Colonization of preservation solution in kidney transplantation: Clinical impact and risk of secondary acute graft pyelonephritis

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ORIGINAL ARTICLE

Colonization of preservation solution in kidney transplantation: Clinical impact and risk of secondary acute graft pyelonephritis

Colonisation des solutions de conservation en transplantation rénale : inﬂuence sur les pyélonéphrites aiguës secondaires du greffon

F. Encatassamy

^a^,∗

, A.-S. Valentin

^b

, J. Capsec

^c

, M. Buchler

^d^,^e

, F. Bruyère

^a^,^e

aDepartmentofUrology,UniversityHospitalofTours,LoireValley,2,boulevardTonnellé, 37044Tours,France

bDepartmentofBacteriology,UniversityHospitalofTours,LoireValley,avenuedela République,37170Chambray-lès-Tours,France

cDepartmentofMedicalInformation,EpidemiologyandHealthEconomics,University HospitalofTours,LoireValley,2,boulevardTonnellé,37044Tours,France

dDepartmentofNephrologyandClinicalImmunology,UniversityHospitalofTours,Loire Valley,2,boulevardTonnellé,37044Tours,France

eFranc¸ois-RabelaisUniversity,PRESCentreValdeLoire,37032Tourscedex1,France

Received21December2016;accepted31December2017 Availableonline1February2018

KEYWORDS

Preservativesolution;

Renal

transplantation;

Acutegraft pyelonephritis

Summary

Introduction.—Bacterialcolonizationofpreservativesolutions(PS)remainspoorlydescribed inrenaltransplantation.WeinvestigatedthebacterialcolonizationofthePSanditsinﬂuence ongraftpyelonephritiswithinoneyearfromtherenaltransplantation.

Patientsandmethods.—Wecultured2samplesofPSfrom424patientswhounderwentarenal transplantation.Thefollow-upperiodwasoneyear.Anacutegraftpyelonephritiswasdeﬁned asapositivebacteriologicalurineanalysis,withtemperaturehigherthan38.5^◦Corgraftpain.

Results.—Intotal,424samplesofPSweretestedand195werepositiveforcolonization(46%).

Forty-ﬁvepatientsdevelopedanacutegraftpyelonephritisduringthefollow-upperiod(10.6%), ofwhich,21(46.7%)showedacolonizationoftheirPS.Twenty-fourhadnocolonization(53.3%).

Thisdifferencewasnotsigniﬁcant(P=0.697).

∗Correspondingauthor.

E-mailaddress:ﬂorence.encatassamy@icloud.com(F.Encatassamy).

https://doi.org/10.1016/j.purol.2017.12.016

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Discussion.—OurdatasuggestthatthebacterialcolonizationofPSsamplesdoesnotseemto increasetheriskofacutegraftpyelonephritisinrenaltransplantrecipients.

Levelofevidence.——3.

MOTSCLÉS Liquidede conservation; Colonisation; Transplantation rénale; Pyélonéphrite; Infectiontransmise parledonneur

Résumé

Introduction.—Lacolonisationdesliquidesdeconservationdemeurepeuétudiéeentransplan- tationrénale.Nousavonsanalysélacolonisationbactériennedesliquidesdeconservationainsi quesoninﬂuencesurledéveloppementd’unepyélonéphritedugreffondansl’annéesuivant satransplantation.

Matérielsetméthodes.—Deux échantillons de liquide de conservation pour chacun des 424patientstransplantésrénauxparticipantsontétéenvoyésenbactériologiepouranalyse.

Pendantun anaprèsl’intervention, nousavonsrepérélespyélonéphrites développéeschez cespatients.Lapyélonéphritedugreffonétait déﬁnieparuneculturepositivedel’examen cytobactériologiquedesurinesdansuncontextedeﬁèvresupérieureà38,5^◦Cetunedouleur dugreffon.

