CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2006;4:1373–1377
Periportal Lymphadenopathy in Patients Without Identifiable
Pancreatobiliary or Hepatic Malignancy
NAVEEN B. KRISHNA, LAURA GARDNER, BRIAN T. COLLINS, and BANKE AGARWAL
Division of Gastroenterology and Hepatology and Department of Pathology, Saint Louis University School of Medicine, St. Louis, Missouri
Background & Aims: Enlarged periportal lymph nodes
often are noticed during imaging of the upper abdomen. Ma-
lignant infiltration and enlargement of periportal nodes occur
in patients with cancers of the liver, gallbladder, biliary tree, and
pancreas and lymphoma. However, there are no published data
on the significance and differential diagnosis of enlarged peri-
portal lymph nodes in patients without the above mentioned
cancers. Methods: We searched our database for patients who
(1) underwent endoscopic ultrasound for evaluation of en-
larged periportal nodes or (2) were found to have enlarged
periportal lymph nodes (ⱖ10 mm) during endoscopic ultra-
sound (EUS) examination. Patients with identifiable pancreatic,
biliary, gallbladder, or liver cancers were excluded. EUS-guided
fine-needle aspiration of one or more nodes was performed.
Results: Sixty-four patients with periportal lymph nodes
10 – 40 mm in size met the inclusion criteria. In 24 patients,
enlarged periportal nodes were noted in the computerized to-
mography or magnetic resonance imaging scans. Fifty-one pa-
tients had multiple enlarged periportal nodes. Concomitantly,
enlargement was seen in peripancreatic nodes (n ⫽ 14), celiac
nodes (n ⫽ 14), and mediastinal nodes (n ⫽ 11). Twelve of the
64 patients (18.8%; 95% confidence interval, 9.2%–28.4%) had a
malignant cause of enlarged periportal lymph nodes: 5 with
metastatic carcinoma and 7 with non-Hodgkin’s lymphoma.
Significant cytologic findings in benign nodes included granu-
lomas (n ⫽ 4) and lipogranulomatosis (n ⫽ 8).
Conclusions: A significant number of patients with en-
larged periportal lymph nodes without identifiable pancreato-
biliary and liver cancer harbor malignancy and other identifi-
able pathologic processes. We recommend that these nodes be
sampled with fine-needle aspiration at the time of EUS
examination.
P eriportal nodes frequently are enlarged in patients with
cancers of the liver, gallbladder, biliary tree, and pancreas
and lymphoma, and their identification is an essential step in
the staging and treatment planning of these cancers.1–5 Often,
enlarged periportal lymph nodes are encountered during im-
aging of the upper abdomen in patients without the earlier-
mentioned cancers.6 Several studies have reported enlargement
of periportal lymph nodes in patients with liver disease.7–9
However, there are no published data on the significance and
differential diagnosis of enlarged periportal lymph nodes in
patients without the above mentioned cancers. We studied the
significance and differential diagnosis of enlarged periportal
lymph nodes in patients without identifiable malignancy or
liver disease.
Patients and Methods
Methods
This was a retrospective analysis of our database of
patients who underwent endoscopic ultrasound (EUS) at Saint
Louis University Hospital between March 2002 and August
2005 (⯝1500 EUS examinations). We searched our database for
patients who (1) underwent EUS for evaluation of enlarged
periportal lymph nodes or (2) were found to have enlarged
periportal lymph nodes during EUS examination. The medical
records of these patients then were reviewed for detailed infor-
mation. Patients were considered to have identifiable cancers if
cancer was suspected in the pancreas, biliary tree, gallbladder, or
liver at the time of EUS examination and was confirmed by the
clinical work-up including EUS fine-needle aspiration (FNA).
One patient diagnosed with metastatic cancer in the periportal
lymph nodes by EUS FNA in whom no tumor was suspected in
the liver at the time of EUS FNA, however, was included in the
study. Patients who presented with clinical suspicion of pan-
creatobiliary or liver cancer and were found not to have cancers
at those sites were considered eligible for inclusion.
