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Fowler et al.
Adrenal Artery Embolization
A
drenal artery embolization is a Adrenal arteries are of small caliber, can
minimally invasive procedure that be visualized at catheter aortography in 57–
can be used as an alternative or 92% of patients without adrenal disease [3],
adjunct to surgery [1]. Because and can occasionally be seen on CT angio-
this procedure is rarely encountered in routine grams of the abdomen acquired with small
clinical practice, published reports of its use slice thickness (Figs. 1B–1E). Further visu-
are limited to case reports and small case se- alization of the subsequent branches of these
ries. The purpose of this review is to describe arteries is beyond the resolution of catheter
adrenal arterial anatomy and the indications, angiography. Most divide into 10–50 smaller
outcomes, and technical considerations for branches over the capsule [6, 7].
adrenal artery embolization. Small capsular arteries form a capsular
plexus from which relatively straight cap-
Arterial Supply to the Adrenal Gland illaries pass through the zona fasciculata to
Proper interpretation of adrenal arteriograms form a deep vascular plexus of capillary si-
obtained for embolization relies on a thorough nusoids near the zona reticularis. They end so
Keywords: adrenal metastasis, adrenal tumor, knowledge of the complex vascular supply to abruptly that it has been referred to as a vas-
aneurysm, retroperitoneal hemorrhage, transarterial
embolization, trauma
the adrenal gland. The adrenal gland classical- cular dam [7]. This configuration is one pos-
ly has three arterial sources (Fig. 1A). Superior sible reason that the adrenal gland is particu-
DOI:10.2214/AJR.12.9507 adrenal arteries, which are often multiple, sup- larly prone to hemorrhagic necrosis [8].
ply the superomedial gland and arise almost ex- Because of the complex vascular supply to
Received September 22, 2012; accepted after revision
clusively from the inferior phrenic artery [2]. In the adrenal gland by three arteries, emboli-
January 7, 2013.
rare instances, they arise from the aorta, celiac zation of a single artery will not likely result
Presented as an educational poster (abstract 327) at the axis, or an intercostal artery [2, 3]. The middle in infarction of the entire gland. If infarction
2012 annual meeting of Society of Interventional adrenal artery supplies the anteromedial gland does occur, the presence of an intact contra-
Radiology, San Francisco, CA. and most often arises from the lateral aspect of lateral gland will prevent the development of
1Mallinckrodt Institute of Radiology, Washington University, the aorta [2]. Less frequently, it originates from life-threatening adrenal insufficiency.
660 S Euclid Ave, Campus Box 8131, St. Louis, MO 63110. the inferior phrenic artery, renal artery, or celiac
Address correspondence to S. K. Kim (kims@mir.wustl.edu). axis [2, 3]. Often it is replaced by the superior Indications for Adrenal Artery
or inferior adrenal artery [2]. Inferior adrenal Embolization
2 Mid-South Imaging and Therapeutics, Memphis, TN.
arteries supply the posterior and inferolateral A variety of indications exist for adrenal
CME/SAM gland, which is the thickest portion of the gland, artery embolization. Most involve oncologic
This article is available for CME/SAM credit. and most often arise from the superior aspect of applications for palliation, such as pain relief,
the renal artery [2]. In rare instances, they arise reduction of tumor bulk, and preoperative re-
AJR 2013; 201:190–201 from the aorta, a polar renal artery, or inferior duction of tumor vascularity. Emergency em-
0361–803X/13/2011–190
phrenic artery [2, 3]. The left inferior adrenal bolization for hemostasis of ruptured tumors
artery has also been reported to arise from the with retroperitoneal hemorrhage is an addi-
© American Roentgen Ray Society celiac axis or gonadal artery [4, 5]. tional oncologic application. Adrenal artery
Dead at 3 mo of disease
progression and brain
Alive at least 18 mo
Outcome
Alive at least 3 mo
Alive at least 1 mo
Alive at discharge
Alive at least 28 d
Alive at least 21 d
Alive at least 11 d
from 12 to 8 cm
Palliative Pain Relief and Tumor Debulking
metastasis
Large adrenal tumors can be painful for
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NRa
Coil
Coil
NR
embolization, Adrenalectomy
embolization, Adrenalectomy
embolization, adrenalectomy
