(Radiographics. 2002;22:35-46.)
© RSNA, 2002
Obstetric Iatrogenic Arterial Injuries of the Uterus: Diagnosis with US and Treatment with Transcatheter Arterial Embolization1
Jung Hyeok Kwon, MD and
Gi Sung Kim, MD
1 From the Department of Diagnostic Radiology, Dongkang General Hospital, 123-3 Taehwa-dong, Ulsan 681-320, Korea. Presented as an education exhibit at the 2000 RSNA scientific assembly. Received April 19, 2001; revision requested May 31 and received July 20; accepted July 23. Address correspondence to J.H.K. (e-mail: KJH2603@chollian.net).
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Abstract
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Uterine curettage or surgical trauma can cause uterine vascular abnormalities, including pseudoaneurysms, acquired arteriovenous malformations (AVMs), arteriovenous fistulas, and rupture of vessels. Recognition of these abnormalities as the cause of hemorrhage is important, since these abnormalities can be treated safely and effectively with transcatheter arterial embolization but may be worsened by uterine curettage, precipitating massive uterine bleeding. Ultrasonography (US) is the most commonly performed initial imaging examination for evaluation of abnormal uterine bleeding. Color and duplex Doppler US allows convincing detection and diagnosis of these vascular abnormalities and helps differentiate vascular abnormalities that require embolization from nonvascular abnormalities. In cases of pseudoaneurysms, color and duplex Doppler US shows a blood-filled cystic structure with swirling arterial flow. In cases of AVMs, color Doppler US shows an intense vascular tangle, whereas duplex Doppler US shows low-resistance, high-velocity arterial flow. Cases of an AVM combined with a pseudoaneurysm demonstrate the findings of both AVMs and pseudoaneurysms. Transcatheter arterial embolization after angiography is the therapy of choice for these vascular abnormalities, with the advantage of retained reproductive capacity. Routine use of color and duplex Doppler US during examination of abnormal uterine bleeding is recommended to identify and characterize the vascular abnormality.
© RSNA, 2002
Index Terms: Aneurysm, uterine, 969.458, 969.732 • Arteries, therapeutic embolization, 969.1264 • Arteries, uterine, 969.412, 969.458 • Arteriovenous malformations, uterine, 969.494
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Introduction
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The vascular supply to the uterus is primarily through the uterine artery, which approaches the uterus at the level of the cervix and lower uterine segment. Branches of the uterine artery, the arcuate arteries, extend inward and run circumferentially between the outer and middle thirds of the myometrium. The radial arteries arise from the arcuate arteries and are directed toward the uterine cavity to become the spiral arteries in the endometrium. Uterine venous channels follow a course similar to that of the arteries. The arcuate venous plexus accompanies the arcuate arteries, passing circumferentially within the myometrium (1,2). Color Doppler ultrasonography (US) shows a circular pattern of blood flow signals in the outer myometrium from the arcuate arteries and venous plexus and a radial pattern of blood flow signals in the middle and inner myometrium from the radial and spiral arteries and accompanying veins (2).
Hemorrhage is one of the principal complications of uterine curettage or pelvic surgery, developing in 0.05%–4.9% of abortion procedures (3,4). Intractable hemorrhage refractory to conservative measures may be potentially attributed to uterine arterial injuries. In a recent report, three of 14 patients who underwent transcatheter arterial embolization for intractable delayed postpartum hemorrhage had causative uterine vascular abnormalities (5). Uterine vascular abnormalities have been reported to occur following uterine curettage or surgical trauma in sporadic reports (5–14). These vascular abnormalities include pseudoaneurysms (5–9), acquired arteriovenous malformations (AVMs) (10–12), arteriovenous fistulas (5,13), and direct vessel ruptures (14). These abnormalities may be a cause of massive uterine bleeding and may be aggravated by dilation and curettage (D&C), unlike the more common causes of excessive uterine bleeding (10). In the past, in the event of failure of conservative local measures, patients were traditionally treated with bilateral hypogastric artery or uterine artery ligation or surgical hysterectomy.
Until relatively recently, such lesions were occasionally overlooked by obstetricians and gynecologists without performance of diagnostic imaging or therapeutic embolization (15). It seems that these lesions occur more frequently than has been suggested in the literature or previously thought. Increasing awareness of these pathologic entities coupled with more widespread use of the appropriate investigations allows us to more frequently detect uterine vascular abnormalities.
