Disponibleenlignesur
ScienceDirect
www.sciencedirect.com
ORIGINAL ARTICLE
Comparing laparoscopic and percutaneous renal biopsy for diagnosing native kidney disease: A matched pair analysis
Comparaison entre la biopsie rénale transpéritonéale laparoscopique et la biopsie rénale percutanée guidée par l’imagerie : une étude cas-témoin
F. Aoun
a,∗, R. Mansour
a, C. Chalouhy
b, J.M. Ruck
b, S. Albisinni
c, S. Finianos
d, H. Azar
d, D. Chelala
d, C. Ghorra
e, T. Roumeguere
c, M. Moukarzel
aaServiced’urologie,Hôtel-DieudeFrance,universitéSaint-Joseph,Beyrouth,Lebanon
bDepartmentofSurgery,JohnsHopkinsSchoolofMedicine,Baltimore,MD,USA
cServiced’urologie,cliniquesuniversitairesdeBruxelles,hôpitalErasme,universitélibrede Bruxelles,Bruxelles,Belgium
dServicedenéphrologie,Hôtel-DieudeFrance,universitéSaint-Joseph,Beyrouth,Lebanon
eServiced’anatomopathologie,Hôtel-DieudeFrance,universitéSaint-Joseph,Beyrouth, Lebanon
Received17April2018;accepted29October2018 Availableonline19December2018
KEYWORDS Renalbiopsy;
Medicalrenal disease;
Laparoscopic approach
Summary
Background.—Percutaneousrenalbiopsyisawell-establisheddiagnosticprocedureinpatients withunderlyingmedicalrenaldisease.Aimofthisstudyistocomparetheadequacyofthebiopsy material,thediagnosticyield,andthecomplicationratesofthetrans-peritoneallaparoscopic approachandtheimage-guidedpercutaneousapproachtorenalbiopsyinthediagnosisofnative kidneydisease.
Methods.—Weperformedamatched-pairanalysismatching 1:340patients whounderwent trans-peritoneallaparoscopicrenalbiopsyto120patientswhounderwentpercutaneousrenal biopsy inthe same years. Patientswere retrospectively analyzed. Differences inadequacy ofbiopsymaterial(i.e.number ofglomeruli, continuous),diagnosticyield(categorical)and postoperativecomplicationsacrossthetwogroupswereassessedusingWilcoxonRanksumor 2test.
∗Correspondingauthorat:Serviced’urologie,institutJules-Bordet,1,rueHéger-Bordet,1000Bruxelles,Belgium.
E-mailaddress:[email protected](F.Aoun).
https://doi.org/10.1016/j.purol.2018.10.005
1166-7087/©2018ElsevierMassonSAS.Allrightsreserved.
Results.—Laparoscopic biopsy was associated with a highernumber of harbored glomeruli (median 50, IQR20—77) compared to the percutaneous approach (median 10, IQR 7—15), P<0.001.Adequate biopsiescontainingatleasttenglomeruliwere obtainedinasignifican- tly higherpercentage ofpatients in thelaparoscopic group versus the percutaneous group (92.5%vs.57.1%,P<0.001).Thelaparoscopicapproachwasalsoassociatedwithasignificantly higherdiagnosticyieldthanthepercutaneousapproach(82.5%vs.63.5%,P=0.027).Patients whounderwentlaparoscopicbiopsyhadnoperioperativeorpostoperativecomplications,resul- tinginasignificantlylowercomplicationratethanpercutaneousbiopsy(0%vs.4%,P<0.001), particularlyintheneedfortransfusionforpost-procedurebleeding(0%vs.1.8%,P<0.001).
Conclusions.—Inthisretrospectivematched-pairanalysiscomparingpatientsundergoingrenal biopsyfor medicalkidney disease,trans-peritoneallaparoscopic renalbiopsy wassafer and moreeffective for thediagnosis ofmedicalrenal diseasescomparedtopercutaneousrenal biopsy.Prospectivetrialswithagoodfollow-upareneededtodefinethebestcandidatefor eachapproach.
