Escherichia coli spontaneous community-acquired meningitis in adults: A case report and literature review

Accepted Manuscript Title: Escherichia coli spontaneous community-acquired meningitis in adults: a case report and literature review Authors: A. Bichon, C. Aubry, G. Dubourg, H. Drouet, J-C. Lagier, D. Raoult, P. Parola PII: DOI: Reference:

S1201-9712(17)30315-6 https://doi.org/10.1016/j.ijid.2017.12.003 IJID 3111

To appear in:

International Journal of Infectious Diseases

Received date: Revised date: Accepted date:

2-10-2017 28-11-2017 1-12-2017

Please cite this article as: Bichon A, Aubry C, Dubourg G, Drouet H, Lagier J-C, Raoult D, Parola P.Escherichia coli spontaneous community-acquired meningitis in adults: a case report and literature review.International Journal of Infectious Diseases https://doi.org/10.1016/j.ijid.2017.12.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Escherichia coli spontaneous community-acquired meningitis in adults: a case report and literature review

A. BICHON, C. AUBRY, G. DUBOURG, H. DROUET, J-C. LAGIER, D. RAOULT and P.

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PAROLA

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1. Aix Marseille Univ, CNRS 7278, IRD 198, INSERM 1095, AP-HM, URMITE, IHU

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Méditerranée-Infection, 19-21 Boulevard Jean Moulin, 13385 Marseille Cedex 5, France

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Text word count = 1781

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Abstract = 88

Escherichia coli spontaneous community-acquired meningitis is poorly reported

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Highlights

in the literature with only 43 cases described since 1946. Underestimated annual incidence of Escherichia coli spontaneous community-

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acquired meningitis ranges from 2 to 5 cases for 100,000 persons. Nine percent of diagnosed patients were previously healthy.

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Mortality rate is higher than for other bacterial meningitides, up to 100%.

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Systematic screening regarding strongyloidiasis should be made for symptomatic

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patients returning from an endemic territory.

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Abstract Bacillary, Gram negative meningitis occurring post-trauma and following neurosurgical procedures have been widely described. However, reports of spontaneous cases are sparse, particularly community-acquired cases. Spontaneous Escherichia coli communityacquired meningitis is a rare, though increasing, and specific entity which is poorly reported

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in literature. Between 1946 and 2016, only 43 cases of community acquired Escherichia coli meningitis have been described. In this paper, we report on two cases of spontaneous,

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community-acquired Escherichia coli meningitis encountered in Marseille, France, followed by a literature review of spontaneous community-acquired E. coli meningitis.

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Keywords: Escherichia coli meningitis; spontaneous community-acquired

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Introduction

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Gram negative bacilli (GNB) are an uncommon cause of community-acquired meningitis

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in adults, ranging from 0.7% in Netherlands,[1] to 3.6% in the United States, [2] and 7% in

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Spain.[2] It is reported that 36 to 50% of cases of GNB meningitis occur after neurosurgical procedures.[3][4] Neurosurgery, head trauma within the past month, a neurosurgical device,

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and cerebrospinal fluid (CSF) leak represent portals of entry in 75% cases of nosocomial cases.[5] Spontaneous, non-traumatic Gram negative bacillary meningitis is usually

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community-acquired and occurs in patients with identified risk factors. Spontaneous community-acquired Gram-negative bacilli meningitis represents 8.7% of all spontaneous

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community-acquired meningitis, with an annual incidence of two cases per 100,000 adults. Escherichia coli represents 41.9% of these cases.[2] In this paper, we report two cases of spontaneous community-acquired E. coli meningitis diagnosed in our institution and review other cases reported in the literature. Our objective

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was to identify risk factors, collect demographic, microbiological and therapeutic data to prevent death and optimize management of those patients. Key words: Escherichia coli meningitis, spontaneous community-acquired

Case 1

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A sixty-seven-year-old woman who had previously been in good health was admitted to the emergency department for fever and alteration of consciousness. Two days after

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admission, she presented a sporadic episode of vomiting, symptoms of a urinary infection, and non-specific, diffuse abdominal pain. She had no medical, surgical or cranial trauma

history and was not receiving any daily treatment. Upon admission, the patient presented a

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fever (39°C), blood pressure of 147/66 mmHg, a heart rate of 94 beats per minute, and

