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doi:10.3748/wjg.v16.i12.1527

World J Gastroenterol 2010 March 28; 16(12): 1527-1532

ISSN 1007-9327 (print)

2010 Baishideng. All rights reserved.

BRIEF ARTICLE

Surgically treated primary malignant tumor of small bowel:

A clinical analysis
Shao-Liang Han, Jun Cheng, Hong-Zhong Zhou, Sheng-Cong Guo, Zeng-Rong Jia, Peng-Fei Wang
colectomy (n = 15), pancreaticoduodenectomy (n =
10), and others (n = 19). Twenty-seven adenocarcinoma patients and 13 malignant lymphoma patients
received adjuvant chemotherapy with 5-fluorouracil
and cyclophosphamide, adriamycin, vincristine and
prednisone, respectively. Information about 120 patients was obtained during the follow-up. The median
survival time of PMTSB patients was 20.3 mo. The
1-, 3- and 5-year survival rate was 75.0% (90/120),
40.0% (48/120) and 20.8% (25/120), respectively.
Adenocarcinoma was found in 73.7% (42/57), 21.1%
(12/57) and 15.8% (9/57) of the patients, respectively. Gastrointestinal stromal tumor was observed in
80.0% (20/25), 72.0% (18/25) and 36.0% (9/25) of
the patients, respectively. Carcinoid was detected in
100.0% (15/15), 80.0% (12/15) and 46.7% (7/15) of
the patients, respectively. Malignant lymphoma was
demonstrated in 69.2% (9/13), 30.8% (4/13) and 0%
(0/13) of the patients, respectively.

Shao-Liang Han, Jun Cheng, Hong-Zhong Zhou, ShengCong Guo, Zeng-Rong Jia, Peng-Fei Wang, Department of
General Surgery, First Affiliated Hospital of Wenzhou Medical
College, Wenzhou 325000, Zhejiang Province, China
Author contributions: Han SL wrote and revised the manu
script; Cheng J and Zhou HZ collected the clinical data; Guo SC,
Jia ZR and Wang PF observed the patients during the follow-up.
Correspondence to: Dr. Shao-Liang Han, Department of
General Surgery, First Affiliated Hospital of Wenzhou Medical
College, Wenzhou 325000, Zhejiang Province,
China. slhan88@yahoo.com.cn
Telephone: +86-577-88069307 Fax: +86-577-88069555
Received: November 26, 2009 Revised: December 27, 2009
Accepted: January 4, 2010
Published online: March 28, 2010

Abstract
AIM: To evaluate the clinical presentation, treatment
and survival of patients with primary malignant tumor
of small bowel (PMTSB).

CONCLUSION: En bloc resection is the principal therapy for most PMTSB and chemotherapy is the important treatment modality for malignant lymphoma and
other malignant tumors of small bowel which cannot
be radically removed.

METHODS: Clinicopathologic data about 141 surgically treated PMTSB patients (91 males and 50 females)
at the median age of 53.5 years (range 23-79 years)
were retrospectively analyzed.

2010 Baishideng. All rights reserved.

RESULTS: The most common initial clinical features

of the patients were intermittent abdominal discomfort or vague abdominal pain (67.4%), abdominal
mass (31.2%), bowel obstruction (24.1%), hemotochezia (21.3%), jaundice (16.3%), fever (14.2%), coexistence of bowel perforation and peritonitis (5.7%),
coexistence of gastrointestinal bleeding and shock
(5.0%), and intraabdominal bleeding (1.4%). Ileum
was the most common site of tumor (44.7%), followed by jejunum (30.5%) and duodenum (24.8%).
PMTSB had a nonspecific clinical presentation. Segmental bowel resection (n = 81) was the most common surgical procedure, followed by right hemi-

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Key words: Small bowel; Malignant tumor; Diagnosis;

Surgical treatment; Chemotherapy
Peer reviewer: Rene Lambert, Professor, International Agency

for Research on Cancer, 150 Cours Albert Thomas, Lyon 69372

cedex 8, France
Han SL, Cheng J, Zhou HZ, Guo SC, Jia ZR, Wang PF.
Surgically treated primary malignant tumor of small bowel: A
clinical analysis. World J Gastroenterol 2010; 16(12): 1527-1532
Available from: URL: http://www.wjgnet.com/1007-9327/full/v16/
i12/1527.htm DOI: http://dx.doi.org/10.3748/wjg.v16.i12.1527

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Han SL et al . Primary malignant tumor of small bowel

Statistical analysis
Data were analyzed using the SPSS software (version
13.0; SPSS, Inc., Chicago, IL). Patient records were reviewed during the follow-up or by direct contact with
the patients, their relatives, or office visit. Survival rate
was calculated on the day of histological diagnosis until
death or last follow-up with the Kaplan-Meier method
for analysis of censored data. Cox regression analysis
was performed to assess the independent prognostic
significance of parameters. P < 0.05 was considered statistically significant.

