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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, Didier Raoult,
Philippe Parola
To cite this version:
A. Bichon, C. Aubry, G. Dubourg, H. Drouet, J. -C. Lagier, et al.. Escherichia coli spontaneous
community-acquired meningitis in adults: A case report and literature review. International Journal
of Infectious Diseases, Elsevier, 2018, 67, pp.70-74. �10.1016/j.ijid.2017.12.003�. �hal-01780648�
Case
Report
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,
P.
Parola
*
AixMarseilleUniversité,CNRS7278,IRD198,INSERM1095,AP-HM,URMITE,IHUMéditerranée-Infection,19-21BoulevardJeanMoulin,13385Marseille, Cedex5,France
ARTICLE INFO Articlehistory: Received2October2017
Receivedinrevisedform28November2017 Accepted1December2017
Corresponding Editor: Eskild Petersen, Aarhus,Denmark Keywords: Escherichiacoli Gram-negatiivemeningitis Spontaneouscommunity-acquired ABSTRACT
Gram-negativebacillarymeningitisoccurringpost-traumaandfollowingneurosurgicalprocedureshas beendescribedwidely.However, reportsofspontaneouscasesaresparse,particularly community-acquired cases. Spontaneous community-acquired Escherichia coli meningitis is a rare (although increasinglyseen)andspecificentitythatispoorlyreportedintheliterature.Areviewoftheliterature identifiedonly43casesofcommunity-acquiredE.colimeningitisreportedbetween1946and2016.This articledescribestwonewcasesofspontaneouscommunity-acquiredE.colimeningitisencounteredin Marseille,France,andpresentstheresultsofaliteraturereviewonspontaneouscommunity-acquiredE. colimeningitis.
©2017TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases. ThisisanopenaccessarticleundertheCCBY-NC-NDlicense( http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Gram-negative bacilli (GNB) are an uncommon cause of community-acquiredmeningitisin adults,rangingfrom0.7% in theNetherlands (van deBeek et al., 2004) to3.6% in the USA (Pomar et al.,2013) and 7%in Spain (Pomar et al., 2013).It is reported that 36–50% of cases of GNB meningitis occur after neurosurgicalprocedures(BerkandMcCabe,1980;Huangetal., 2001). Neurosurgery, head trauma within the past month, a neurosurgicaldevice,andcerebrospinalfluid(CSF)leakrepresent portalsofentryin75%ofnosocomialcases(Durandetal.,1993). Spontaneous,non-traumaticGNBmeningitisisusually communi-ty-acquired and occurs in patients withidentified risk factors. Spontaneous community-acquired GNB meningitis represents 8.7% of all spontaneous community-acquired meningitis, with anannualincidenceoftwocasesper100000adults.Escherichia colirepresents41.9%ofthesecases(Pomaretal.,2013).
This articledescribestwo casesof spontaneous community-acquiredE.colimeningitisdiagnosedattheauthors’institutionand providesa reviewof othercasesreportedintheliterature. The objectivewastoidentifyriskfactorsandtocollectdemographic, microbiological,andtherapeuticdatainordertopreventdeathand optimizethemanagementofthesepatients.
Casereports Case1
A67-year-oldwomanwhohadpreviouslybeeningoodhealth wasadmittedtotheemergencydepartmentwithfeverandaltered consciousness.Twodaysafteradmission,shepresentedanepisode ofsporadicvomiting,symptomsofaurinarytractinfection,and non-specificdiffuseabdominalpain.Shehadnohistoryofmedical, surgical, or cranial trauma and was not receiving any daily treatment.Uponadmission,thepatientpresentedafever(39C), blood pressure of 147/66mmHg, a heart rate of 94 beats per minute,andcapillaryglycemiaof1.16g/l.HerGlasgowComaScale (GCS)scorewas9,withrespectivescoresof5,2,and2formotor, eye, and verbal responses. She showed no localized motor or sensorydeficits,butwasagitatedandneckstiffnesswasnoted.She reportedimpairedhearinginherrightear.Theclinical examina-tionwasotherwisenormal.
A rapid urine test was positive for leukocytes and nitrites, althoughasubsequenturinetestculturewassterile.Bloodcultures werealsosterile.Alumbarpunctureshowed900elements/mm3, including90%neutrophils,hypoglycorrhachialessthan0.1mmol/l, andanelevatedproteinlevelintheCSFat4.36g/l.CulturesofCSF grew E. coli expressing low levels of AmpC beta-lactamase. Computed tomography (CT)of the brain, chest, abdomen, and pelvisshowednodeepinfectionorevidenceofneoplasia.