Résultats.—Surles424échantillonstestés,195étaientcolonises(46%).Quarante-cinqpatients ontdéveloppéunepyélonéphritedugreffondurantlapériodedesuivi(10,6%);parmieux, 21avaientunliquidedeconservationinitialementcolonisé(46,7%)alorsque24présentaient des liquides de conservation deleur greffon stériles (53,3 %). Cettedifférence n’étaitpas signiﬁcative(p=0,697).

Conclusion.—Notreétudesuggèrequelacolonisationbactérienned’unliquidedeconservation n’estpaspourvoyeusedepyélonéphritesdugreffonaprèsunetransplantationrénale.

Niveaudepreuve.— 3.

Introduction

The prevalenceof infectionfollowingtransplantation may be explained by numerous risk factors, for example immunosuppressive therapies. During the last 30 years, hospitalization due to infection in the 2 years following transplantation,hasexceededthatofhospitalizationdueto acuterejection[1].Thisisexempliﬁedinrenaltransplanta- tion,inwhichnearlyhalfofthenumberofhospitalizations areduetoinfections[2,3],themajorityofwhichareurinary tractinfections(UTI)[4].

Fungalcolonization oftheconservativeliquidhasbeen observed insolid organtransplantation. Furthermore, the frequency of donor-derivedcandidiasis is estimated tobe 1/1000inrenaltransplantationandmaybecausedbyacolo- nizedpreservativesolution(PS)[4].Severalcaseshavebeen describedinmycology,buttheissueofbacterialcoloniza- tioninrenaltransplantationhaspoorlybeendiscussed.

Thepresentstudyaimedtodeterminetheimpactofthe bacterialcolonizationofpreservativesolution(PS)samples onthedevelopmentofagraftpyelonephritisinrenaltrans- plantation.

Material and methods

Allpatientswhounderwentrenaltransplantationinourcen- terbetweenJanuary2010andDecember2013wereeligible

forinclusioninthisstudy.Allthegraftscamefromcadav- ericdonors. Exclusion criterionwas alack of information concerningthepostoperativefollow-up.

Beforetransplantation,twosamplesof20mL(milliliters) ofPSwerecollectedbyanurologistandanalyzedforbac- terialorfungalcontamination.

Specimens were examined microscopically for the presence of bacterial or fungal agents. Each sample was cultured in a thioglycolate broth and on 2 blood agar plates that were incubated aerobically and anaer- obically, respectively, at 37.1^◦C for 5 days. Cultures were examined daily for the presence of bacterial or fungal colonies until specimens were examined microscopically for the presence of bacterial or fungal agents.

Intotal,0.1mLofsample wasculturedin abloodagar andchocolateagarthatwereincubatedaerobically,andon bloodagarplatesthatwereincubatedanaerobicallyat37^◦C for5days.

OnemLofsampleswasculturedontwoSabourauddex- troseagarwithchloramphenicol slantswereincubated at 37^◦Cand30^◦Cfor30days.

Cultureswereexamineddailyforthepresenceofbacte- rialorfungalcolonies.

Inparallel,5mLofsampleswasculturedononeaerobic andoneanaerobicbloodculturebottleswereseeded with 5mLofsampleseachandincubatedfor5daysintheBacTec FXSystem.

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Finally,1mLofsampleswasculturedonCandidaID2for 5daysat37^◦C.

Thedetectionlimitwas10CFU/mL,asstatedinthe2008 BiomedicineAgencyGuidelines[5].

Patients at low immunological risk received basilix- imabasan induction, aswell assteroids, cyclosporine or tacrolimus and mycophenolate mofetil. High-risk patients received intravenous anti-lymphocyte immunoglobulins, steroids, high-dose intravenous immunoglobulins, tacrolimusandmycophenolatemofetil.

All patients, with the exception of those with aller- gies, weregiven an antibioticprophylaxis withpeﬂoxacin andamoxicillin—clavulanicacidduringthetransplantation, followedby trimethoprim-sulfamethoxazole fromthe sec- ond day post-transplantation. If cytopenia or cholestasis occurred,thelatterwaschangedtopentamidine. Prophy- lacticantibiotic therapy was administered for a duration of 4 to6 months, or until thelymphocyte count reached aminimumthresholdof200/mm³.

