AJR 2001; 176:155-158
© American Roentgen Ray Society
Diagnosis of Symptomatic Intestinal Metastases Using Transabdominal Sonography and Sonographically Guided Puncture
Hans Peter Ledermann1,
Christoph Binkert2,
Eckhart Fröhlich3,
Norbert Börner4,
Christoph Zollikofer5 and
Gerd Stuckmann5
1
Department of Radiology, University Hospital Basel, Petersgraben 4, 4031
Basel, Switzerland.
2
Department of Radiology, University Hospital Balgrist, Forchstr. 340, 8008
Zürich, Switzerland.
3
Department of Internal Medicine, Karl Olga Krankenhaus, Schwarenbergstr. 7,
70190 Stuttgart, Germany.
4
Praxis Innere Medizin und Gastroenterologie, Parcusstr. 8, 55116 Mainz,
Germany.
5
Department of Radiology, Kantonsspital Winterthur, Brauerstr. 15, 8400
Winterthur, Switzerland.
Received March 9, 2000;
accepted after revision June 8, 2000.
Address correspondence to H. P. Ledermann, c/o Mark E. Schweitzer,
Department of Radiology, Thomas Jefferson University Hospital, 111 S. 11th
St., 3390 Gibbon, Philadelphia, PA 19107.
Abstract
OBJECTIVE. We studied the sonographic findings of symptomatic
intestinal metastases and the use and safety of subsequent sonographically
guided 22-gauge fine-needle aspiration or 18-gauge core biopsy.
CONCLUSION. Symptomatic intestinal metastases can be diagnosed by
transabdominal sonography. Extensive hypoechoic segmental bowel wall
thickening with loss of stratification and intussusception can be observed.
Sonographically guided fine-needle aspiration or 18-gauge core biopsy
performed at the end of the examination allows definite diagnosis and is a
safe procedure.
Introduction
Secondary involvement of the bowel typically occurs well into the course of
metastatic cancer, and most patients have metastases to sites other than the
gastrointestinal tract. Malignant melanoma, breast cancer, and bronchial
cancer show a predilection to metastasize hematogenously to the
gastrointestinal tract. Sixty percent of patients with malignant melanoma had
gastrointestinal metastases in an autopsy series
[1], whereas 14% and 10% of
patients with lung and breast cancer respectively were found to have
gastrointestinal metastases at autopsy
[2,
3]. Most patients with
gastrointestinal metastases have no symptoms or only nonspecific abdominal
symptoms [2]. Therefore,
gastrointestinal metastases are often not suspected, and only a minority of
these secondary tumors are diagnosed after radiologic examination or endoscopy
[4]. Because modern cancer
therapy leads to prolonged survival of patients with metastatic disease, the
number of patients with symptomatic gastrointestinal metastases may
increase.
Transabdominal sonography is often used to examine cancer patients with
abdominal pain because liver metastases, lymph node enlargement,
hydronephrosis, and ascites are readily diagnosed as potential sources of
nonspecific abdominal symptoms. Intestinal metastases, however, are usually
revealed on CT or small-bowel enema because most radiologists do not examine
the gastrointestinal tract by transabdominal sonography. We report seven
patients in whom transabdominal sonography allowed diagnosis of symptomatic
bowel metastases. Sonographically guided bowel wall puncture allowed
pathologic proof in five of these patients.
Materials and Methods
We retrospectively reviewed the reports of transabdominal sonography from
January 1992 until December 1998 to select all cases in which transabdominal
sonography allowed the diagnosis of intestinal metastases. Seven cases with
documented transabdominal sonography and complete clinical data were found.
The results of sonographically guided bowel punctures, clinical data, and
clinical history were reviewed for each patient. Patient age ranged from 49 to
71 years (mean, 59.3 years); four patients were men and three, women. All
patients had a known primary malignancy: malignant melanoma (n = 4),
bronchial carcinoma (n = 2), and gastric carcinoma (n = 1).