*Correspondingauthor.
E-mailaddress:philippe.parola@univ-amu.fr(P. Parola).
https://doi.org/10.1016/j.ijid.2017.12.003
1201-9712/©2017TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).
ContentslistsavailableatScienceDirect
International
Journal
of
Infectious
Diseases
Initialantimicrobialtherapyincluded75mg/kg/dayof ceftri-axone,75mg/kg/dayofamoxicillin,and15mg/kg/dayofacyclovir (probabilistic).Antimicrobial therapy was then adapted to CSF samplefindingswithceftriaxonegivenatameningealdoseof2g twiceadayfor21days.Thepatientdidnotreceivecorticosteroid treatment. The patient’s evolution was favorable, with partial regressionofherneurologicalsymptoms;biologicalinflammatory parametersandlumbarpuncturetestresultsreturnedtonormal. Acoustictestsandreferraltoaspecialistforconsultationrevealeda righttransmissionhearingimpairmentduetochronicotitiswith noCTscanabnormality.Aslightandfluctuatinganosognosiawas noted2monthsaftertheendofantimicrobialtherapy.
Case2
A 34-year-old man presenting with coma due to status epilepticuswas transferred toTimone UniversityHospital. The patient’s medical history included chronic alcoholism in an attempt to withdraw from baclofen, as well as sciatica which wasbeingtreatedwithcorticosteroids.Hewasfoundunconscious athomethedaybeforeadmission.Hisvitalsignsshowedanormal blood pressure at 120/80mmHg, tachycardia at 150 beats per minute,alteredGCSat7,andanisocoria.Histemperature(36.5C) andcapillaryglycemia(1.15g/l)werenormal.Seizuresceasedafter a 10-mg intravenous injection of diazepam. As the patient continued to display neurological failure, he was sedated, intubated, and transferred immediately to the local hospital. Bloodanalysisrevealed bicytopeniawithplatelets at10109/l, leukopenia at 2109/l, and neutropenia at 0.2109/l. Atypical lymphocyteswerefoundinthebloodanalysis.Aninflammatory syndromewas noted with elevated C-reactiveprotein (CRP) at 330mg/l.Theprothrombinratio(PR)waspreservedat98%,while cholestaticcytolysiswithelevatedbilirubinwasnoted.Lactatewas elevatedat3.92mmol/l.Thestatusepilepticuswastreatedandthe patientwassedatedbeforebeingtransferredonthesamedayto TimoneUniversityHospital.
Uponadmission,thepatientshowedsignsofsepticshockwith ahighfever(39.5C)associated witha lowblood pressure.His
neurologicalevaluationwasunchanged.Hisserumwasnegative for ethanol, andhe was treated forhypokalemia (potassiumat 2.2mmol/l). The hematological analysis indicated probable
disseminatedintravascularcoagulation(DIC)witha fallinPRto 61%andthrombocytopeniaat4109
/l.SerologyforHIV,hepatitis B virus, and hepatitis C virus was negative; furthermore, the patienthadbeenvaccinatedagainsthepatitisB.Alumbarpuncture showedturbidCSF,hypoglycorrhachialessthan0.1g/lwithnormal glycemia,anelevatedCSFproteinlevelat3g/l,and144elements/ mm3including90%neutrophils.DirectGram-stainingoftheCSF showedGram-negativebacilli.ACTofthebrain,chest,abdomen, andpelviswasnormal.
Antimicrobial therapywasinitiated withmeningeal dosesof amoxicillin,ceftriaxone,andacyclovir(probabilistic).Thepatient’s conditiondeterioratedrapidly,withgingivalbleeding and area-ctivemydriasis,followedbybraindeathonthedayofadmissionto thehospital.Post-mortemCSFculturesrevealedanE.coliproducer of low-level penicillinase with resistance to trimethoprim– sulfamethoxazole.Thesamebacteriumwasencounteredonblood cultureandurinalysis.
