AJR 2003; 180:1567-1570
© American Roentgen Ray Society
MR Imaging–Guided Adrenal Biopsy Using an Open Low-Field-Strength Scanner and MR Fluoroscopy
Claudius W. König1,
Philippe L. Pereira,
Jochen Trübenbach,
Jan Fritz,
Stephan H. Duda,
Fritz Schick and
Claus D. Claussen
1 All authors: Department of Diagnostic Radiology, Eberhard-Karls-University of
Tuebingen, Hoppe-Seyler-Str.3, D-72076 Tuebingen, Germany.
Received March 27, 2002;
accepted after revision October 28, 2002.
Address correspondence to C. W. König
(claudius.koenig{at}med.uni-tuebingen.de).
Abstract
OBJECTIVE. The aim of our study was to test the feasibility and
specific properties of MR imaging–guided adrenal biopsy using an open
0.2-T scanner and MR fluoroscopic fast imaging with steady-state free
precession sequences.
CONCLUSION. MR imaging–guided biopsy of the adrenal gland is
feasible and safe. In all patients, appropriate specimens were obtained with
full diagnostic yield and accuracy. MR fluoroscopy is particularly useful to
establish an oblique paravertebral access without pleural transgression. For
final needle placement, supplementary breath-hold multislice sequences are
required in most cases.
Introduction
Abdominal biopsy is routinely performed with sonographic or CT guidance.
However, accessing targets located subphrenically without passing the pleural
space can be difficult using these modalities. High lesion contrast resolution
and multiplanar imaging capabilities have rendered MR imaging valuable for
this area, particularly after the introduction of open configuration MR
systems [1] and interactive
continuous real-time imaging sequences (MR fluoroscopy). Subsecond imaging
with rapid image reconstruction has been established mainly on high-field
imagers [2] because those
techniques have low signal-to-noise ratios in low-field-strength units. We
present our experience with MR imaging–guided adrenal biopsy using a
fast imaging with steady-state free precession (FISP) sequence for near
real-time MR fluoroscopy in an open configuration low-field system.
Subjects and Methods
MR imaging–guided adrenal biopsies were performed in seven patients
(four men, three women; 47–74 years old; mean age, 62 years). Three had
a known history of nonpulmonary malignancy, two had imaging findings
suspicious for bronchogenic carcinoma, and two were referred with newly
diagnosed potentially malignant extraadrenal tumors. Six of seven adrenal
tumors were located on the left side. Tumor size ranged from 2.4 x 1.2
cm to 10 x 5 cm. Five lesions were nearly spherical, measuring
2.8–5.5 cm (mean, 3.9 cm) in the short axis. Endocrinologic screening
was performed before biopsy in patients with suspected pheochromocytoma. The
study was approved by our institutional review board, and written informed
consent was obtained from all patients before biopsy.
We used an open configuration clinical 0.2-T MR scanner (Magnetom Open,
Siemens, Erlangen, Germany) equipped with 15 mT/m gradients and dedicated
interventional accessories such as flexible ring-shaped receiver coils, a
fiber optic light source, and a shielded liquid crystal display in-room
monitor [1]. In one patient,
diagnostic imaging was performed with the patient in a supine position and
then in a prone position before biopsy. The other patients were primarily
placed in a prone (n = 5) or semilateral (n = 1) position.
Breath-averaged T1-weighted spin-echo and T2-weighted fast spin-echo sequences
(11 slices, 6-mm thickness, 2-mm interslice gap) were applied for anatomic
survey. Supplementary breath-hold sequences (expiration) were performed in a
transverse and sagittal orientation, using T1-weighted fast low-angle shot (TE
range, 7–12) and breath-hold T2-weighted fast spin-echo sequences
(echo-train length, 17). Slice thickness was reduced to 5 mm if necessary.
Additional sagittal images of the posterior pleural space obtained in deep
inspiration were used for access planning. Contrast agent (gadopentetate
dimeglumine) was applied in only one patient for diagnostic purposes before
biopsy. The basic principles of MR imaging–guided biopsy have been
described elsewhere [1,
3]. After sterile draping,
local anesthetic administration and skin incision, we advanced an MR
imaging–compatible needle subcutaneously, and the table was moved into
the magnet. Cephalad navigation of the needle into the retroperitoneal space
was performed with MR fluoroscopy or conventionally with multislice sequences.