Levelofevidence.— 4.
©2018ElsevierMassonSAS.Allrightsreserved.
MOTSCLÉS Biopsierénale; Insuffisancerénale; Méthodedebiopsie
Résumé
Introduction.—Labiopsierénalepercutanéeestunetechniquebiendéfiniepourlediagnostic desmaladiesrénales.Lebutdecetteétudeestdecomparerl’abondancedumatérielbiopsique, lerendementdiagnostiqueetletauxdecomplicationsentrelabiopsierénaletranspéritonéale laparoscopiqueetlabiopsierénalepercutanéeguidéeparl’imagerie.
Méthodes.—Uneétuderétrospectivecas-témoinaportésur40patientsayantbénéficiéd’une biopsierénaletranspéritonéalelaparoscopiqueappariésà120patientsayantbénéficiéd’une biopsierénalepercutanéeguidéeparl’imagerie.Lesdifférencesentrelesdeuxgroupesportant surl’abondancedumatérielbiopsique,lerendementdiagnosticetletauxdecomplicationsont étéanalyséesenutilisantleWilcoxonRanksommeorletestde2.
Résultats.—La biopsie rénaletranspéritonéale laparoscopiqueest associéeàunplus grand nombredeglomérulestrouvésdansl’échantillon(médiane50,IQR20—77)comparéàl’approche percutanée(médiane10,IQR7—15),p<0,001.L’approchelaparoscopiqueapermisd’avoirun nombreplussignificatifdebiopsiescontenantaumoins10glomérulesparrapportàl’approche percutanée(92,5 %vs 57,1%, p<0,001).Lerendement diagnostique del’approche laparo- scopiqueétaitsignificativementsupérieuràceluiobtenuavecl’approchepercutanée(82,5% vs63,5%, p=0,027).Aucunecomplication périopératoiren’aétérencontréedanslegroupe laparoscopiquevs4%decomplicationdanslegroupepercutanée(p<0,001).
Conclusion.—Dans cette étuderétrospective cas-témoin comparantdeux techniques diffé- rentesdebiopsierénale,labiopsierénaletranspéritonéalelaparoscopiqueétaitassociéeàun matérielplusabondant etunrendement diagnosticplusélevéqu’une approchepercutanée guidéeparl’imagerie.Letauxdecomplicationétaitégalementmoindredanslegroupelaparo- scopique.Desétudesprospectivespourrontdéfinirlecandidatidéalpourchaqueapproche.
Niveaudepreuve.— 4.
©2018ElsevierMassonSAS.Tousdroitsr´eserv´es.
Introduction
Renal biopsy is a well-established diagnostic procedure in patients with underlying medical renal disease [1]. It is mainly indicated in unexplained renal failure, isolated glomerularhematuria, isolatednon-nephroticproteinuria, acutenephriticsyndrome,nephroticsyndrome,renaltrans- plant rejection or dysfunction and in some cases of connective tissue diseases [2]. To date, image-guided
percutaneous renalbiopsy remains thestandard approach in all patients without contraindications [3]. The proce- dureiswelltolerated underlocalanesthesiawithminimal post-proceduralmorbidity.Themostcommoncomplication followingpercutaneous renalbiopsy isbleeding,while the mostworrisomeisarteriovenousfistulaformation[4].Percu- taneousrenalbiopsytypicallyyieldsanadequatespecimen foraccurateinterpretationincontemporaryseries,andthe diagnostic yield is as high as 80% of cases [5]. However,
obtaining a specimen that is sub-optimal or inadequate canresultin delaysindiagnosis andtreatment, increased health-carecosts,andadditionalriskstothepatientdueto theneedforarepeatedbiopsyprocedure.