embolization, adrenalectomy
embolization, adrenalectomy
embolization, adrenalectomy
embolization, chemotherapy
adrenalectomy
adrenalectomy
Adrenocortical neoplasmb
Metastatic hepatocellular
Pheochromocytoma
Pheochromocytoma
Pheochromocytoma
Pheochromocytoma
Myelolipoma
carcinoma
38a
68
54
32
67
37
37
62
42
31
51
M
F
192
Hemorrhagic Adrenal Masses
TABLE 2: Reported Cases of Embolization Used for Adrenal Hormone Suppression
Source Sex Age (y) Pathologic Finding Treatment Embolization Agent Outcome
Bunuan et al. 1978 [45] M 45 Pheochromocytoma Right inferior adrenal artery Gelatin sponge Asymptomatic at least 5 mo
embolization, adrenalectomy (Gelfoam, Pfizer)
Horton et al. 1983 [46]; M 13 Pheochromocytoma Left adrenal artery embolization, Polyvinyl alcohol foam, gelatin sponge Asymptomatic more than 1 y
Hrabvosky et al. 1982) [68] adrenalectomy (Gelfoam, Pfizer)
O’Halpin et al. 1984 [47] M 35 Pheochromocytoma (inoperable) Left middle and inferior adrenal Bucrylate-iophendylate (Myodil, Initial response then
artery embolization Glaxo) recurrence and death after
6 wk
Fowler et al.
Hokotate et al. 2003 [48] 8 M, 25 F 28–68 Aldosteronoma Adrenal artery embolization High-concentration ethanol-iohexol 82% success rate
D’Angelo 2007 [49] F 56 Aldosteronoma Left adrenal artery embolization Alcohol–iodized oil (Lipiodol, Guerbet) Asymptomatic 4 mo
Uflacker et al. 1986 [50] F 32 Adrenal cortical carcinoma, Right middle adrenal artery Absolute ethanol Symptom and hormone
Cushing syndrome embolization reduction for at least 1 y
O’Keeffe et al. 1988 [9] F 63 Adrenal cortical carcinoma, Left inferior adrenal and left Polyvinyl alcohol foam (Ivalon, Initial clinical and biochemi-
Cushing syndrome inferior phrenic artery Unipoint Industries) 150–590 μm cal response with relapse at
embolization 1y
Ueno et al. 1999 [66] F 45 Adrenal adenoma, Cushing Left inferior adrenal artery Ethanol-iohexol Symptom and hormone
syndrome embolization reduction for at least 9 mo
Ueno et al. 1999 [66] F 42 Adrenal adenoma, Cushing Right inferior adrenal artery Ethanol-iohexol Procedure aborted because
syndrome embolization of marked tachycardia and
hypertension
Inoue et al. 1993 [69] F 55 Adrenal hyperplasia, corticotropin- Left superior adrenal artery Absolute ethanol Symptom and hormone
dependent Cushing syndrome embolization reduction for at least 7 mo
Blunt et al. 1989 [70] F 51 Ectopic corticotropin syndrome from Bilateral superior and middle Dura mater, alcohol, miniature steel Asymptomatic at least 10 mo
medullary thyroid carcinoma adrenal artery embolization, coils
metyrapone, bilateral
adrenalectomy
Bourlet et al. 2007 [71] M 56 Ectopic corticotropin syndrome from Left inferior adrenal artery Trisacryl gelatin microspheres Symptom and hormone
medullary thyroid carcinoma embolization, hepatic artery (Embosphere Microspheres, reduction for at least 5 mo
chemoembolization, mitotane, Biosphere Medical) (900–1200 μm)
TABLE 3: Reported Cases of Traumatic Adrenal Hemorrhage Treated With Embolization
Source Sex Age (y) Mechanism of Injury Angiographic Findings Embolization Agent Outcome
Igwilo et al. 1999 [53] F 58 Motor vehicle Right inferior adrenal Platinum coil (3 mm/2 cm; Tornado, Cook) Alive at least 8 d
collision artery, extravasation
Dinc et al. 2002 [54] F 23 Motor vehicle Right inferior adrenal Polyvinyl alcohol particles (45–150 μm) Alive at least 4 mo
collision artery, extravasation
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Kish et al. 2004 [55] M 33 Fall from height, Inferior adrenal artery, N-butyl cyanoacrylate glue with Alive at least 3 wk
suicide attempt extravasation ethiodized oil
Ikeda et al. 2006 [56] M 50 Fall Right inferior adrenal Vortex microcoils (Boston Scientific) and Alive at least 3 mo
artery, extravasation interlocking detachable coils
Two reports [40, 44] have been published alone had an initial response then recurrence size and deep location in the retroperitone-
regarding the use of transarterial emboliza- of symptoms and died after 6 weeks [47]. Be- um. However, adrenal hemorrhage has been
tion for acute control of retroperitoneal hem- cause approximately 10% of pheochromocy- found in 13 of 50 (26%) autopsies of patients
orrhage due to adrenal gland metastases from tomas are malignant and embolization alone who died of severe blunt trauma to the chest
hepatocellular carcinoma and non–small cell appears to be inadequate for long-term symp- or abdomen [51].
