indications for UterineItely EmbolizationAJR:172, April 1999 989Pictorial EssayArterial Anatomy of the Female Genital Tract: Variationsand Relevance to Transcatheter Embolization of the UterusJean-Pierre Pelage12, Olivier Le Dref1, Philippe Soyer1, Denis Jacob3, Mourad KardaChe1, Henri Dahan1, Jean-Pierre Lassau2,Roland Rymer1T ranscatheter arterial embolizationis commonly performed in themanagement of intractable bleed-ing due to various causes, including obstetricand gynecologic disorders and pelvic trauma[I, 2]. Recently, arterial embolization of theuterine arteries as a preoperative adjunct or asan alternative to surgery has been used in treat-ing uterine leiomyoma [3]. The widespread ac-ceptance of this technique necessitates greaterknowledge of the arterial anatomy of the fe-male genital tract so that safer embolizationprocedures can be performed and untargettedembolization avoided. Angiographic studiesprovide a comprehensive assessment of theanatomy of the internal iliac artery, especiallyof its patterns of division and branches. In thispictorial essay, we report the main arterial van-ations in uterine vascularization.Material and MethodsThis pictorial essay is based on the retrospec-tive study of 197 patients who underwent uterineembolization between July 1994 and November1997. Although most vascular malformations andcervical malignancies have complex and abnormalvascularization, women with postpartum or Ii-broid-related bleeding are usually young and oth-erwise healthy. with normal arterial supply.Indications to perform embolotherapy were uter-me myoma (n = 133); postpartum (ii = 49), post-abortion (, = 5). and postoperative (n = 2)hemorrhage: and bleeding related to adenomyosis(a = 3), malformation (ii = 1 ), or cancer (n = 4)(Table I). Angiography of the contralateral inter-nal iliac artery and selective study of the anteriordivision were performed to find the origin of theuterine artery. Superselective catheterization of thecontralateral uterine artery was then performed us-ing a 5-French cobra catheter (Radifocus: Terumo.Tokyo, Japan) in 186 patients (95% ) and a hydro-philic polymer-coated 0.032-inch guidewire(Radifocus) in all 197 patients. Each injection ofnonionic contrast media consisted of 10-15 ml ofiohexol (Omnipaque 300; Nycomed, Paris,France). In six patients, a 3-French microcatheter(Tracker 18; Target Therapeutics, Fremont,CA) was needed to perform superselective cathe-terization. Selective study of the anterior stem ofthe ipsilateral internal iliac artery and superselec-tive study of the uterine artery was then performedusing the same catheter in all patients. Because ofethical considerations regarding the potential toxic-ity of iodinated contrast material and radiation ex-posure, the study of branches of the internal iliacartery and other anastomotic arteries was limited tothe procedure-relevant arteries in all patients.Angiographic and anatomic examinations wereperformed by two observers independently. Of the394 angiographic studies (two each for 197 pa-tients) that were available for review. 19 angio-grams (5% ) were excluded because they did notinclude the internal iliac artery. Thus. 375 angio-Received August 3, 1998; accepted after revision September 24, 1998.1 Department of Body andVascular Imaging, H#{244}pital Lariboisi#{232}re, AP-HP, 2 rue Ambroise Pare, 75475 Paris Cedex 10, France. Address correspondence to J.-P. Pelage.2 Institut dAnatomie des Saints-P#{232}res,45 rue des Saints-P#{232}res,75270 Paris Cedex 06, France.3 Department of Obstetrics and Gynecology, H#{227}pital Lariboisi#{232}re, 75475 Paris Cedex 10, France.AJR 1999;172:989-994 0361-803X/99/1724-989 American Roentgen Ray SocietyDownloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved Fig. 1.-Anatomic drawing shows lateral view of division offemale internal iliac artery into two main stems. Notethat uterine artery is branch of anterior division of internal iliac artery. Piriformis muscle (orange), sacrospinalligament (light green), and sacrotuberal ligament (dark green) are also portrayed.Fig. 4-41-year-old woman with uterine fibroids.Digital subtraction angiogram of left internal iliac ar-tery shows division into three stems. 1 = posteriorbranches, 2 = common trunk between internal puden-dal artery and inferior gluteal artery, 3 = genitourinarybranches. Arrow indicates uterine artery.Pelage et al.990 AJR:172, April 1999grams of the internal iliac artery were available forreview. During the review, special attention wasgiven to trunk formation and the sequence of mainbranches from the internal iliac artery. The origin,width, course, and branches of the uterine arterywere noted. Anastomoses were searched for. Ar-teries that mimicked the uterine artery and otherarteries selectively studied were analyzed.ResultsSuperselective catheterization of the uterineartery was successful in 97% of cases, includ-ing two different procedures in nine women. In10 cases of life-threatening hemorrhage, em-bolization of the anterior division of the inter-nal iliac artery was preferred to shorten theprocedure and reduce radiation exposure.Internal IliacArteryThe internal iliac artery terminated intotwo main stems, one anterior and one poste-rior, in 77% of cases (Figs. 1-3). Othermodes of division of the internal iliac arterywere three stems in 14%, four or more stemsin 3% , and one main stem in 4% of cases(Fig. 4). No systematization was possible in2% of cases. In all cases, the posterior trunkgave rise to the iliolumbar, the lateral sacral,and the superior gluteal arteries (Fig. 3). Thesuperior gluteal artery was invariably the ter-minal branch. The anterior division was notas well defined as the posterior stem: UsuallyFig. 