Patients with concomitant lymph node enlargement in
peripancreatic, celiac, or mediastinal nodes were included if
(1) they were referred for EUS FNA specifically for evaluation of
periportal lymph nodes and had liver disease, (2) enlarged
lymph nodes in other groups were not noted on computerized
tomography (CT) scans before EUS, or (3) enlarged mediastinal
nodes were not detected before EUS because the patient only
had a CT scan of the abdomen and pelvis and not a chest CT.
Sixty-four patients with enlarged periportal lymph nodes
were included in this study. This retrospective study was ap-
proved by the Institutional Review Board at Saint Louis Uni-
versity School of Medicine (St. Louis, MO).
Endoscopic Ultrasound Examination
All patients underwent EUS-guided FNA by a single
operator (B.A.). EUS examination was performed using a radial
echoendoscope (EUM-130; Olympus, Melville, NY), and a linear
echoendoscope (FG32; Pentax, Orangeburg, NY) was used for
EUS FNA whenever an enlarged periportal node was noted.
Periportal lymph nodes were considered enlarged if they were
10 mm or larger in diameter. FNA of one or more nodes was
Abbreviations used in this paper: CLL, chronic lymphocytic leuke-
mia; CT, computerized tomography; EUS, endoscopic ultrasound; FNA,
fine-needle aspiration; HCC, hepatocellular carcinoma; MRI, magnetic
resonance imaging; NHL, non-Hodgkin’s lymphoma.
© 2006 by the AGA Institute
1542-3565/06/$32.00
doi:10.1016/j.cgh.2006.09.002
1374 KRISHNA ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 4, No. 11

performed. Immediate assessment of fine-needle aspirates was were obstructive jaundice (n ⫽ 15), abnormal imaging (n ⫽ 32),
performed by cytologists after the smears were stained with and abdominal pain (n ⫽ 13). Patients who had EUS examina-
Diff-quik and the Papanicolaou method. EUS-FNA specimens tion for abnormal abdominal cross-sectional imaging included
also were collected for immunostaining and flow cytometry those with lymph node enlargement (n ⫽ 20) and abnormal
whenever indicated. Multiple passes were made until the cytol- appearance of the pancreas (n ⫽ 9; 4 of these patients had
ogists were satisfied with the adequacy of the sample (2– 6 enlarged periportal nodes that were noted by the interpreting
passes). The morphology of periportal nodes was reassessed by radiologist). In 3 patients enlarged periportal lymph nodes were
a review of EUS pictures for the purpose of this study in an noted during an intraductal ultrasound examination that was
attempt to identify morphologic characteristics that might sug- performed for the evaluation of bile duct abnormalities at the
gest a particular diagnosis. time of endoscopic retrograde cholangiopancreatography. Two
patients underwent EUS for work-up of increased serum gastrin
Follow-Up Evaluation and Final Diagnosis levels; 1 patient was noted to have enlarged periportal lymph
Patients diagnosed with benign lymph node enlarge- nodes during surgery, and 1 patient was undergoing EUS ex-
ment with EUS FNA had a clinical follow-up period of 6 amination for suspected pancreatic malignancy as a result of
months or more to exclude a false-negative diagnosis of cancer. new-onset ascites and weight loss (but was found not to have
Final diagnosis was based on definitive cytology, immunohis- pancreatobiliary malignancy).
