Literature DB >> 28785577

Acute Bacterial Meningitis in Qatar: A Hospital-Based Study from 2009 to 2013.

Fahmi Yousef Khan1, Mohammed Abu-Khattab2, Eman Abdulrahman Almaslamani3, Abubaker Ahmed Hassan2, Shehab Fareed Mohamed4, Abdurrahman Ali Elbuzdi5, Nada Yagoub Elmaki2, Deshmukh Anand6, Doiphode Sanjay6.   

Abstract

BACKGROUND AND OBJECTIVES: Bacterial meningitis is a common medical condition in Qatar. The aim of this study was to describe the clinical characteristics of bacterial meningitis, the frequency of each pathogen, and its sensitivity to antibiotics and risk factors for death. PATIENTS AND METHODS: This retrospective study was conducted at Hamad General Hospital between January 1, 2009, and December 31, 2013.
RESULTS: We identified 117 episodes of acute bacterial meningitis in 110 patients. Their mean age was 26.4 ± 22.3 years (range: 2-74) and 81 (69.2%) of them were male patients. Fifty-nine episodes (50.4%) were community-acquired infection and fever was the most frequent symptom (94%), whereas neurosurgery is the most common underlying condition. Coagulase-negative staphylococci were the most common causative agent, of which 95% were oxacillin-resistant, while 63.3% of Acinetobacter spp. showed resistance to meropenem. The in-hospital mortality was 14 (12%). Only the presence of underlying diseases, hypotension, and inappropriate treatment were found to be independent predictors of mortality.
CONCLUSION: Acute bacterial meningitis predominantly affected adults and coagulase-negative staphylococci species were the common causative agent in Qatar with majority of infections occurring nosocomially. More than 90% of all implicated coagulase-negative staphylococci strains were oxacillin-resistant.

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Year:  2017        PMID: 28785577      PMCID: PMC5530415          DOI: 10.1155/2017/2975610

Source DB:  PubMed          Journal:  Biomed Res Int            Impact factor:   3.411


1. Introduction

Despite medical advances, acute bacterial meningitis (ABM) constitutes a global public health problem, especially in developing countries with poor health facilities due to high rates of malnutrition, poor living conditions, and lack of access to appropriate preventive and curative services that may predispose people to the disease and reduce their chances of receiving optimal treatment [1, 2]. In developed countries, the burden of the disease has reduced and its epidemiology has changed as a result of the widespread use of vaccines against the most common meningeal pathogens [3]. Accurate information on important etiologic agents and populations at risk is needed to determine public health measures and ensure appropriate management of ABM [3]. In Qatar, although ABM is a common medical condition that physicians face, there are few reports describing this disease [4-6]. We conducted the present study, the purposes of which were to (1) describe the demographic and clinical characteristics of ABM, (2) determine the relative frequency of each pathogen and its susceptibility to various antimicrobial agents, and (3) determine the outcome and the significant predictors of the outcome among patients with ABM in Qatar.

2. Materials and Methods

2.1. Design and Setting

This retrospective descriptive study, which involved all in-patients with ABM, was conducted at Hamad General Hospital between January 1, 2009, and December 31, 2013. This hospital is a 603-bed tertiary care center that covers all specialties except for hematology-oncology, cardiology, and obstetrics and it has been Joint Commission International (JCI) accredited since 2006 and is the first hospital system in the region to achieve institutional accreditation from the Accreditation Council for Graduate Medical Education-International (ACGME-I). Currently, there are three adult ICUs in Hamad General Hospital, namely, Medical ICU (MICU) with 22 beds, Surgical ICU (SICU) with 12 beds, and Trauma ICU (TICU) with 15 beds.

