ORI GI NALPAPER 81 Ultrasound Obstet Gynecol 2002; 19 : 8187 Blackwell Science Ltd Prospective sonographic assessment of uterine artery embolization for the treatment of fibroids F. TRANQUART*, L. BRUNEREAU, J.-P. COTTIER, H. MARRET, S. GALLAS, J.-L. LEBRUN, G. BODY D. HERBRETEAU and L. POURCELOT* * Service de Mdecine Nuclaire et Ultrasons, Service de Radiologie Adultes, Service de Neuroradiologie and Service de Gyncologie-obsttrique, CHU Bretonneau, Tours, France KEYWORDS : Doppler ultrasound, Embolization, Fibroid, Sonography, Uterine arteries ABSTRACT Objectives To evaluate sonographic features following uterineartery embolization and to assess using ultrasound the efficacyof embolization as the primary treatment of fibroids. Design Fifty-eight women (mean age, 44.5 years; range, 3365 years)sufferingfromsymptomsduetofibroids(meno-metrorrhagia,bulk-relatedsymptoms,pelvicpain)werefollowed-up after uterine artery embolization by ultrasoundexamination at 3 months, 6 months, 1 year and 2 years withassessment of volume and vascularization of fibroids as wellas uterine vascularization. Results Fifty-eight patients were examined at 3 months, 46at 6 months, 36 at 1 year and 19 at 2 years. Most patients wereimproved or free of symptoms at 3 months (90%), 6 months(92%) and 1 year (87%) and all monitored patients were freeof symptoms at 2 years. Clinical failure of treatment occurredin only two cases (3%). Progressive significant reduction infibroid size with reference to the baseline was demonstratedduring follow-up from 3 months (29%) to 24 months (86%).Absenceofintrafibroidvesselswasobservedinallexceptthree cases as early as 3 months, whereas perifibroid vesselspersisted in 21 cases. No changes in uterine vascularizationor uterine artery resistance were noted. Conclusions Uterinearteryembolizationisavaluableendovascular method for the treatment of fibroids, resultinginmarkedreductioninfibroidsizeanddisappearanceofintrafibroid vessels without reduction in uterine vasculariza-tion which is well depicted by sonography. I NTRODUCTI ON Fibroidsarethemostfrequenttumorsofthefemalegenitaltract,occurringin2060%ofwomenagedover40 years 1 . Many factors are involved in the developmentofsuchfibroids.Non-acuteabnormalbleeding,pelvicpain, sensation of a mass or pressure, frequency of urinationanddiscomfortarethemajorcomplaintsmentionedbypatients. Medical treatment based on hormone therapy isusuallyprescribedfirsttoreduceoreliminaterelatedsymptoms.Surgicaltreatment 2 suchasmyomectomyorhysterectomyissubsequentlyproposedforcaseswithpersistentsymptoms,accordingtothedesireforandpossibilityofuterinepreservation.However,hysterec-tomy is a more radical surgical procedure than is myomec-tomyanditisrefusedbysomepatients.Thehighrateofrecurrenceofsymptoms(1525%ofcases)followingmyomectomylimitsitsuse 3,4 .Thisemphasizestheneedforanalternativemethodprovidingdefinitivetreatmentwithout adverse effects. Arterial embolization 310 daysbefore myomectomy was first proposed in the 1990s 5 . In1995 Ravina et al . 6 proposed embolization of uterine arteriesasasingletreatmentforsymptomaticuterinefibroids.Recentreports 710 haveconfirmedthesafetyofthisapproachwhichissuccessfulforabnormalbleeding,bulk-related symptoms and pelvic pain related to fibroids. How-ever, the follow-up in these series was frequently limitedtoclinicalassessmentandwasrelativelyshort(26 months) 7,8,1113 for assessing the long-term effectiveness ofthis treatment.Sonographyiswidelyusedforthediagnosisoffibroids.Gray-scaleimagingallowscorrectassessmentofthenumber, volume and location of fibroids as well as study ofvascularization, which could guide therapy 1416 . Its non-invasiveness, relatively low cost, and repeatability, which arethe main advantages of this method, are valuable in the follow-up of fibroids following embolization.Thepurposeofthisstudywastoevaluateusingsono-graphic methods, the impact of uterine artery emboliza-tion