In this article, we present the gray-scale US, color and duplex Doppler US, and angiographic findings of uterine vascular abnormalities. Examples from our clinical experience include pseudoaneurysm, acquired AVM, AVM combined with a pseudoaneurysm, and direct arterial branch rupture. The value of color and duplex Doppler US in detection and diagnosis of these conditions is discussed, as is the value of transcatheter arterial embolization in treating these conditions. Possible causes of embolization failure are also discussed.
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Clinical Experience
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During the past 8 years, we diagnosed 24 cases of iatrogenic uterine arterial injuries, which consisted of seven pseudoaneurysms, nine acquired AVMs, six cases of combined AVM and pseudoaneurysm, and two cases of uterine arterial branch rupture. All patients were within the reproductive age group (21–39 years old) and were referred for intractable vaginal bleeding from many clinics and hospitals in our city and neighboring cities. Twenty-one patients had a history of causative D&C (one to five D&C procedures per patient), two had a history of causative cesarean section, and one had delivery trauma. Because otherwise asymptomatic individuals had experienced abnormal bleeding shortly after these procedures, we suspected a causal link. All patients underwent transabdominal and endovaginal gray-scale, color Doppler, and duplex Doppler US and angiography with therapeutic embolization (one embolization procedure in 22 cases, two embolization procedures in two cases). Hysterectomy was performed in two cases of pseudoaneurysm in which embolization was not effective. All patients except the two who were surgically treated underwent follow-up Doppler US immediately after embolization and then usually at 3-month intervals for 1 year and yearly for up to 3 years. No recurrence was detected at follow-up US.
The gray-scale US, color and duplex Doppler US, and angiographic findings of these vascular abnormalities were retrospectively reviewed. The effects of embolization and causes of embolization failure were also reviewed.
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Pseudoaneurysm
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Pseudoaneurysms result from inadequate sealing of a laceration or puncture of the arterial wall during surgery or penetrating trauma (6,7). Under the influence of sustained arterial pressure, blood dissects into the tissues around the damaged artery and forms a perfused sac that communicates with the arterial lumen (6,7). D&C, cesarean section, and other surgery on the uterus may cause pseudoaneurysms (5–9).
There were seven cases of pseudoaneurysms in our clinical experience, which were diagnosed with Doppler US and treated with transcatheter arterial embolization. Gray-scale US showed an anechoic sac (n = 5) (Figs 1a, 2a) or two (n = 1)or more (n = 1) sacs (Fig 3a). Color Doppler US showed a blood-filled cystic structure with varying colors (Figs 1b, 2b, 3b). Duplex Doppler US showed turbulent arterial flow (n = 3) (Figs 1c, 2c) or less disturbed, high-velocity, high-resistance arterial flow (n = 4) (Fig 3c) within the sac, depending on the variable degree of turbulence.
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Figure 1a. Pseudoaneurysm after D&C in a 28-year-old woman. The patient had intermittent vaginal bleeding after a spontaneous abortion followed by D&C 7 months earlier. At presentation, the serum ß-human chorionic gonadotropin (HCG) test was negative. (a) Longitudinal gray-scale US image shows a cystic lesion (between cursors) in the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrow). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrows), which is supplied by the left uterine artery (arrowhead). After embolization with a 3-mm-diameter coil, the pseudoaneurysm disappeared. Follow-up US showed no evidence of the pseudoaneurysm.
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Figure 1b. Pseudoaneurysm after D&C in a 28-year-old woman. The patient had intermittent vaginal bleeding after a spontaneous abortion followed by D&C 7 months earlier. At presentation, the serum ß-human chorionic gonadotropin (HCG) test was negative. (a) Longitudinal gray-scale US image shows a cystic lesion (between cursors) in the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrow). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrows), which is supplied by the left uterine artery (arrowhead). After embolization with a 3-mm-diameter coil, the pseudoaneurysm disappeared. Follow-up US showed no evidence of the pseudoaneurysm.
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Figure 1c. Pseudoaneurysm after D&C in a 28-year-old woman. The patient had intermittent vaginal bleeding after a spontaneous abortion followed by D&C 7 months earlier. At presentation, the serum ß-human chorionic gonadotropin (HCG) test was negative. (a) Longitudinal gray-scale US image shows a cystic lesion (between cursors) in the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrow). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrows), which is supplied by the left uterine artery (arrowhead). After embolization with a 3-mm-diameter coil, the pseudoaneurysm disappeared. Follow-up US showed no evidence of the pseudoaneurysm.