2.2. Definitions

ABM was diagnosed on the basis of at least one of the following compatible clinical pictures with no other apparent cause: fever (38°C), headache, meningeal signs, cranial nerve signs, and impaired mental status, plus one of the following [7, 8]: Positive cerebrospinal fluid (CSF) culture Positive CSF bacterial antigen test (with latex agglutination counterimmunoelectrophoresis) associated with pleocytosis mainly neutrophilic, defined as absolute WBC ≥ 100 cells/mm3, with a decreased glucose level ≤ 40 mg/dL and an increased protein concentration ≥ 60 mg/dL. ABM was considered nosocomial if the diagnosis was made after more than 48 hours of hospitalization or within a short period of time (i.e., usually within one month after discharge from the hospital where the patient had received an invasive procedure, especially a neurosurgical procedure) [9]. On the other hand, ABM was considered as community-acquired if the diagnosis was made within the first 48 hours of hospitalization and the patient was not hospitalized in the preceding month [10]. Empirical antimicrobial therapy was deemed to be inappropriate if the antibiotics were administered more than 24 hours after CSF collection and/or when the dosage, route, and duration of treatment were not in accordance with hospital guidelines [11]. Hypotension was defined as blood pressure < 90/60 mmHg. Multidrug-resistant organisms are defined as microorganisms, predominantly bacteria, that are resistant to one or more classes of antimicrobial agents [12]. Viral, fungal, mycobacterial, polymicrobial, and drug induced meningitis were excluded. ABM episodes with the same organism were included only once. Coagulase-negative staphylococci and viridans streptococci are considered as causative agents if CSF showed pleocytosis mainly neutrophilic, defined as absolute WBC ≥ 100 cells/mm3, or a decreased glucose level ≤ 40 mg/dL or an increased protein concentration ≥ 60 mg/dL. The primary outcome was in-hospital mortality which included all causes of death during admission.

2.3. Isolation, Identification, and Antimicrobial Susceptibility Test of Microorganisms

Identification of isolates was based on colony morphology, Gram stain, oxidase, catalase, VITEK 2 Compact (bioMérieux, Durham, USA), and Phoenix (Becton Dickinson, NJ, USA). The antimicrobial minimal inhibitory concentrations (MICs) for the isolates were determined by using Phoenix (Becton Dickinson, NJ, USA) for GNB and staphylococci and enterococci (among Gram-positive cocci). For fastidious bacteria, susceptibility was determined with a gradient strip method (E-test strips, bioMérieux, Marcy-l'Étoile, France). The breakpoint interpretation was determined according to the recommendations of the Clinical Laboratory Standards Institute (CLSI) [13].

2.4. Source of Data and Data Collection

Cases were identified via hospital's discharge records, infection control records, and cerebrospinal fluid records maintained by the microbiology unit. These records were reviewed carefully by two investigators, in order not to miss any case. Records of all patients with bacterial meningitis were reviewed retrospectively to retrieve data on patients' demography, sign-symptoms, underlying medical conditions, investigations, names of microorganisms and their drug susceptibility, name and duration of therapy offered, appropriateness of therapy, and outcome.

2.5. Statistical Analysis

Quantitative variables were expressed as mean ± SD. Univariate logistic regression was performed to determine the probable predictors of in-hospital mortality. All potential risk factors at ≤0.1 level in the univariate analysis were entered in the multiple logistic regression to identify the independent predictors of mortality at P < 0.05. The data were analyzed with SPSS software (v 17; IBM Corp., Armonk, NY, USA).

2.6. Ethical Approval

Ethical approval (#13254/13) and a waiver of informed consent were obtained from the medical research ethical committee at Hamad Medical Corporation, Qatar.

3. Results

3.1. Demographic and Clinical Data

During the study period, we identified 117 episodes of ABM in 110 patients. There were 43, 22, 21, 12, and 18 episodes in 2009, 2010, 2011, 2012, and 2013, respectively. The study sample comprised 81 (69.2%) male and 29 (30.8%) female patients. Their mean age was 26.4 ± 22.3 years (range: 2–74), and 28 (23.9%) patients were Qatari. The peak frequency of ABM episodes was noted among adults (15–64 years old) (92.3%) (see Table 1). From a clinical point of view, fever was the most frequent symptom (110, 94%), followed by mental alteration (55, 47%), headache (43, 36.8%), and vomiting (35, 29.9%). Moreover, meningismus was detected in 31 (26.5%) patients (see Table 1).
Table 1

Demographic and clinical data of the 117 patients involved in this study.