INTRODUCTION
Primary malignant tumor of the small bowel (PMTSB)
accounts for 2% of all gastrointestinal (GI) tumors and
1% of GI tumor-related deaths[1-5]. The small bowel is
relatively resistant to carcinogenesis although it is considerably long (accounting for 70% of the whole digestive tract) and exposed to a wide variety of potentially
noxious substances. In a review of over 11000 primary
GI malignant tumors, Martin[6] found that only 2.4%,
10.8%, 16.4%, and 70.3% of primary malignancies are
originated from the small bowel, esophagus, stomach,
and colorectum, respectively. However, the diagnosis of
PMTSB is difficult, because its symptoms and signs are
nonspecific at presentation. Therefore, it is usually discovered at its advanced stage and often needs a surgical
intervention due to acute complications. Sometimes, it is
occasionally found during other surgical procedures[6-11].
This retrospective study was to evaluate the clinical presentation, treatment and survival of PMTSB patients.

RESULTS
Clinical and diagnostic features
Of the 141 PMTSB patients, 91 were male and 50 were
female. Their median age was 53.5 years (range 23-79
years). Ileum was the most common site of PMTSB
(44.7%), followed by jejunum (30.5%) and duodenum
(24.8%). The most common clinical features of PMTSB
patients at initial presentation were intermittent abdominal discomfort or vague abdominal pain (67.4%),
abdominal mass (31.2%), bowel obstruction (24.1%),
hemotochezia (21.3%), jaundice (16.3%), fever (14.2%),
coexistence of bowel perforation and peritonitis (5.7%),
coexistence of gastrointestinal bleeding and shock
(5.0%), and intraabdominal bleeding (1.4%). Other
symptoms were loss of appetite, diarrhea, anemia and
loss of bodyweight (Table 1). The median time of symptoms was 2 mo (range 0-41 mo).
The preoperative diagnostic rate was decreased to
91.7% (11/12) at the duodenum, 70.6% (36/51) at the
jejunum, and 60.3% (47/78) at the ileum, respectively.
The most commonly used diagnostic techniques were ultrasonography (US) of the abdomen (90.1%), followed by
computed tomography (CT) of the abdomen (80.1%), upper gastrointestinal radiography (31.9%) and upper endoscopy (25.5%). Additional techniques included ultrasonography, endoscopic retrograde cholangiopancreatography
(ERCP), superior mesenteric arteriography, colonoscopy
and bone scanning.
All the patients were diagnosed histopathologically
after operation. Of the 141 patients, 61 (43.3%) were
diagnosed as adenocarcinoma, 28 (19.8%) as GIST, 17
(12.1%) as carcinoid, 14 (9.9%) as malignant lymphoma,
10 (7.1%) as leiomyosarcoma, 6 (4.3%) as malignant melanoma, 3 (2.1%) as malignant neurilemmoma, and 2 (1.4%)
as fibrosarcoma, respectively (Table 2). Twenty-three of
the 61 patients (37.7%) who underwent curative resection
were found to have lymph node metastases after surgery,
which were not suspected before operation.

MATERIALS AND METHODS

Medical records of PMTSB patients at the tumor registry of our hospital between January 1988 and December
2007 were analyzed. Patients with tumor at the ampulla
of Vater, pancreatic head, and ileocecal valve and metastatic cancer were excluded from the study. Only those
with primary tumor arising from the duodenum, jejunum, or ileum were included.
One hundred and forty-one patients entered the
study. Data on demography, clinical presentation, diagnosis, surgical treatment, histopathological findings,
postoperative course, and survival time were collected
from each patient. The TNM staging classification (AJCC
system, 6th edition)[12] was used to classify the extent
of adenocarcinoma and carcinoid based on the histopathological and surgical reports. Stage(T1-2, N0)
was defined as tumor extending to muscularis propria,
stage (T3-4, N0) as tumor extending to subserosa,
mesentery, and adjacent viscera, stage (any T, N1) as
tumor with regional lymph node metastasis, and stage
(any T, any N, M1) as tumor with distant metastasis.
Adenocarcinoma at stages- was detected in 3, 14,
37 and 7 patients, respectively. Carcinoid at stages-
was found in 4, 8, 5 and 2 patients, respectively. Operation reports on the type, extent, and necessity of en bloc
resection were reviewed. Operation was defined as radical if the tumor was completely removed both grossly
and microscopically, and as palliative if the patients had
distant metastasis at presentation, gross residual tumor
at surgery, or positive margins microscopically. The
World Health Organization standard grading system (well
differentiated, moderately differentiated, poorly differentiated, and undifferentiated) was used to classify the
histological types[12]. In addition, Ann Arbor staging classification[13] was used to classify the extent of malignant
lymphoma. The diagnosis of gastrointestinal stromal
tumor (GIST) was made as previously described[14-16].