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capillary glycemia of 1.16 g/L. Her Glasgow Coma Score (GCS) was evaluated at 9 with

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respectively 5, 2 and 2 for motor, eye and verbal responses. She showed no localized motor or

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sensitive deficiencies but was agitated and neck stiffness was noted. She reported impaired

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hearing in her right ear. Clinical examination was otherwise normal. A rapid urine test was positive for leucocytes and nitrites, although a subsequent urine

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test culture was sterile. Blood cultures were also sterile. A lumbar puncture showed 900 elements/mm3, including 90% neutrophils, hypoglycorrhachia inferior to 0.1mmol/L, and

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elevated protein level in CSF at 4.36g/L. Cultures of cerebrospinal fluid (CSF) grew Escherichia coli expressing low levels of AmpC beta-lactamase. Computed tomography of

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the brain, chest, abdomen and pelvis showed no deep infection or evidence of neoplasia. Initial antimicrobial therapy included probabilistic 75mg/kg/day of ceftriaxone,

75mg/kg/day of amoxicillin and 15mg/kg/day of acyclovir. Antimicrobial therapy was then adapted to CSF sample findings with ceftriaxone at meningeal doses of 2g twice a day for twenty-one days. The patient did not receive corticosteroid treatment. The patient’s evolution was favorable, with partial regression of neurological symptoms, and the return to normal of 3

biological inflammatory parameters, and lumbar puncture tests. Acoustic tests and dedicated consultation with a specialist revealed a right transmission hearing impairment due to chronic otitis with no CT scan abnormality. A slight and fluctuating anosognosia was noted two months after the end of antimicrobial therapy. Case 2

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A thirty-four-year-old man presenting with coma due to status epilepticus was

transferred to the Timone hospital. The patient’s medical history included chronic alcoholism

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in an attempt to withdraw from baclofen, as well as sciatica which was being treated with

corticosteroids. He was found unconscious at home the day before admission. His vital signs showed normal blood pressure at 120/80mmHg, tachycardia at 150 beats per minute, altered

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Glasgow Coma Score (GCS) at 7, and anisocoria. Temperature and capillary glycemia were

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normal at 36.5°C and 1.15 gram per liter respectively. Seizures ceased after a ten-milligram

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intravenous injection of diazepam. As the patient continued to display neurological failure, he

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was sedated, intubated and immediately transferred to the local hospital. Blood analysis found

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bicytopenia with platelets at 10G/L, leucopenia at 2G/L and neutropenia at 200/mm3. Atypical lymphocytes were found in the blood analysis. An inflammatory syndrome was noted with

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elevated C Reactive Protein (CRP) at 330mg/L. The prothrombin ratio (PR) was preserved at 98% while cholestatic cytolysis with elevated bilirubin was noted. Lactatemia was elevated at

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3.92mmol/L. Status epilepticus was treated and the patient was sedated before being transferred on the same day to the Timone university hospital.

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Upon admission, the patient showed signs of septic shock with a high fever (39.5°C)

associated with low blood pressure. His neurological evaluation was unchanged. The serum ethanol rate was negative and hypokalemia at 2.2mmol/L was treated. Hematological analysis aggravated towards a probable disseminated intravascular coagulation (DIVC) with a fall of PR at 61% and thrombopenia at 4G/L. Human Immunodeficiency Virus (HIV), B and C viral

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hepatitis serologies were negative and the patient had been vaccinated against hepatitis B. A lumbar puncture showed turbid cerebrospinal fluid (CSF), hypoglycorrhachia inferior to 0.1g/L with normal glycemia, elevated CSF protein levels at 3g/L, 144 elements/mm3 including 90% neutrophils. CSF direct Gram coloration showed Gram negative bacilli. Computed tomography (CT scan) of the brain, chest, abdomen and pelvis was normal.

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Probabilistic antimicrobial therapy was initiated with meningeal doses of amoxicillin, ceftriaxone and acyclovir.

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A poor outcome was noted with gingivorrhagia, areactive mydriasis, followed by brain death on the day of admission to the Timone hospital. Post-mortem CSF cultures revealed an Escherichia coli producer of low level penicillinase and resistant to trimethoprim-

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sulfamethoxazole. The same bacterium was encountered in blood cultures and urinalysis.