VariableNumber (%), mean ± SD (range)
Gender
M81 (69.2)
F29 (30.8)
Age (mean ± SD), years26.4 ± 22.3 (2–74)
Age group (years)
<126 (22.2)
1–511 (9.4)
6–146 (5.1)
15–2412 (10.3)
25–3413 (11.1)
35–4417 (14.5)
45–5423 (19.7)
55–646 (5.1)
≥653 (2.6)
Nationality
Qatari28 (23.9)
Non-Qatari82 (76.1)
Underlying conditions
Diabetes mellitus9 (7.7)
Hypertension26 (22.2)
Head injury6 (5.1)
Neurosurgery54 (46.2)
Alcoholic4 (3.4)
Prematurity7 (6.0)
Liver cirrhosis1 (0.9)
Otitis media5 (4.3)
Malignancy8 (6.8)
Immunosuppression2 (1.7)
Clinical presentation
Fever110 (94)
Mental alteration55 (47)
Headache43 (36.8)
Vomiting35 (29.9)
Meningism31 (26.5)
Seizures23 (19.7)
Bulging fontanel16 (13.7)
Hypotension (BP < 90/60 mmHg)12 (10.2)
Focal signs11 (9.4)
Photophobia7 (6.0)
Behavioral changes3 (2.6)
Petechial rash3 (2.6)
Complications
Hydrocephalus19 (16.2)
Ischemic stroke5 (4.3)
Brain abscess4 (3.4)
Subdural empyema1 (0.9)
Adrenal insufficiency1 (0.9)
Vasculitis1 (0.9)

3.2. Underlying Conditions

The most frequent underlying conditions were neurosurgery (54, 46.2%), hypertension (26, 22.2%), and diabetes mellitus (9, 7.7%) (see Table 1).

3.3. Cerebrospinal Fluid (CSF) Findings

The CSF findings of the 117 ABM episodes are listed in Table 2.
Table 2

Clinical data of the 117 patients involved in this study.

VariableNumber (%), mean ± SD (range)
Acquisition of infection
Community-acquired59 (50.4)
Nosocomial58 (49.6)
CSF
Cells/µL3880.4 ± 8654.6 (20–66000)
Neutrophils%74.1 ± 26.1 (1–99)
Lymphocytes%22.9 ± 24.8 (1–98)
Protein (g/dL)222.8 ± 205.9 (38–936)
Glucose (mmol/L)2.1 ± 1.6 (0.1–6)
Positive Gram stain93 (79.5)
Positive culture112 (95.7)
Positive latex agglutination23 (19.7)
Type of microorganism
Gram-positive62 (53)
Gram-negative55 (47)
Positive blood culture 37 (31.6)
Antimicrobial therapy
Appropriate97 (82.9)
Inappropriate20 (17.1)
Outcome
Died14 (12.0)
Alive103 (88.0)

3.4. Setting of Infection and Types and Distributions of the Microorganisms

Fifty-nine episodes (50.4%) were community-acquired and the other 58 (49.6%) were nosocomially acquired ABM (see Table 3). The causative pathogens of the 117 enrolled ABM episodes are listed in Tables 3 and 4. Gram-positive pathogens accounted for 62 (53%) episodes and Gram-negative pathogens accounted for the other 55 (47%). In general, the most common causative agent of ABM in our cohort was coagulase-negative staphylococci; however, among the 59 community-acquired meningitis cases, the most common etiological agent was Streptococcus pneumoniae, whereas coagulase-negative staphylococci species were the leading cause of nosocomially acquired ABM. Among the implicated Gram-positive pathogens, coagulase-negative staphylococci were the most common (20, 17%), followed by Streptococcus pneumoniae (19, 16.2%). Among Gram-negative pathogens, Klebsiella pneumoniae was the most common (12, 10.2%) followed by Neisseria meningitidis (11, 9.4%).
Table 3

Distribution of different isolates in relation to setting of acquisition of meningitis.

Microorganism Setting of acquisitionTotal
NosocomialN (%)Community-acquired N (%)
Gram-positive
Abiotrophia species1 (100)01
Enterococcus faecalis 5 (71.4)2 (28.6)7
Enterococcus gallinarum 1 (100)01
Gemella haemolysans 1 (100)01
Leuconostoc species1 (100)01
Listeria monocytogenes 03 (100)3
Staphylococcus aureus 01 (100)1
Staphylococcus capitis 2 (100)02
Staphylococcus epidermidis 14 (87.5)2 (12.5)16
Staphylococcus haemolyticus 2 (100)02
Streptococcus agalactiae 03 (100)3
Streptococcus bovis II 01 (100)1
Streptococcus intermedius 01 (100)1
Streptococcus milleri 01 (100)1
Streptococcus mitis 01 (100)1
Streptococcus pneumoniae 019 (100)19
Streptococcus salivarius 01 (100)1
Gram-negative
Acinetobacter baumannii 8 (100)08
Acinetobacter lwoffii 2 (66.7)1 (33,3)3
Brucella spp.01 (100)1
Chryseobacterium (Flavobacterium) meningosepticum01 (100)1
Chryseobacterium indologenes 01 (100)1
Enterobacter aerogenes 1 (100)01
Enterobacter cloacae 3 (100)03
Escherichia coli 3 (75)1 (25)4
Haemophilus influenzae 1 (50)1 (50)2
Klebsiella pneumoniae ssp. pneumoniae7 (58.3)5 (41.7)12
Neisseria meningitides 011 (100)11
Pseudomonas aeruginosa 5 (100)05
Pseudomonas putida 1 (100)01
Salmonella group B01 (100)1
Serratia marcescens 01 (100)1
Total 58 59 117
Table 4

