Fatal case of necrotizing fasciitis due to Myroides odoratus

CASE REPORTFatal case of necrotizing fasciitis due to Myroides odoratusN.F.Crum-Cianflone •R.W.Matson •G.Ballon-LandaReceived:9April 2014/Accepted:21April 2014/Published online:8May2014ÓSpringer-Verlag Berlin Heidelberg 2014Keywords Myroides ÁLife-threatening infection ÁNecrotizing fasciitis ÁSeptic shock ÁCirrhosisIntroductionSevere skin and soft tissue infections (SSTIs),including necrotizing forms,that are monomicrobial in nature are most commonly caused by a Staphylococcus and Streptococcus species [1].Among those with underlying conditions,including cirrhosis,Gram-negative bacteriasuch as Vibrio and Aeromonas species may occasionally cause necrotizing infections [2,3].Other organisms are less commonly implicated in severe SSTIs,but their rec-ognition is important,especially when these organisms are associated with unique antimicrobial susceptibilities and potentially fatal outcomes.Flavobacterium odaratum ,reclassified in 1996based on genotypic and phenotypic data as Myroides odoratus [4],was described nearly a century ago as an avirulent organ-ism of unclear human significance [5].Since then,there are few data on the potential pathogenicity of this organism [6].Furthermore,the risk factors and clinical course of infections caused by this organism are poorly character-ized.Given the unique characteristics of this organism,including its resistance to a large number of antibiotics,further clinical data on Myroides infections are important.We present a case of rapidly fatal necrotizing fasciitis due to M.odoratus and provide a review of the literature.While the pathogenicity of Myroides sp.has previously been debated,this case and our review clearly demonstrate this organism’s virulence especially in the setting of risk factors such as cirrhosis and open wounds.Case reportA 55-year-old Caucasian female presented with leg pain and was found to be in septic shock.She had been hospi-talized a month previously for bilateral lower extremity cellulitis and open wounds,treated initially with cefazolin and subsequently with vancomycin after a wound culture showed methicillin-resistant Staphylococcus aureus (MRSA).She had previously received piperacillin-tazo-bactam and levofloxacin for a sacral wound infection.Her past medical history included cirrhosis (Child-Pugh scoreThe content and views expressed in this publication is the sole responsibility of the authors.N.F.Crum-Cianflone (&)ÁR.W.Matson ÁG.Ballon-Landa Scripps Mercy Hospital,4077Fifth Ave,San Diego,CA 92103,USA e-mail:nancy32red@Infection (2014)42:931–935DOI 10.1007/s15010-014-0626-0B)due to chronic hepatitis C virus,morbid obesity,and lymphedema.On presentation,vital signs included a blood pressure of 58/26mmHg and a temperature of34.3°C via Foley catheter measurement.Examination revealed a confused patient with multiple left lower extremity open wounds on the calf area,the largest being694cm;the right lower extremity had multiple smaller ulcerative lesions.There were initially no purpuric lesions or boratory values included a white blood count of1,100cells/mm3 with48%neutrophils and10%band forms,hemoglobin 9.0g/dL,platelets19,000/mm3,creatinine0.7mg/dL,AST 98units/L,ALT39units/L,total bilirubin3.2mg/dL,INR 3.6,positive DIC panel,and arterial lactic acid level 6.2mmol/L.The patient was intubated,received vaso-pressors,and empiric broad-spectrum antibiotics with vancomycin1g intravenously every12h,piperacillin-ta-zobactam4.5g intravenously every8h,and levofloxacin 750mg intravenously daily.Within6h of initial presentation,purpuric discoloration of her left lower extremity occurred beginning at the large open wound site.Within18h,the purpuric rash extended up to the left thigh and bullous lesions appeared,with similarfindings subsequently appearing on the right leg (Fig.1).The wounds were noteworthy for a fruity odor. Antibiotics were expanded to imipenem/cilastatin500mg intravenously every12h,daptomycin500mg intrave-nously every48h,and clindamycin900mg intravenously every8h(adjusted for a rising creatinine to1.3mg/dL), and an emergent left above the knee amputation was performed.Within12h,the right lower extremity purpuric lesions progressed and a right above the knee amputation was performed.Pathologic examination from both surger-ies revealed necrotizing fasciitis.Gram stains of blood and wound specimens revealed Gram-negative bacilli without other organisms.All blood (two sets)and wound cultures(n=3,including from the deep fascia)grew only an oxidase positive,non-fermenting Gram-negative bacillus.Antibiotics were modified to imi-penem/cilastatin500mg intravenously every8h(renally dosed)and doxycycline100mg intravenously every12h awaitingfinal identification of the organism.Vasopressors as well as mechanical ventilation were continued.Acute kidney injury due to acute