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Discussion

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Data was collected from Pubmed, Research gate, and google scholar

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investigation. Key words included Escherichia coli, coli bacillus, community-acquired

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meningitis, adults, spontaneous. A total of 43 cases of spontaneous community-acquired Escherichia coli meningitis were reported between 1946 and 2016, in addition to our two

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cases described above [Table 1]. Eight articles were excluded from our study due to lack of information about the type of meningitis between nosocomial and/or post-traumatic

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versus spontaneous community-acquired, or in presence of exclusion criteria meaning hospital-acquired and post-traumatic meningitis. Articles concerning minors were also

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excluded as Escherichia coli meningitis is more common in this population. The excluded studies are referenced in [Table 2]. From literature review and our two reported cases (N=45), mean age was fifty-six years. The patient’s age was unknown in 16% of cases. The sex ratio at 1.4 showed a slight tendency towards feminine population, with twenty women and fourteen men. The sex was unknown in 24% of cases. Risk factors are reported in

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[Table 3]. In order of frequency, the identified risk factors were chronic alcoholism and cirrhosis accounting each for 20% of cases, diabetes mellitus for 16% of cases, disseminated strongyloidiasis in 6%, HIV positive patients, chronic obstructive pulmonary disease, and chronic organ insufficiency in 4% each. Hemochromatosis, myelodysplasia, hemophagocytic lymphohistiocytosis, urinary tract instrumentation, B lymphoma, long-term glucocorticoid

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therapy, Marfan syndrome and HTLV1 seropositivity were also reported as risk factors, each representing 1% of cases in our study. Risk factors were unknown for eleven patients (24%),

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while 9% of cases were previously healthy. Concerning our reported cases, one displayed chronic alcoholism as a risk factor but the second patient, who was previously healthy,

displayed no risk factors. Finally, the cause of infection was unknown in 40% of cases. When

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identified, portals of entry were represented by 31% bacteremia, 24% urinary tract infection,

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spondylodiscitis) and 2% for primary peritionitis.

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9% pneumonia, 4% for septic arthritis (including one case of Escherichia coli

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Microbiology, treatment and outcome are presented in [Table 4]. When available,

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microbiological data revealed a majority of wild Escherichia coli, in 20% of cases. E. coli was a producer of penicillinase in 9% of cases and was rarely quinolone or trimethoprim-

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sulfametoxazole resistant with 2% each. Preoccupying significant rate of E.coli producer of extended spectrum beta-lactamases (ESBLs) was encountered in 7% of community-acquired

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cases. Bacterial sensibility was not reported in 60% of cases. One of our reported cases exhibited a high resistance profile with an Escherichia coli producer of penicillinase and

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resistance to trimethoprim-sulfamethoxazole. The other case displayed a wild type of E.coli. Concerning antimicrobial agents, the most widely used drugs included ceftriaxone (22%), gentamicin (13%), ampicillin (11%), penicillin G and amoxicillin (9% each), and meropenem (7%). Most therapy courses used either beta-lactamins or penicillins, and more rarely amikacin, moxalactam, sulfathiazole and chloramphenicol. Treatment was not provided for

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twelve patients. The average duration of therapy was 15.81 [1-21.25] but was unknown in 68% of cases. Both of our reported cases received meningeal doses of cephalosporin, for a course of twenty-one days in the case of the first patient. The outcome showed high mortality rates at 47% [25-100], including one death from status epilepticus and DICV on day one after admission. Those findings display similar

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features with previous studies, in which mortality ranges from 50 to 90%, reaching 86% when associated with disseminated strongyloidiasis, or 100% in cirrhotic patients.[3] [6] [7] [8]

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However, the hypothesis that concomitant bacteremia or a coma may worsen the prognosis is strengthened by the second patient we reported on, who died after being admitted with an initial coma. Our study focused on a binary outcome (death or survival) but neurological

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sequela should also be taken in consideration, occurring in between 30 and 50% of cases,

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two months after the end of antimicrobial therapy.