lung cancer. Yang et al. [40] used coil embo- tom and hormone control, surgical resection Several mechanisms have been proposed
lization before adrenalectomy, and Ambika et remains the definitive treatment of choice. to explain why adrenal hemorrhage occurs in
al. [44] used it as the sole treatment method. Primary aldosteronism (Conn syndrome) blunt trauma. The first mechanism involves
The former patient was alive 18 months after is caused by excessive secretion of aldoste- direct compression of the gland against the
treatment, and the latter died of overall disease rone from the outer layer (zona glomerulo- spinal column. The anterior surface of the
progression and brain metastasis 3 months af- sa) of the adrenal cortex and results in sec- right adrenal gland closely opposes the liv-
ter embolization. Figures 3 and 4 show the ondary hypertension and hypokalemia. Most er, and this may be why hemorrhage involv-
cases of two patients with retroperitoneal cases are caused by an adenoma, or so-called ing the right adrenal gland is more common
hemorrhage arising from adrenal gland metas- aldosteronoma. Adrenalectomy is the treatment than hemorrhage involving the left [51, 52].
tases (one with metastatic lung cancer and one of choice; however, ethanol embolization has Furthermore, most adrenal hemorrhages oc-
with metastatic melanoma) treated with tran- been used for patients refusing surgery and pa- cur on the same side as the side affected by
sarterial embolization to achieve hemostasis. tients at high risk of surgical complications [48, the blunt traumatic event, supporting the di-
49]. Hokotate et al. [48] reported on the larg- rect compression mechanism [51, 52]. A sec-
Adrenal Hormone Suppression est series, consisting of 33 cases of aldosterono- ond proposed mechanism is a secondary reac-
Reported cases of transarterial embolization ma treated with embolization. They reported an tion due to an acute increase in intraadrenal
for suppression of excess adrenal hormone 82% primary success rate using superselective venous pressure from compression of the in-
production (catecholamines, aldosterone, cor- adrenal arterial embolization with high-con- ferior vena cava. This again would be expect-
tisol) are summarized in Table 2. Endocrino- centration ethanol, compared with greater than ed to occur more commonly on the right be-
logically active adrenal tumors treated with 90% with open or laparoscopic adrenalectomy, cause the right adrenal vein drains directly into
embolization include pheochromocytoma, al- and observed no severe complications. the inferior vena cava whereas the left adre-
dosteronoma, adrenal cortical carcinoma, and Cushing syndrome can be caused by exces- nal vein first joins the left renal vein. Last, de-
adrenal adenoma. sive secretion of cortisol from the middle lay- celeration forces may shear small vessels that
Pheochromocytoma is a neuroendocrine tu- er (zona fasciculata) of the adrenal cortex and penetrate the gland capsule.