tubular necrosis from sepsis worsened,and continuous hemodialysis was initiated. Despite maximum medical care,extension of the necro-tizing infection occurred into perineum and sacral/lumbar areas.The patient’s family opted for comfort care and the patient expired\48h after admission.Blood and wound culture isolates were identified as M. odoratus using manual(rapid NF Plus System TM:[99.9% probability)and automated(Becton–Dickinson Phoenix TM automated microbiology system:99%confidence)micro-biological methods.No other organisms were identified.Antibiotic susceptibility testing of the Myroides sp.inthe blood and wound cultures using the BD Phoenix auto-mated microdilution system showed resistance to amika-cin(MIC[32l g/mL),gentamicin and tobramycin(MIC[8l g/mL),aztreonam(MIC[16l g/mL),ceftri-axone(MIC[32l g/mL),ciprofloxacin(MIC[2l g/mL),tetracycline(MIC[8l g/mL),trimethoprim-sulfa-methoxazole(TMP/SMX,MIC[2/38l g/mL),and van-comycin(MIC[16l g/mL).Isolates had intermediatesusceptibility to piperacillin-tazobactam(MIC=64/4l g/mL),cefepime(MIC=16l g/mL),and imipenem/cila-statin(MIC=4–8l g/mL),and was only fully susceptibleto meropenem(MIC=2l g/mL).Review of the literatureA PubMed search of the English literature using the searchterms‘‘Flavobacterium’’or‘‘Myroides’’and‘‘necrotizingfasciitis’’,‘‘cellulitis’’,or‘‘soft tissue infection’’was con-ducted.Cases of Flavobacterium sp.were then limited tothe species of odoratum.We also utilized references ofarticles to search for additional cases.One additional case of necrotizing fasciitis and septicshock due to F.odoratum was identified[7].This case alsooccurred in a person with underlying cirrhosis,with thepatient surviving after amputation of the affected leg and aprolonged course of antibiotics[7].Six additional cases ofnon-necrotizing skin and soft tissue infections(SSTIs) Fig.1Purpuric rash on the bilateral lower extremeties due necro-tizing fasciitis caused by Myroides odoratus932N.F.Crum-Cianflone et al.were identified(Table1)[8–13].All cases(n=8)had concurrent bacteremia,except one which involved a localized soft tissue infection after a child sustained a pig bite.A second case of SSTI after pig bite due to a Fla-vobacterium sp.was identified,but the species was unknown,hence this case was not included[14].Cases predominantly occurred in adults(mean age63, range49–72years),with the most common underlying condition being cirrhosis.All infections involved the lower extremities,except two that occurred at upper body sites after trauma to these specific areas.Six of the eight cases, including our case,had a wound present before the onset of infection.Antimicrobial treatment of the Myroides sp. infection was based on antibiotic susceptibility patterns of the isolate,and most commonly utilized ciprofloxacin, imipenem/cilastatin,TMP-SMX,piperacillin or piperacil-lin/tazobactam.Most commonly a single agent was ulti-mately utilized for treatment,with the mean duration of antibiotics of25days(range14–40).The outcome was favorable in all cases except the current case. DiscussionMyroides sp.,formerly F.odoratum,was discovered in 1923within the intestines of patients,but without known pathogenicity[5].Subsequently,the organism was descri-bed as a potential‘‘opportunist pathogen’’[6],and was occasionally cultured from open,albeit uninfected,wounds [6,15].Our case demonstrates the potential explosive pathogenicity of Myroides sp.The presence of specific factors such as open wounds,underlying liver disease,and prior exposure to broad-spectrum antibiotics altering the normal gut and skinflora may be important for Myroides sp.to cause rapidly invasive infections.In summary,this report updates the older notion that Myroides is a non-pathogenic species,and may serve as an important alert regarding a potential change in the pathogenicity of the organism.Myroides sp.should be considered with other Gram-negative bacilli,such as Vibrio vulnificus and Aeromonas hydrophila,as a potential cause of necrotizing fasciitis, among persons with liver disease[2,3].Similar to these pathogens,Myroides sp.resides in water[8,12,16].The mechanism by which our patient was exposed to contam-inated water is unknown,but may have occurred within home or healthcare settings.A Myroides sp.infection has also been reported after trauma and water exposure during recent tsunamis[17].After exposure to this water-associ-ated organism,our patient may have become bacteremic with Myroides sp.from her gastrointestinal tract with subsequent seeding of her leg,or the organism may haveTable1Skin and soft tissue infections due to Myroides sp.,formerly Flavobacterium odoratumReferences Organism Diagnosis Age/sex UnderlyingconditionAntibiotic/surgical treatment OutcomeHsueh[7] F.odoratum Necrotizing fasciitis(LLE),bacteremia,septic shock 71/F Cirrhosis Amputation(above the knee),ciprofloxacin