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Figure 1d. Pseudoaneurysm after D&C in a 28-year-old woman. The patient had intermittent vaginal bleeding after a spontaneous abortion followed by D&C 7 months earlier. At presentation, the serum ß-human chorionic gonadotropin (HCG) test was negative. (a) Longitudinal gray-scale US image shows a cystic lesion (between cursors) in the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrow). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrows), which is supplied by the left uterine artery (arrowhead). After embolization with a 3-mm-diameter coil, the pseudoaneurysm disappeared. Follow-up US showed no evidence of the pseudoaneurysm.
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Figure 2a. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2b. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2c. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2d. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2e. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2f. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 2g. Recurrent pseudoaneurysm after embolization in a 35-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. She had markedly aggravated, intractable vaginal bleeding after therapeutic D&C 2 weeks earlier for abnormal vaginal bleeding. (a) Longitudinal gray-scale US image shows a septate cystic lesion (arrows) at the left wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structure is filled with blood and has varying colors (arrows). (c) Longitudinal duplex Doppler US image shows turbulent arterial flow within the sac. (d) Left internal iliac angiogram shows the pseudoaneurysm (arrow), which is supplied by the left uterine artery. Arterial embolization with a 3-mm-diameter coil was performed. (e) Follow-up longitudinal US image obtained 3 days later shows thrombosis of the pseudoaneurysm (arrows). Two weeks later, the bleeding recurred and Doppler US showed recanalization of the pseudoaneurysm. (f, g) Photograph of the pathologic specimen (f) and photomicrograph (original magnification, x100; hematoxylin-eosin stain) (g) show degenerating retained chorionic villi (arrowheads in g) against a background of hematoma in placenta accreta (arrows in f). Scale in f is in centimeters.
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Figure 3a. Four pseudoaneurysms supplied by the right uterine artery and right internal pudendal artery in a 30-year-old woman who underwent embolization twice. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Longitudinal gray-scale US image shows cystic lesions (arrows) in the right wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structures are filled with blood (arrows). (c) Longitudinal duplex Doppler US image shows less disturbed, high-velocity, high-resistance arterial flow within the sacs (peak systolic velocity [PSV], 50 cm/sec; resistive index [RI], 0.98). (d) Right internal iliac angiogram shows four pseudoaneurysms (arrows). After bilateral embolization of the uterine arteries with pledgets of absorbable gelatin sponge (Gelfoam; Pharmacia & Upjohn, Kalamazoo, Mich), the bleeding decreased but was still present. (e) Subsequent repeat right internal iliac angiogram obtained during the late arterial phase shows cross-filling of a pseudoaneurysm (arrow) supplied by the right internal pudendal artery, which demonstrates proximal occlusion (arrowhead) of unknown origin. Follow-up US after embolization showed no evidence of pseudoaneurysms.
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Figure 3b. Four pseudoaneurysms supplied by the right uterine artery and right internal pudendal artery in a 30-year-old woman who underwent embolization twice. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Longitudinal gray-scale US image shows cystic lesions (arrows) in the right wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structures are filled with blood (arrows). (c) Longitudinal duplex Doppler US image shows less disturbed, high-velocity, high-resistance arterial flow within the sacs (peak systolic velocity [PSV], 50 cm/sec; resistive index [RI], 0.98). (d) Right internal iliac angiogram shows four pseudoaneurysms (arrows). After bilateral embolization of the uterine arteries with pledgets of absorbable gelatin sponge (Gelfoam; Pharmacia & Upjohn, Kalamazoo, Mich), the bleeding decreased but was still present. (e) Subsequent repeat right internal iliac angiogram obtained during the late arterial phase shows cross-filling of a pseudoaneurysm (arrow) supplied by the right internal pudendal artery, which demonstrates proximal occlusion (arrowhead) of unknown origin. Follow-up US after embolization showed no evidence of pseudoaneurysms.
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Figure 3c. Four pseudoaneurysms supplied by the right uterine artery and right internal pudendal artery in a 30-year-old woman who underwent embolization twice. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Longitudinal gray-scale US image shows cystic lesions (arrows) in the right wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structures are filled with blood (arrows). (c) Longitudinal duplex Doppler US image shows less disturbed, high-velocity, high-resistance arterial flow within the sacs (peak systolic velocity [PSV], 50 cm/sec; resistive index [RI], 0.98). (d) Right internal iliac angiogram shows four pseudoaneurysms (arrows). After bilateral embolization of the uterine arteries with pledgets of absorbable gelatin sponge (Gelfoam; Pharmacia & Upjohn, Kalamazoo, Mich), the bleeding decreased but was still present. (e) Subsequent repeat right internal iliac angiogram obtained during the late arterial phase shows cross-filling of a pseudoaneurysm (arrow) supplied by the right internal pudendal artery, which demonstrates proximal occlusion (arrowhead) of unknown origin. Follow-up US after embolization showed no evidence of pseudoaneurysms.