In the conventional mode, the cannula was placed in a stepwise fashion with
repeated image updating with a set of three to five slices (fast low-angle
shot or fast spin echo) centered parallel to the needle (scanning time,
7–16 sec). For fluoroscopic guidance, a single-slice FISP sequence
(TR/TE, 17.8/8.1; flip angle, 90°; matrix, 48–64 x 128;
rectangular field of view, 30–35 cm) in-plane with the desired needle
path was continually measured with immediate image reconstruction and shown on
the in-room liquid crystal display. An appropriate sagittal imaging plane was
chosen, displaying the pleural recess and the tumor itself or the renal
capsule close to the tumor to ensure that the kidney was not injured. The
cannula was aligned with the target and advanced during continuous near
real-time imaging. MR fluoroscopy was terminated after the needle was placed
deeply in the retroperitoneal space, and final positioning was performed with
repeated multislice sequences in most patients. Usually, the tumor was
centrally targeted.
In two patients, specific parts of the mass were selectively sampled. One
tumor revealed a target sign on contrast-enhanced CT; the other lesion was
heterogeneous because of acute eccentric adrenal hemorrhage 2 days before
biopsy (Figs. 1A,
1B,
1C,
1D). IV analgetics and
sedatives (pethidine hydrochloride, midazolam) were administered when
necessary. A coaxial biopsy system was used in six patients, consisting of a
16-gauge MR imaging–compatible trocar made of titanium alloy
(CoaxNeedle, MRI Devices Daum, Schwerin, Germany; Puncture Needle, Biopsy Gun
MRI, Somatex, Berlin, Germany) placed in front of the lesion, and a non-MR
imaging–compatible spring-loaded biopsy gun (ASAP 18-gauge, Boston
Scientific, Watertown, MA) for coaxial sampling of one or two biopsies. In one
patient, a single pass with a noncoaxial titanium gun (Biopsy Gun MRI,
16-gauge, MRI Devices Daum) was performed. Samples were fixed in formaldehyde
solution and sent to the pathologist. After needle withdrawal, T2-weighted
fast spin-echo imaging was performed to reveal short-term complications.
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Fig. 1A. —74-year-old man with symptomatic adrenal metastasis from
small cell lung cancer. Transverse T2-weighted fast spin-echo MR image (TR/TE,
5447/134) for biopsy planning shows acute hemorrhage (arrow).
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Fig. 1B. —74-year-old man with symptomatic adrenal metastasis from
small cell lung cancer. Sagittal fluoroscopic fast imaging with steady-state
free precession image shows needle guidance towards lesion
(arrow).
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Fig. 1C. —74-year-old man with symptomatic adrenal metastasis from
small cell lung cancer. Sagittal (C) and Paraaxial (D)
breath-hold T2-weighted fast spin-echo MR images (1856/105, 5 slices in 14
sec) before biopsy show sampling from nonhemorrhagic parts of lesion
(arrow, D).
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Fig. 1D. —74-year-old man with symptomatic adrenal metastasis from
small cell lung cancer. Sagittal (C) and Paraaxial (D)
breath-hold T2-weighted fast spin-echo MR images (1856/105, 5 slices in 14
sec) before biopsy show sampling from nonhemorrhagic parts of lesion
(arrow, D).
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Results
Tissue samples sufficient for histopathologic diagnosis were obtained in
all patients. Adrenal tumors were malignant in four of seven patients.
Malignancy was correctly diagnosed or excluded in each case. A specific
histopathologic diagnosis could be established in six of seven patients. In
one patient, specimens containing complete necrosis and fibrin were obtained,
and nested polymerase chain reaction analysis revealed Mycobacterium
genavensae. These findings corresponded well to the patient's history of
high-dose chemotherapy for lymphoma with subsequent leukopenia and atypical
mycobacteriosis. The mass remained unchanged in size until the patient's
death.