TheLich-Gregoirureterovesicalanastomosiswasusedfor 408 patients (96.2%),9 patients had a pyeloureterostomy reconstruction(2.1%),1patientunderwentanuretero-colic anastomosisbecauseofhispastofenterocystoplastyand5 hadanothertypeohureterovesicalanastomosis(1.2%).One patientdidnot have aurinary anastomosisbecauseof an immediaterenalgraftfailure.

Ureteralstentingwasdoneto423recipients.Thestent wasremoved after a mean timeof 36.5 daysafter renal transplant.

Afollow-upperiodof12monthspostoperationwasper- formedforallpatients,consideringasurgicalsiteinfection withanimplant(ureteralstent)inplace[6].

VascularCT-scanormagnetic resonanceangiogram was systematicallyperformed at 3 months postoperation, and pyelonephritis was deﬁned as a positive urine analysis (bacteria≥10⁵CFU/mL),withfever≥38.5^◦Corgraftpain, occurring in the ﬁrst year after transplantation. Antibi- oticsensitivityofbacteriafoundinthepatients’urinewas comparedwiththatfoundinthepreviouslyextractedcon- servativeliquid.

QualitativedatawasanalyzedbyPearson’sChi-squared testand quantitativedataby Studenttest. Thenormality testwasnotperformedbecausealloftheconditionsofthe Studenttestwereveriﬁed.Associationofpyelonephritisto everyvariablewastestedbyamultivariatelogisticregres- sion.Statisticalanalyseswereperformed usingJMPv.10.0 software(SASInstituteInc,Cary,NC,USA).AP-value<0.05 wasconsideredsigniﬁcant.

Results

Fourhundredandtwentyfourpatientswereoperatedonfor transplantationbetweenJanuary2010andDecember2013 (Table1),andamongthe424conservativesolutionssentfor analysis,195(46%)werecolonized.Twohundredandtwenty ninesamples(54%)remainsterile(Fig.1).

One hundred and ﬁfty-eight (81%) positive PS samples weremonomicrobial,and37 (21.5%)weremultimicrobial.

Twohundred andﬁfty-onemicrobial agents were isolated fromthose195colonizedPS(Table2).

Table1 Baselinecharacteristics(n=424).

Transplantrecipientage(mean±SD)years 48.3±16.2 Sex

Female(%) 160(37.7%)

Male(%) 264(62.3%)

Causeofrenalfailure

Glomerulonephritis 95(22.4%)

Polycystickidneydisease 58(13.6%)

Diabetes 52(12.3%)

Vascular 38(8.9%)

Uropathy 25(5.9%)

Tubulo-interstitialnephritis 24(5.7%)

Unknown 102(24.1%)

Other 30(7.1%)

Historyofkidneytransplant

None 370(87.2%)

1 44(10.4%)

2 8(1.9%)

3 2(0.5%)

Donorage(mean±SD)years 50.0±25.0 Useofaperfusionmachine

Yes(%) 82(19.3%)

No(%) 342(80.7%)

Conservativesolution

Celsior 263(62.0%)

IGL1 52(12.3%)

Custodiol 46(10.8%)

Scot15 23(5.4%)

KPS1 5(1.2%)

Other 35(8.3%)

Coldischemiatime(mean±SD)hours 16.8±7.2 Warmischemiatime(mean±SD)minutes 58.5±27.3

Candida albicans were found on 5 colonized PS samples(2.6%);thesepatientswerepre-emptivelytreatedwith caspofungin,followedbyﬂuconazole.Noneofthemdevel- oped systemic candidiasis or mycotic aneurysm. Vascular CT-scan or MRA, systematically performed at 3 months in searchofamycoticaneurism,werestrictlynormal.

Pyelonephritiswasfoundin45patients(10.6%)inamean timeof136.8daysaftertransplantationduringthefollow- up. The bacterialurine culture is summarized in Table 3.

