Uterine Arteriovenous Malformations: Primary Treatment with Therapeutic Embolization 1 Robert L. Vogelzang, MD Albert A. Nemcek, Jr, MD Zeke Skrtic, MD Jan Gorrell, MD John R. Luraln, MD
Index terms: Arteries, therapeutic blockade,969.1299 • Arteriovenous malformations, pelvic, 969.14, 969.715 • Arteriovenous malformations, uterine, 969.14, 969.716 • Uterus, hemorrhage, 854.319, 969.716 JVIR 1991; 2:517-522
1 From the Departments of Diagnostic Radiology (RL.v., A.A.N., Z.S.) and Obstetrics and Gynecology (J.RL.), Northwestern University Medical School and Northwestern Memorial Hospital, 710 N Fairbanks Ct, Chicago, IL 60611, and the Department of Obstetrics and Gynecology, Michael Reese Hospital, Chicago (J.G.). From the 1991 SCVIR annual meeting. Received April 28, 1991; revision requested June 6; revision received June 24; accepted July 9. Address reprint requests to RL.V.
©
SCVIR, 1991
Uterine arteriovenous malformations are rare lesions that can cause massive vaginal bleeding and spontaneous abortions. The majority are either congenital or related to gestational trophoblastic disease. Hysterectomy has been the treatment of choice. The authors successfully treated four patients with symptomatic uterine arteriovenous malformations by means of transcatheter embolization; three of the lesions were related to gestational trophoblastic disease and one was congenital. All were supplied by the uterine arteries that were subselectively embolized with particulate material. This resulted in prompt cessation of uterine hemorrhage. There were no complications, and one pregnancy was achieved. The three other women have normal menstruation and no recurrence of bleeding at follow-up 10-48 months after treatment. On the basis of this experience and that of others, embolotherapy should be the treatment of first choice in these lesions, as it appears safe and effective. Additionally, uterine function is preserved in patients who are usually reproductively active. UTERINE arteriovenous malformations are a rare cause of massive uterine bleeding. These lesions, variably described as cirsoid aneurysm, arteriovenous malformation, racemose aneurysm, cavernous hemangioma, or arteriovenous aneurysm, can be acquired or congenital (1-11). The causes of acquired lesions include previous surgery on the uterus, endometrial adenocarcinoma, maternal diethylstilbestrol exposure, and trophoblastic disease (11-23). Recognition of this abnormality as the cause of hemorrhage is important since uterine instrumentation is clearly not indicated and may only worsen the condition. Hysterectomy has traditionally been the treatment of choice, but transcatheter embolization, first reported by Forssman et al in 1982 and described in a number of single case reports since then, appears to allow successful treatment while sparing uterine childbearing capacity (20,22,24-26). In this report we document our results in four patients with uterine arteriovenous
malformations treated with subselective transcatheter embolization and compare our results and techniques with those reported previously. To our knowledge, this is the largest such series to date.
PATIENTS AND METHODS Between January 1987 and July 1990, four patients with uterine arteriovenous malformations were seen and treated at Northwestern Memorial Hospital. Ages of these women ranged from 16 to 34 years (Table); all presented with recurrent episodes of heavy uterine bleeding ranging in duration from 3 weeks to 2 years. Transfusions were required in three. Three patients had gestational trophoblastic disease. After a term pregnancy, one woman had metastatic gestational choriocarcinoma, which was successfully treated with chemotherapy. Another was beginning chemotherapy for postmolar gestational trophoblastic tumor. In the third pa-
517
518 • Journal of Vascular and Interventional Radiology November 1991
Summary of Patient Data Age Obstetric Duration of AVM Arterial Supply Embolic (Embolized) Patient (y) History Hemorrhage Etiology Material 1 21 Gl, PI 8wk Gestational chorio- Bilateral uterine PYA arteries carcinoma
Duration of Follow-up (mo) 48
2
34 G4, Pl,A3
3wk
Invasive mole
Right uterine artery
PYA, Gelfoam
13
3
31 G2, PO,A2
5mo
Bilateral uterine PYA, Gelfoam arteries
10
4
16 G4,PO,A4
2y
Partial hydatidiform mole Congenital
Right uterine artery
14
PYA, Gelfoam
Results Normal menses, no bleeding, no pregnancy Normal menses, no bleeding, no pregnancy Normal menses, no bleeding, no pregnancy Resumed normal menses; pregnant at 8 months, but pregnancy was terminated by means of elective hysterectomy at 16 weeks
Note.-AVM = arteriovenous malformation, PYA = polyvinyl alcohol.