The other six diagnoses were adrenal metastasis (n = 3, each with
an immunoprofile correctly identifying the primary tumor), pheochromocytoma
(n =1), and adrenal tissue (n = 2). Diagnosis of adrenal
adenoma was confirmed on follow-up CT in both patients with adrenal tissue at
MR imaging biopsy. The diagnosis of pheochromocytoma was confirmed surgically.
The tumor was classified as nonfunctioning and nonmalignant. This finding
explained the unremarkable endocrinologic screening results before biopsy.
MR fluoroscopy was performed in all except one case (n = 6),
starting with the second patient in our series. MR fluoroscopy was used in
these six patients for interactive definition of skin entry site
(fingerpointing). Needle angulation and advancement into the retroperitoneum
were performed with MR fluoroscopic guidance in five patients, with particular
focus on avoidance of the pleural recess. The only patient in whom MR
fluoroscopy was deemed unnecessary for this purpose had a tumor far away from
the pleura (Fig. 2). Entire
fluoroscopic needle-tracking into the lesion was performed in two of five
patients, one with the largest tumor in this series (10 x 5 cm) (Figs.
3A,
3B,
3C,
3D). MR fluoroscopy was
additionally, but not exclusively, applied for needle navigation in the
retroperitoneum in another two of five patients. In these patients, the final
steps of cannula placement were guided with conventional-mode breath-hold
imaging in a biplanar angulation for navigation in close vicinity to the
kidney and spleen. In the remaining patient, MR fluoroscopy was used only to
avoid the pleura. Further guidance was performed conventionally because of
anatomic narrowness caused by splenomegaly.
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Fig. 2. —53-year-old woman with pheochromocytoma with needle placement
before biopsy. Transverse unenhanced T1-weighted three-section breath-hold
fast low-angle shot MR image (TR/TE, 54/7.4; flip angle, 70°; scanning
time, 7 sec) shows stylet partially withdrawn in 16-gauge cannula for detailed
depiction of its tip.
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Fig. 3A. —47-year-old man with large adrenal metastasis from
adenocarcinoma of lung. Sagittal MR fluoroscopic fast imaging with
steady-state free precession image (TR/TE, 17.8/8.1; flip angle, 90°)
shows angulated approach with 13-gauge cannula.
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Fig. 3D. —47-year-old man with large adrenal metastasis from
adenocarcinoma of lung. MR fluoroscopic image shows needle advancement into
lesion with easy avoidance of pleura and kidney (asterisk). Only two
fluoroscopic series (each with 23-sec scanning time for 20 images) were
needed. Note that needle conspicuity and anatomic survey were not compromised
by low spatial resolution (48 x 128 pixels) of MR fluoroscopic
sequence.
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Generally, application of MR fluoroscopy for needle-tracking in the
retroperitoneal fat was hampered by lateral deflection of the needle tip
during respiratory motion. This deflection precluded the use of thin slices
for needle-tracking. Selections of 6- to 8-mm slice thicknesses resulted in
better signal-to-noise ratio and artifact-tracking but also raised the risk
for unrecognized needle deviation due to partial volume effects. For the same
reasons, adjacent structures, mainly the kidneys, were also occasionally
displayed in the tracking slice and mimicked the risk of needle injury. In
this case, biplanar breath-hold multislice imaging was indispensable to
clarify anatomic relations.
The guiding procedure could be performed completely inside the magnet in
six of seven patients. The only table movements necessary were for insertion
of (non-MR imaging–compatible) biopsy guns in these patients. Time
between the first images after needle insertion and the last image before
needle withdrawal (needle time) varied from 13 min for the largest to 40 min
for the smallest tumor, with an average of 25.8 min. Major complications did
not occur.
Discussion
Several techniques have been proposed to obviate pleural transgression in
CT-guided adrenal biopsy, such as using the ipsilateral decubitus position,
triangulation, gantry tilting, an anterior or transhepatic approach, and
saline injection [4].