Among the 45 patients who developed graft pyelonephri- tisduringthe yearfollowing theirtransplantation, 21had colonizedconservativeliquid(46.7%).Oftheremaining379 patients,theconservativeliquidwascolonizedin174cases (45.9%).Thisdifferencewasnotsigniﬁcant(P=0.697).

Instead,resultsfromtheunivariateanalysishighlighted asriskfactors:femalegender andantibodyinductionwith an anti-lymphocyte serum (Table 4). Similarly, the results from the multivariate analysis (Table 5) showed that the risk of developing graft pyelonephritis was signiﬁcantly increasedforfemales(OR=2.557;P=0.0043)andforindi- viduals treated with anti-lymphocyte serum (OR=2.711;

P=0.0037).

Atotalof17differentbacterialspecieswereidentiﬁedon the21colonizedPSsamples.FivePSsamples(23.8%)were foundtobecolonizedbymultiplebacteria:Staphylococcus haemolyticus andStaphylococcus hominis; Staphylococcus hominis and Streptococcus mitis; Klebsiella pneumoniae,

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Figure1. Flowchartofourretrospectivestudydesign.

Table2 Microbialagentsisolatedfromthe208positivePS.

Organisms Numberofisolateson

colonizedPS (n=251)

Secondaryacutegraft pyelonephritis (n=28)

Nopyelonephritis (n=223)

Gram-negativebacilli (n%)

40(19.2%) 10(4.8%) 30(14.4%)

Escherichiacoli 16(7.7%) 4(1.9%) 12(5.8%)

Others 24(11.5%) 6(2.9%) 18(8.6%)

Gram-positivecocci (n%)

164(78.8%) 13(6.2%) 151(72.6%)

Coagulase-negative staphylococci

121(58.2%) 12(5.8%) 109(52.4%)

Staphylococcus aureus

9(4.3%) 0(0.0%) 9(4.3%)

Streptococcus 18(8.6%) 1(0.4%) 17(8.2%)

Others 16(7.7%) 0(0.0%) 16(7.7%)

Gram-positivebacilli (n%)

41(19,7%) 3(1.4%) 38(18.3%)

Yeasts(n%) 6(2.9%) 2(1.0%) 4(1.9%)

Candidaalbicans 5(2.4%) 2(1.0%) 3(1.4%)

Candidaglabrata 1(0.4%) 0(0.0%) 1(0.4%)

MultimicrobialPS(n%) 37(17.8%) 6(2.9%) 31(14.9%)

Table3 Bacteriaorfungifoundinurineanalysisofthe 45patientssufferingfromgraftpyelonephritis.

Strain Value(%)

Escherichiacoli 24(53.3%)

Enterococcusfaecalis 6(13.3%)

Klebsiellapneumoniae 5(11.1%)

Enterococcusfaecium 1(2.2%)

Proteusvulgaris 1(2.2%)

Enterobactercloacae 1(2.2%)

Salmonellatyphymurium 1(2.2%)

Candidaglabrata 1(2.2%)

Multiplestrains 5(11.1%)

ClostridiumjejuniandKlebsiellapneumoniae;Clostridium jejuniandEscherichiacoli;CandidaalbicansandKlebsiella pneumoniae.Only2patientshadthesamemicrobialagent intheirPSsample andintheirurinesample(4.4%).These 2 patients, for whom pyelonephritis was associated with E. coli infection, E. coli wasalso found tobe present in theirPSsample; however,antibiogram resultsshowedthe strainstobedifferent(Table6).

Discussion

Althoughbacterialcolonizationoftheconservativeliquidis acommon occurrence,the exact rateof colonization has yettobe published.In thisstudy we found the preserva- tivesolutionof195graftedpatientstobecolonizedduring transplantation(46%).Twohundredandﬁftyoneorganisms

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Table4 Riskfactorsofpyelonephritis(univariateanalysis).