Distribution of microorganisms in relation to the age group.

Microorganism Age groupTotal
<11–56–1415–2425–3435–4445–5455–64≥65
Abiotrophia species0000010001 (0.8)
Acinetobacter baumannii 0000023218 (6.8)
Acinetobacter lwoffii 0110100003 (2.6)
Brucella spp.0000001001 (0.8)
Chryseobacterium (Flavobacterium) meningosepticum 1000000001 (0.8)
Chryseobacterium indologenes 1000000001 (0.8)
Enterobacter aerogenes 1000000001 (0.8)
Enterobacter cloacae 0000012003 (2.6)
Enterococcus faecalis 2100012107 (5.9)
Enterococcus gallinarum 0000001001 (0.8)
Escherichia coli 2100010004 (3.4)
Gemella haemolysans 0001000001 (0.8)
Haemophilus influenzae 0101000002 (1.6)
Klebsiella pneumoniae ssp. pneumoniae20021142012 (10.3)
Leuconostoc species0000001001 (0.8)
Listeria monocytogenes 3000000003 (2.6)
Neisseria meningitidis 01033120111 (9.4)
Pseudomonas aeruginosa (PSA)0010211005 (4.2)
Pseudomonas putida 0000100001 (0.8)
Salmonella group B1000000001 (0.8)
Serratia marcescens 1000000001 (0.8)
Staphylococcus aureus 0010000001 (0.8)
Staphylococcus capitis 0000011002 (1.6)
Staphylococcus epidermidis 62021311016 (13.6)
Staphylococcus haemolyticus 0000110002 (1.6)
Streptococcus agalactiae 2000000013 (2.6)
Streptococcus bovis II 1000000001 (0.8)
Streptococcus intermedius 0000010001 (0.8)
Streptococcus milleri 0001000001 (0.8)
Streptococcus mitis 0100000001 (0.8)
Streptococcus pneumoniae 32323240019 (16.2)
Streptococcus salivarius 0100000001 (0.8)

Total26 (22.2)11 (9.4)6 (5.1)12 (10.3)13 (11.1)17 (14.5)23 (19.7)6 (5.1)3 (2.6)117 (100)

3.5. Trends of Antimicrobial Susceptibility

Details of antimicrobial susceptibility are shown in Tables 5 and 6. Among the Gram-positive cases, 3 (18.6%) episodes of Streptococcus pneumoniae were resistant to ceftriaxone, while out of all coagulase-negative staphylococci isolates, 19 (95%) were methicillin-resistant. Among the Gram-negative cases, 100% of Chryseobacterium species were resistant to meropenem and colistin, while 63.3% of Acinetobacter species showed resistance to meropenem but none for colistin. All Pseudomonas spp. were sensitive to piperacillin-tazobactam and meropenem. Among Klebsiella isolates, 2 (16.6%) were extended spectrum beta-lactamase (ESBL) producers, but all of them were sensitive to meropenem and colistin. Of the 11 episodes with Neisseria meningitides infection, rifampicin resistance was found in 2 (25%). Multidrug resistance was observed in 38 (32.4%) of all episodes.
Table 5

Antimicrobial resistance rate of Gram-positive CSF isolates.