tochemistry, and flow cytometry. Even though suspected pancreatobiliary cancer was the rea-
son for the EUS examination in several patients in the study,
none of the patients had identifiable primary cancer at the time
Results
of EUS examination, or was finally diagnosed to have pancre-
Patient Characteristics atobiliary cancer. One patient with metastatic liver cancer in
The characteristics of patients included in this study are periportal lymph nodes diagnosed by EUS FNA was included
summarized in Table 1. Thirty-two of 64 patients were males because liver cancer was not suspected before EUS, and the
and the mean age of the 64 patients in this study was 56.5 ⫾ primary liver tumor was found in this patient only in the
16.2 years (range, 13– 88 y). In 24 of the 64 patients in this surgical resection specimen. A past history of cancer was
study, the enlarged lymph nodes were noted on CT or magnetic present in 10 patients, including 3 patients with hepatocellular
resonance image (MRI) scans. The major indications for EUS carcinoma (HCC) who had been treated with liver transplanta-
tion, 1 patient with gastric carcinoid tumor, and 1 patient each
with cancer of the appendix, uterus, colon, urinary bladder,
Table 1. Patient Characteristics esophagus, and breast. Ten patients had a history of hepatitis,
including 1 patient infected with both hepatitis B and C, and 1
n (% of total) with autoimmune hepatitis. Ten patients had a history of
chronic pancreatitis.
Sex
Male 32 (50%)
Female 32 (50%)
Endoscopic Ultrasound Findings
Age, y (range) 56.5 ⫾ 16.2 (13–88) The largest dimension of the periportal lymph nodes in
Indications for EUS the study patients ranged from 10 to 40 mm. Fifty-one patients
Obstructive jaundice 15 (24%) had multiple enlarged periportal nodes, and in 13 patients a
Abnormal imaging single periportal lymph node was noted. Concomitant lymph
Enlarged lymph nodes 20 (31.3%)
node enlargement was seen in the peripancreatic node (n ⫽ 14),
Abnormal pancreas 9 (14.1%)
celiac (n ⫽ 14), and mediastinal (n ⫽ 11) groups.
Abnormal IDUS 3 (4.7%)
Abdominal pain 13 (20.3%)
Others 4 (6.3%) Final Diagnosis
Enlarged lymph nodes detected by The final diagnosis of the enlarged periportal lymph
CT/MRI 24 (37.5%) nodes in the study patients is summarized in Table 2. Twelve of
EUS 40 (62.5%) the 64 patients (18.8%; 95% confidence interval, 9.2%–28.3%) in
Associated disease this study had a malignant cause for enlarged periportal lymph
Hepatitis
nodes. Seven of these patients had non-Hodgkin’s lymphoma
Hepatitis C 8 (12.5%)
(NHL)/chronic lymphocytic leukemia (CLL) that was identified
Hepatitis B ⫹ C 1 (1.5%)
Autoimmune 1 (1.5%) by flow-cytometric analysis of the fine-needle aspirate from the
Chronic pancreatitis 10 (16%) periportal lymph nodes. The remaining 5 patients were found
Past history of cancer to have metastatic carcinoma in the periportal lymph nodes.
Hepatocellular 3 (4.7%) Two of the 5 patients with metastatic cancer had a past history
Appendiceal 1 (1.6%) of cancer including colon cancer (2 years prior) and appendiceal
Colon 1 (1.6%) cancer (1 year prior), and the metastatic tumor in their peri-
Cancer of the uterus 1 (1.6%) portal lymph nodes matched the primary tumor. Of the 3
Bladder 1 (1.6%) patients without a history of cancer, 1 patient had metastatic
Esophageal 1 (1.6%)
HCC, and 2 patients had metastatic adenocarcinoma from an
Carcinoid tumor 1 (1.6%)
unknown primary in the periportal lymph nodes that was not
Breast 1 (1.6%)
identified before EUS FNA. In 52 patients the periportal lymph
NOTE. n ⫽ 64. node enlargement was considered benign. Granulomas were
November 2006 ENLARGED PERIPORTAL LYMPH NODES 1375

Table 2. Differential Diagnosis of Enlarged Periportal Lymph Nodes Noted Before EUS and During EUS/IDUS
Enlarged nodes detected by CT/MRI Enlarged nodes detected by EUS/IDUS
Final diagnosis (n ⫽ 24) (n ⫽ 40) Total (n ⫽ 64)

Benign
Lipogranulomatosis 5 (21%) 3 (7.5%) 8 (12.5%)
Granulomas 3 (12.5%) 1 (2.5%) 4 (6.3%)
Polyclonal lymphoycyte proliferation 10 (42%) 30 (75%) 40 (62.5%)
Malignant
Lymphoma (CLL/lymphoma) 3 (12.5%) 4 (10%) 7 (10.9%)
Metastatic cancer 3 (12.5%) 2 (5%) 5 (7.8%)

identified in 4 patients, and lipogranulomatosis was seen in
another 8 patients. All other lymph nodes had a mixed (poly-
clonal) lymphocyte population. EUS-FNA specimens from
lymph nodes with granulomas were submitted to microbiology
to look for fungi or acid-fast bacilli (smears and culture).