mor of the adrenal medulla that secretes exces- can result in central obesity, hypertension, At least four published case reports have
sive amounts of catecholamines. This tumor and insulin resistance. Transarterial emboli- described the successful treatment of isolated
can cause life-threatening hypertensive crisis zation has been used to treat corticotropin-in- adrenal artery hemorrhage after blunt trauma
and cardiac arrhythmia. The use of transarteri- dependent causes (adrenal adenoma, adrenal with embolization [53–56] (Table 3). The pro-
al embolization to deactivate an endocrinolog- cortical carcinoma) and corticotropin-depen- cedures described in these reports were per-
ically active tumor was reported first in 1978 dent causes (ectopic corticotropin syndrome formed with microcoils, PVA particles, and
and again in 1983 for patients with pheochro- from medullary thyroid carcinoma) of Cush- N-butyl cyanoacrylate glue. Figure 5 shows
mocytoma with the intended goals of reduc- ing syndrome (Table 2). Embolization was ef- a case of right inferior adrenal artery hem-
ing intraoperative and perioperative compli- fective in hormone and symptom control for orrhage treated with coil embolization in an
cations related to blood pressure control and two of the three patients with Cushing syn- 18-year-old male pedestrian struck by a mo-
decreasing the vascularity of the tumor to min- drome due to inoperable adrenal cortical car- tor vehicle. Follow-up CT after embolization
imize blood loss [45, 46]. Although the out- cinoma reported by O’Keeffe et al. [9] and for is helpful to document resolution of the hem-
comes for these patients were good with no the one patient reported by Uflacker et al. [50] orrhage and to exclude an underlying mass.
recurrence of symptoms after 5 months and for at least 1 year.
1 year after adrenalectomy, one patient with Iatrogenic Adrenal Hemorrhage
hypertension and heart failure due to inoper- Posttraumatic Adrenal Hemorrhage An iatrogenic cause of adrenal artery hemor-
able pheochromocytoma treated with bucry- The adrenal glands are relatively protect- rhage is also conceivable, yet to our knowledge
late (isobutyl-2-cyanoacrylate) embolization ed from blunt trauma because of their small no reports exist in the literature. Unintentional
from the remnant right inferior adrenal artery tery puncture with an 18-gauge puncture nee-
Alive at least 12 mo
Alive at least 11 mo
treated with glue and microcoils in a 35-year- dle in a single-wall modified Seldinger tech-
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Not reported
old woman who had undergone right adrenal- nique. A guidewire is passed centrally under
least 20 d
ectomy for adrenal cortical adenoma. fluoroscopic guidance, and a 6-French vascu-
lar sheath is placed and connected to a low-
Adrenal Artery Aneurysms pressure heparinized saline flush. Through the
Visceral artery aneurysms are uncommon sheath, a 5-French pigtail catheter can be used
Polyvinyl alcohol particles (355–500 μm) distally,
but have a high risk of rupture and life-threat- for nonselective aortography to define the ar-
ening hemorrhage, particularly for hyperten- terial supply to the adrenal gland. Because of
Coils (interlocking detachable and metric)
sive patients and pregnant women in the third the variable anatomy, additional arteriograms
Microcoils (2 × 20 mm fibered platinum)
trimester [57]. Aneurysms involving the adre- of the inferior phrenic and renal arteries are
Embolization Agent
nal arteries are particularly rare, there being obtained. For catheterization of the inferior
limited reports in the literature [58–63]. phrenic artery, main renal artery, and mid-
Spontaneous rupture may be related to dle adrenal artery originating from the aorta,
states of increased blood flow as seen dur- a 5-French SOS Omni (AngioDynamics), C2
ing pregnancy or uncontrolled hypertension Cobra (Terumo Medical), or Mickelson cath-
[57]. At least three published case reports eter (Cook Medical) can be used.
have described successful treatment of spon- For superselection, a 3-French microcath-
taneously ruptured adrenal artery aneurysms eter system is used with coaxial technique.
with embolization [58–60] (Table 4). These Examples include Mass Transit (Cordis) and
TABLE 4: Reported Cases of Adrenal Artery Aneurysms Treated With Embolization
reports all involved men with hypertension. Progreat (Terumo Medical) microcatheters
The embolic agents used included microcoils and GT (Terumo Medical) and Transcend
Left inferior adrenal artery aneurysm
with or without PVA particles. Coil emboli- (Boston Scientific) microguidewires. Digital
Left middle adrenal artery aneurysm
was also performed for active extravasation firm appropriate catheter placement. The em-
from the left middle adrenal artery found at bolic agent is administered by flow-control
catheter angiography in a 32-year-old preg- technique [65]. Postembolization angiography
with extravasation
with extravasation
nant (39 weeks) woman with retroperitoneal is performed to evaluate for additional arteries
hemorrhage; however, no direct evidence of that may be supplying the tumor.