Six patients were suffering from advanced disease with metastases in other
organs. One patient suffering from malignant melanoma had local lymph node
metastases. All patients were referred to abdominal sonography as a first
screening examination after admission to the hospital with the following
abdominal symptoms: intermittent lower gastrointestinal bleeding (n =
3), acute peritonitis (n = 2), and abdominal pain (n = 2).
Sonography was performed on a DRF 400 scanner (Diasonics, Milpitas, CA) in two
patients and on an XP 128 scanner (Acuson, Mountain View, CA) in five
patients. Curved 3.5- and 3.75-MHz probes were initially used in all patients.
Four lesions were additionally examined with a 7-MHz curved-array probe.
Besides 4-hr fasting, no special preparation was undertaken for sonography or
sonographically guided puncture.
Sonographically guided fine-needle aspiration (n = 5) and
additional biopsies (n = 2) were performed during the initial
sonography with a standard aseptic technique and local anesthesia (10 mL of 1%
lidocaine hydrochloride) but without conscious sedation. Fine-needle
aspiration was performed with Chiba needles ranging from 11 to 15 cm in length
with a diameter of 0.7 mm (22 gauge). Multiple aspiration passes were
performed in each patient. If aspiration was insufficient, one or two cores
were obtained via an 18-gauge biopsy gun at the same session. All punctures
were performed with needle guides in a plane tangential to the bowel to obtain
a long sample of the affected bowel wall
(Fig. 1). Because the needle
does not transgress the lumen, the mucosa is not violated. Emergent surgery
was performed in two patients with acute peritonitis without prior fine-needle
aspiration or biopsy. Five patients had fine-needle aspiration. Two of these
patients had additional 18-gauge core biopsies during the same examination
because fine-needle puncture resulted in insufficient aspiration. Cytologic
and histologic results from sonographically guided puncture were later
confirmed by postoperative histology in two patients.
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Fig. 1. —Sonographically guided 18-gauge core biopsy in 53-year-old
woman with metastasis to ascending colon from gastric cancer. Transverse
sonogram of ascending colon shows diffusely thickened wall. Note optimal
placement of 18-gauge core biopsy device with tangential approach to bowel
without violation of hyperechoic narrowed lumen (open arrow).
Trajectory of needle is indicated with dashed line. Tip of needle is marked
with solid white arrow.
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Results
Striking segmental hypoechoic bowel wall thickening ranging from 1.2 to 4
cm in diameter (mean diameter, 2.4 cm) was found in six patients. The affected
bowel segments showed no peristalsis, and bowel wall stratification was
completely destroyed (Figs.
2A,2B
and
3A,3B).
Ileoileal invagination with a typical "ring in ring" sign (Fig.
4A,4B,4C,4D)
was seen in one patient with a mucosal metastasis from malignant melanoma. Six
metastases were found in the small bowel (ileum, n = 3; jejunum,
n = 1; location not known, n = 2); one metastasis was found
in the ascending colon.
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Fig. 2A. —57-year-old man with metastatic malignant melanoma who
presented with acute peritonitis. Transverse sonogram of ileal metastasis
shows marked hypoechoic thickening of bowel wall (as much as 1.5 cm in
diameter) and loss of normal stratification. Note slitlike luminal narrowing
with hyperechoic gas and adjacent lymph node between crosses.
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Fig. 2B. —57-year-old man with metastatic malignant melanoma who
presented with acute peritonitis. Pathologic specimen after resection confirms
marked segmental bowel wall thickening with narrowing of lumen.
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Fig. 3A. —61-year-old woman with bronchial carcinoma who presented with
nonspecific intermittent right lower quadrant pain due to sonographically
diagnosed ileal metastasis. Transverse sonogram of terminal ileum shows
excessive segmental hypoechoic bowel wall thickening as much as 1.8 cm in
diameter with loss of stratification and peristalsis.