on fibroid size and vascularization as well as uterinevascularizationoveraperiodof324 monthsfollowingembolization. Correspondence: Dr F. Tranquart, INSERM U316, CHU Bretonneau, 37044 Tours Cdex 1, France (e-mail: tranquart@med.univ-tours.fr) Accepted 26-6-01 UOG_535.fmPage 81Friday, December 28, 20018:31 AM Uterine fibroid embolization efficacy Tranquart et al. 82 Ultrasound in Obstetrics and Gynecology PATI ENTSANDMETHODS We used gray-scale ultrasound imaging, power Doppler andspectral analysis in a prospective study of adult women withameanageof 44.5 (range,3365) years referred from thebeginningof1997forfibroidembolization.Embolizationwas proposed as an alternative to surgery in all women withoneormoreuterinefibroidsresponsibleforsymptomsjudged sufficiently severe by an experienced gynecologist towarrant intervention, or for fibroids considered to be resist-anttomedicaltreatment.Fifty-eightpatientswithwell-defined fibroids were referred consecutively. The distributionofsymptomswasasfollows:abnormalbleeding( n = 29),bulk-related symptoms ( n = 11), pelvic pain ( n = 5), abnormalbleedingwithbulk-relatedsymptoms( n = 8),abnormalbleedingwithpelvicpain( n = 2),bulk-relatedsymptomswith pelvic pain ( n = 2), and abnormal bleeding with bulk-related symptoms and pelvic pain ( n = 1). Moreover, abnormalbleedingwasresponsibleforanemiain10patientswithhemoglobin levels between 4.0 and 11.5 g/dL.All patients gave informed consent according to local eth-ics committee recommendations. Fifty-five patients preferredembolization to surgery in order to maintain pelvic integrityor because of fear of a surgical procedure. Embolization waspreferredbythreepatientsbecauseofpotentialoperativerisks(onewithpriorthromboembolicdiseaseandtwopatients with severe obesity).ASequoia512ultrasoundscanner(Acuson,MountainView, CA, USA) with a 4V2 phased array probe (2.54 MHzwith harmonic imaging) and a EVC8 transvaginal probe (58 MHz) was used for gray-scale imaging and Doppler sono-graphy. Sonography of the uterus was performed by the sameexaminer. The same sonographic approach was used for allpatientsthroughoutfollow-up:suprapubicexaminationwas performed first with the 4V2 probe followed by trans-vaginalexamination.Inthecaseoflargefibroids,onlytheresultsfromthesuprapubicexaminationweretakenintoaccount.UterinevolumewasdeterminedbytheformulaL l e 0.523 where L, l and e are the dimensions of theuterus in the three orientations assuming the uterus to havean ellipsoid shape. The fibroid volume was determined by theformula 4/6 x y z , where x , y and z are the dimensionsof the fibroid determined on two orthogonal ultrasound views,respectively,assumingthefibroidtobeasphere.Fibroidvolumes were determined only for the four main fibroids incases with four or more fibroids. The percentage of reductionwas determined by subtracting the value on each follow-upfromthepre-embolizationvaluethendividingbythepre-embolization value and expressing the result as a percentage.Power Doppler imaging was performed with gain adjustedtoavoidcolornoise,thusallowingdetectionofthevesselsinside(intrafibroidvessels)andjustoutside(perifibroidvessels) the fibroid and those in the normal myometrium,andidentificationofuterinearteriesneartheirorigin.TheDoppler sample volume (3 mm) was then placed withoutangle correction on the detected vessel in order to recordblood flow signals from the various arteries detected. Thefrequency shifts were displayed as velocities assuming thattheinsonationanglewaszero.Peaksystolicvelocityandend-diastolic velocity were determined in intrafibroid andperifibroidvesselsanduterinearteriesbyaveragingthereadings from three consecutive waveforms for the calcu-lation of the resistance index (RI) according to the formuladefined by Pourcelot to assess changes in local blood flowresistance.Fibroids were required to be well documented by a sono-graphicexaminationofthegenitaltractperformedduringthe week