Microorganisms TNPpenampoxcerytclindamclvcotrcfrvanlineteic
Abiotrophia spp.100NT0000NT0NTNT
Enterococcus faecalis 7NT0NTNTNTNTNTNT000
Enterococcus gallinarum 1NT0NTNTNTNTNTNT1 (100)00
Gemella haemolysans 100NTNTNTNTNT00NTNT
Leuconostoc species100NTNT00NT1 (100)1 (100)00
Listeria monocytogenes 300NTNTNTNT0NTNTNTNT
Staphylococcus aureus 11 (100)1 (100)NT0000NT000
Coagulase-negative staphylococci2020 (100)20 (100)19 (95)19 (95)10 (50)20 (100)9 (45)NT000
Streptococcus spp.81 (0.2)1 (0.2)01 (0.2)1 (0.2)01 (0.2)1 (0.2)000
Streptococcus pneumoniae 196 (31.5)6 (31.5)6 (31.5)6 (31.5)6 (31.5)6 (31.5)3 (15.7)3 (15.7)000

TNP: total number of patients; pen: penicillin; amp: ampicillin; oxc: oxacillin; eryt: erythromycin; clind: clindamycin; amclv: amoxicillin/clavulanic acid; cotr: cotrimoxazole; cfr: ceftriaxone; van: vancomycin; line: linezolid; teic: teicoplanin; NT: not tested.

Table 6

Antimicrobial resistance rate of Gram-negative cerebrospinal fluid isolates.

Microorganisms TNPcfrgenfeptazcipamclvctzamkmempenrifcoltig
Acinetobacter spp.118 (72.7)8 (72.7)8 (72.7)8 (72.7)7 (63.6)NT7 (63.6)7 (63.6)7 (63.6)NTNT00
Brucella species1NTNTNTNTNTNTNTNTNTNTNTNTNT
Chryseobacterium spp.21 (50)2 (100)01 (50)0NT2 (100)2 (100)2 (100)NTNT2 (100)2 (100)
Enterobacter species43 (75)01 (25)3 (75)04 (100)3 (75)00NTNTNTNT
Escherichia coli 41 (25)1 (25)1 (25)01 (25)1 (25)1 (25)00NTNTNTNT
Haemophilus influenzae 20NT00NT0NTNTNTNTNTNTNT
Klebsiella pneumoniae ssp. pneumoniae123 (25)03 (25)2 (16.6)2 (16.6)7 (58.3)4 (33.3)00NTNT00
Neisseria meningitidis 80NT002 (25)0NTNT002 (25)NTNT
Pseudomonas aeruginosa 5NT0000NT000NTNT00
Pseudomonas putida 1NT0000NT000NTNT00
Salmonella group B101 (100)0000000NTNTNTNT
Serratia marcescens 1000001 (100)000NTNTNTNT

TNP: total number of patients; cfr: ceftriaxone; gen: gentamicin; fep: cefepime; taz: piperacillin/tazobactam; cip: ciprofloxacin; amclv: amoxicillin/clavulanic acid; ctz: ceftazidime; amk: amikacin; mem: meropenem; pen: penicillin; rif: rifampicin; col: colistin; tig: tigecycline; NT: not tested.

3.6. Treatment and Outcome

Antimicrobial treatment was initiated for all patients. Ceftriaxone plus vancomycin combination was the most widely used antimicrobial treatment followed by meropenem. Empiric therapy was inappropriate in 20 (17.1%) episodes. The crude in-hospital mortality in our study was 14 (12%).

3.7. Univariate and Multivariate Logistic Regression Analysis of Factors Associated with Death

By the univariate analysis, the following variables were found to be probable predictors of in-hospital mortality: presence of underlying diseases, nosocomial infection, multidrug-resistant episodes, hypotension, mental alteration, and inappropriate treatments (see Table 7). Only the presence of underlying diseases, hypotension, and inappropriate treatment were found to be independent predictors of mortality by multivariate logistic regression analysis (see Table 8).
Table 7

Results of univariate analysis of in-hospital mortality predictors.

VariableUnadjusted odds ratio (95% CI) P value
Presence of underlying diseases2.4 (1.4–3.9)0.001
Nosocomial infection3.2 (1.5–6.5)0.1
Multidrug-resistant episodes4.7 (3.8–5.7)0.08
Mental alteration4.9 (1.0–24.0)0.06
Hypotension2.3 (0.7–7.3)0.003
Inappropriate treatments1.9 (1.2–3.07)0.01
Table 8

Results of multivariate analysis of in-hospital mortality independent factors.