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Fig. 3B. —61-year-old woman with bronchial carcinoma who presented with
nonspecific intermittent right lower quadrant pain due to sonographically
diagnosed ileal metastasis. CT scan confirms concentric thickening of terminal
ileum.
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Fig. 4A. —70-year-old man with metastatic malignant melanoma who
presented with intermittent crampy abdominal pain. Transverse sonogram of
right lower abdomen shows ileoileal intussusception seen as "ring in
ring sign." Outer hypoechoic ring is formed by intussuscipiens
(invaginating ileum). Inner hypoechoic round area is formed by intussusceptum
(entering limb of invaginated ileum) with mucosal melanoma metastasis in
center. Hyperechoic crescent between two rings is formed by invaginated
mesenteric fat.
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Fig. 4B. —70-year-old man with metastatic malignant melanoma who
presented with intermittent crampy abdominal pain. Transverse sonogram at apex
of intussusception shows invaginated hypoechoic irregularly bordered melanoma
metastasis in ileal lumen.
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Fig. 4C. —70-year-old man with metastatic malignant melanoma who
presented with intermittent crampy abdominal pain. Doppler sonogram of
intraluminal mucosal metastasis reveals strong capillary blood flow.
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Fig. 4D. —70-year-old man with metastatic malignant melanoma who
presented with intermittent crampy abdominal pain. CT scan shows ileum with
contrast material in its lumen being invaginated by mesenterically thickened
ileum segment.
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Sonographically guided fine-needle aspiration confirmed secondary tumor
growth in three patients. In two patients, in whom 22-gauge fine-needle
puncture resulted in insufficient aspiration, subsequent 18-gauge core biopsy
allowed histologic diagnosis. No complications were observed after punctures.
Postoperative specimens were pathologically examined in four patients.
Histologic and cytologic examinations revealed bowel metastases from malignant
melanoma (n = 4), bronchogenic carcinoma (n = 2), and
gastric carcinoma (n = 1).
All intestinal metastases were considered symptomatic. Direct proof could
be established by operation or colonoscopy in four patients, and performation
of the metastases in two patients was found intraoperatively. Surgically
documented ileoileal intussusception caused intermittent crampy abdominal pain
in one patient. Bleeding from a metastasis in the ascending colon was seen on
colonoscopy in one patient. In the other three patients the intestinal
metastases were considered symptomatic because no other plausible cause for
the abdominal symptoms was found. In two patients upper and lower
gastrointestinal endoscopy did not reveal another bleeding source, and
sonography and follow-up CT did not disclose other causes for abdominal pain
in one patient.
Discussion
Abdominal symptoms lead to numerous radiologic investigations in patients
suffering from cancer in advanced stages. Sonography is frequently chosen as a
first screening method because it is noninvasive and does not require special
preparation. Sonography is, furthermore, readily accessible and inexpensive.
Common manifestations such as liver metastases, lymph node involvement,
ascites, or hydronephrosis are sought, but the gastrointestinal tract is
usually not examined by most radiologists. To our knowledge, diagnosis of
symptomatic intestinal metastases, other than lymphoma, by transabdominal
sonography has not yet been reported. However, transabdominal sonography of
the gastrointestinal tract has become widely recognized as a directed tool to
examine bowel disorders in patients with abdominal pain. Bowel wall thickening
greater than 4 mm is generally considered abnormal. Experienced investigators
can identify many bowel abnormalities, depending on location and amount of
bowel wall thickening, loss of stratification, and the presence of mural and
perimural alterations [5].
However, mild bowel wall thickening, small mucosal processes such as polyps,
or ulcerations cannot, even in expert hands, be reliably diagnosed. Sonography
is heavily operator dependent and may be limited as a result of markedly
gas-distended bowel loops, obese patients, and severe abdominal pain in
patients with peritonitis.
Six of the seven symptomatic bowel wall metastases in our small patient
group showed extensive hypoechoic bowel wall thickening (Figs.