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Figure 3d. Four pseudoaneurysms supplied by the right uterine artery and right internal pudendal artery in a 30-year-old woman who underwent embolization twice. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Longitudinal gray-scale US image shows cystic lesions (arrows) in the right wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structures are filled with blood (arrows). (c) Longitudinal duplex Doppler US image shows less disturbed, high-velocity, high-resistance arterial flow within the sacs (peak systolic velocity [PSV], 50 cm/sec; resistive index [RI], 0.98). (d) Right internal iliac angiogram shows four pseudoaneurysms (arrows). After bilateral embolization of the uterine arteries with pledgets of absorbable gelatin sponge (Gelfoam; Pharmacia & Upjohn, Kalamazoo, Mich), the bleeding decreased but was still present. (e) Subsequent repeat right internal iliac angiogram obtained during the late arterial phase shows cross-filling of a pseudoaneurysm (arrow) supplied by the right internal pudendal artery, which demonstrates proximal occlusion (arrowhead) of unknown origin. Follow-up US after embolization showed no evidence of pseudoaneurysms.
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Figure 3e. Four pseudoaneurysms supplied by the right uterine artery and right internal pudendal artery in a 30-year-old woman who underwent embolization twice. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Longitudinal gray-scale US image shows cystic lesions (arrows) in the right wall of the lower uterus. (b) Longitudinal color Doppler US image shows that the cystic structures are filled with blood (arrows). (c) Longitudinal duplex Doppler US image shows less disturbed, high-velocity, high-resistance arterial flow within the sacs (peak systolic velocity [PSV], 50 cm/sec; resistive index [RI], 0.98). (d) Right internal iliac angiogram shows four pseudoaneurysms (arrows). After bilateral embolization of the uterine arteries with pledgets of absorbable gelatin sponge (Gelfoam; Pharmacia & Upjohn, Kalamazoo, Mich), the bleeding decreased but was still present. (e) Subsequent repeat right internal iliac angiogram obtained during the late arterial phase shows cross-filling of a pseudoaneurysm (arrow) supplied by the right internal pudendal artery, which demonstrates proximal occlusion (arrowhead) of unknown origin. Follow-up US after embolization showed no evidence of pseudoaneurysms.
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Within the pseudoaneurysm, swirling arterial flow with different directions and velocities is seen, with varying colors according to the variable degree of turbulence at color Doppler US. In the neck of the pseudoaneurysm, the to-and-fro pattern may be potentially identified at duplex Doppler US because the arterial blood flows like a jet (forward flow) into the aneurysm cavity during systole, then reverses (backward flow) into the original artery during diastole (16). This pattern is explained by the pressure gradient between a distended, high-pressure pseudoaneurysm and a low-pressure artery during diastole (7). However, in the case of a uterine artery pseudoaneurysm, demonstration of the neck of the pseudoaneurysm at US may be difficult because of the small size of the parent artery (6,8).
Angiography clearly demonstrated one or more pseudoaneurysms supplied by one or more feeding arteries (Figs 1d, 2d, 3d). In general, urgent intervention is required, as pseudoaneurysms are at risk of rupturing or expanding. Pseudoaneurysms can be treated successfully with arterial embolization (5–9).
When retained villi are abundantly present within a pseudoaneurysm, rapid recruitment of collateral vessels following arterial embolization may occur from pelvic arteries, recanalizing the pseudoaneurysm (17,18). In our clinical experience, there were pseudoaneurysms with retained villi in two cases of placenta accreta (Fig 2). Therefore, particular attention to the serum ß-HCG test should be stressed. In this situation, methotrexate therapy or a retrial of uterine curettage immediately after embolization may decrease recanalization of pseudoaneurysms. These recommendations may also apply to cases of AVMs.
Another cause of embolization failure is inadequate embolization of a pseudoaneurysm supplied by extrauterine feeding arteries, such as the internal pudendal artery (Fig 3), ovarian artery, inferior epigastric artery, or contralateral uterine artery (5,6,17). A meticulous search for other feeding arteries is recommended, including detection of simultaneous cross-filling of the sac by two or more arteries. US cannot demonstrate retained villi or extrauterine feeding arteries. Therefore, the serum ß-HCG test and a meticulous search for possible feeding arteries during angiography are recommended.