Sonographic guidance is usually limited to fine-needle aspiration via a
transabdominal approach. Recently MR imaging guidance has been introduced to
facilitate a markedly angulated approach to subphrenic targets
[1]. To the best of our
knowledge, no report specifically dedicated to MR imaging–guided adrenal
biopsy using MR fluoroscopy has been previously published. Adrenal biopsy
seems particularly amenable to MR fluoroscopy because of high adrenal contrast
in the retroperitoneal fat, abolishing limitations in lesion contrast usually
inherent in steady-state precession sequences on low-field scanners.
The favorable outcome achieved in our preliminary study revealing full
diagnostic yield and accuracy without notable complications is in line with
previous reports from CT-guided biopsy
[5,
6,
7], suggesting that MR
imaging–guided biopsies can be as safe and accurate as CT-guided
procedures. This finding is not surprising because MR imaging guidance
primarily affects the needle pass, but tissue sampling itself is essentially
comparable to CT-guided procedures.
Key advantages of MR imaging versus CT guidance are the ability to
establish a cephalad approach by sagittal monitoring of the needle course and
to have permanent access to the patient during imaging (hands-on technique)
without exposure of the radiologist to radiation. The true extension of the
posterior costophrenic sulcus and the target moving with respiration can be
depicted near real time. MR fluoroscopy was particularly useful to determine
an appropriate needle angulation during transgression of the extraperitoneal
back muscles because further needle angulation can be limited after the ribs
are crossed in sturdy patients. MR fluoroscopy further aided to some degree in
needle tracking in the retroperitoneal fat.
However, in close vicinity to the kidney or spleen, MR fluoroscopic guiding
was not considered accurate enough; thus, stepwise guidance with conventional
breath-hold multislice imaging was indispensable in these situations.
Exclusive MR fluoroscopic guidance is justified only in patients with large
tumors. Spatial resolution was considerably reduced to a 48 x 128 matrix
to provide a frame rate of virtually one image per second, even improving
needle conspicuity and anatomic survey. This type of MR fluoroscopy sequence
proved to be sufficient for regions with intrinsically high lesion contrast
like the adrenals embedded in fatty tissue. A similar technique based on
T2-like refocused steady-state precession could also be applied if available
[8]. Subsampling techniques
continuously updating the lower frequency domains of k-space (keyhole, LoLo,
[2,
9,
10]) seem to be less promising
in areas moving with respiration.
Multiplanar imaging is another pivotal facility of MR imaging guidance.
Precise alignment of the imaging plane to the angulated cannula aids in
appropriate needle depiction particularly in close vicinity to vital
structures like the kidney, spleen, and large vessels. Biplanar imaging is
indispensable for accurate needle placement before biopsy to avoid missampling
in small adrenal tumors. Chemical-shift techniques can, to some extent, also
be applied in low-field systems, potentially obviating biopsy in case the
tumor fits the benign criteria.
Conversely, some limitations of MR imaging guidance must also be
considered. Needle-artifact size strongly depends on angulation toward the
main magnetic field, which is vertically oriented in our magnet. Thus needle
angulation away from the vertical line is not only favorable to avoid the
pleural space but is crucial to maintain needle contrast. Biplanar imaging
with repeated adjustment of slice orientation is time-consuming and outweighs
time-savings achieved by the hands-on technique. Bony structures are less
conspicuous on MR imaging than on CT, and they must be thoroughly identified
in the planning sequences.
Irrespective of the imaging modality, biopsy of moving targets requires the
patient's cooperation in breathing. With MR imaging guidance, respiratory
motion can be tolerated to some extent using MR fluoroscopy, but precise
needle-positioning finally requires breath-hold imaging. Thus, patients
apparently unable to consistently suspend respiration should not be referred
for MR imaging biopsy, and IV analgesics rather than sedatives should be
applied to maintain the patient's consciousness. In this study, non-MR
imaging–compatible disposable biopsy guns were predominantly used
because of superior specimen quality compared with that collected with
titanium tools [11]. The
disposable guns can be easily handled in or near the low-field magnet because
the ASAP gun contains a relatively low amount of steel. Obviously, precautions
must be taken to prevent harm to the patient if ferromagnetic tools are
introduced to the MR imaging suite.
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Abstract
Introduction