tient human chorionic gonadotropin levels spontaneously returned to normal following treatment of a partial hydatidiform mole 2 years earlier. In the fourth patient, a large congenital arteriovenous malformation had caused four spontaneous abortions and several episodes of massive vaginal bleeding over a 2-year period. Diagnostic testing prior to the procedure included hysteroscopy in two (patients 1 and 3), which demonstrated the arteriovenous malformation as a pulsatile fundal mass. Arteriography showed similar findings in all patients: a lesion consisting of dilated irregular vascular spaces supplied by a single enlarged uterine artery in two patients and by both uterine arteries in two others. Early and prominent venous filling was seen in the middle or late arterial phase in all patients. This finding was particularly well demonstrated on selective internal iliac or superselective uterine arterial injection (Figs 1, 2a, 3a, 3b). The uterine artery was always the sole arterial supply; no other pelvic feeding vessels were found in any case. Embolization of the involved uterine arteries was performed from the femoral (three cases) or axillary (one case) approach. Embolization was
Figure 1. Patient 1. Pelvic arteriogram demonstrates hypervascular mass (arrows) predominantly supplied by right uterine artery, although there is contribution from the left uterine vessel.
carried out first with polyvinyl alcohol particles 150-600 J.Lm in diameter followed by gelatin sponge pledgets (Gelfoam; Upjohn, Kalamazoo, Mich) to an endpoint of complete arterial occlusion. A completion internal iliac angiogram helped confirm obliteration of the mass (Figs 2b, 3c).
RESULTS Prompt and complete cessation of abnormal uterine bleeding occurred
within 24 hours in all patients. Clinical follow-up ranging between 10 and 48 months showed continued lack of bleeding and restoration of normal menses in all four patients. Patient 4 became pregnant 8 months after embolization. Ultrasound depicted placenta previa and, due to the patient's grave concerns about prior bleeding episodes, the pregnancy was terminated by elective hysterectomy at 16 weeks gestation. Pathologic examination of the uterus showed obliteration of the arteriovenous malforma-
Vogelzang et al • 519 Volume 2 Number 4
a.
b.
Figure 2. Patient 2. (a) Selective left uterine artery injection demonstrates uterine artery (curved arrow) supply of hypervascular fundal mass (*) with early venous drainage (straight arrow). (b) Pelvic arteriogram obtained after embolization.
tion; vascular enlargement consistent with a normal pregnancy was found. Additionally, placenta accreta was identified. None of the other three patients has become pregnant, although this was not specifically attempted. Patients tolerated the embolization well in all cases. Moderate uterine cramping and/or pelvic pain was noted in two patients the evening following the procedure, and a minimal postembolization fever of 100.3 0 F (38 C) was seen in one of these. There were no other complications. 0
DISCUSSION Arteriovenous malformations of the uterus are rare lesions. Since the first case in 1926 reported by Dubreuil and Loubat, a total of 54 cases have been documented (1-33). In this group, the malformation was acquired in 24 and congenital in 30. Of the acquired abnormalities, 14 were associated with gestational trophoblastic disease, six with previous surgery, three with maternal diethylstilbesterol exposure, and one with endometrial carcinoma. If, however,
one considers only those lesions that involved the uterus (and not the cervix) and if postsurgical fistulas between extrauterine vessels are excluded (14,23), congenital lesions outnumber acquired lesions (30 vs 19, respectively), and the majority (74%) of acquired cases were associated with gestational trophoblastic disease. Although they have been seen in older women (4,7), congenital malformations of the uterus are usually seen in young women of childbearing age and are often associated with repetitive spontaneous abortion accompanied by severe hemorrhage (17,32), as was true in patient 4 in our series. The congenital nature of these lesions has been debated, since older postmenopausal women with the condition have been described and often these women had undergone one or more uterine curettage procedures. However, careful examination of most reports suggests that there was a previous history of marked vaginal bleeding prior to any uterine instrumentation. Interestingly, the disorder is very rare in women who have never been pregnant, raising the possibility that placental development
may contribute in some way to the development of such malformations. Over 50 years ago, Burwell suggested that the normal placenta represented a modified arteriovenous fistula (35); however, in an angiographic study of pelvic vessels in a large number of women with gynecologic and obstetric conditions, Borell and Fernstrom found abnormal venous opacification in only one of 112 normal intrauterine pregnancies. Early venous filling was noted in 20% of missed and spontaneous abortions and 29% of ectopic pregnancies, which suggested to those authors that necrosis of chorionic villi accounted for establishment of a communication between artery and vein. They also noted, however, that the majority of these fistulas probably close spontaneously and concluded that true congenital arteriovenous malformations of the uterus do occur (36). Acquired arteriovenous malformations are most frequently associated with a history of gestational trophoblastic disease. The angiographic appearance of molar pregnancy and invasive moles has been previously reported; most reports stress the presence of hypervascular uterine
520 • Journal of Vascular and Interventional Radiology November 1991
a. Figure 3. Patient 4. Congenital AVM. (a) Pelvic arteriogram demonstrates enlarged right uterine artery supplying vascular mass (*). Note normal left uterine artery (arrow). (b) In the late arterial phase, early venous filling is seen (arrow). (c) Mter embolization with polyvinyl alcohol and Gelfoam, right common iliac injection shows obliteration of the arteriovenous malformation.