2.-28-year-old woman with primary postpartumhemorrhage. Digital subtraction angiogram of right in-ternal iliac artery in left anterior oblique projection(contralateral oblique) shows division into two mainstems. Note anteriortrunk (arrow) and posterior trunk(arrowhead). 1= enlarged uterine artery, 2 = umbilicalartery, 3= vaginal artery, 4 = inferior gluteal artery, 5 =obturator artery, 6 = pudendal artery.three panietal branches (obturator, inferiorgluteal, and internal pudendal) and three vis-ceral vessels (vesical, uterovaginal, and mid-dle rectal) were identified (Figs. 1 and 2).Origin ofthe Uterine ArteryThe origin of the uterine artery was usuallynot visible on anteroposterior views. Contralat-end anterior oblique was the best projectionwhen the uterine artery arose from the anteriordivision ofthe internal iliac artery (Fig. 2). W henFig. 3.-39-year-old woman with uterine fibroids. Dig-ital subtraction angiogram of left internal iliac artery inright anterior oblique projection (contralateral ob-lique) shows division into two main stems. Note poste-nor branches: 1= iliolumbar artery, 2 = superior sacralartery, 3 = inferior sacral artery, 4 = superior gluteal ar-tery. Uterine artery is indicated by arrow.the uterine artery originated from one, three, orfour stems, ipsilateral anterior oblique was thebest projection (Fig. 5). The width of the uterineartery was subject to great variation: Evaluationwas based on successful catheterization and in-jection in free-flow in 191 patients (97% ) with a5-French cobra catheter (1 French = 0.33 mm).Thus, the width of the uterine artery was be-tween 2 and 5 mm. Vasospasm was noticed in 97arteries (26% ) (Fig. 6). Va.sodilators were notused to prevent or treat uterine artery spasm.Downloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved Fig. 5.-42-year-old woman with uterine fibroids. Digital subtraction angiograms of left internal iliac artery inright anterior oblique projection (contralateral) 300 oblique (A) and left anterior (homolateral) 30#{176} oblique (B). Or-igin of uterine artery (arrow, A and B) is well identified on homolateral oblique because of its upper origin.Fig. 6.-43-year-old woman with uterine fibroids treated Fig. 1.-40-year-old woman with uterine fibroids. Digitalwith gonadotropin-releasing hormone agonists. Digital subtraction angiogram of selective injection into left inter-subtraction angiogram of right internal iliac artery. nal iliac artery shows characteristic course of left uterineSpasm of right uterine artery (arrow) was observed be- artery panetal segment (1). arch part (2). and marginal orfore superselective catheterization was attempted. ascending segment(3). Cathetershould be carefully placedintodescending segment of uterine arteryfor embolization.Arterial Anatomy of the Female Genital TractAJR:172, April 1999 991Course ofthe Uterine ArteryW e identified the characteristic U-shapedcourse of the uterine artery 141, which consistsof a panietal or descending segment runningdownward and medially (Fig. 7). a transversalligament segment coursing medially, the uter-me arch part, and the marginal or ascendingsegment running along the side of the uterus[4] (Fig. 8). At the superior angle of the uterus,the artery penetrated into the broad ligamentand divided into its terminal branches-tubaland ovarian-creating anastomoses with theovarian artery branches [4, 5] (Figs. 9 and 10).Branches ofthe Uterine ArteryM ost branches of the uterine artery were iden-tified. The cervicovaginal artery (Fig. I 1) was vis-ible arising from the arch in 201 (53%) (left, 112;tight, 89) of 375 arteries. W hen the utetine arteryoriginated from the internal iliac artery, the ceM -covaginal branch was not seen because of itssmall size. Intramural branches arising along theside of the uterus (also called arcuate arteries)were observed in all cases (Fig. 8). The terminalbranches ofthe arcuate arteries were anastomosedwith those ofthe contralateral side (Fig. 12).Ovarian ArteryIdentification ofthe ovarian artery, which arisesanterolaterally from the abdominal aorta belowthe renal artery, was possible on aortography intwo patients when the catheter was positioned atthe level ofthe second lumbar vertebral body (Fig.13). The ovarian artery presentedth its charac-teristic sinuous course (Fig. 14). This artery anas-tomosed with the uterine artery (Figs. 9 and 10).Arteria!AnastomosesThree types of anastomoses were identified.Transversal anastomoses between right andFig. 