Nopyelonephritis(n=379) Pyelonephritis(n=45) P

Sex 0.0011

Female 133(35.1%) 27(60.0%)

Male 246(64.9%) 18(40.0%)

Preservativesolution 0.9233

Colonized 174(45.9%) 21(46.7%)

Sterile 205(54.1%) 24(53.3%)

Graftonperfusionmachine 0.3591

Yes 71(18.7%) 11(24.4%)

No 308(81.3%) 34(75.6%)

Anti-lymphocyteserum 0.0010

Yes 163(43.0%) 31(68.9%)

No 216(57.0%) 14(31.1%)

Coldischemiameantime(minutes) 1017 966 0.3287

Warmischemiameantime(minutes) 56.3 55.6 0.7744

Table5 Risk factors of pyelonephritis (multivariate analysis).

Oddsratio(CI=95%) P-value Colonizedpreservation

ﬂuid

0.880(0.464—1.669) 0.6965 Femalesex 2.557(1.343—4.867) 0.0043 Anti-lymphocyteserum 2.711(1.384—5.313) 0.0037

Table6 Differences between the Escherichia coli strainsonthepreservationsolutionsandtheurines.

Antibiogramof thepreservation solution

Antibiogramof theurines PatientA

Quinolones

Nalidixicacid Sensitive Resistant Ciprofloxacin Sensitive Resistant Norfloxacin Sensitive Resistant Ofloxacin Sensitive Resistant PatientB

Bêta-lactam

Amoxicillin Sensitive Resistant Quinolones

Nalidixicacid Sensitive Resistant Ciprofloxacin Sensitive Resistant Norfloxacin Sensitive Resistant Ofloxacin Sensitive Resistant

wereisolatedfromthose195PS.Coagulase-negativestaphy- lococciwerethemostfrequentlyisolatedmicrobialagent, suggestingaskincontamination.

The use of a high-sensitivity culture method might increasetheprevalenceofPScontamination.Thehighpro- portionofskinmicroorganisms,suchasCoagulase-negative staphylococci found in the PS samples indicated that in the majority of the cases of positive PS cultures, the

contaminationoccurredduringtheinoculationprocessand was not due to infected PS; thus the patients were not treated.

SimilardatawerepreviouslyreportedbyBertrandetal.

Inhisstudy,Gram-positivecocciwerefoundon70%ofthe colonized PS, and 52% of them were coagulase-negative staphylococci[7].

Themost commoncauseofinfectionafterrenaltrans- plantationareUTIs[8]andpyelonephritisrateisestimated tobebetween12and20%[9].

The statistical analysis did not suggest a correlation betweentheconservativeliquidcolonizationandtheinci- dence of pyelonephritis during the postoperative year.

PatientsfoundtohaveGram-negativebacilliintheirpreser- vativeliquidweresystematicallytreatedwithceftriaxone, followed byan efﬁcientantibiotic selectedinresponseto bacterialsusceptibility.

PScontaminationwithcoliformagentsisassociatedwith severecomplications,fromthegraftinfectiontothebreak- down. The presence ofE.coli inboth conservative liquid and urine was found for 2 patients. However, the bacteria were determined to be of different strains. Those foundinthePSsamplesweremultisensitive,whereasthose found in the urine during pyelonephritis showed a resistance for quinolones (patients A and B) and amoxicillin (patient B). Resistance in these cases may be explained by several factors, such as routine antibiotic prophylaxis aftertransplantation(trimethoprim-sulfamethoxazole),the antibiotic used to manage the colonization of the conservative liquid (ceftriaxone), or by the presence of a communityderivedE.coliUTI,forwhichnowadays, resistance to quinolones varies from 3 to 25% [10]. It can be admitted that a pre-emptive antibiotherapy based on thePS colonization witha high-sensitivityculture method is associated with the emergence of resistances in this population.

Mycoticarteritisoraneurysmssecondarytofungalinfec- tion are rare but mostly caused by Candida albicans and severeconsequencesfromgraftremovaltodeathhavebeen described [11,12]. No patientcontracted an infectious or a vascular complicationdue to fungal colonization in our study.

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Theresultsfromthemultivariateanalysissuggestasig- niﬁcant increase in the risk of developing pyelonephritis forfemales andforpatients treatedwithanti-lymphocyte serum.Femalegenderisawell-knownriskfactoroflower UTIduetotheshortnessoftheurethra,andalsoappearsto beariskfactorforpyelonephritis,aspreviouslydescribed [13,14].