Discussion
A search of PubMed, ResearchGate, and GoogleScholar was performed, and data were collected for analysis. Keywords included Escherichia coli; coli bacillus; community-acquired meningitis; adults; and spontaneous. A total of 43 cases of spontaneous community-acquired E. coli meningitis reported between1946and2016wereidentified;inadditiontothetwo newcasesdescribedabove(Table1).
Eightarticleswereexcludedfromthis studyduetoalackof information onthetypeofmeningitis(nosocomialand/or post-traumatic versus spontaneous community-acquired), or the presence of exclusion criteria indicating hospital-acquired or post-traumaticmeningitis.Articlesconcerningchildrenwerealso excluded,asE.colimeningitisismorecommoninthispopulation. TheexcludedstudiesarelistedinTable2.
Datafromtheliteraturereviewcasesandthetwonewreported caseswerecombined(n=45).Themeanageofthesubjectswas56 years;thepatient’sagewasunknownin16%ofcases.Thefemaleto malesexratiowas1.4,showingaslightpredominanceoffemale cases(20femaleand14male);thesexwasunknownin24%of cases.
Table1
Reportedcasesofspontaneouscommunity-acquiredEscherichiacolimeningitisinaliteraturereview—1946to2016.
Year Reference Numberofcases
2016 IshidaK,etal.ClinCaseRep2016;4:323–6(Ishidaetal.,2016) 1 2015 KohlmannR,etal.BMCInfectDis2015;15:567(Ishidaetal.,2016) 1 2013 KangathRV,etal.BMJCaseRep2013;2013(KangathandMidturi,2013) 1 2013 PomarV,etal.BMCInfectDis2013;13:451(Pomaretal.,2013) 1 2012 WeyrichP,etal.AnnClinMicrobiolAntimicrob2012;11:4(Weyrichetal.,2012) 1 2009 CabellosC,etal.Medicine(Baltimore)2009;88:115–9(Cabellosetal.,2009) 6 2008 CabellosC,etal.ClinMicrobiolInfect2008;14:35–40(Cabellosetal.,2008) 5 2008 Briongos-FigueroLS,etal.RevClinEsp2008;208:262 1 2008 MileticD,etal.Orthopedics2008;31:182(Mileticetal.,2008) 1 2007 SamsonD,etal.AnnFrAnesthReanim2007;26:88–90(Samsonetal.,2007) 1 2007 AshishA,etal.CritCareShock2007;10:148–50(SuleandTai,2007) 1 2005 ChangKH,etal.JFormosMedAssoc2006;105:756–9(Changetal.,2006) 1 2005 YangTM,etal.JpnJInfectDis2005;58:168–70(Yangetal.,2005) 4 2004 VandeBeekD,etal.NEnglJMed2004;351:1849–59(vandeBeeketal.,2004) 4 2002 HovetteP,etal.PressMed2002;22:1021–3(Hovetteetal.,2002) 1 2000 MofredjA,etal.ScandJInfectDis2000;32:699–700(Mofredjetal.,2000) 1 1998 AlmiranteB.ClinInfectDis1998;27:176–80(Almiranteetal.,1998) 1 1986 SmallmanL,etal.JClinPathol1986;39:366–70(Smallmanetal.,1986) 2 1985 ChristopherGW,etal.ArchInternMed1985;145:1908(Christopher,1985) 1 1978 CraneLR,etal.Medicine(Baltimore)1978;57:197–209(CraneandLerner,1978) 4 1965 KuninC,etal.ArchInternMed1965;115:652–8(Kuninetal.,1965) 2 1965 ManesisJ,etal.ArchNeurol1965;13:214–6(ManesisandStanosheck,1965) 1 1946 CrawleyFE,etal.Lancet1946;247:461–2(Crawley,1946) 1
RiskfactorsarereportedinTable3.Inorderoffrequency,the riskfactorsidentifiedwerechronicalcoholismandcirrhosis(each accounting for 20% of cases),diabetes mellitus (16% of cases), disseminated strongyloidiasis (6% of cases), and HIV, chronic obstructive pulmonary disease,and chronic organinsufficiency (eachaccountingfor4%of cases).Hemochromatosis, myelodys-plasia,hemophagocyticlymphohistiocytosis,urinarytract instru-mentation,Blymphoma,long-termglucocorticoidtherapy,Marfan syndrome,andhumanT-lymphotropicvirustype1seropositivity werealsoreportedasriskfactors,eachrepresenting1%ofcasesin thisstudy.Riskfactorswereunknownfor11patients(24%),while 9%ofcaseswerepreviouslyhealthy.Concerningthetwonewly reportedcases,onedisplayedchronicalcoholismasariskfactor, butthesecondpatient,whowaspreviouslyhealthy,displayedno riskfactors.Finally,thecauseofinfectionwasunknownin40%of cases.Whenidentified,portals ofentrywerebacteremia(31%), urinary tract infection (24%), pneumonia (9%), septic arthritis
(includingonecaseofE.colispondylodiscitis)(4%),andprimary peritonitis(2%).