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Acquired AVM
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AVMs are characterized by multiple communications of varying sizes between arteries and veins in the same vicinity, whereas an arteriovenous fistula is an abnormal direct passage between an artery and an adjoining vein (19). Traditionally, uterine AVMs have been classified as congenital or acquired (12). Congenital uterine AVMs arise from an abnormality in the embryologic development of primitive vascular structures, which results in multiple abnormal communications between arteries and veins (12). Acquired uterine AVMs are really multiple small arteriovenous fistulas between intramural arterial branches and the myometrial venous plexus and appear as a vascular tangle, mimicking congenital AVMs (20,21). An acquired AVM may potentially belong to an arteriovenous fistula (22). An acquired pelvic arteriovenous fistula is an abnormal direct passage between an artery and an adjoining vein without a network of abnormal vessels, potentially arising outside the uterus (23).
Although endometrial carcinoma, cervical carcinoma, gestational trophoblastic disease, and maternal diethylstilbestrol exposure have been implicated (10,24–26), acquired uterine AVMs more commonly occur on a traumatic basis, as there is usually a history of D&C, uterine surgery, or trauma to the uterus (10–12). These conditions have the potential for subsequent development of abnormal fistulous communications between arteries and veins in the uterine wall, which may develop into and persist as an AVM (20,21). Acquired AVMs tend to have single or bilateral feeding uterine arteries without being supplied by extrauterine arteries and do not have a nidus, whereas congenital AVMs tend to have multiple feeding arteries and draining veins and an intervening nidus (22,25,27). Because of these different structural characteristics, acquired AVMs are much easier to treat with transcatheter arterial embolization than are congenital AVMs (25). The patient history, coupled with the angiographic findings, is helpful in differentiating between acquired and congenital AVMs. The pattern of bleeding is intermittent and torrential, suggestive of arterial hemorrhage (21). Uterine bleeding is thought to occur when vessels of the AVM are exposed from sloughing of the endometrium iatrogenically during D&C or during menses (12).
There were nine cases of acquired AVMs in our clinical experience, which were diagnosed with Doppler US and treated with transcatheter arterial embolization. The gray-scale US morphology of uterine AVMs is nonspecific and includes subtle myometrial inhomogeneity and multiple distinct, small anechoic spaces in the thickened myometrium or endometrium, which are focally or asymmetrically distributed (Figs 4a, 5a). Color and duplex Doppler US is a good screening and diagnostic test, as the Doppler features of uterine AVMs are highly suggestive of the diagnosis. Color Doppler US shows a tangle of tortuous vessels with multidirectional, high-velocity arterial flow, which is focally or asymmetrically distributed (Figs 4b, 5b). Some authors have described this feature as two color mosaic patterns: color aliasing with different flow velocities and apparent flow reversals of juxtaposed reds and blues with different flow directions (12). Duplex Doppler US shows the classic features of arteriovenous shunting, which manifests as fast arterial flow with low resistance: high PSV, an arterial spectral waveform with a high diastolic component, and a pulsatile high-velocity venous waveform with little variation in systolic-diastolic velocities (Figs 4c, 5c) (12). In our nine cases, the PSV was 20–67 cm/sec (mean ± standard deviation, 43.6 cm/sec ± 15.7) and the RI was 0.17–0.52 (mean, 0.30 ± 0.11). In contrast, in the healthy reproductive-age women in our control group (n = 118), the PSV was 4–38 cm/sec (mean, 11.6 cm/sec) and the RI was 0.53–0.98 (mean, 0.72) in the radial arteries. In our experience with acquired AVMs, the PSV is relatively high but is highly variable according to the site or angle of the Doppler sample volume with interobserver and intraobserver variations.
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Figure 4a. Acquired AVM in a 26-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows a thickened endometrium and myometrium with subtle inhomogeneity (arrows) in the left posterior aspect of the uterus. (b) Transverse color Doppler US image shows focally increased arterial vascularity in the corresponding area (arrows). (c) Transverse duplex Doppler US image shows arterial flow with a high diastolic component (PSV, 42 cm/sec; RI, 0.52). (d) Left internal iliac angiogram shows a markedly opacified vascular tangle (arrows) supplied by the left uterine artery (arrowhead). Follow-up Doppler US examinations after embolization with a 3-mm-diameter coil showed disappearance of the lesion.
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Figure 4b. Acquired AVM in a 26-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows a thickened endometrium and myometrium with subtle inhomogeneity (arrows) in the left posterior aspect of the uterus. (b) Transverse color Doppler US image shows focally increased arterial vascularity in the corresponding area (arrows). (c) Transverse duplex Doppler US image shows arterial flow with a high diastolic component (PSV, 42 cm/sec; RI, 0.52). (d) Left internal iliac angiogram shows a markedly opacified vascular tangle (arrows) supplied by the left uterine artery (arrowhead). Follow-up Doppler US examinations after embolization with a 3-mm-diameter coil showed disappearance of the lesion.