8.-29-year-old woman with primary postpartumhemorrhage related to uterine atony. Digital subtractionangiogram of superselective injection into left uterine ar-tery shows ascending segment (1) and numerous intra-mural branches (2).Downloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved Fig. 9.-Anatomic drawing of normalvascularization of uterus and ad-nexa shows internal iliac artery (IIA);ovarian artery (0) originating fromabdominal aorta (not shown); uter-me artery (UA); uterus (U); intramu-ral branches (IM); bladder (B); andcervicovaginal artery (CV). A = anas-tomoses between uterine and ova-nan arteries.Fig. 10-37-year-old woman with uterine fibroids. Digitalsubtraction angiogram of superselective injection of 10ml ofiodinated-contrast material into left uterine artery beforeembolization shows anastomosis between tubal part of leftuterine artery (1) and uterine part of left ovarian artery (2).Fig. 11.-31-year-old woman with delayed post-partum bleeding. Digital subtraction angiogram ofsuperselective injection into left uterine arteryshows left cervicovaginal artery (1) arising fromarch part of uterine artery (2).Fig. 12.-35-year-old woman with uterine fibroids. Digital subtraction angiogram of superselective injection showsenlarged left uterine artery (1) and anastomosis (2) with right uterine artery (not shown).992 AJR:172, April 1999left uterine arteries (Figs. 1 2 and 15) were visi-ble in 19 patients (10%). Anastomoses be-tween the uterine and ovarian arteries (Fig. 10)were visible in 22 patients (11 % ) (left, six;right, nine; both sides, seven). A round liga-ment artery that was a branch of the proximalepigastric artery was an anastomosic supplierto a previously embolized uterine artery in onepatient(Fig. 16).Other Procedure-Relevant Pelvic VesselsThe vaginal artery arising from the anteriordivision of the internal iliac artery just belowthe uterine artery was identified in 186 cases(50% ) (left, 50; right, 32; both sides, 52) (Figs.I , 2, and SB). In I 8 patients (9% ), the vaginalartery arose from a common trunk formedwith the uterine artery. The vesical artery, anis-ing from the anterior division of the internal il-iac artery usually above the uterine artery, wasidentified in 345 (92%) of 375 cases. A com-mon trunk with the uterine artery was found inthree cases (1% ) (Fig. 17). It took a downwardmedial course to reach the lateral part of thebladder and gave off three terminal branches,which were easily identified when the bladderwas full (Fig. l7B).DiscussionSeveral methods of analysis of variations inthe arterial anatomy of the female genital tracthave been used in previous studies. To ourknowledge, until now, information gained fromdissections of cadavers or during surgical proce-dures has been the basis of the most comprehen-sive accounts in the literature [6). Angiographyhas been used occasionally to establish trunkformation of the internal iliac artery and identifythe origin of visceral and parietal branches [4].In our series, the relative frequencies of modesofdivision ofthe internal iliac artery were differ-ent from those previously reported in the litera-ture. The pattern most frequently encountered inour study was division into two main stems,which was found in 77% of all arteries, morethan the 60% that was previously reported [4].The internal iliac artery terminates at the upperlimit of the greater sciatic notch into two mainstems, one anterior and one posterior, in mostcases [4]. The posterior division must be pre-served during the embolization of the anteriorbranches of the internal iliac artery [2]. The ante-rior division of the internal iliac artery is subjectto numerous variations. During angiographic pro-cedures, identification of these anterior branches,especially the parietal ones, is facilitated if bonylandmarks are established and superselectivecatheterization performed. Right and left symme-try ofthe branching pattern ofthe internal iliac an-tery was observed in 91% of patients.The uterine artery arises from the anteriordivision of the internal iliac artery. W e describeDownloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved Arterial Anatomy of the Female Genital TractAJR:172, April 1999 993a simple and useful technique of identificationand catheterization using oblique incidence: Inpractical terms. if the internal iliac artery is di-vided into two main trunks, the best projectionto identify the origin of the uterine artery is thecontralateral anterior oblique with 20-30#{176}ofinclination. The width of the artery is subjectto great variation; enlargement is common inpregnant patients and those with leiomyoma[5]. In the midline, the terminal parts of arcu-ate branches of the uterine artery anastomosewith those of the contralateral side [5].The paired ovarian arteries arise from theanterolateral abdominal aorta below the renalarteries [7]. Although the uterine artery pro-vides the dominant blood flow to the uterus,the ovarian artery is frequently involved inpathologic hypervascularized processes [7].Each ovarian artery usually anastomoseswith the corresponding terminal branches ofthe uterine artery [5].The round ligament artery plays a minorrole in physiologic conditions [8]. Thisbranch, which arises either from the inferiorepigastric artery or from the external iliac ar-tery, may be responsible for persistent bleed-ing after hysterectomy.The vesical artery arises from the anteriordivision of the internal iliac artery, sometimesfrom a common trunk with the uterine artery,Fig. 13-27-year-old woman with primary postpar-tum hemorrhage. Aortogram obtained with 5-Frenchpigtail catheter located just below level of renal ar-teries shows enlarged ovarian arteries (arrows) sup-plying uterus.Fig. 14-28-year-old woman with numerous uterine fi-broids. Digital subtraction angiogram of superselectivecatheterization ofrightovarian artery providing uterine vas-culanzation to posterolateral intramural myoma (arrow)shows characteristic sinuous course of ovarian artery.Fig. 15-39-year-old woman with polymyomatous uterus. Gross specimen obtained af-ter hysterectomy. Red dye injection into left uterine artery (arrows) and blue dye injec-tion into right uterine artery (arrowhead). Anastomoses between both sides identifiedin myometrium.Fig. 16.-27-year-old woman with persistent bleeding after bilateral embolization of uterinearteriesfor primary postpartum hemorrhage. Digital subtraction angiogram of selective in-jection into left external iliac artery shows left round ligament artery(1) arising frominferiorepigastric artery (2) providing blood supplyto previously embolized left uterine artery (3).Downloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved use of a hydrophilic polymer-coated 0.032-inch(rather than 0.035-inch) guidewire can preventvasospasm of the uterine artery.In this study of pelvic angiograms, the bloodsupply ofthe uterus is discussed. Precise knowl-edge of the normal and variant anatomy of thefemale genital tract should be the basis for accu-rate interpretation of angiographic studies andsafe performance of embolization of the uterus.ReferencesAFig. 17.-41-year-old woman with uterine fibroids. Digital subtraction angiogram ofselective injection into right in-ternal iliac artery before embolization shows right vesical artery mimicking course of uterine artery.A, Selective injection into internal iliac artery shows common trunk of vesical artery (1) with uterine artery (2).B, Superselective catheterization of vesical artery shows characteristic terminal branches (arrowheads) allow-ing vesical and uterine arteries to be identified.as in three of our patients. It has three vesical fere with the safety of the procedure, even if thebranches that supply 80% of the blood flowto the bladder. Special care should be takenduring uterine embolotherapy to avoid blad-der necrosis, which has been reported afteruntargeued embolization [9].Identification of all branches of the internaliliac artery is necessary to avoid untargetted em-bolization [2, 9]. Anatomic variants may inter-high degree offlow to the uterus tends to protectagainst unexpected reflux of the embolic mate-rial. To perform safer embolization in free-flow,the catheter should be carefully placed into thedescending segment of the uterine artery. Simi-larly, failure of superselective catheterization ofthe uterine artery may lead to unilateral embo-lization and lack of therapeutic effect [3]. ThePelage et al.994 AJR:172, April 19991. Ring EJ. Athanasoulis C, W altman AC, M argoliesM N. Baum S. Arteriographic management ofhemorrhage following pelvic fracture. Radiology1973; 109:65-702. Greenwood LH, Glickman M G, Schwartz PE,M orse 55, Deny DE Obstetric and nonmalignantgynecologic bleeding: treatment with angiographicembolization. Radiology 1987:164:155-1593. Ravina JH, Herbreteau D, Ciraru-Vigneron N, etal. Arterial embolisation to treat myomata. LancetB 1995:346:671-6724. M erland JJ. Chiras J. Normal angiography. In:M erland JJ, Chiras J. eds. Arteriographv of thepelvis: diagnostic and therapeutic procedures.Berlin: Springer-Verlag, 1981:5-685. Farrer-Brown 0. Beilby JO, Tarbit M H. The bloodsupply to the uterus: arterial vasculature. J ObstetG ynaecol Br Corn.rnrnonw 1970;77:% 7-9756. Lipshutz B. A composite study of the hypoga.stricartery and its branches. Ann Surg 1918;67:584-6087. M arx M V, Picus D, W eyman PJ. Percutaneous em-bolization of the ovarian artery in the treatment ofpelvic hemorrhage. AiR 1988;150: 1337-13388. Chait A, M oltz A, Nelson JH. The collateral arte-nal circulation in the pelvis: an angiographicstudy. AiR 1968:102:392-4009. Braf ZF, Koontz W W . Gangrene of bladder: com-plication of hypogastric artery embolization.Urology 1977;9:670-671Downloaded from www.ajronline.org by 191.251.131.118 on 07/20/15 from IP address 191.251.131.118. Copyright ARRS. For personal use only; all rights reserved