Absolute contraindications to renal biopsy include uncorrectable bleeding diathesis, chronic anticoagulation therapy,skininfectionatbiopsysite,uncooperativepatient, and uncontrollable severe hypertension [6]. Relativecon- traindications totheprocedure include morbid obesity or patients with anatomic abnormalities such as small kid- ney, solitary kidney, retro-renal colon, or high localized retroperitoneal kidneys.These patientsarebestmanaged bytrans-peritoneallaparoscopicapproachwithdirectvisu- alization of the biopsy site and good hemostatic control [7]. The laparoscopic approach can also be preferred in caseswheretheinitialbiopsybyimage-guidedpercutaneous approachwasinconclusive.
Authors from the John Hopkins Hospital were the first to report their experience with the trans-peritoneal laparoscopic renal biopsy. They demonstrated adequate tissue sampling in 96% of patients with a mean opera- tive time of 123min and a mean estimated blood loss of 67ml [8]. The laparoscopic technique was feasible but serious complications were encountered in initial cases using this approach. As their expertise increased, complication rates and operative duration decreased, as demonstratedrecently. Therefore,while thefeasibilityof the trans-peritoneal laparoscopic renal biopsy has been demonstrated,itsefficacyandsafetyhavenotbeendirectly comparedtothoseofthestandardpercutaneousapproach.
Wesoughttocomparetheadequacyofthebiopsymaterial, thediagnosticyield,andthecomplicationratesofthetrans- peritoneal laparoscopic approach and the image-guided percutaneousapproachtorenalbiopsy inthe diagnosisof nativekidneydisease.
Patients and methods Study population
After institutional review board approval, a retrospective chart review of all renal biopsies performed at our cen- terwas undertakenbetween January2000 and December 2013 (n=806). Age was determined at the time of the biopsy. We excluded patients younger than 16 years old (n=256),biopsiesofrenalmasses(n=41),andrenalbiopsies of transplanted grafts(n=82). We also excluded patients with incomplete data in their medical records (n=56).
Oursamplepopulationconsistedof371adultpatientswho underwentanativerenalbiopsyforamedicalkidneydisease duringthestudytimeperiod.
Renal biopsy procedure
Renal biopsies were performed percutaneously under CT scanguidancein331casesandlaparoscopicallyin40cases.
PercutaneousCT scan-guided biopsieswere performed by 3expert nephrologistsunderlocalanesthesiainall cases.
Written informedconsent,athorough history, acomplete blood countandacoagulationprofile wereobtainedfrom
allpatients.The CT scanwasperformed withthepatient proneandlandmarksweretaken.A16Goran18Gco-axial- needlewereusedtoobtainoneortwobiopsycoresfromthe lowerpolethatweresentimmediatelytothehistopathology department.We recommendedthat allpatients have bed restandobservation(i.e.pulseandbloodpressuremonitor- ing)overthefirst24hoursfollowingtheprocedure,andwe ensuredregularinquiriesaboutpainandhematuria.
Alltrans-peritoneallaparoscopicrenalbiopsieswereper- formed in the operating room under general anesthesia by a singleexpert operator with a large experience with laparoscopiclivingdonornephrectomy.Trocarinsertionand configurationweresimilartotrans-peritoneallaparoscopic nephrectomy. A surgical specimenwas obtained fromthe lower pole using cold scissors and the defect was closed by suturingthe edges of the wound witha multifilament absorbablesuture.Adrainwasinsertedfor24hoursfollow- ingtheprocedureandthenremoved.
Matching
Patientswitha trans-peritoneal laparoscopic renal biopsy werematched 1:3 with patients whounderwent percuta- neousrenalbiopsyinthesameyears.Patientsandcontrols were matched on year of procedure and biopsy indica- tion.Of note,patients andcontrols werenotmatched on outcome.Toconfirmtheappropriatenessofmatching,clin- icalandpathologiccharacteristicswerecomparedbetween patients and controls using the Wilcoxon Rank-sum test for continuous variables and the 2 test for categorical variables.Univariate logistic regression wasperformed to analyzetheassociation between the biopsyapproachand risk of complications. Complications were retrospectively collected based on the charts. We performed Wilcoxon Rank-sumor2 test,asappropriate,totestdifferencesin adequacyofbiopsymaterial(i.e.numberofglomeruli,con- tinuous)anddiagnosticyield(categorical).Aspecimenwas consideredadequateifitcontainedatleasttenglomerulifor lightmicroscopy.Thediagnosticyieldwasconsideredclini- callyrelevantiftheinformationobtainedfromthespecimen helpedthenephrologistsintheirdiagnosticwork-up.Statis- ticalsignificancewasconsideredforP<0.05.Analyseswere performedusingStataversion11(CollegeStation,Texas).