2A,2B
and
3A,3B),
which allowed easy sonographic recognition of the neoplasms. All patients had
gastrointestinal symptoms that were directly related to these bowel wall
tumors. One may assume that bowel wall metastases have to reach a certain size
to become symptomatic. It is, therefore, possible that sonography may be quite
sensitive in diagnosing symptomatic intestinal metastases. However, this
presumption needs further investigation in large prospective studies comparing
transabdominal sonography with other methods such as CT and small-bowel enema.
Transabdominal sonography can be used as a first screening method and may
identify symptomatic intestinal metastases but does not allow exclusion of
bowel metastases. Complete radiologic workup to diagnose potential bowel
metastases requires high-quality enteroclysis to examine mucosal tumors and CT
to exclude mesenteric infiltration and mural and serosal implants
[6]. The main differential
diagnoses in marked segmental bowel wall thickening are Non-Hodgkin's Lymphoma
[7], colonic carcinoma
[8], other primary bowel
neoplasms, and severe inflammatory changes in diverticulitis and Crohn's
disease.
Malignant melanoma is the tumor that spreads most frequently hematogenously
to the gastrointestinal tract with the small intestine involved most
frequently. This preponderance of melanoma metastases is also reflected in our
patient group with four of seven patients suffering from symptomatic secondary
tumor involvement of the small intestine. Although a cutaneous primary tumor
may not be found in up to 46% of patients with melanoma of the
gastrointestinal tract [4],
gastrointestinal involvement is assumed to be metastatic
[9]. On luminal contrast
studies melanoma metastases may be diagnosed as mucosal filling defects,
mucosal ulcerations, or stenoses
[6]. On CT diffuse bowel wall
infiltration, serosal implants, and mesenteric masses may be seen
[6].
A well-known complication of intestinal metastases is intussusception. The
clinical symptoms may suggest partial obstruction of the intestine, but
diagnosis may be difficult because symptoms are often nonspecific. An organic
cause can be shown in up to 90% of adults, but there is no clearly preferred
anatomic site. The leading mass is nearly always a tumor of the intestinal
wall, usually malignant in intussusceptions of the colon and mostly benign in
intussusceptions of the small intestine
[10]. The sonographic hallmark
of intussusception was first described as a "target"
[11], doughnut, or bull's eye
sign. Typically one finds two hypoechoic rings being separated by a
hyperechoic ring or crescent in axial images
(Fig. 4A).
Percutaneous sonographically guided fine-needle aspiration was performed in
all our patients who were not scheduled for emergent operations. Two patients
were additionally biopsied with an 18-gauge core after insufficient
aspiration. Because most metastases in our small patient group were located in
the small bowel, definite histologic diagnosis would have otherwise required
laparoscopy or laparotomy. Sonographically guided puncture is quickly
performed after diagnostic sonography and requires no preparation other than
local anesthesia. Puncture can be performed with real-time control, and the
bowel segment may be fixed by means of compression with the sonographic probe.
Tangential puncture of the bowel wall without passing through the lumen allows
safe cytology aspiration or biopsy without violation of the mucosa
(Fig. 1). Thin-needle
aspiration and percutaneous 18-gauge core biopsy of bowel wall lesions have
been shown to be safe procedures
[12,
13]. The percentage of
sufficient samples gained by 18-gauge core devices was estimated to be more
than 90% [13] and probably
higher than those performed with fine-needle aspiration. We consider
sonographically guided percutaneous puncture an ideal method to reach
definitive diagnosis during the initial examination. In all our patients with
sonographically guided puncture, definitive pathologic diagnosis was
established without any complications.
We conclude that sonography of the gastrointestinal tract should be
included in abdominal sonography in patients suffering from advanced
metastatic cancer because symptomatic intestinal metastases can be diagnosed.
Sonographically guided fine-needle aspiration or 18-gauge core biopsy at the
end of the examination establishes definitive diagnosis and is a safe
procedure.
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Abstract
Introduction