VariableAdjusted odds ratio (95% CI) P value
Presence of underlying diseases1.8 (1.03–3.2)0.02
Hypotension3.2 (1.4–7.3)0.04
Inappropriate treatments1.7 (1.0–2.8)0.01

4. Discussion

Acute bacterial meningitis is a serious disease which necessitates early diagnosis and aggressive therapy to improve prognosis. Regional information regarding demographic data of patients, associated underlying conditions, etiology, and antimicrobial susceptibility is essential for correct and timely management of this disorder. Our study was the first to attempt to determine the clinical picture and the spectrum of pathogens of bacterial meningitis in patients of all ages in Qatar. This retrospective series revealed some observations that deserve attention: firstly, in contrast with the previous study [6], the trend was seen to decrease from 2009 to 2013. Among the total 117 episodes, 43 (36.7%) were reported in the year 2009, which decreased to 18 (15.4%) in 2013. Furthermore, the disease in our series predominantly affected adults rather than infants and young children. This picture is similar to what was found in west countries and it may be attributed to vaccine-related decline in H. influenzae and pneumococcal diseases [3, 9, 14, 15]. These data show that adults are the main target population which requires interventions to prevent and control diseases in Qatar. Secondly, sex distribution of the disease showed male predominance in agreement with the previous report [6] and other reports from different countries [9, 10, 16–19]. The reason for this is obscure, and further studies are needed to identify the cause. Thirdly, compared with the previous studies [4, 6], changes of common causative pathogens of ABM had been noted in our series. Coagulase-negative staphylococci species were the most common causative agents followed by Streptococcus pneumoniae. This can be explained by the expansion of neurosurgical services in our hospital with a consequent increase in the number of patients with postneurosurgical state. Similarly, reports from Taiwan [15-18] showed that there has been an increasing incidence of staphylococcal infection in ABM patients. However, in agreement with many reports worldwide [2, 7, 20–23], Streptococcus pneumoniae remain the common causative agent for community-acquired infection in our study. Fourthly, drug resistance pattern showed that 95% of the implicated coagulase-negative staphylococci species were oxacillin-resistant and 63.3% of the implicated Acinetobacter species were meropenem-resistant. Both infections were predominantly nosocomial, which raised doubt regarding the infection control program in our hospital. Moreover, these findings result in therapeutic challenge in the choice of empiric antibiotics in the initial management of ABM. These findings are consistent with reports coming from Taiwan recently [9, 18, 19]. Fortunately, so far, we have not encountered vancomycin-resistant coagulase-negative staphylococci strains or colistin-resistant Acinetobacter strains. Finally, in an attempt to identify independent predictors of mortality in patients with ABM, many studies had been conducted. The concluded prognostic factors among these studies were diverse [9, 10, 18, 19, 22, 23]. Our study revealed many probable prognostic factors; however, only the presence of underlying diseases, hypotension, and inappropriate treatment were found to be independent predictors of mortality by multivariate logistic regression analysis. This hospital-based study has the following limitations. First, the study was retrospective rather than prospective, and this design did not allow us to obtain additional details such as severity of the disease and long-term follow-up to evaluate the long-term sequelae of meningitis in our patients. Second, it was performed at a single hospital; the results may not be applicable to other hospitals. Third, we included patients who had a positive CSF culture or positive CSF bacterial antigen test. Despite these limitations, we believe that our study remains the largest to date to provide comprehensive information on the epidemiology of ABM in Qatar. In conclusion, our study revealed that there is a change in the predominantly affected age group and common causative agents of ABM. Coagulase-negative staphylococci species are the common causative agent in Qatar with majority of infections occurring nosocomially. More than 90% of all implicated coagulase-negative staphylococci strains were oxacillin-resistant. Thus, improving our infection control programs in addition to enhancing antimicrobial stewardship is essential to overcome this problem.
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Journal:  Int J Environ Res Public Health       Date:  2021-05-31       Impact factor: 3.390

5.  Bacterial Meningitis Among Adult Patients at University of Gondar Comprehensive Specialized Referral Hospital.

Authors:  Abiye Tigabu; Abiyot Jember; Temesgen Nega; Getachew Wubishet; Hana Misganaw; Tigist Goshu; Markos Negash
Journal:  Infect Drug Resist       Date:  2021-02-15       Impact factor: 4.003

6.  Epidemiology Profile of Viral Meningitis Infections Among Patients in Qatar (2015-2018).

Authors:  Shilu Mathew; Hebah A Al Khatib; Khalid Al Ansari; Joanne Nader; Gheyath K Nasrallah; Nadin N Younes; Peter V Coyle; Asmaa A Al Thani; Muna A Al Maslamani; Hadi M Yassine
Journal:  Front Med (Lausanne)       Date:  2021-06-16
  6 in total

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