masses with varying degrees of arteriovenous shunting resulting in early and prominent venous opacifkation (34). Cockshott and Hendrickse (11) first described the persistence of these arteriovenous communications and subsequent formation ofvascular uterine lesions after successful treatment of malignant trophoblastic disease, a finding that has been subsequently confirmed by a number of authors (15,22). Our cases showed findings identical to those previously reported with initial filling of large vascular spaces followed by venous opacification in the middle to late arterial phase. Until recently, therapy for all uterine arteriovenous malformations consisted of hysterectomy, but in the last 9 years there have been a number of reports of successful embolization without complication. The advan-
b.
c.
tages of such an approach are obvious since reproductive capacity is preserved and pregnancy and subsequent normal childbirth can be achieved. Embolization has been successful in the treatment of eight patients, beginning with the first intraoperative embolization performed by Forssman et al in 1982 (20,22,24-
26,28-31). The first reported percutaneous embolization was performed by Chapman and Lutz in 1985 (22). A variety of embolic materials have been used including Gelfoam, polyvinyl alcohol particles, Gianturco coils, bucrylate, and thrombin. Successful results apparently can be achieved by embolizing either the internal iliac
Vogelzang et al • 521 Volume 2 Number 4
artery or the uterine artery; only two reports indicate that the uterine artery was the sole vessel treated. In the other six cases, internal iliac artery embolization was performed. One patient experienced recurrence of the lesion 21;2 years after embolization; hysterectomy was curative (37). Of significance is the fact that four successful pregnancies and normal deliveries have occurred subsequent to embolotherapy in these eight patients (20,22,29,31). Concerns about the possibility of producing uterine infarction seem unwarranted in light of the absence of this complication and the rich collateral blood supply of the pelvis (33). Our series of four patients is noteworthy in that it constitutes one of the largest clinical experiences with uterine arteriovenous malformations, and we believe it is the largest reported group who have undergone embolization. A group of nine patients with congenital pelvic malformations who were treated by means of embolization has been described previously (37). Several points about our cases deserve mention. The angiographic appearance of these lesions was fairly characteristic, with one or both uterine arteries supplying a mass of dilated vascular channels with fairly early venous drainage. This venous drainage, however, was not fistulous; that is, venous filling did not occur simultaneously with the appearance of arterial contrast. Furthermore, although the uterine arteries were of greater than normal size, the increase was not marked or massive even in our patient with a congenital arteriovenous malformation. The uterine arteries also appeared to be the sole supply of these lesions. This finding is in contradistinction to our experience with the congenital pelvic arteriovenous malformations, which generally arise in the broad ligament of young women and have multiple feeders including the inferior mesenteric artery. These are extremely difficult to cure with embolotherapy. Whether congenital lesions of the uterus represent a small subset of all congenital pelvic