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supported by the first case we report.[8] This patient manifested persistent slight anosognosia,

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Concerning our study limitations, the first regards the important lack of data in

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the literature, ranging from sixteen to sixty-three percent. As summarized in Table 2, 423 cases have been excluded due to imprecise information. Conclusions of this review

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are made of a small sample of cases; thus, a bigger group of patients would be required to confirm our results. Finally, the oldest cases come from reports of 1946, when

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microbiological identification and antimicrobial sensibility were not as reliable as they are now, inducing potential mistakes. The same concern should be raised with the

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antimicrobial agents for whom recommendations have changed. For instance, chloramphenicol and sulfathiazole are no longer recommended in first intention in the treatment of Escherichia coli meningitis. Conclusion and perspective

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In conclusion, spontaneous community-acquired Escherichia coli meningitis in adults, although described as a rare entity, is likely to be underestimated and not as sporadic as reported in most articles. New underlying conditions have been described as risk factors, in addition to chronic alcoholism, cirrhosis, diabetes mellitus, HIV seropositive status, chronic obstructive pulmonary disease and chronic organ

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insufficiency. These latter concern urinary and digestive tract disorders. Among them are Marfan syndrome, large meningocele in contact with bowels, disseminated

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strongyloidiasis, urinary tract infection and pyelonephritis. Although the wild type of

Escherichia coli still remains in a large majority, the emergence of statistically relevant community-acquired ESBLs producer E.coli meningitis is concerning. Finally, prognosis

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is determined by the diagnosis and the rapidity of antimicrobial drug administration.

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Presence of coma, bacteremia or disseminated strongyloidiasis worsens the prognosis.

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Prospective studies with large cohorts are required to confirm those results and

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properly collect demographic, clinical, microbiological and therapeutic information.

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Conflict of Interest/Funding: None

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16. Ashish A Sule, Dessmon YH Tai. Spontaneous Escherichia coli meningitis in an adult. 2007; :148–150. 17. Chang K-H, Lyu R-K, Tang L-M. Spontaneous Escherichia coli Meningitis Associated with Hemophagocytic Lymphohistiocytosis. J. Formos. Med. Assoc. 2006; 105:756–759. 18. Yang T-M, Lu C-H, Huang C-R, et al. Clinical characteristics of adult Escherichia coli meningitis. Jpn. J. Infect. Dis. 2005; 58:168–170.

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32. Seydi M, Soumaré M, Sow AI, Diop BM, Sow PS. [Escherichia coli meningitis during bacteremia in the Ibrahima-Diop-Mar infectious diseases clinic, Dakar Fann National Hospital Center (Senegal)]. Med. Mal. Infect. 2005; 35:344–348. 33. Pauwels A, Pinès E, Abboura M, Chiche I, Lévy VG. Bacterial meningitis in cirrhosis: review of 16 cases. J. Hepatol. 1997; 27:830–834.

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34. Gilmore RL, Lebow R, Berk SL. Spontaneous Escherichia coli K1 meningitis in an adult. South. Med. J. 1983; 76:1202–1203.

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Table 1. Reported cases of spontaneous community-acquired E. coli meningitis in a literature review from 1946 to 2016.

2016 2015 2013 2013 2012 2009 2008 2008 2008 2007 2007 2005 2005 2004 2002 2000 1998 1986 1985 1978 1965 1965 1946

Ishida K. et al. Clin Case Rep 2016; 4(4): 323-6.[9] Kohlmann R et al. BMC Infect Dis. 2015; 15: 567 [9] Kangath RV et al. BMJ Case Rep. 2013; 2013 [10] Pomar V. et al. BMC Infect Dis 2013; 13:451 [2] Weyrich P et al. Ann Clin Microbiol Antimicrob. 2012; 11: 4. [11] Cabellos C et al. Medicine (Baltimore). 2009 Mar;88(2):115-9 [12] Cabellos C et al. Clin Microbiol Infect. 2008 Jan;14(1):35-40 [13] Briongos-Figuero LS et al. Rev Clin Esp 2008; 208(5):262. Miletic D et al. Orthopedics. 2008 Feb;31(2):182. [14] Samson D. et al. Ann Fr Anesth Reanim 2007 Jan; 26(1):88-90.[15] Ashish A. et al. Crit Care & Shock 2007; 10:148-150. [16] Chang K-H. et al. J Formos Med Assoc. 2006; 105(9):756-9. [17] Yang T-M. et al. 2005; 58: 168-170.[18] Van de Beek D. et al. N Engl J Med 2004; 351:1849-1859 [1] Hovette P. et al. Press Med 2002; 22:1021-3.[19] Mofredj A. et al. Scand J Infect Dis 2000 ; 32: 699-700. [20] Almirante B. Clin Infect Dis 1998; 27:176-80. [21] Smallman L. et al. J Clin Pathol 1986; 39:366-370. [22] Christopher GW. et al. Arch Intern Med. 1985; 145(10):1908. [23] Crane LR. et al. Medicine (Baltimore) 1978; 57:197-209 [24] Kunin C. et al. Arch Intern Med 1965; 115(6):652-658. [25] Manesis J. et al. Arch Neurol 1965; 13(2):214-216. [26] Crawley F.E. et al. The Lancet 1946; 247:461-462. [27]