before embolization. Endovascular treatment wasnot performed when surgery was justified for an associatedlesion (adnexal mass, uterine prolapse, stress incontinence)or for pediculated fibroids. The arteriography and emboliza-tion techniques used were as previously described 17 . Vascularaccess was obtained via the right common femoral artery andbilateral catheterization of the uterine arteries was achievedwith a single 4- or 5-F cobra catheter. Diagnostic injection wasperformed in each uterine artery using a 1024 1024 matrixADVANTX angiographic unit (General Electric, Milwaukee,WI,USA)todemonstratehypervascularizationoffibroids.Free-flowembolizationwasperformedusing150250 mpolyvinylalcoholparticlesandabsorbablegelatinsponge.Success of the procedure was assessed by the stagnation ofcontrastmediumintheuterinecapillarynetworkandtheabsence of uterine flow after contrast injection into hypo-gastricarteries.Twodaysafterthisprocedure,allpatientswere discharged home.Systematic follow-up after discharge from hospital includedclinical and sonographic examinations at 3 months, 6 months,1 yearand2 years.Thesamesonographicmethodswereapplied for each patient before embolization and on all follow-up examinations. Clinical evolution of symptoms was classi-fied as increased, unchanged, improved or free of symptoms,based on direct questioning.Resultswereexpressedasmean standarddeviationormedian (range) where appropriate. A Wilcoxon test was per-formedbetweeneachfollow-upandthebaselinereferencevalues to assess differences in sonographic data. A P -value of< 0.05 was considered significant. RESULTS Among the patients included, 58 patients were examined at3 months,46at6 months,36at1 yearand19at2 years(Table 1). Embolization was considered to be successful in 57Table 1 Reduction in uterine and fibroid volumes on follow-up examinations 3 months, 6 months, 1 year and 2 years after embolizationVolume reduction (% (range))Follow-upUterus (Baseline volume 305 (651403) cm3)Fibroid (Baseline volume 112 (10723) cm3)3 months (n = 58) 17 296 months (n = 46) 26 461 year (n = 36) 37 552 years (n = 19) 45 861 new fibroid (1 cm3) UOG_535.fmPage 82Friday, December 28, 20018:31 AM Ultrasound in Obstetrics and Gynecology 83 Uterine fibroid embolization efficacy Tranquart et al. patients at the end of the endovascular procedure. Embolizationwas performed only on the left side in the last patient becauseof dissection of the right external iliac artery.The mean uterus volume was 305 (range, 651403) cm 3 beforeembolizationandthemeanvolumeofthelargestfibroid was 112 (range, 10723) cm 3 (Table 1). In 18 of thesepatients the uterus contained two or more fibroids. Vascu-larization was detected within 32 fibroids (RI, 0.57 0.10)whereas peripheral surrounding vessels were observed for27fibroids(RI, 0.68 0.11)(Table 2andFigures1and2).Vascularization of the normal myometrium was consideredashomogeneousinallcases.TheRIoftheuterinearterieswas 0.75 0.11.At3 months(58patients)sixpatients(10%)remainedunchanged, 44 (76%) were improved and 8 (14%) werefreeofsymptoms(Table 3).Sonographicexaminationsdemonstrated a mean reduction in uterus volume of 17% andinthevolumeofthelargestfibroidof29%( P = 0.0001;Table 1).Thefibroidvolumeincreasedinonewoman(+42%) who was clinically unchanged. The same numberoffibroidsasthebaselinewasidentifiedbygray-scalesonographywithnochangesinechogenicity.Novesselsweredetectedwithinthefibroidsexceptinthreepatients(RI, 0.62) who remained symptomatic. In contrast, peripheralsurrounding vessels remained present in 21 cases (RI, 0.66 0.11). Vascularization of the normal myometrium remainedhomogeneousinallcases.TheRI from the uterine arteriesremained stable (RI, 0.68 0.12; Table 2).At 6 months (46 patients), there was increased bleeding intwowomennecessitatingahysterectomyinonecaseandarepeat embolization in the other, two patients (4%) remainedunchanged, 10 (22%) were improved and 32 (70%) were