arteriovenous malformations cannot be stated with certainty. It does seem that the former can be cured with embolotherapy alone, although Beller et al reported recurrence of a congenital uterine malformation 2V2 years after embolization (37). This report would indicate that congenital lesions may indeed be variants of the more complex, aggressive pelvic malformations. Nevertheless, we believe that embolization, not hysterectomy, should be the treatment of choice. The apparent complete obliteration of a congenital uterine lesion on pathologic examination as well as curative embolizations of the other congenital malformations that have been reported would indicate that these lesions are probably more hemangiomatous in nature. It should be noted, however, that embolization of the nidus of the lesion or at least all feeding vessels should be accomplished to achieve complete cure, since Bottomley and Whitehouse reported that ligation of a single uterine artery did not eliminate the malformation in one of their cases (16). In summary, our experience indicates that uterine arteriovenous malformations may occasionally be seen in patients with abnormal uterine bleeding, particularly in a woman with a history of trophoblastic disease. Congenital lesions may result in repetitive spontaneous abortion associated with massive hemorrhage. When angiographic investigation shows the characteristic findings, we believe that transcatheter embolization of the feeding artery or arteries should be the treatment of choice, since uterine childbearing capacity can be preserved in most cases. References 1. Dubreuil G, Loubat E. Aneurisme cirsoide de l'uterus. Ann d'Anat Path 1926; 3:679-718. 2. Graves WP, Smith G, Van S. Cirsoid aneurysm of the uterus. Am J Obstet Gynecol1927; 14:30-34. 3. Reynolds RP, Owen CI, Cantor MO. Arteriovenous aneurysm of uterine artery and vein. JAMA 1949; 141: 841-842. 4. Gaines JA, Greenwald JC. Uterine
5. 6. 7. 8. 9. 10.
11.
12. 13.
14.
15.
16.
17.
18.
19.
arteriovenous fistula. Am J Obstet Gynecol1953; 65:997-1005. Williams GA. Arteriovenous aneurysm of the uterus. Am J Obstet GynecoI1954; 67:198-200. Gardner HI. Cirsoid aneurysm of the uterus. Am J Obstet Gynecol 1954; 68:845-853. Hoge RH. Arteriovenous fistula of the uterus. South Med J 1955; 48: 18-20. Salm R. Diffuse cavernous haemangioma of the uterus. J Pathol Bacteriol1959; 77:111-116. Liggins GC. Uterine arteriovenous fistula. Obstet Gynecol1964; 23: 214-217. Frencken VAM, Landman GHM. Cirsoid aneurysm of the uterus: specific arteriographic diagnosis. AJR 1965; 95:775-781. Cockshott WP, de V Hendrickse JP. Persistent arteriovenous fistulae following chemotherapy of malignant trophoblastic disease. Radiology 1967; 88:329-333. Von Magdolna G. Die hamangiome der weiblichen gesch lechtsorgane. Gynaecologia 1967; 164:307-315. Hibbard BM, Jones DP, Scarrow GD. Cirsoid aneurysm of the uterus as a cause of menorrhagia. J Obstet Gynecol Br Commonw 1972; 79:855-859. Gaylis H, Levine E, van Dongen LGR, Katz MB. Arteriovenous fistulas after gynecologic operations. Surg Gynecol Obstet 1973; 137:655658. Antebi E, Adar R, Deutsch V, Mozes M. Arteriovenous fistula complicating gynecologic operations. Obstet Gynecol1974; 44:858-861. Bottomley JP, Whitehouse GH. Congenital arteriovenous malformations of the uterus demonstrated by angiography. Acta Radiol [Diagn] 1975; 16:43-48. McLachlan MSF, Bird CC, Naiem EA, Scott JS. Uterine cirsoid aneurysm. Br J Obstet Gynaecol1978; 85:390-395. Szalay S, Bardach G, Janisch H, Leodolter S. Zur klinischen bedeutung arterio-venoser shuntmibbildungen im bereiche des inneren weiblichen genitales. Arch Gynecol 1979; 227:355-360. Treisser A, Cahen G, Laaban J, Kiin P, Sureau C. Fistules arteveineuses interessant les vaisseaux uterins. J Gynecol Obstet BioI Reprod 1979; 8:423-427.
522 • Journal of Vascular and Interventional Radiology November 1991
20.
21.
22.
23.
24.
25.