Anadditionalriskfactoridentiﬁedinourstudyispatient treatment withanti-lymphocyte serum. Induction therapy blocks T cell activation and antigen recognition at the time of transplantation, particularly in recipients at high immunologicriskofgraftrejection,sensitizedpatientsand inrecipientsfromanexpanded-criteriadonor.

It has been described that antibody induction with anti-lymphocyte serum was associated with significantly increased risks for infectious deaths during the first 6 monthsafterrenaltransplantation[15].Itisalsowellknown thatCMVinfectionis acommoncomplicationafterkidney transplantation associated with induction treatment with anti-lymphocyte globulin. A near-significant trend toward higher risk for acute graft pyelonephritis was found for cytomegalovirus infectionin Fiorante’smodel [16]. More- over, Kamath et al. [17] found a positive association between both events, suggesting that the cytokine-based responsetobacterialinfectionmaytriggerCMVreplication throughthegenerationofthenuclear transcriptionfactor kappaB(NF-␬B). It makessensethatinduction withanti- lymphocyte serum, and CMV infection may increase graft pyelonephritis.

Ourstudyconﬁrmsthatthereisnocorrelationbetween bacterial colonization of the conservative liquid and the occurrenceofgraftpyelonephritis.

However, this study may be subject to certain bias, including a potential under-estimation of the rate of pyelonephritis.We found pyelonephritis incidence rateat theendofthe1-yearfollow-upperiodtobe10%;lowerthan previouslypublishedrates[13].Thisreducedincidencerate could result from several factors. Moreover, post-surgery follow-upwascarriedoutforthemajorityofpatients,however,incaseofemergency,patientsmayhavepresentedat analternativehospitalduringthefollow-upperiod,sothe ﬁndingsofthisstudymaybelimitedastheyderivefroma single-center.Also,pyelonephritiswasdeterminedwhenthe patientpresented witha combination of fever, graft pain and positiveurinanalysis. However, it mayalsobe associ- atedwithanisolatedfever.Similarly,wedidnotincluded febrilepatientswithoutbacteriologicalproof,thusitispos- siblethat ourlow incidencerate,compared topreviously publisheddata,istheresultofunder-diagnosis.

ThehighpercentageofPScontaminatedbyagentsfrom skin ﬂora could be decreased with a standard culture method,butglobally, theadvances inmicrobial detection becamemoreandmoresensitiverecently[18,19],asinItaly [20],UnitedKingdom[18]orSpain[21].

Finally,itcouldbeinterestingtoaddastandardculture method in the protocol to remove the microbial agents which come from skin ﬂora, as they do not seem to be dangeroustothetransplant.

Further studies should include a greater number of patients, by screening recipients in other centers, add a standard culture method and enlargedpyelonephritis cri- teriatoincreasestatisticalpower.

Conclusion

Theresultsofourstudysuggestthatthereisnoconnection betweencontaminationofthesolutionforpreservingorgans andanacutegraftpyelonephritisoccurringduringthepost- transplantyear.

Althoughmostcontaminationwaswithagentsfromskin ﬂora,microorganismswithhighpotentialformorbiditylike Candidawerefound.Theresultsofhigh-sensivitybacteriol- ogycultureofthePSshouldbeinterpretedwithcaution.

Author’s contribution

F.Encatassamy: datacollection;dataanalysis;manuscript writing.

F.Bruyère:projectdevelopment;manuscriptediting.

M.Buchler:manuscriptediting.

A.S.Valentin:datacollection.

J.Capsec:dataanalysis.

Acknowledgements

Notapplicable.

Disclosure of interest

Theauthorsdeclarethattheyhavenocompetinginterest.

Asamedicalresearchinvolvinghumansubjects,thewell- beingof the individual research subjecttook precedence overallotherinterests,asdescribedbytheDeclarationof Helsinkiof1975.

Informedconsenthasbeencollectedfromeachpatient.

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