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Figure 4c. Acquired AVM in a 26-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows a thickened endometrium and myometrium with subtle inhomogeneity (arrows) in the left posterior aspect of the uterus. (b) Transverse color Doppler US image shows focally increased arterial vascularity in the corresponding area (arrows). (c) Transverse duplex Doppler US image shows arterial flow with a high diastolic component (PSV, 42 cm/sec; RI, 0.52). (d) Left internal iliac angiogram shows a markedly opacified vascular tangle (arrows) supplied by the left uterine artery (arrowhead). Follow-up Doppler US examinations after embolization with a 3-mm-diameter coil showed disappearance of the lesion.
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Figure 4d. Acquired AVM in a 26-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 9 weeks earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows a thickened endometrium and myometrium with subtle inhomogeneity (arrows) in the left posterior aspect of the uterus. (b) Transverse color Doppler US image shows focally increased arterial vascularity in the corresponding area (arrows). (c) Transverse duplex Doppler US image shows arterial flow with a high diastolic component (PSV, 42 cm/sec; RI, 0.52). (d) Left internal iliac angiogram shows a markedly opacified vascular tangle (arrows) supplied by the left uterine artery (arrowhead). Follow-up Doppler US examinations after embolization with a 3-mm-diameter coil showed disappearance of the lesion.
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Figure 5a. Acquired AVM in a 30-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 110 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) with a small internal anechoic component in the right posterolateral wall of the uterus. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) in the corresponding myometrium. (c) Transverse duplex Doppler US image shows high-velocity arterial flow with a high diastolic component (PSV, 63 cm/sec; RI, 0.19). (d) Selective angiogram of the right uterine artery obtained during the arterial phase shows a markedly opacified vascular tangle (arrows) and early venous drainage (arrowheads). After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 5b. Acquired AVM in a 30-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 110 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) with a small internal anechoic component in the right posterolateral wall of the uterus. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) in the corresponding myometrium. (c) Transverse duplex Doppler US image shows high-velocity arterial flow with a high diastolic component (PSV, 63 cm/sec; RI, 0.19). (d) Selective angiogram of the right uterine artery obtained during the arterial phase shows a markedly opacified vascular tangle (arrows) and early venous drainage (arrowheads). After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 5c. Acquired AVM in a 30-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 110 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) with a small internal anechoic component in the right posterolateral wall of the uterus. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) in the corresponding myometrium. (c) Transverse duplex Doppler US image shows high-velocity arterial flow with a high diastolic component (PSV, 63 cm/sec; RI, 0.19). (d) Selective angiogram of the right uterine artery obtained during the arterial phase shows a markedly opacified vascular tangle (arrows) and early venous drainage (arrowheads). After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 5d. Acquired AVM in a 30-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 110 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) with a small internal anechoic component in the right posterolateral wall of the uterus. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) in the corresponding myometrium. (c) Transverse duplex Doppler US image shows high-velocity arterial flow with a high diastolic component (PSV, 63 cm/sec; RI, 0.19). (d) Selective angiogram of the right uterine artery obtained during the arterial phase shows a markedly opacified vascular tangle (arrows) and early venous drainage (arrowheads). After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Angiography is the traditional diagnostic tool. The classic angiographic features consist of a complex tangle of vessels supplied by enlarged feeding arteries, in association with early venous drainage during the arterial phase and stasis of contrast medium within the abnormal vasculature (Figs 4d, 5d) (25). Angiography is essential to demonstrate the blood supply to the lesion and the presence of collateral vessels and to guide treatment, but it is no longer performed for purely diagnostic purposes because Doppler US can replace angiography as a screening tool.
Transcatheter arterial embolization has become the therapy of choice, with the advantage of retaining reproductive capacity (15). Both uterine arteries may have to be embolized because of cross-filling, which may not be evident at the time of initial angiographic therapy (6,21). Doppler US is the diagnostic method of choice for following up patients after treatment.
Gestational trophoblastic disease demonstrates increased vascularity with low-resistance arterial flow because the proliferation of trophoblastic tissue and its invasion of the endometrium and myometrium lead to development of abundant small vessels that penetrate the invading trophoblast, coupled with a prominent arteriovenous shunt (28). Retained products of conception may also show abundant color signal composed of low-resistance arterial flow (29). When the clinical history, gray-scale US findings, and serum ß-HCG test results are considered, AVMs can potentially be differentiated from these pathologic conditions with an arteriovenous shunt (12,28,29).