Acid-fast bacilli were detected in 1 of 4 patients with granulo-
mas and the underlying cause remained unclear in 3 patients.
Among the 9 patients with hepatitis C in this group, 1
patient had metastatic hepatocellular cancer (without a prior
diagnosis of liver cancer), another 2 patients had lymphoma in
the periportal lymph nodes, 1 patient had lipogranulomatosis,
and the remaining 5 patients had enlarged periportal lymph
nodes with a polyclonal lymphocyte population consistent with
a reactive process.
The number of enlarged periportal lymph nodes with ma-
lignant infiltration was distributed evenly between patient
groups in whom the enlarged periportal lymph nodes were
identifiable on cross-sectional imaging with CT or MRI scans
(6 of 24 [25%]) and patients in whom the enlarged lymph nodes
were not seen on CT or MRI but were identified by EUS or
intraductal ultrasound imaging (6 of 40 [15%]) (Table 2). The
lymph nodes that were detected only by EUS were smaller
(18.8 ⫾ 8.2 vs 23.1 ⫾ 7.3 mm for nodes noted on CT/MRI,
P ⫽ .03) and had a significantly higher number of reactive
nodes with polyclonal lymphocytic proliferation (75% vs 42%,
P ⫽ .008).
Distribution of Lymph Node Enlargement and
Cause of Lymphadenopathy
Table 3 summarizes the cause of lymphadenopathy
when there was concomitant enlargement of lymph nodes in
the peripancreatic, celiac, and/or mediastinal groups. Enlarge-
ment of lymph nodes in 2 or more groups was noted in 26
patients; 5 of these patients had malignancy: 4 with non-
Hodgkin’s lymphoma and 1 with metastatic liver cancer (in-
volving the periportal and celiac nodes). Of the 38 patients with
lymph node enlargement confined to the periportal group, 7
patients had malignancy: 3 with non-Hodgkin’s lymphoma and

Table 3. Differential Diagnosis of Enlarged Periportal Lymph Nodes Based on the Presence of Associated Lymphadenopathy
Periportal nodes (N ⫽ 64) Peripancreatic nodes (N ⫽ 14) Celiac nodes (N ⫽ 14) Mediastinal nodes (N ⫽ 11) Final diagnosis

⫹ ⫹ ⫹ ⫹ NHL/CLL
⫹ ⫹ ⫹ ⫹ Mixed lymphocytes
⫹ ⫹ ⫹ ⫹ Mixed lymphocytes
⫹ ⫹ ⫹ ⫹ Lipogranulomatosis
⫹ ⫹ ⫹ Absent Mixed lymphocytes
⫹ ⫹ ⫹ Absent NHL/CLL
⫹ ⫹ ⫹ Absent Granuloma
⫹ ⫹ Absent ⫹ Lipogranulomatosis
⫹ ⫹ Absent Absent NHL/CLL
⫹ ⫹ Absent Absent Lipogranulomatosis
⫹ ⫹ Absent Absent Mixed lymphocytes
⫹ ⫹ Absent Absent Mixed lymphocytes
⫹ ⫹ Absent Absent Mixed lymphocytes
⫹ ⫹ Absent Absent Mixed lymphocytes
⫹ Absent ⫹ ⫹ Granuloma
⫹ Absent ⫹ Absent HCC
⫹ Absent ⫹ Absent Mixed lymphocytes
⫹ Absent ⫹ Absent Mixed lymphocytes
⫹ Absent ⫹ Absent Mixed lymphocytes
⫹ Absent ⫹ Absent Mixed lymphocytes
⫹ Absent ⫹ Absent Mixed lymphocytes
⫹ Absent Absent ⫹ NHL/CLL
⫹ Absent Absent ⫹ Mixed lymphocytes
⫹ Absent Absent ⫹ Mixed lymphocytes
⫹ Absent Absent ⫹ Mixed lymphocytes
⫹ Absent Absent ⫹ Granuloma
1376 KRISHNA ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 4, No. 11

Table 4. Distribution of Lymph Node Involvement in lymph node(s) are identified on CT/MRI imaging, are fol-
Patients With NHL lowed-up by serial imaging in 3– 6 months. As our data suggest,
that might not be the best strategy for management of these
Periportal Peripancreatic Celiac Mediastinal Diagnosis
patients, and valuable time might be lost in patients with
⫹ Absent Absent Absent NHL/CLL malignant periportal adenopathy.