Results
Study population
Patientsundergoingbiopsyviathepercutaneousandlaparo- scopic approaches were of similar age, sex and body mass index (all P>0.05) (Tables 1 and 2). The indica- tions for renal biopsies in each group are summarized in Table 3. The indications for trans-peritoneal approach to renalbiopsyratherthanapercutaneousrenalbiopsywere:
obesity (n=4), patient intolerance of percutaneous pro- cedure (n=2), severe hypertension (n=3), chronic use of antiplateletoranticoagulation(n=5),coagulopathy(n=4), inconclusivepriorpercutaneousbiopsy(n=9)andunknown (n=13).
Table1 Patientcharacteristicsaftermatching.
Laparoscopictrans-peritonealkidneybiopsy Percutaneouskidneybiopsy P-value
Numberofpatients 40 120
Age 43±17 43±16 0.830
Sex(F/M) 16/24 161/170 0.319
BMI(mean±SD) 25.2±4 24.4±2.6 0.460
Table2 Theindicationsforrenalbiopsiesineachgroup.
Reasonforbiopsy Laparoscopictrans-peritonealkidneybiopsy Percutaneouskidneybiopsy
Isolatednon-nephroticproteinuria 10 24
Connectivetissuediseases 2 7
Nephroticsyndrome 12 38
Acutenephriticsyndrome 3 10
Isolatedglomerularhematuria 5 16
Unexplainedrenalfailure 8 25
Table3 Theindicationstotrans-peritonealapproachto renalbiopsy.
Reason Numberofpatients
Obesity 4
Uncooperativepatient 2
Severehypertension 3
Chronicuseof antiplatelet
3 Chronicuseof
anticoagulation
2
Coagulopathy 4
Inconclusiveprior percutaneousbiopsy
9
Unknown 13
Biopsy results
Laparoscopicbiopsywasassociatedwithahighernumberof harboredglomeruli(median50,IQR20—77)comparedtothe percutaneous approach(median 10, IQR 7—15),P<0.001.
Adequate biopsies containing at least ten glomeruliwere obtained in a significantly higher percentage of patients in the laparoscopic group versus the percutaneous group (92.5% vs. 57.1%, P<0.001). The laparoscopic approach was also associated with a significantly higher diagnostic
yield than the percutaneous approach (82.5% vs. 63.5%, P=0.027).Patientswhounderwentlaparoscopicbiopsyhad noperioperative orpostoperative complications,resulting in a significantly lower complication rate than percuta- neousbiopsy(0%vs.4%,P<0.001),particularlyintheneed for transfusion for post-procedure bleeding (0% vs. 1.8%, P<0.001). One patient in the percutaneous group devel- opedanarteriovenousfistula,whichwaswell-managedwith embolization.Nopatientsinthelaparoscopicgroupdevel- opeda fistula.Nocasesof deathwererecorded ineither group(Table4).
Discussion
Inthissingle-centerretrospectivematchedpairanalysisof percutaneousversuslaparoscopicrenalbiopsyapproaches, we found that trans-peritoneal laparoscopic renal biopsy hada significantlyhigher frequencyof adequate sampling anddiagnosticyieldandasignificantlylowerfrequency of complications,includingpost-procedurebleeding. Anade- quate sample of glomeruli (≥10 glomeruli) was obtained in nearlyall patients whounderwentlaparoscopic biopsy, versusonlyabout halfofthosepatientsundergoingpercu- taneousbiopsy(92.5%vs.57.1%,P<0.001).Insummary,we foundthatlaparoscopicrenalbiopsyisasafeandeffective methodof obtainingrenal tissue,withsuperior diagnostic yield and lower rates of complications than the standard
Table4 Comparisonbetweenthetwoapproaches.