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AVM Combined with a Pseudoaneurysm
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D&C, cesarean section, or other trauma to the uterus may cause a pseudoaneurysm, an AVM, or both. The vessels of an AVM are apt to be injured even by minute trauma, with a resulting concomitant pseudoaneurysm (10,22).
There were six cases of both an acquired AVM and a pseudoaneurysm in our clinical experience. Such cases demonstrate the combined findings of an AVM and a pseudoaneurysm at gray-scale US, color and duplex Doppler US, and angiography (Fig 6). Gray-scale US shows subtle myometrial inhomogeneity plus an anechoic sac (Fig 6a). Color Doppler US shows a tangle of tortuous vessels (color mosaic patterns) plus a blood-filled cystic structure (Fig 6b). Duplex Doppler US shows the findings of both an AVM and a pseudoaneurysm (Fig 6c). Angiography shows a vascular tangle and a pseudoaneurysm (Fig 6d). Such cases can be treated successfully with arterial embolization, with no difference in the results in comparison with treatment of an AVM or treatment of a pseudoaneurysm.
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Figure 6a. AVM combined with a pseudoaneurysm in a 24-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 50 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) in the left lateral wall of the uterus and an anechoic sac (arrowhead) in the endometrium. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) and a blood-filled cystic structure (arrowhead) in the corresponding area. (c) Transverse duplex Doppler US image shows fast arterial flow with low resistance in the myometrium (PSV, 67 cm/sec; RI, 0.43). (d) Left internal iliac angiogram obtained during the late arterial phase shows a markedly opacified vascular tangle (arrows) and a pseudoaneurysm (black arrowheads) supplied by the left uterine artery. Early draining veins (white arrowhead) are seen. After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 6b. AVM combined with a pseudoaneurysm in a 24-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 50 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) in the left lateral wall of the uterus and an anechoic sac (arrowhead) in the endometrium. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) and a blood-filled cystic structure (arrowhead) in the corresponding area. (c) Transverse duplex Doppler US image shows fast arterial flow with low resistance in the myometrium (PSV, 67 cm/sec; RI, 0.43). (d) Left internal iliac angiogram obtained during the late arterial phase shows a markedly opacified vascular tangle (arrows) and a pseudoaneurysm (black arrowheads) supplied by the left uterine artery. Early draining veins (white arrowhead) are seen. After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 6c. AVM combined with a pseudoaneurysm in a 24-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 50 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) in the left lateral wall of the uterus and an anechoic sac (arrowhead) in the endometrium. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) and a blood-filled cystic structure (arrowhead) in the corresponding area. (c) Transverse duplex Doppler US image shows fast arterial flow with low resistance in the myometrium (PSV, 67 cm/sec; RI, 0.43). (d) Left internal iliac angiogram obtained during the late arterial phase shows a markedly opacified vascular tangle (arrows) and a pseudoaneurysm (black arrowheads) supplied by the left uterine artery. Early draining veins (white arrowhead) are seen. After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Figure 6d. AVM combined with a pseudoaneurysm in a 24-year-old woman. The patient had intermittent vaginal bleeding after D&C for a therapeutic abortion 50 days earlier. The serum ß-HCG test was negative at presentation. (a) Transverse gray-scale US image shows subtle myometrial inhomogeneity (arrows) in the left lateral wall of the uterus and an anechoic sac (arrowhead) in the endometrium. (b) Transverse color Doppler US image shows a tangle of tortuous vessels (arrows) and a blood-filled cystic structure (arrowhead) in the corresponding area. (c) Transverse duplex Doppler US image shows fast arterial flow with low resistance in the myometrium (PSV, 67 cm/sec; RI, 0.43). (d) Left internal iliac angiogram obtained during the late arterial phase shows a markedly opacified vascular tangle (arrows) and a pseudoaneurysm (black arrowheads) supplied by the left uterine artery. Early draining veins (white arrowhead) are seen. After embolization with absorbable gelatin sponge pledgets, no bleeding recurred.
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Direct Arterial Branch Rupture
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Bleeding from a uterine or cervical perforation during instrumentation of the uterus in the area of the uterine artery and vein can lead to severe blood loss. Direct rupture of an arterial branch can manifest as rapid catastrophic bleeding during the trauma or operation, necessitating immediate embolization (14,30).