Microbiology,treatment, and outcomedata arepresentedin
Table4.Whenavailable,microbiologicaldatarevealedamajority of wild-type E. coli (20% of cases). E. coli was a producer of penicillinase in 9% of cases and was rarely quinolone- or trimethoprim–sulfamethoxazole-resistant (2% each). A notable andsignificantrateofE.coliproducingextended-spectrum beta-lactamases(ESBLs)wasencountered:7%ofcommunity-acquired cases.Bacterialsensitivitywasnotreportedfor60%ofcases.Oneof thenewlyreportedcasesexhibitedahighresistanceprofile,with an E. coli producing penicillinase and with resistance to trimethoprim–sulfamethoxazole. The other case displayed a wild-typeE.coli.
Table2
Escherichiacolimeningitiscasesexcludedfromthestudybecauseoftheirnosocomialorpost-traumaticcharacter,ortheabsenceofdetailsaboutthetypeofmeningitis.
Year Reference Numberofcases
2015 TeckieG,etal.IntJInfectDis2015;30:38–40(TeckieandKarstaedt,2015) 9 2014 OkikeIO,etal.ClinInfectDis2014;59:e150–7(Okikeetal.,2014) 353 2013 PomarV,etal.BMCInfectDis2013;13:451(Pomaretal.,2013) 15 2010 Laguna-DelEstalP,etal.RevNeurol2010;50:458–62(Laguna-delEstaletal.,2010) 3 2006 BouadmaL,etal.ClinMicrobiolInfect2006;12:287–90(Bouadmaetal.,2006) 23 2005 SeydiM,etal.MedMalInfect2005;35:344–8(Seydietal.,2005) 10 1997 PauwelsA,etal.JHepatol1997;27:830–4(Pauwelsetal.,1997) 9 1983 GilmoreRL,etal.SouthMedJ1983;76:1202–3(Gilmoreetal.,1983) 1
Table3
Riskfactorsandsuspectedcausesofspontaneouscommunity-acquiredEscherichia colimeningitis. N=45 n % Riskfactors Chronicalcoholism 9 20 Cirrhosis 9 20 Diabetesmellitus 7 16 Disseminatedstrongyloidiasis 3 7 COPD 2 4 HIV 2 4
Chronicorganinsufficiency 2 4
Hemochromatosis 1 2
Myelodysplasia 1 2
Hemophagocyticlymphohistiocytosis 1 2 Urinarytractinstrumentation 1 2
Blymphoma 1 2 Long-termcorticosteroids 1 2 HTLV1 1 2 Healthy 4 9 Othersa Unknown 11 24 Suspectedcause Bacteremia 13 30
Urinarytractinfection 10 23
Pneumonia 4 9
Peritonitis 1 2
Septicarthritis 1 2
Unknown 1 41
COPD,chronicobstructivepulmonarydisease;HTLV1,humanT-lymphotropicvirus type1.
a
Others: chronic organ failure (n=6), hemophagocytic lymphohistiocytosis (n=1),hemochromatosis(n=1),chronicobstructivepulmonary disease(n=1), myelodysplasia(n=1),humanT-lymphotropicvirus1(n=1).
Table4
Microbiologytreatment,andoutcomeofpatientsdiagnosedwithspontaneous community-acquiredEscherichiacolimeningitis.