⫹ Absent Absent Absent NHL/CLL There were no defining clinical characteristics that poten-
⫹ Absent Absent Absent NHL/CLL tially could identify patients with a malignant cause of enlarged
⫹ Absent Absent ⫹ NHL/CLL periportal lymph nodes in our cohort. The patients with ma-
⫹ ⫹ Absent Absent NHL/CLL lignant periportal lymph nodes were older (mean age, 65.9 ⫾
⫹ ⫹ ⫹ Absent NHL/CLL 9.7 vs 54.7 ⫾ 16.7 y for those with benign diagnosis), but there
⫹ ⫹ ⫹ ⫹ NHL/CLL
was considerable overlap. There was no significant difference in
the likelihood of malignancy (25% vs 15%, P ⫽ .32) between
lymph nodes that were and those that were not visualized on
4 with metastatic cancer. The distribution of enlarged lymph cross-sectional abdominal imaging with CT or MRI. The indi-
nodes in the study patients who were diagnosed with NHL/CCL cations for performing EUS in the 12 patients with malignant
is summarized in Table 4. periportal nodes included abnormal CT/MRI (n ⫽ 8, with
enlarged lymph nodes in 7 and suspected pancreatic mass on
Discussion CT in 1 patient), enlarged lymph node felt during laparotomy
In this study we retrospectively evaluated the cause of (n ⫽ 1), obstructive jaundice caused by chronic pancreatitis
enlarged periportal lymph nodes in patients without identifi- (n ⫽ 1), abnormal gastrin level (n ⫽ 1), and recent-onset ascites
able pancreatobiliary or liver malignancy. Of the 64 patients with wasting (n ⫽ 1, EUS performed in search of malignant
included in this study, 12 patients were found to have malig- cause). Only 2 of 12 patients had a history of significant weight
nant periportal lymph node enlargement: 5 with metastatic loss at presentation. In 11 of the 12 patients, multiple peripor-
cancer and 7 with non-Hodgkin’s lymphoma/chronic lympho- tal lymph nodes were enlarged, but only in 5 of these patients
cytic leukemia. In 52 patients, enlarged periportal lymph nodes were lymph nodes enlarged in 2 or more groups. The enlarged
were nonmalignant, including 4 patients with granulomas, periportal lymph nodes in patients with metastatic cancer met
8 with lipogranulomatosis, and the remaining 40 patients with the EUS morphologic criteria of malignant nodes, that is, in
reactive polyclonal lymphoid proliferation. addition to being larger than 10 mm in diameter, they were
Enlarged periportal lymph nodes are not infrequently seen round and hypoechoic with sharp margins (Figure 1A).10 –12
during upper-EUS examination or noted on cross-sectional Lymph nodes infiltrated with non-Hodgkin’s lymphoma in our
abdominal imaging by CT or MRI.6 Although these nodes are patient cohort were larger (⬎20 mm in size) but did not have
looked for and often undergo a biopsy examination in patients morphologic characteristics of nodes with metastatic cancer.