Forssman L, Lungberg J, Schersten T. Conservative treatment ofuterine arteriovenous fistula. Acta Obstet Gynecol Scand 1982; 61:85-87. Diwan RV, Brennan IN, Selim MA, et al. Sonographic diagnosis of arteriovenous malformation of the uterus and pelvis. JCU 1983; 11: 295-298. Chapman DR, Lutz MH. Report of a successful delivery after nonsurgical management of a choriocarcinoma-related pelvic arteriovenous fistula. Am J Obstet Gynecoll985; 153:155-157. Follen MM, Fox HE, Levine RU. Cervical vascular malformation as a cause of antepartum and intrapartum bleeding in three diethylstilbestrol-exposed progeny. Am J Obstet Gynecoll985; 153:890-891. MarkoffG, Quagliarello J, Rosen RJ, Beckman EM. Uterine arteriovenous malformation successfully embolized with a liquid polymer, isobutyl 2-cyanoacrylate. Am J Obstet Gynecoll986; 155:659-660. Vujic I, Stanley JH, Gobien RP, Bruce RJ, Lutz MH. Embolic management of rare hemorrhagic gyne-
26.
27 .
28. 29.
30.
31.
cologie and obstetrical conditions. Cardiovasc Intervent Radioll986; 9:69-74. Wilms GE, Favril A, Baert AL, Poppe W, Van Assche FA. Transcatheter embolization of uterine arteriovenous malformations. Cardiovase Intervent Radioll986; 9:61-64. El-Torky M, Giltman L, Maijub A. Uterine arteriovenous fistula: a case report. J Reprod Med 1986; 31:283286. Ghosh TK. Arteriovenous malformation of the uterus and pelvis. Obstet Gynecol 1986; 68:408-43S. Poppe W, Van Assche FA, Wilms G, Favril A, Baert A. Pregnancy after transcatheter embolization of a uterine arteriovenous malformation. Am J Obstet Gynecoll987; 156:11791180. Finnegan MF, Tisnado J, Bezirdjian DR, Cho SR. Transcatheter embolotherapy of massive bleeding after surgery for benign gynecologic disorders. J Can Assoc Radioll988; 39: 172-177. Tacchi D, Loose HW. Successful pregnancy after selective embolization of a post-molar vascular malfor-
32.
33.
34.
35.
36. 37.
mation. Br J Obstet Gynaecoll988; 95:814-817. Fleming H, Ostor AG, Pickel H, Fortune DW. Arteriovenous malformations of the uterus. Obstet Gynecol 1989; 73:209-213. Belli AM, Hemingway AP, Neal FE, Millar DR. Arteriovenous malformation of the uterus related to trophoblastic disease: a case for surgery or embolisation? J Intervent Radiol 1989; 4:118-112. Brewis RAL, Bagshawe KD. Pelvic arteriography in invasive trophoblastic neoplasia. Br J Radioll968; 41:481-495. Burwell CS. The placenta as a modified arteriovenous fistula consideration in relation to the circulatory adjustments to pregnancy. Am J Med Sci 1938; 195:1-12. Borell U, Fernstrom I. Arteriovenous fistulae of the uterus and adnexa. Acta Radioll958; 49:1-16. Beller U, Rosen RJ, Beckman EM, Markoff G, Bernstein A. Congenital arteriovenous malformation of the female pelvis: a gynecologic perspective. Am J Obstet Gynecoll988; 159:1153-1160.
Index terms: Arteries, therapeutic blockade,969.1299 • Arteriovenous malformations, pelvic, 969.14, 969.715 • Arteriovenous malformations, uterine, 969.14, 969.716 • Uterus, hemorrhage, 854.319, 969.716 JVIR 1991; 2:517-522
1 From the Departments of Diagnostic Radiology (RL.v., A.A.N., Z.S.) and Obstetrics and Gynecology (J.RL.), Northwestern University Medical School and Northwestern Memorial Hospital, 710 N Fairbanks Ct, Chicago, IL 60611, and the Department of Obstetrics and Gynecology, Michael Reese Hospital, Chicago (J.G.). From the 1991 SCVIR annual meeting. Received April 28, 1991; revision requested June 6; revision received June 24; accepted July 9. Address reprint requests to RL.V.