Not reported
Spontaneous
Spontaneous
middle adrenal artery without evident aneu- choosing an embolic agent include the clini-
Cause
rysm formation. The patient was a 54-year- cal application and endpoint desired (perma-
Trauma
old man treated with gelatin sponge particle nent versus temporary occlusion), experience
and microcoil embolization. and preference of the radiologist, and cost
Pseudoaneurysm formation, which is con- and availability of the agent [1].
Age (y)
68
49
42
70
tained rupture of the vessel wall, can occur Permanent proximal vessel occlusion can
in cases of trauma, postbiopsy or postsurgical be achieved with microcoils. An advantage
Sex
complication, vascular invasion by malignant of coils over glue or gelatin sponge particles
M
tumor, and vasculitis secondary to adjacent is that they occlude the proximal part of the
inflammation [63]. It can result in massive artery and can preserve the distal and paren-
González Valverde et al. 2007 [59]
hemorrhage, and conventional treatment has chymal circulation. Use of coils may be prob-
been surgical ligation or resection of the an- lematic if the vessel is of small caliber or tor-
tuous. Coils have been predominately used
Manners et al. 2010 [58]
ly to occlude the main arterial supply to stop anterior spinal artery occurred at adrenal ar- terials with proven success include ethanol,
the acute bleeding, and the PVA particles are tery embolization for adrenal metastasis from PVA particles, microcoils, gelatin sponge,
used distally to prevent later recanalization hepatocellular carcinoma [12]. The spinal ar- and N-butyl cyanoacrylate glue. With care-
from the distal arterial collateral supply [58]. tery can originate from the middle adrenal ar- ful embolization technique to avoid nontarget
Gelatin sponge particles (Gelfoam, Pfiz- tery, and embolization was thus not performed embolization, patients tolerate the procedure
er) are the least expensive particulate embolic in a different patient with aldosteronoma to well with self-limited symptoms that can be
agent and have a temporary effect. They have avoid possible spinal infarction [48]. treated conservatively.
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been used to treat hemorrhagic adrenal mass- Precise microcoil placement is important.
es and to suppress the hormonal function of The proximal end of a 2 × 20 mm fibered Acknowledgments
pheochromocytomas (Tables 1 and 2). Mix- platinum coil placed in a left middle adrenal We thank G. M. Salazar (Division of Vas-
ing the particles with a contrast agent aids in artery for hemostasis due to vessel rupture in cular Imaging and Intervention, Massachusetts
visualization during placement, so nontarget a 32-year-old pregnant woman was noted to General Hospital, Harvard Medical School,
embolization can be identified immediately project into the aortic lumen at the ostium of Boston, MA), K. R. Kim (Department of Ra-
and the procedure terminated. the adrenal artery, indicating a more proxi- diology, University of North Carolina at Cha-
Semipermanent particulate agents include mal location of coil deployment than intend- pel Hill, Chapel Hill, NC), and J. H. Shin (De-
PVA and trisacryl gelatin microspheres (Em- ed [64]. Because the coil was thought to be a partment of Radiology and Research Institute
bosphere Microspheres, Biosphere Medical). potential source of thrombus, it was removed of Radiology, University of Ulsan College of
These have mainly been used for tumor em- with a gooseneck snare 26 days after emboli- Medicine, Asan Medical Center, Seoul, Korea)
bolization and traumatic adrenal hemor- zation without complication. for contributing images.
rhage (Tables 2 and 3). PVA particles can Patients generally tolerate adrenal artery
clump and occlude the catheter, which is a embolization well with typically self-limited References
disadvantage of this agent. Trisacryl gelatin symptoms that can be treated conservative- 1. Ginat DT, Saad WE, Turba UC. Transcatheter re-
microspheres are less susceptible to clump- ly. Mild to moderate flank pain lasting less nal artery embolization for management of renal
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crylate (isobutyl-2-cyanoacrylate), and N-bu- the diaphragm from embolization of the in- phrenic, ureteral and gonadal arteries: a statistical
tyl-2-cyanoacrylate. These agents have low ferior phrenic artery [48]. Persistent hiccups analysis based on 185 dissections and review of
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Inferior
Superior adrenal phrenic
artery artery
Fig. 1—40-year-old woman undergoing CT evaluation
for hereditary hemorrhagic telangiectasia.