with identifiable pancreatobiliary or liver malignancy for stag- Rather, they were oblong with poorly delineated margins and
ing, there are no published data on the differential diagnosis of often were hyperechoic. In 3 of 7 patients with lymphoma,
periportal lymph node enlargement in patients without an enlargement of lymph nodes was confined to the periportal
obvious malignant source. As a result, there are no guidelines group. Enlarged lymph nodes with lipogranulomatosis or gran-
for management or follow-up evaluation of these patients. ulomatous infiltration had morphology indistinct from lymph
Most of the patients, particularly those in whom the enlarged nodes enlarged as a result of lymphoma (Figure 1B–D).

Figure 1. Endosonographic appearance of enlarged

periportal lymph nodes (by using a linear echoendoscope):
(A) metastatic colon cancer, (B) non-Hodgkin’s lympho-
ma/chronic lymphocytic leukemia, (C) lipogranulomatosis,
and (D) granulomatous infiltration. Note that there is con-
siderable overlap in the EUS appearance of lymph nodes
with non-Hodgkin’s lymphoma, lipogranulomatosis, and
granulomatous infiltration.
November 2006
Nine patients in this group had hepatitis C, including
1 patient who had co-infection with hepatitis B and C. Enlarge-
ment of periportal and retroperitoneal lymph nodes in patients
with hepatitis has been well documented.13–15 However, the
cytologic or flow-cytometry characteristics of enlarged nodes in
patients with hepatic C is not known. Although the number of
patients with hepatitis C in this study is too small to draw
definitive conclusions, our data clearly show that not all en-
larged lymph nodes in patients with hepatitis C are benign. The
significance of periportal and retroperitoneal lymphadenopathy
in patients with hepatitis C seems worthy of further investiga-
tion.
Enlargement of periportal lymph nodes in 8 patients in our
cohort was caused by the presence of lipogranulomas. Li-
pogranulomatosis is a benign cause of lymph node enlargement
commonly involving lymph nodes related to the portal circula-
tion and the probable result of deposition of lipids related to
the diet and to bile metabolites.16,17 Lipogranulomas are com-
posed of loose aggregates of lymphocytes and macrophages
with a few poorly developed epithelioid cells and occasional
multinucleated giant cells. Lipid material is seen around cells
and within macrophages.
The limitations of this study include its retrospective design
and relatively small number of patients. Nonetheless, our data
clearly show that a clinically significant number of patients
(18.8%; 95% confidence interval, 9.2%–28.4%) with enlarged pe-
riportal lymph nodes harbor malignancy. Therefore, enlarged
periportal lymph nodes seen on cross-sectional imaging of the
abdomen, or when unexpectedly encountered during EUS ex-
amination in patients without pancreatobiliary or hepatic ma-
lignancy, should be sampled routinely by EUS FNA regardless
of their EUS appearance. Another potential limitation of our
study was that patients with Hodgkin’s lymphoma may have
been missed because it can be diagnosed only with histology of
the lymph nodes (requiring a laparoscopy or laparotomy to
sample the nodes).
In conclusion, this retrospective study of patients with en-
larged periportal lymph nodes without any identifiable pancre-
atobiliary or hepatic malignancy shows that a significant num-
ber of periportal lymph nodes harbor malignancy and other
disease states (ie, granulomatous disorders) and should be sam-
pled by EUS FNA and evaluated by cytology and flow cytom-
etry.
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Address requests for reprints to: Banke Agarwal, MD, Director,
Therapeutic Endoscopy, Associate Professor of Medicine, Division of
Gastroenterology and Hepatology, Saint Louis University School of
Medicine, FDT 9 South, 3635 Vista Avenue, St. Louis, Missouri 63110.
e-mail: agarwalb@slu.edu; fax: (314) 577-8757.