Laparoscopic
transperitonealbiopsy
Percutaneous renalbiopsy
P-value Mediannumberofharboredglomeruli(IQR) 50(20—77) 10(7—15) <0.001 Adequatebiopsiescontainingatleasttenglomeruli 92.5% 57.1% <0.001
Diagnosticyield 82.5% 63.5% 0.027
Perioperativecomplications 0% 4% <0.001
Needfortransfusionforpost-procedurebleeding 0% 1.8% <0.001
Arteriovenousfistula 0% 0.3% <0.019
percutaneousapproach.However,itisnoteworthytomen- tionthatpatientswhoreceivedthelaparoscopicapproach werecontraindicatedforpercutaneous renalbiopsyinour series. Consequently, laparoscopic approach can’t be the firstchoiceinallpatientsduetothemoreinvasivenature of the procedure, the fact that it is performed under general anesthesia and its cost. Our study demonstrated thatlaparoscopic approachis a safealternative topercu- taneous biopsy when uncorrectable contraindications are present.
The diagnosticyieldof 63.5%obtainedinpercutaneous biopsiesinthisseriesislowcomparedtowhatwasreported inrecentstudies,wherediagnosticyieldwasreportedtobe 69—100%[9,10].However,thosestudiesincludebiopsiesof renalmasses,whichlikelyincreaseddiagnosticyield.Addi- tionally,percutaneousbiopsiesinthisstudywereperformed usingan18-gaugeneedle,versusthemorecommonlyused 14-gaugeneedle.Theuseofthesmaller-boreneedleisstan- dardatourcenterandisintendedtodecreasecomplication rates.Despitetheuseofrisk-mitigatingstrategiesinpercu- taneousbiopsyatourcenter,wefoundthatthelaparoscopic approachstillhadsignificantlylowerratesofcomplications thanthepercutaneousbiopsyapproach.
Pneumoperitoneumduringandfollowinglaparoscopyhas been found to have renal side effects. This has primar- ilybeen demonstratedin animalmodels,where prolonged pneumoperitoneumresultedinincreasedapoptosisofrenal tubular cells [11] decreased renal blood flow, oliguria, andimpaired creatinineclearance[12—14];andincreased xanthine oxidase activity and decreased glutathione con- sistent with renal oxidative stress [15]. However, studies of the effect of pneumoperitoneum on renal function in humans, largely following laparoscopic renal transplanta- tion, have shown no significant detrimental effects [16].
Similarly,wedidnotobserveanyrenalsideeffectsofpneu- moperitoneum; no patients in our study who underwent laparoscopicrenalbiopsyhadanycomplications.
Weacknowledgeseverallimitationstoourstudy.Oneof thelimitationsis thesingle-centerretrospectivedesignof the study and the lack of long-term follow-up. However, weanticipatedthatpatientsundergoinglaparoscopicbiopsy wouldbeahigher-riskcohort,astheywerecontraindicated for percutaneous biopsy. Instead, we found that patients undergoing laparoscopic biopsy had fewer complications, including fewer of the most common (e.g. bleeding) and severecomplications(e.g.arteriovenousfistulaformation).
Additionally,mostcomplicationsofrenalbiopsywouldhave been evident during the follow-up time period available for analysis.Finally, the number of glomeruli required in asampletoconsideritanadequatebiopsydiffersbetween studies.Inthis study,we aprioriselected10glomerulias thedefinitionofanadequatesampleafterconsultationwith pathologists andnephrologistsat ourcenter.However,we recognizethatthenumberofglomerulirequiredfordiagno- sisvariesbydiseaseandthesample;oneglomeruluscould be sufficient to diagnose crescentic glomerulonephritis, whereas more than 20 glomeruli are required to diag- nose focal segmental glomerulonephritis. As a result, we
presentedboththefrequencyofadequateglomerularyield anddiagnosticyieldinthisstudy.