©
SCVIR, 1991
Uterine arteriovenous malformations are rare lesions that can cause massive vaginal bleeding and spontaneous abortions. The majority are either congenital or related to gestational trophoblastic disease. Hysterectomy has been the treatment of choice. The authors successfully treated four patients with symptomatic uterine arteriovenous malformations by means of transcatheter embolization; three of the lesions were related to gestational trophoblastic disease and one was congenital. All were supplied by the uterine arteries that were subselectively embolized with particulate material. This resulted in prompt cessation of uterine hemorrhage. There were no complications, and one pregnancy was achieved. The three other women have normal menstruation and no recurrence of bleeding at follow-up 10-48 months after treatment. On the basis of this experience and that of others, embolotherapy should be the treatment of first choice in these lesions, as it appears safe and effective. Additionally, uterine function is preserved in patients who are usually reproductively active. UTERINE arteriovenous malformations are a rare cause of massive uterine bleeding. These lesions, variably described as cirsoid aneurysm, arteriovenous malformation, racemose aneurysm, cavernous hemangioma, or arteriovenous aneurysm, can be acquired or congenital (1-11). The causes of acquired lesions include previous surgery on the uterus, endometrial adenocarcinoma, maternal diethylstilbestrol exposure, and trophoblastic disease (11-23). Recognition of this abnormality as the cause of hemorrhage is important since uterine instrumentation is clearly not indicated and may only worsen the condition. Hysterectomy has traditionally been the treatment of choice, but transcatheter embolization, first reported by Forssman et al in 1982 and described in a number of single case reports since then, appears to allow successful treatment while sparing uterine childbearing capacity (20,22,24-26). In this report we document our results in four patients with uterine arteriovenous
malformations treated with subselective transcatheter embolization and compare our results and techniques with those reported previously. To our knowledge, this is the largest such series to date.
PATIENTS AND METHODS Between January 1987 and July 1990, four patients with uterine arteriovenous malformations were seen and treated at Northwestern Memorial Hospital. Ages of these women ranged from 16 to 34 years (Table); all presented with recurrent episodes of heavy uterine bleeding ranging in duration from 3 weeks to 2 years. Transfusions were required in three. Three patients had gestational trophoblastic disease. After a term pregnancy, one woman had metastatic gestational choriocarcinoma, which was successfully treated with chemotherapy. Another was beginning chemotherapy for postmolar gestational trophoblastic tumor. In the third pa-
517
518 • Journal of Vascular and Interventional Radiology November 1991
Summary of Patient Data Age Obstetric Duration of AVM Arterial Supply Embolic (Embolized) Patient (y) History Hemorrhage Etiology Material 1 21 Gl, PI 8wk Gestational chorio- Bilateral uterine PYA arteries carcinoma
Duration of Follow-up (mo) 48
2
34 G4, Pl,A3
3wk
Invasive mole
Right uterine artery
PYA, Gelfoam
13
3
31 G2, PO,A2
5mo
Bilateral uterine PYA, Gelfoam arteries
10
4
16 G4,PO,A4
2y
Partial hydatidiform mole Congenital
Right uterine artery
14
PYA, Gelfoam
Results Normal menses, no bleeding, no pregnancy Normal menses, no bleeding, no pregnancy Normal menses, no bleeding, no pregnancy Resumed normal menses; pregnant at 8 months, but pregnancy was terminated by means of elective hysterectomy at 16 weeks
Note.-AVM = arteriovenous malformation, PYA = polyvinyl alcohol.
tient human chorionic gonadotropin levels spontaneously returned to normal following treatment of a partial hydatidiform mole 2 years earlier. In the fourth patient, a large congenital arteriovenous malformation had caused four spontaneous abortions and several episodes of massive vaginal bleeding over a 2-year period. Diagnostic testing prior to the procedure included hysteroscopy in two (patients 1 and 3), which demonstrated the arteriovenous malformation as a pulsatile fundal mass. Arteriography showed similar findings in all patients: a lesion consisting of dilated irregular vascular spaces supplied by a single enlarged uterine artery in two patients and by both uterine arteries in two others. Early and prominent venous filling was seen in the middle or late arterial phase in all patients. This finding was particularly well demonstrated on selective internal iliac or superselective uterine arterial injection (Figs 1, 2a, 3a, 3b). The uterine artery was always the sole arterial supply; no other pelvic feeding vessels were found in any case. Embolization of the involved uterine arteries was performed from the femoral (three cases) or axillary (one case) approach. Embolization was
Figure 1. Patient 1. Pelvic arteriogram demonstrates hypervascular mass (arrows) predominantly supplied by right uterine artery, although there is contribution from the left uterine vessel.
carried out first with polyvinyl alcohol particles 150-600 J.Lm in diameter followed by gelatin sponge pledgets (Gelfoam; Upjohn, Kalamazoo, Mich) to an endpoint of complete arterial occlusion. A completion internal iliac angiogram helped confirm obliteration of the mass (Figs 2b, 3c).