Adrenal Middle A, Diagram shows classic arterial anatomy of adrenal
gland adrenal
artery
gland.
B, CT angiogram shows inferior phrenic (arrow),
middle adrenal (asterisk), and inferior adrenal
Inferior Aorta
(arrowhead) arteries. Superior adrenal arteries were
adrenal too small to visualize.
artery C–E, T31-year-old women undergoing CT evaluation
Kidney for living renal donor.
C, Transverse maximum-intensity-projection (MIP)
Renal artery CT image shows right inferior phrenic artery (arrow)
arising from celiac axis. Left inferior phrenic artery
(arrowhead) also is evident. Superior adrenal arteries
were too small to visualize.
D, Transverse MIP CT image shows right middle
adrenal artery arising from aorta.
E, Coronal CT image of right adrenal gland shows
small inferior adrenal arteries.
A B
C D E
A B
Fig. 2—43-year-old woman with metastatic melanoma and bilateral flank pain.
A, Coronal CT image shows bilateral adrenal gland metastases.
B, Arteriogram of right middle adrenal artery shows tumor blush and neovascularity (arrow). Adrenal artery
embolization for pain palliation was performed with 300- to 500-μm polyvinyl alcohol particles.
C, Postembolization arteriogram shows cessation of flow in right middle adrenal artery. Embolization was also
performed on left middle adrenal artery (not shown).
A B C
Fig. 3—58-year-old man with metastatic lung cancer and left flank pain.
A, CT image shows bilateral adrenal masses and left retroperitoneal hemorrhage.
B, Left middle adrenal arteriogram shows contrast extravasation from inferior branch (arrow) of left middle adrenal artery and tumor staining from superior branch
(arrowhead).
C, Angiogram obtained after polyvinyl alcohol particle (300–500 μm) embolization shows no extravasation from inferior branch and minimal residual tumor staining.
B C
Fig. 4—38-year-old woman with metastatic melanoma and left flank pain.
A, CT image shows left retroperitoneal hemorrhage and left adrenal mass.
B, Angiogram shows left superior adrenal artery (arrow) arising from left inferior phrenic artery and contrast
blush (arrowheads) in region of left adrenal hemorrhagic mass.
C, Angiogram obtained after polyvinyl alcohol particle (300–500 μm) and coil embolization (two 3-mm platinum
microcoils [Tornado, Cook]) shows complete stasis of flow in left superior adrenal artery.
A B
C D
Fig. 5—18-year-old male pedestrian struck by motor vehicle. (Courtesy of Kim KR, University of North Carolina
at Chapel Hill, NC)
A, Coronal CT image shows lacerations of right hepatic lobe and right kidney, large perinephric and
retroperitoneal hematoma, and right adrenal hematoma with active extravasation.
B, Right inferior adrenal arteriogram via renal artery shows contrast extravasation (arrow).
C, Right renal arteriogram obtained after coil embolization of right inferior adrenal artery shows additional site
of active extravasation (arrow) from small artery off proximal portion of right renal artery.
D, Angiogram obtained after microcoil embolization shows complete occlusion of right inferior adrenal artery
and small renal artery branch.
A B C
Fig. 6—35-year-old woman who has undergone right adrenalectomy for adrenal cortical adenoma. (Courtesy of Shin JH, University of Ulsan College of Medicine, Asan
Medical Center, Seoul, Korea)
A, CT image shows hematoma in right adrenal resection bed with central active extravasation.
B, Right renal arteriogram shows contrast extravasation from remnant right inferior adrenal artery (arrow).
C, Angiogram obtained after embolization with glue and microcoils (arrowhead) shows complete occlusion of right inferior adrenal artery.
A B C
Fig. 7—54-year-old man with spontaneous adrenal hemorrhage. (Courtesy of Salazar GM, Massachusetts General Hospital, Harvard Medical School, Boston, MA)
A, CT image shows right adrenal hematoma extending into right anterior pararenal space with active extravasation (arrow).
B, Right middle adrenal arteriogram from aorta shows contrast extravasation (arrows).
C, Angiogram obtained after gelatin sponge and microcoil embolization shows complete occlusion of right middle adrenal artery.
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