There were two cases of arterial branch rupture in our clinical experience, which were detected with US and treated with embolization. US shows only heterogeneous hematomas in the mural and cavitary regions of the uterus (Fig 7a). Rarely, color and duplex Doppler US shows slowly moving blood without pulsation or fluctuation in the uterine cavity outside the vascular lumen (Fig 7b). This finding suggests massive hemorrhage. However, detection of this Doppler US finding is unusual. Angiographic findings are conclusive and consist of contrast medium extravasation from branches of the uterine artery (Fig 7c). This condition can be definitely treated with transcatheter arterial embolization.
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Figure 7a. Direct rupture of an arterial branch in a 33-year-old woman. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Transverse gray-scale US image shows a markedly enlarged uterus (arrowheads) with large, heterogeneous hematomas (arrows) in the uterine cavity. (b) Longitudinal color Doppler US image shows slowly moving blood without fluctuation (arrows) within the hematomas, a finding suggestive of extravascular blood. (c) Left internal iliac angiogram shows extravasation of contrast medium (arrows) from branches of the left uterine artery. The uterus (arrowheads) is markedly enlarged by the hematomas. After arterial embolization with absorbable gelatin sponge pledgets, the bleeding stopped and did not recur.
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Figure 7b. Direct rupture of an arterial branch in a 33-year-old woman. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Transverse gray-scale US image shows a markedly enlarged uterus (arrowheads) with large, heterogeneous hematomas (arrows) in the uterine cavity. (b) Longitudinal color Doppler US image shows slowly moving blood without fluctuation (arrows) within the hematomas, a finding suggestive of extravascular blood. (c) Left internal iliac angiogram shows extravasation of contrast medium (arrows) from branches of the left uterine artery. The uterus (arrowheads) is markedly enlarged by the hematomas. After arterial embolization with absorbable gelatin sponge pledgets, the bleeding stopped and did not recur.
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Figure 7c. Direct rupture of an arterial branch in a 33-year-old woman. The patient had massive vaginal bleeding during D&C for a therapeutic abortion. (a) Transverse gray-scale US image shows a markedly enlarged uterus (arrowheads) with large, heterogeneous hematomas (arrows) in the uterine cavity. (b) Longitudinal color Doppler US image shows slowly moving blood without fluctuation (arrows) within the hematomas, a finding suggestive of extravascular blood. (c) Left internal iliac angiogram shows extravasation of contrast medium (arrows) from branches of the left uterine artery. The uterus (arrowheads) is markedly enlarged by the hematomas. After arterial embolization with absorbable gelatin sponge pledgets, the bleeding stopped and did not recur.
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Treatment with Transcatheter Arterial Embolization
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Transcatheter arterial embolization has emerged as a highly effective technique for controlling obstetric and gynecologic hemorrhage (15). Its advantages include outstanding success rates, low complication rates, avoidance of surgical risks, and preservation of fertility (15). Complications of transcatheter arterial embolization are extremely uncommon, and the complication risk is negligible when it is performed by expert interventional radiologists.
The steps of a typical embolization procedure are as follows: By using the Seldinger technique through the common femoral artery, initial pelvic angiography is performed, followed by selective internal iliac angiography and uterine angiography on the side presumed to be affected at US examination. Embolic materials are carefully introduced into the uterine artery or other feeding artery until stasis of flow is confirmed angiographically. Ipsilateral internal iliac angiography is repeated to exclude the possibility of additional feeding arteries, which occasionally become apparent only after the major feeding artery is occluded. The contralateral internal iliac artery and uterine artery are then examined in the same manner. Embolization of the contralateral uterine artery is performed because of the possibility of cross-filling and is followed by contralateral internal iliac angiography. If bleeding does not stop or the vascular abnormality does not disappear, other feeding arteries, such as the ovarian artery, inferior epigastric artery, or middle sacral artery, should be examined. The treatment is usually successful after one or two sessions.
Although various embolization materials have been used, including gelatin sponge, coils, isobutyl-2-cyanoacrylate, detachable balloons, thrombin, and polyvinyl alcohol, most iatrogenic uterine vascular abnormalities can be safely and effectively treated by embolization with pledgets of absorbable gelatin sponge (Gelfoam) (5,15). Absorbable gelatin sponge pledgets are usually the material of choice for embolization of acquired AVMs, pseudoaneurysms arising from small branches, cases of combined AVM and pseudoaneurysm, and direct arterial rupture because of the ease of delivery and the duration of effect. The 3–5-week duration of occlusion by absorbable gelatin sponge pledgets is sufficient to stop hemorrhage while still permitting slow development of collateral vessels (31). For occlusion of the proximal vessel in cases of pseudoaneurysms arising from lar
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Abstract
Introduction