forapproximately28daysSurvivedBachman[8] F.odoratum Cellulitis(BUE),bacteremia63/M COPD,steroiduse,skinbreakdown Imipenem/cilastatin910days,then TMP-SMX914days;Recurrence wastreated with piperacillin910days,then TMP-SMXfor30daysSurvivedGreen[9M.odoratus Cellulitis(RLE),bacteremia69/M Heart disease TMP-SMX914days SurvivedMotwani[10]M.odoratus Cellulitis(RLE),bacteremia,septic shock 62/M Diabetes,openwound/ulcerCiprofloxacin and TMP-SMX(unknown duration)SurvivedBachmeyer [11]M.odoratimimus Cellulitis(RLE),bacteremia49/M Cirrhosis,traumaticwoundsImipenem/cilastatin andciprofloxacin.Ciprofloxacincontinued for21daysSurvivedBenedetti[12]M.odoratimimus Amputation site infection(UE/chest),pneumonia,bacteremia,septic shock 72/M Trauma withwoundPiperacillin/tazobactam andteicoplanin.28day antibioticcourseSurvivedMaraki[13]M.odoratimimus Cellulitis,osteolytic lesions(RLE)13/M Pig bite Ciprofloxacin920days SurvivedCurrent case M.odoratus Necrotizing fasciitis(BLE),bacteremia,septic shock55/F Cirrhosis,wound Imipenem DiedBLE bilateral lower extremity,BUE bilateral upper extremity,COPD chronic obstructive pulmonary disease,F female,LLE left lower extremity, M male,RLE right lower extremity,UE upper extremityFatal case of necrotizing fasciitis933entered through the open leg wound leading to a systemic infection.Gram-negative pathogens(e.g.,Vibrio sp.) among cirrhotic patients have been described as rapidly progressive and associated with a high mortality[2]—our case suggests that Myroide s sp.may have a similar presentation.The diagnosis of Myroides sp.is by culture.A recent study found that PCR techniques did not accelerate the diagnosis of the causative pathogen compared with cultures for SSTI cases;hence,culture remains the diagnostic test of choice[18].Microbiologic characteristics of Myroides sp.include being Gram-negative,yellow-pigmented,non-motile,obligate aerobic rods that are halotolerant,oxidase positive,and non-fermenters.Further,the organism exhibits a classic fruity smell,which was readily detected in our case both from the open leg wound and after plating on MacConkey agar.This genus was formerly F.odora-tum,but was redefined in1996by genotypic and pheno-typic criteria as M.odoratus,with a second related species of Myroides odoratimimus,a name chosen to signify the small differences between the two species[4].Given the increasing use of molecular typing/automated identification techniques and the rising number of compromised patients, the emergence of this pathogen as a cause of invasive infections may be on the horizon.Myroides sp.may not be initially considered in the differential diagnosis of SSTIs or necrotizing infections. However,early recognition is important given the need for specific antibiotic susceptibility testing and this organism’s resistance to a wide range of antibiotics[6].Broth micro-dilution is the antibiotic susceptibility of choice as disk diffusion methods are generally unreliable[19,20]. Myroides sp.are typically resistant tofirst-and second-generation cephalosporins,aminopenicillins,ampicillin/ sulbactam,aztreonam,ertapenem,colistin and polymixin B,making antibiotic treatment options challenging.Some have reported susceptibility toflouroquinolones and TMP-SMX[9,10],but this is variable and our case’s isolates were resistant.Of note,fluoroquinolone resistance has increased in the past several years and is now present in almost all bacterial species[21],including in Myroides sp. We utilized a carbapenem for treatment,but resistance has been previously described to this antibiotic in other cases due to the production of chromosome-encoded metallo-b-lactamases in both M.odoratus(TUS-1)and M.odora-timimus(MUS-1)isolates that hydrolyze penicillins, cephalosporins,axtreonam,and carbapenems[22].A KPC-2carbapenem-hydrolizing enzyme has been described[23].In summary,Myroides sp.is an emerging pathogen that can cause severe,life-threatening SSTIs,especially among adults with liver disease and open wounds.Although pre-viously described as a relatively avirulent organism,the pathogenic nature of this bacterium is demonstrated by this case of rapidly fatal necrotizing fasciitis and septic shock. Recent antibiotic usage may be an important predisposing factor due to this organism’s intrinsic resistance to most antibiotics and the concurrent loss of normalflora may allow for its unimpeded growth.Myroides sp.should be considered with SSTIs and necrotizing infections unresponsive to traditional antibiotics,and antimicrobial therapy including a carbapenem andfluoroquinolone con-sidered while awaiting identification and susceptibility results.Conflict of interest The authors have nofinancial interest in this work.All authors contributed to the content of the manuscript and concurred with the decision to submit it for publication. 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