Spanjaard L, Weisfelt M, Reitsma JB, Vermeulen M. Clinical features and prognostic factors in adults with bacterial meningitis. N Engl J Med. 2004 Oct 28; 351(18):1849-59.
  22. Abro AH, Abdou AS, Ustadi AM, Saleh AA, Younis NJ, Doleh WF. CSF lactate level: a useful diagnostic tool to differentiate acute bacterial and viral meningitis. J Pak Med Assoc. 2009 Aug; 59(8):508-11.
  23. Alkholi UM, Abd Al-Monem N, Abd El-Azim AA, Sultan MH. Serum procalcitonin in viral and bacterial meningitis. J Glob Infect Dis. 2011 Jan; 3(1):14-8
  24. Moradi G, Zahraei SM, Khazaei Z, Mohammadi P, Hemmatpour S, Hajibagheri K et al. Epidemiology incidence and geographical distribution of Meningitis using GIS and its incidence prediction in Iran in 2021. Med J Islam Repub Iran. 2021 Aug 31; 35:110.
  25. Østergaard C, Benfield T. Macrophage migration inhibitory factor in cerebrospinal fluid from patients with central nervous system infection. Crit Care. 2009; 13(3):R101.
  26.  Zhang H, Wang X, Yang Y, Wu J. Meningitis in patients with a Gram-negative direct cerebrospinal fluid examination: the value of cytochemical markers for the differential diagnosis. Crit Care. 2011; 15(5):439.
  27. Reis JN, Palma T, Ribeiro GS, Pinheiro RM, Ribeiro CT, Cordeiro SM, et al. Transmission of Streptococcus pneumoniae in an urban slum community. J Infect. 2008 Sep; 57(3):204-13.
  28. Sabra A, Benger J. Meningococcal disease in children: a clinical review. Turk J Pediatr. 2011 Sep-Oct; 53(5):477-88.
  29. Kriz P, Bobak M, Kriz B. Parental smoking, socioeconomic factors, and risk of invasive meningococcal disease in children: a population based case-control study. Arch Dis Child. 2000 Aug; 83(2):117-21.
  30. Coen PG, Tully J, Stuart JM, Ashby D, Viner RM, Booy R. Is it exposure to cigarette smoke or to smokers which increases the risk of meningococcal disease in teenagers? International Journal of Epidemiology. 2006; 35(2), 330–336.
  31. Watle S, Caugant D, Tunheim G, Bekkevold T, Laake I, Brynildsrud, O, et al. Meningococcal carriage in Norwegian teenagers: Strain characterisation and assessment of risk factors. Epidemiology and Infection J. 2020; 148, E80.
  32. Franco-Paredes C. Lammoglia L. Hernandez I.Santos-Preciado J.I. Epidemiology and outcomes of bacterial meningitis in Mexican children: 10-year experience (1993–2003). Int J Infect Dis. 2008; 12: 380-386.
  33. Vasilopoulou V.A. Karanika M. Theodoridou K. Katsioulis A.T.  Theodoridou M.N. Hadjichristodoulou C.S. Prognostic factors related to sequelae in childhood bacterial meningitis: data from a Greek meningitis registry. BMC Infect Dis. 2011; 11: 214.
  34. Snaebjarnardottir K. Erlendsdottir H. Reynisson I.K. Kristinsson K. Halldórsdóttir S. Hardardóttir H.et al. Bacterial meningitis in children in Iceland, 1975–2010: a nationwide epidemiological study. Scand J Infect Dis. 2013; 45: 819-824
  35. Singhi SC, Bansal A. Serum cortisol levels in children with acute bacterial and aseptic meningitis. Pediatr Crit Care Med. 2006 Jan; 7(1):74-8.
  36. van de Beek D, Cabellos C, Dzupova O, Esposito S, Klein M, Kloek AT et al. ESCMID Study Group for Infections of the Brain (ESGIB). ESCMID guideline: diagnosis and treatment of acute bacterial meningitis. Clin Microbiol Infect. 2016 May; 22 Suppl 3:S37-62.
  37. Makoo  ZB,  Ahadi  N,  Hasani  A,  Makoo  RB, Mashrabi O. Cerebrospinal fluid (CSF) ferritin for differentiation of aseptic and bacterial meningitis in adults. American Journal of Infectious Diseases. 2010; 6(4), 98–102.
  38. El-Kapany, R. A. Serum and CSF cortisol level in patients with meningitis. Egyptian Journal of Neurology, Psychiatry and Neurosurgery. 2011; 48(4), 391–397.
  39. Khatib U, van de Beek D, Lees JA, Brouwer MC. Adults with suspected central nervous system infection: A prospective study of diagnostic accuracy. J Infect. 2017 Jan; 74(1):1-9.