Number of cases 1 1 1 1 1 6 5 1 1 1 1 1 4 4 1 1 1 2 1 4 2 1 1

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Year

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Table 2. Escherichia coli meningitis cases excluded from study because of their character nosocomial and post-traumatic, or absence of specification about the type of meningitis.

2015 2014 2013 2010 2006 2005 1997 1983

Teckie G et al. Int J Infect Dis. 2015 Jan;30:38-40. [28] Okike IO et al. Clin Infect Dis. 2014 Nov 15;59(10):e150-7. [29] Pomar V. et al. BMC Infect Dis 2013; 13:451 [2] Laguna-Del Estal P. et al. Rev Neurol 2010; 50:458-462. [30] Bouadma L. et al. Clin Microbiol Infect 2006, 12:287-290. [31] Seydi M. et al. Med Mal Infect 2005 Jun; 35(6):344-8 [32] Pauwels A. et al. J Hepatol. 1997 Nov;27(5):830-4. [33] Gilmore RL. et alSouth Med J 1983; 76(9) : 1202-3. [34]

Number of cases 9 353 15 3 23 10 9 1

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Reference

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Table 3. Risk factors, suspected causes and microbiology of patients diagnosed with spontaneous community-acquired Escherichia coli meningitis. %

9 9 7 3 2 2 2 1 1 1

20 20 16 7 4 4 4 2 2 2

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N = 44 Risk factors Chronic alcoholism Cirrhosis Diabetes mellitus Disseminated strongyloidiasis COPD** HIV* Chronic organ insufficiency Hemochromatosis Myelodysplasia Hemophagocytic lymphohistiocytosis Urinary tract instrumentation B lymphoma Long-term corticosteroids HTLV1 Healthy Unknown

1 1 1 1 4 11

2 2 2 2 9 24

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Suspected cause Bacteremia 13 30 Urinary tract infection 10 23 Pneumonia 4 9 Peritonitis 1 2 Septic arthritis 1 2 Unknown 1 41 * HIV: human immunodeficiency virus ** COPD: chronic obstructive pulmonary disease *** Others: six chronic organ failures, one hemophagocytic lymphohistiocytosis, one hemochromatosis, one chronic obstructive pulmonary disease, one myelodysplasia, one human T lymphotropic virus 1

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Table 4. Microbiology, treatment and outcome of patients diagnosed with spontaneous communityacquired Escherichia coli meningitis. n

%

9 4 1 1 3 27

20 9 2 2 7 60

Treatment Ceftriaxone Gentamicin Penicillin G Amoxicillin Ampicillin Chloramphenicol Cefotaxime Meropenem Amikacine Moxalaxtam Ceftazidime Cephalothin Vancomycin Ciprofloxacin Sulphathiazole Unknown

10 6 4 4 5 2 2 3 1 1 1 1 1 1 1 12

22 13 9 9 11 4 4 7 2 2 2 2 2 2 2 27

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Duration of treatment Days Unknown

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N=44 Microbiology Wild type Penicillinase producer Fluoroquinolone-resistant Trimethoprim-sulfametoxazole resistant ESBLs* Unknown

15.81 [1-21.25] 31

69

21 15 9

47 [25-100] 33 20

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Outcome Death Favorable Unknown * ESBLs: extended spectrum bectalactamases

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** Others: amikacin, cefotaxime, ceftazidime, cephalothin, meropenem, sulfathiazole, moxalactam, chloramphenicol

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