RESULTS Prompt and complete cessation of abnormal uterine bleeding occurred
within 24 hours in all patients. Clinical follow-up ranging between 10 and 48 months showed continued lack of bleeding and restoration of normal menses in all four patients. Patient 4 became pregnant 8 months after embolization. Ultrasound depicted placenta previa and, due to the patient's grave concerns about prior bleeding episodes, the pregnancy was terminated by elective hysterectomy at 16 weeks gestation. Pathologic examination of the uterus showed obliteration of the arteriovenous malforma-
Vogelzang et al • 519 Volume 2 Number 4
a.
b.
Figure 2. Patient 2. (a) Selective left uterine artery injection demonstrates uterine artery (curved arrow) supply of hypervascular fundal mass (*) with early venous drainage (straight arrow). (b) Pelvic arteriogram obtained after embolization.
tion; vascular enlargement consistent with a normal pregnancy was found. Additionally, placenta accreta was identified. None of the other three patients has become pregnant, although this was not specifically attempted. Patients tolerated the embolization well in all cases. Moderate uterine cramping and/or pelvic pain was noted in two patients the evening following the procedure, and a minimal postembolization fever of 100.3 0 F (38 C) was seen in one of these. There were no other complications. 0
DISCUSSION Arteriovenous malformations of the uterus are rare lesions. Since the first case in 1926 reported by Dubreuil and Loubat, a total of 54 cases have been documented (1-33). In this group, the malformation was acquired in 24 and congenital in 30. Of the acquired abnormalities, 14 were associated with gestational trophoblastic disease, six with previous surgery, three with maternal diethylstilbesterol exposure, and one with endometrial carcinoma. If, however,
one considers only those lesions that involved the uterus (and not the cervix) and if postsurgical fistulas between extrauterine vessels are excluded (14,23), congenital lesions outnumber acquired lesions (30 vs 19, respectively), and the majority (74%) of acquired cases were associated with gestational trophoblastic disease. Although they have been seen in older women (4,7), congenital malformations of the uterus are usually seen in young women of childbearing age and are often associated with repetitive spontaneous abortion accompanied by severe hemorrhage (17,32), as was true in patient 4 in our series. The congenital nature of these lesions has been debated, since older postmenopausal women with the condition have been described and often these women had undergone one or more uterine curettage procedures. However, careful examination of most reports suggests that there was a previous history of marked vaginal bleeding prior to any uterine instrumentation. Interestingly, the disorder is very rare in women who have never been pregnant, raising the possibility that placental development
may contribute in some way to the development of such malformations. Over 50 years ago, Burwell suggested that the normal placenta represented a modified arteriovenous fistula (35); however, in an angiographic study of pelvic vessels in a large number of women with gynecologic and obstetric conditions, Borell and Fernstrom found abnormal venous opacification in only one of 112 normal intrauterine pregnancies. Early venous filling was noted in 20% of missed and spontaneous abortions and 29% of ectopic pregnancies, which suggested to those authors that necrosis of chorionic villi accounted for establishment of a communication between artery and vein. They also noted, however, that the majority of these fistulas probably close spontaneously and concluded that true congenital arteriovenous malformations of the uterus do occur (36). Acquired arteriovenous malformations are most frequently associated with a history of gestational trophoblastic disease. The angiographic appearance of molar pregnancy and invasive moles has been previously reported; most reports stress the presence of hypervascular uterine
520 • Journal of Vascular and Interventional Radiology November 1991
a. Figure 3. Patient 4. Congenital AVM. (a) Pelvic arteriogram demonstrates enlarged right uterine artery supplying vascular mass (*). Note normal left uterine artery (arrow). (b) In the late arterial phase, early venous filling is seen (arrow). (c) Mter embolization with polyvinyl alcohol and Gelfoam, right common iliac injection shows obliteration of the arteriovenous malformation.