  40. Bedetti L, Marrozzini L, Baraldi A, Spezia E, Iughetti L, Lucaccioni L, Berardi A.  Pitfalls in the diagnosis of meningitis in neonates and young infants: the role of lumbar puncture. J Matern Fetal Neonatal Med. 2018:1–7.
  41. Kanegaye JT, Soliemanzadeh P, Bradley JS. Lumbar puncture in pediatric bacterial meningitis: defining the time interval for recovery of cerebrospinal fluid pathogens after parenteral antibiotic pretreatment. Pediatrics. 2001; 108:1169–1174.
  42. Nigrovic LE, Malley R, Macias CG, Kanegaye JT, Moro-Sutherland DM, Schremmer RD et al.; American Academy of Pediatrics, Pediatric Emergency Medicine Collaborative Research Committee. Effect of antibiotic pretreatment on cerebrospinal fluid profiles of children with bacterial meningitis. Pediatrics. 2008; 122:726–730.
  43. Ali S M.,  Saeed HH, Suliman, HR. Meningitis In Sulaimani Pediatric Teaching Hospital : A Retrospective Study. Mustansiriya Medical Journal.2017. 16(2), 13–20.
  44. Fitch MT, van de Beek D. Emergency diagnosis and treatment of adult meningitis. Lancet Infect Dis. 2007 Mar; 7(3):191-200.
  45. Farag HF, Abdel-Fattah MM, Youssri AM. Epidemiological, clinical and prognostic profile of acute bacterial meningitis among children in Alexandria, Egypt. Indian J Med Microbiol. 2005 Apr; 23(2):95-101. 
  46. Youssef FG, El-Sakka H, Azab A, Eloun S, Chapman GD, Ismail T, et al. Etiology, antimicrobial susceptibility profiles, and mortality associated with bacterial meningitis among children in Egypt. Ann Epidemiol. 2004 Jan; 14(1):44-48.
  47. Afifi S, Wasfy MO, Azab MA, Youssef FG, Pimentel G, Graham TW, et al. Laboratory-based surveillance of patients with bacterial meningitis in Egypt (1998-2004). European Journal of Clinical Microbiology and Infectious Diseases 2007; 26(5), 331–340.
  48. Girgis NI, Sippel JE, Kilpatrick ME, Sanborn WR, Mikhail IA, Cross E et al. Meningitis and encephalitis at the Abbassia Fever Hospital, Cairo, Egypt, from 1966 to 1989. American Journal of Tropical Medicine and Hygiene, 1993; 48(1), 97–107.
  49. Nakhla I, Frenck RW, Teleb NA, El Oun S, Sultan Y, Mansour H, Mahoney F. The changing epidemiology of meningococcal meningitis after introduction of bivalent A/C polysaccharide vaccine into school-based vaccination programs in Egypt. Vaccine 2005; 23(25), 3288–3293.
  50. Boeddha NP, Schlapbach LJ, Driessen GJ, Herberg JA, Rivero-Calle I, Cebey-López M, et al. Mortality and morbidity in community-acquired sepsis in European pediatric intensive care units: a prospective cohort study from the European Childhood Life-threatening Infectious Disease Study (EUCLIDS). Crit Care. 2018 May 31; 22(1):143.
  51. Riordan FA, Cant AJ. When to do a lumbar puncture. Arch Dis Child. 2002 Sep; 87(3):235-7.
  52. Kanegaye JT, Soliemanzadeh P, Bradley JS. Lumbar puncture in pediatric bacterial meningitis: defining the time interval for recovery of cerebrospinal fluid pathogens after parenteral antibiotic pretreatment. Pediatrics. 2001 Nov; 108(5):1169-74. Erratum in: Pediatrics 2002 Sep; 110(3):651.
  53. Águeda S, Campos T, & Maia, A. Prediction of bacterial meningitis based on cerebrospinal fluid pleocytosis in children. Braz J Infect Dis. 2013 Jul-Aug; 17(4):401-4. 
  54. Nigrovic LE, Malley R, Kuppermann N. Meta-analysis of bacterial meningitis score validation studies. Archives of Disease in Childhood. 2012; 97(9), 799–805.
  55.  Pires FR, Franco AC, Gilio AE, Troster EJ. Comparison of enterovirus detection in cerebrospinal fluid with Bacterial Meningitis Score in children. Einstein (Sao Paulo). 2017 Apr-Jun; 15(2):167-172. 
  56. Delannoy Q, Pean-de-Ponfilly G, Mesnil C, Severin C, Robert J, Plaisance P et al. Validation of the Bacterial Meningitis Score in adults consulting at an emergency department: a retrospective multicentric study. Eur J Emerg Med. 2020 Dec; 27(6):447-453.
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