Conclusion
Inthisretrospectivematched-pairanalysis,trans-peritoneal laparoscopic renal biopsy was safer and more effective for the diagnosis of medical renal diseases compared to percutaneous renal biopsy. Prospective trials witha good follow-upareneededtodefinethebestcandidateforeach approach.
Disclosure of interest
Theauthorsdeclarethattheyhavenocompetinginterest.
References
[1]BandariJ,FullerTW,TurnercapitalI,UiURM,D’AgostinoLA.
Renalbiopsyfor medicalrenal disease:indicationsand con- traindications.CanJUrol2016;23(1):8121—6.
[2]BrachemiS,BolleeG.Renalbiopsypractice:whatisthegold standard?WorldJNephrol2014;3(4):287—94.
[3]UppotRN,HarisinghaniMG,GervaisDA.Imaging-guidedper- cutaneous renal biopsy: rationale and approach.AJR Am J Roentgenol2010;194(6):1443—9.
[4]MannoC,StrippoliGF,ArnesanoL,etal.Predictorsofbleeding complicationsinpercutaneousultrasound-guidedrenalbiopsy.
KidneyInt2004;66(4):1570—7.
[5]AugustoJF,LassalleV,FillatreP,etal.Safetyanddiagnostic yieldofrenalbiopsyintheintensivecareunit.IntensiveCare Med2012;38(11):1826—33.
[6]StilesKP,YuanCM,ChungEM,LyonRD,LaneJD,AbbottKC.
Renalbiopsyinhigh-riskpatientswithmedicaldiseasesofthe kidney.AmJKidneyDis2000;36(2):419—33.
[7]Gupta M, Haluck RS, Yang HC, Holman MJ, Ahsan N.
Laparoscopic-assisted renal biopsy: an alternative to open approach.AmJKidneyDis2000;36(3):636—9.
[8]Shetye KR, Kavoussi LR, Ramakumar S, Fugita OE, Jarrett TW.Laparoscopic renalbiopsy:a9-yearexperience.BJUInt 2003;91(9):817—20.
[9]GellertLL,MehraR,ChenY-B,etal.Thediagnosticaccuracyof percutaneousrenalneedlecorebiopsyanditspotentialimpact ontheclinicalmanagementofrenalcorticalneoplasms.Arch PatholLabMed2014;138(12):1673—9.
[10]MukhtarK,UmairS,MahmoodS.CTguidedpercutaneousrenal biopsyversusultrasoundguidedforobtainingadequatetissue.
JPakMedAssoc2012;62(9):880—2.
[11]TosunM,YucelM,KucukA,SezenS.P53relatedapoptosisin kidneysinCO2pneumoperitoneumratmodel:animmunohis- tochemicalstudy.MolBiolRep2014;41(10):6391—5.
[12]LondonET,HoHS,NeuhausAMC,WolfeBM,RudichSM,Perez RV. Effect ofintravascular volumeexpansion onrenal func- tion during prolonged CO(2) pneumoperitoneum. Ann Surg 2000;231(2):195—201.
[13]Kirsch A, Hensle T, Chang D, KaytonM, Olsson C,Sawczuk I. Renal effects of CO2 insufflation: oliguria and acute renaldysfunctioninaratpneumoperitoneummodel.Urology 1994;43(4):453—9.
[14]CisekLJ,GobetRM,PetersCA.Pneumoperitoneumproduces reversiblerenaldysfunctioninanimalswithnormalandchron- icallyreducedrenalfunction.JEndourol1998;12(2):95—100.
[15]KhouryW,SchreiberL,SzoldA,KlausnerJM,WienbroumAA.
Renal oxidativestress followingCO2 pneumoperitoneum-like conditions.SurgEndosc2009;23(4):776—82.
[16]Parikh BK, Shah VR, Modi PR, Butala BP, Parikh GP. Anaes- thesia for laparoscopic kidney transplantation: influence of Trendelenburgposition and CO2 pneumoperitoneum on car- diovascular,respiratoryand renalfunction.IndianJAnaesth 2013;57(3):253—8.