freeofsymptoms(Table 3).Sonographydemonstratedameanreduction in uterus volume of 26% and in volume of the larg-est fibroid of 46% ( P = 0.0001). Previously increased fibroidvolume increased further (+85%) with persistent symptoms(Table 1). No vessels were detected within the fibroids exceptin the same three cases as at 3 months (RI, 0.55;Figure 3). Twoof these patients were symptomatic. Peripheral surroundingvessels remained present in 20 cases (RI, 0.71 0.10). Myo-metrial vascularization remained unchanged in all cases. Theresistance index of the uterine arteries was 0.75 0.10 (Table 2).At 1 year (36 patients) two patients (5%) remained clini-callystableandthree(8%)wereimproved.Theother31patients (87%) were free of symptoms (Table 3). Sonographydemonstrated a mean reduction in uterus volume of 37%and in the volume of the largest fibroid of 55% ( P = 0.0001;Table 2 Results of follow-up examinations of intrafibroid and perifibroid arteries and uterine arteries 3 months, 6 months, 1 year and 2 years after embolizationFollow-upIntrafibroid vasc. (Baseline: 32 fibroids; RI = 0.57 0.10)Perifibroid vasc. (Baseline: 27 fibroids; RI = 0.68 0.11)Uterine arteries (Baseline: RI = 0.75 0.11)3 months (n = 58)Fibroids (n) 3 21RI 0.62 0.66 0.11 0.68 0.126 months (n = 46)Fibroids (n) 3 20RI 0.55 0.71 0.10 0.75 0.101 year (n = 36)Fibroids (n) 2 16RI 0.60 0.66 0.06 0.73 0.112 years (n = 19)Fibroids (n) 1 5RI 0.61 0.72 0.09 0.76 0.10The number of fibroids corresponds to the fibroids with detected intrafibroid or peripheral vessels. vasc, vascularization; RI, resistance index.Table 3 Clinical outcome at 3 months, 6 months, 1 year and 2 years after embolizationFollow-upIncreased (n)Stable (n)Improved (n)Free of symptoms (n)3 months (n = 58) 6 44 86 months (n = 46) 2 2 10 321 year (n = 36) 2 3 312 years (n = 19) 19Figure 1 Solitary fibroid in a 47-year-old patient with abnormal bleeding and anemia. Sonography showed a fibroid 30 cm3 in volume in the posterior part of the uterus. Power Doppler imaging allowed the detection of intrafibroid vessels and a marked low resistance surrounding the artery (arrow) with a high systolic velocity (0.70 m/s). UOG_535.fmPage 83Friday, December 28, 20018:31 AM Uterine fibroid embolization efficacy Tranquart et al. 84 Ultrasound in Obstetrics and Gynecology Table 1). Fibroid volume which was increased at both earlierfollow-upexaminationsfinallydecreased(35%)com-pared to the last examination according to the disappearanceof symptoms. Five fibroids had completely disappeared. Novessels were detected within the fibroids except in two cases(Figure 4) (RI, 0.60). Peripheral surrounding vessels remainedpresent in 16 cases (RI, 0.66 0.06). Myometrial vasculariza-tion was unchanged. The RI from uterine arteries was 0.73 0.11 (Table 2).At 2 years (19 patients) all 19 patients were free of symp-toms(100%)(Table 3).Sonographydemonstratedameanreduction in uterus volume of 45% and in volume of the largestfibroid of 86% ( P = 0.001). A new avascular fibroid, 1 cm 3 in volume was detected in one asymptomatic patient (Table 1andFigure 5).Somevesselspersistedwithinonefibroid(RI, 0.60), despite further embolization performed after thepreviousfollow-upduetopersistentsymptoms,increasedfibroidvolumeandintrafibroidvascularization.Peripheralsurroundingvesselswerepresentinfivecases(RI, 0.72 0.09). No objective changes in the normal myometrial vas-cularization were detected. The RI from the uterine arterieswas 0.76 0.10 (Table 2).Figure 2 Large uterine fibroid in a 50-year-old patient with bulk-related symptoms. Transverse suprapubic sonography of the uterus demonstrated a large fibroid 633 cm3 in volume (arrows) with marked intrafibroid vascularization before embolization (a). This allowed a spectral Doppler recording of a low resistance intrafibroid arterial flow (RI, 0.41) (b). One year later, sonography showed a 65% decrease in volume (220 cm3) of the fibroid (arrows) and absence of intrafibroid vessels on power Doppler imaging (c).Figure 3 Posterior fibroid (arrows) in a 50-year-old patient with abnormal bleeding and pelvic pain. Before embolization, transvaginal sonography showed a fibroid 8 cm3 in volume with low intrafibroid vascularization (a). Six months after embolization the volume of this fibroid had decreased (5 cm3) and no vessels were detected using power Doppler imaging (b). Twenty-four months after embolization, the volume had decreased further (3 cm3), there was a tendancy to an increase in echogenicity and no vessels were observed (c). Calipers 1 and 2 indicate a second fibroid. UOG_535.fmPage 84Friday, December 28, 20018:31 AM Ultrasound in Obstetrics and Gynecology 85 Uterine fibroid embolization efficacy Tranquart et al. DI SCUSSI ON Uterinefibroidsarebenign,well-definedtumorsofthemyometrium which often demonstrate higher arterial vascu-larization than does the normal adjacent myometrium. Theyare surrounded by peripheral arteries from which centripetalarteries reach the core of the lesion. Uterine arteries usuallyenlarge to supply these hypervascular networks 18 .Amongthevarioustherapeuticapproachesforfibroidssuch as medical treatment and surgery, the single cathetersingle femoral approach appears to be a safe and cost-effectivemethod to perform embolization of uterine arteries 79,12 .However, in view of the recent introduction of this method,careful documentation of the changes in size, appearance andvascularizationisneeded,requiringahighlyaccurateandrepeatable method to assess fibroid size 19 . The use of magneticresonance imaging, which is one of the methods available withperfect assessment of the size of the fibroids as well as other pelvicorgans, is limited by cost, especially when gadolinium contrastmaterial is used 20 . The other well-accepted method is sono-graphy, which, despite its limitation in terms of reproducibility,allows assessment of the size and echogenicity of the fibroidsas well as a real-time depiction of organ vascularization.Progressive reduction in both fibroid and uterus size wasdemonstrated by sonographic examinations in our systematicfollow-up. The mean reduction in uterus size remained limitedcompared to the reduction in fibroid size at every stage offollow-up, demonstrating that the major part of the embolicparticlesreachthe fibroid instead of the remaining normaluterus.Themeanreductioninfibroidsizeobservedinourseriesduringthefirst3 monthsfollowingembolization(29%) was less than that reported by Burn et al . 20 (43%) andbyReidyandBradley 21 (50%).Worthington-Kirsch et al . 8 reporteda46%decreaseinuterinevolume.Spies et al . 13 reporteda50%decreaseinfibroidvolumeat4.4 monthswhereas the reduction was 78% at 1 year but only in 14 ofthe52patientsincluded.Thedifferencesfromthepresentstudymightberelatedtotheuseofsmallparticles(150200 m) which induced ischemia followed by a progressivereduction in size rather than sudden and massive tumor necrosis.This is a progressive process leading to complete disappearance,particularly of small fibroids. The persistence of reduction involumeupto2 yearsaftertheprocedurehasnot,toourknowledge,beenreportedbefore.Ourstudydemonstratesthat an absence of vascularization precedes the decrease infibroid volume and thus is the first objective event with whichto assess the efficacy of this endovascular treatment. Duringthe follow-up in the present study, intrafibroid vascularizationwas only detected in fibroids with prior intrafibroid vessels.This reinforces the potential role of Doppler sonography forthe observation of lack of intrafibroid vascularization. Thiswas previously highlighted by Creighton et al . 