masses with varying degrees of arteriovenous shunting resulting in early and prominent venous opacifkation (34). Cockshott and Hendrickse (11) first described the persistence of these arteriovenous communications and subsequent formation ofvascular uterine lesions after successful treatment of malignant trophoblastic disease, a finding that has been subsequently confirmed by a number of authors (15,22). Our cases showed findings identical to those previously reported with initial filling of large vascular spaces followed by venous opacification in the middle to late arterial phase. Until recently, therapy for all uterine arteriovenous malformations consisted of hysterectomy, but in the last 9 years there have been a number of reports of successful embolization without complication. The advan-
b.
c.
tages of such an approach are obvious since reproductive capacity is preserved and pregnancy and subsequent normal childbirth can be achieved. Embolization has been successful in the treatment of eight patients, beginning with the first intraoperative embolization performed by Forssman et al in 1982 (20,22,24-
26,28-31). The first reported percutaneous embolization was performed by Chapman and Lutz in 1985 (22). A variety of embolic materials have been used including Gelfoam, polyvinyl alcohol particles, Gianturco coils, bucrylate, and thrombin. Successful results apparently can be achieved by embolizing either the internal iliac
Vogelzang et al • 521 Volume 2 Number 4
artery or the uterine artery; only two reports indicate that the uterine artery was the sole vessel treated. In the other six cases, internal iliac artery embolization was performed. One patient experienced recurrence of the lesion 21;2 years after embolization; hysterectomy was curative (37). Of significance is the fact that four successful pregnancies and normal deliveries have occurred subsequent to embolotherapy in these eight patients (20,22,29,31). Concerns about the possibility of producing uterine infarction seem unwarranted in light of the absence of this complication and the rich collateral blood supply of the pelvis (33). Our series of four patients is noteworthy in that it constitutes one of the largest clinical experiences with uterine arteriovenous malformations, and we believe it is the largest reported group who have undergone embolization. A group of nine patients with congenital pelvic malformations who were treated by means of embolization has been described previously (37). Several points about our cases deserve mention. The angiographic appearance of these lesions was fairly characteristic, with one or both uterine arteries supplying a mass of dilated vascular channels with fairly early venous drainage. This venous drainage, however, was not fistulous; that is, venous filling did not occur simultaneously with the appearance of arterial contrast. Furthermore, although the uterine arteries were of greater than normal size, the increase was not marked or massive even in our patient with a congenital arteriovenous malformation. The uterine arteries also appeared to be the sole supply of these lesions. This finding is in contradistinction to our experience with the congenital pelvic arteriovenous malformations, which generally arise in the broad ligament of young women and have multiple feeders including the inferior mesenteric artery. These are extremely difficult to cure with embolotherapy. Whether congenital lesions of the uterus represent a small subset of all congenital pelvic
arteriovenous malformations cannot be stated with certainty. It does seem that the former can be cured with embolotherapy alone, although Beller et al reported recurrence of a congenital uterine malformation 2V2 years after embolization (37). This report would indicate that congenital lesions may indeed be variants of the more complex, aggressive pelvic malformations. Nevertheless, we believe that embolization, not hysterectomy, should be the treatment of choice. The apparent complete obliteration of a congenital uterine lesion on pathologic examination as well as curative embolizations of the other congenital malformations that have been reported would indicate that these lesions are probably more hemangiomatous in nature. It should be noted, however, that embolization of the nidus of the lesion or at least all feeding vessels should be accomplished to achieve complete cure, since Bottomley and Whitehouse reported that ligation of a single uterine artery did not eliminate the malformation in one of their cases (16). In summary, our experience indicates that uterine arteriovenous malformations may occasionally be seen in patients with abnormal uterine bleeding, particularly in a woman with a history of trophoblastic disease. Congenital lesions may result in repetitive spontaneous abortion associated with massive hemorrhage. When angiographic investigation shows the characteristic findings, we believe that transcatheter embolization of the feeding artery or arteries should be the treatment of choice, since uterine childbearing capacity can be preserved in most cases. References 1. Dubreuil G, Loubat E. Aneurisme cirsoide de l'uterus. Ann d'Anat Path 1926; 3:679-718. 2. Graves WP, Smith G, Van S. Cirsoid aneurysm of the uterus. Am J Obstet Gynecol1927; 14:30-34. 3. Reynolds RP, Owen CI, Cantor MO. Arteriovenous aneurysm of uterine artery and vein. JAMA 1949; 141: 841-842. 4. Gaines JA, Greenwald JC. Uterine
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