N=45 n % Microbiology Wild-type 9 20 Penicillinase-producer 4 9 Fluoroquinolone-resistant 1 2 Trimethoprim–sulfamethoxazole-resistant 1 2 ESBL 3 7 Unknown 27 60 Treatment Ceftriaxone 10 22 Gentamicin 6 13 PenicillinG 4 9 Amoxicillin 4 9 Ampicillin 5 11 Chloramphenicol 2 4 Cefotaxime 2 4 Meropenem 3 7 Amikacin 1 2 Moxalactam 1 2 Ceftazidime 1 2 Cephalothin 1 2 Vancomycin 1 2 Ciprofloxacin 1 2 Sulfathiazole 1 2 Unknown 12 27 Durationoftreatment Days 15.81(1–21.25) Unknown 31 69 Outcome Death 21 47(25–100) Favorable 15 33 Unknown 9 20
ESBL,extended-spectrumbeta-lactamase.
Microbiology=resistanceprofileoftheE.colistrains,N=numberofthecases,and %=percentage;Treatment=antibioticsusedforthetreatment,N=numberofcases, %=percentage.
Concerningantimicrobialagents,themostwidelyuseddrugs were ceftriaxone (22%), gentamicin (13%), ampicillin (11%), penicillin G (9%), amoxicillin (9%), and meropenem (7%). Most coursesoftreatmentincludedeitherbeta-lactamsorpenicillins, and more rarely amikacin, moxalactam, sulfathiazole, and chloramphenicol. Treatment was not provided for 12 patients. Theaverage duration oftherapy was 15.81days (range1–21.25 days),butthisdurationwasunknownin68%ofcases.Bothofthe newlyreportedcasesreceivedmeningealdosesofcephalosporin, foracourseof21daysinthecaseofthefirstpatient.
Withregardtotheoutcome,themortalityratewashighat47% (range25–100%);thisincludedonedeathfromstatusepilepticus andDIConday1afteradmission.Thisrateissimilartotherates reportedinpreviousstudies,inwhichmortalityhasrangedfrom 50% to 90%, reaching 86% when associated with disseminated strongyloidiasis,or100%incirrhoticpatients(BerkandMcCabe, 1980;Luetal.,1998;Cherubinetal.,1981;Kohlmannetal.,2015). Thehypothesisthatconcomitantbacteremiaoracoma may worsentheprognosisisstrengthenedbythecaseofthesecond patient reported here, who died after being admitted withan initialcoma.Thisstudyfocusedonabinaryoutcome(deathor survival), but neurological sequelae should also be taken into consideration. Such sequelae occur in 30% to 50% of cases (Kohlmannetal.,2015).Thisissupportedbythefirstofthetwo new cases reported here; the patient manifested persistent slight anosognosia at 2 months after the endof antimicrobial therapy.
Thisstudyhassomelimitations.Thefirstregardstheimportant lackofdataintheliterature,withdatamissingin16%to63%of cases.AssummarizedinTable2,423caseswereexcludedduetoa lack of preciseinformation. The conclusions of this revieware drawnfromasmallsampleofcases;thus,alargergroupofpatients wouldberequiredtoconfirmtheresults.Finally,somecaseswere reportedaslongagoas1946,whenmicrobiologicalidentification andantimicrobialsensitivitytestingwerenotasreliableasthey arenow, whichmayhaveintroducedpotentialerrors.Thesame concernis raisedregarding theantimicrobialagents, for which recommendations havechanged. For instance, chloramphenicol and sulfathiazole are no longer recommended as first-line treatmentforE.colimeningitis.
Inconclusion,spontaneouscommunity-acquiredE.coli menin-gitisinadults,althoughdescribedasarareentity,islikelytobe underestimatedandnotasinfrequentasreportedinmostarticles. Newunderlyingconditionshavebeendescribedasriskfactors,in additiontochronicalcoholism, cirrhosis,diabetes mellitus,HIV seropositive status, chronicobstructive pulmonary disease,and chronicorganinsufficiency.Theseinclude urinaryanddigestive tractdisorders,amongthemMarfansyndrome,largemeningocele incontactwiththebowels,disseminatedstrongyloidiasis,urinary tractinfection,andpyelonephritis.Althoughthemajorityofcases werecaused bywild-typeE.coli, theemergenceof statistically relevantcommunity-acquiredESBL-producingE.colimeningitisis concerning.Finally,theprognosisisdeterminedbythediagnosis and the timeliness of antimicrobial drug administration. The presence of coma,bacteremia, or disseminatedstrongyloidiasis worsenstheprognosis.
Prospectivestudieswithlargecohortsandproperlycollected demographic,clinical,microbiological,and therapeutic informa-tionarerequiredtoconfirmtheseresults.
Funding None.
Conflictofinterest None.
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