22 in a similarfollow-upoffibroidsunderGnRhagonisttherapy.TheyFigure 4 This 43-year-old woman presented two fibroids: one submucosal vascularized fibroid (4 cm3) and a smaller one (1 cm3) located in the anterior part of uterus. Transvaginal ultrasound of the uterus performed 12 months after embolization demonstrated an absence of intrafibroid vessels in the largest fibroid (arrows) (a) with persistent intrafibroid vessels detected in the anterior fibroid (arrows) (b).Figure 5 Uterine embolization was performed in a 33-year-old patient for a solitary fibroid with bulk-related symptoms. Transvaginal sonography showed a residual intramural fibroid (calipers) 1 year after endovascular treatment (a). Two years after embolization, transvaginal sonography revealed a new fibroid (calipers) 1 cm3 in volume close to the initially described fibroid (b) which was reduced in size compared to in the first examination. UOG_535.fmPage 85Friday, December 28, 20018:31 AM Uterine fibroid embolization efficacy Tranquart et al. 86 Ultrasound in Obstetrics and Gynecology observed a marked reduction in fibroid volume with a non-linear relationship between initial size and response to treat-ment and a reduction in blood flow assessed by a decrease inpeak systolic velocity in fibroid arteries. The reproducibilityof Doppler sonography has to be further evaluated with morethan one examiner.Atleast90%ofourmonitoredpatientswereclinicallyimprovedorfreeofsymptomsat3 months,6 monthsand1 year after treatment, and all of them were free of symptomsat 2 years. No difference for persistent symptoms was observedin women who had fibroids with or without remaining vessels.In contrast to the study reported by Vashisht et al . 23 in whicha death was observed in one patient, we did not observe severeadverseeffectssuchasdeathorsepsisduringfollow-up.Improvement in symptoms after endovascular treatment hasalreadybeenreportedinmostpreviousseries 79,13,2427 .Reidy and Bradley 21 reported one case of amenorrhea relatedto ovarian failure caused by embolization. In our series, onepatienthadamenorrhea1yearaftertreatmentandonepatienthadamenorrhea2 yearsaftertreatment,butthissymptomwasclearlyrelatedtomenopauseinbothcases.Despite a partial technical failure related to single side em-bolization in one patient, this procedure was successful onthe basis of clinical and sonographic follow-up. Two cases ofembolization failure (3%) occurred. They were revealed byrecurrenceofabnormalbleeding6 monthsaftertreatmentand by persistent intrafibroid vessels on Doppler ultrasound,requiring surgical treatment (hysterectomy) in one case anda second embolization procedure in the other. This failure ratewas close to those reported in the largest earlier series: 4% forWorthington-Kirsch et al . 8 and 11% for Ravina et al . 27 .Theoccurrenceofnewfibroidswasdemonstratedbysonography in one patient after embolization. To our know-ledge,thishasnotpreviouslybeenreported.Thispatientremained free of symptoms for 2 years after the endovascularprocedure,andsonographicexaminationdemonstratedasignificant reduction in size of the largest fibroid (54% at1 year). The new fibroid measured only 1 cm 3 . This fibroid mighthave already been present but the evidence of this new lesion wasmore probably related to changes in myometrial echogenicity.In fact, the disappearance of intrafibroid vascularization asearly as 3 months after the endovascular procedure, withoutevident changes in uterine vascularization, demonstrates thatthedestinationoftheparticlesispreferentiallythefibroid.This is confirmed by the absence of changes in the RI of theuterine artery and maintenance of adequate uterine vascular-ization as demonstrated by unchanged myometrial vascular-ization.Thisisessentialtopreservereproductivefunctionandtosupportoneoftheadvantagesofthisendovascularmethod. The specific distribution is related to the differencein vascular networks between fibroids (terminal artery) andnormal myometrium (large capillary network). The changesin ovarian vascularization which were suspected on previousstudies 21,24 were not assessed in this series. 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