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Surgical procedures
Of the 141 patients who underwent surgical intervention,
31 (22.0%) had emergency operation and 110 (78.0%) had
selective operation. The emergency indications included
bowel obstruction (n = 24), gastrointestinal bleeding (n
= 4) and bowel perforation (n = 3). The most commonly
used surgical procedure was segmental bowel resection

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Han SL et al . Primary malignant tumor of small bowel

Table 2 Histopathological type of PMTSB (n = 141)

Table 1 Clinical symptoms and signs of PMTSB patients

n (%)

Symptoms
Abdominal pain
Abdominal mass
Bowel obstruction
Hemotochezia
Jaundice
Fever
Bowel perforation coexistent peritonitis
Gastrointestinal bleeding and coexistent Shock
Intraabdominal bleeding

95 (67.4)
44 (31.2)
34 (24.1)
30 (21.3)
23 (16.3)
20 (14.2)
8 (5.7)
7 (5.0)
2 (1.4)

Histopathological type

n (%)

Adenocarcinoma
GIST
Carcinoid
Malignant lymphoma
Leiomyosarcoma
Malignant melanoma
Malignant neurilemmoma
Fibrosarcoma

61 (43.3)
28 (19.8)
17 (12.1)
14 (9.9)
10 (7.1)
6 (4.3)
3 (2.1)
2 (1.4)

GIST: Gastrointestinal stromal tumor.

Others symptoms: Loss of appetite, diarrhea, anemia and loss of body
weight. PMTSB: Primary malignant tumor of small bowel.

Table 4 Complications after operation

Pancreatic anastomotic leak

Wound infection
Prolonged gastric emptying
Subphrenic abscess
Gastrointestinal bleeding
Total

n (%)

Procedure
Operative intervention
Emergent procedure
Elective procedure
Disease for emergent procedure
Bowel obstruction
Gastrointestinal bleeding
Bowel perforation
Surgical procedure
Segmental bowel resection
Right hemi-colectomy
Pancreaticoduodenectomy
Gastric bypass
Biopsy at laparotomy
Feeding jejunostomy
Biliary bypass
Enteric bypass
Radicality of procedure
Radical1
Palliative2

31 (22.0)
110 (78.0)
24 (77.4)
4 (12.9)
3 (9.6)

7 (5.0)
6 (4.3)
3 (2.1)
3 (2.1)
2 (1.4)
21 (14.9)

Postoperative adjuvant therapy

Of the 141 PMTSB patients, 40 (28.4%) received adjuvant chemotherapy after operation. However, adenocarcinoma was treated with 5-fluorouracil (5-FU) and malignant lymphoma was treated with cyclophosphamide,
adriamycin, vincristine and prednisone (CHOP).

92 (65.3)
15 (10.6)
10 (7.1)
13 (9.2)
5 (3.6)
2 (1.4)
2 (1.4)
2 (1.4)

Recurrence patterns
Recurrence of the tumor was found in 32 (22.7%) of the
104 patients after radical resection (at a single site in 13
and at multiple sites in 19). The most common sites of
recurrence were liver and lung (65.6%), peritoneal carcinomatosis (21.9%) and intestinal mesentery (12.5%). Nine
patients (28.1%) underwent further operative intervention,
8 (25.0%) received chemotherapy and/or radiotherapy,
and 4 (12.5%) received no further treatment. Of the 9
patients who underwent a second operation, 7 received a
palliative procedure and died of the disease progression at
a median time of 10 mo (range 2-18 mo) after operation.

104 (73.8)
37 (26.2)

Radical resection: Negative margin, resection of all gross diseases, en bloc

local resection when indicated; 2Palliative resection: Positive margin, gross
residual disease.

(65.3%), followed by right hemicolectomy (10.6%), and

pancreaticoduodenectomy (7.1%). Other procedures
included gastric bypass (n = 13), biopsy only (n = 5), feeding jejunostomy (n = 2), biliary bypass (n = 2), and enteric
bypass (n = 2).
Of the 141 PMTSB patients, 104 (73.8%) received
a radical resection, 37 (26.2%) underwent diagnostic or
palliative operation. Of the 32 patients who underwent a
palliative resection, 15 had synchronous distant metastasis
(liver metastasis in 10 and peritoneal dissemination in 5) in
small bowel and its mesentery (n = 11), retroperitoneum (n
= 5) and ovary (n = 1) (Table 3).

Survival rate of PMTSB patients according to histology

Information was obtained during the follow-up of 120
patients with PMTSB including adenocarcinoma (n =
57), GIST (n = 25), carcinoid (n = 17), malignant lymphoma (n = 17), leiomyosarcoma (n = 3) and malignant
melanoma (n = 1). The median survival time of PMTSB
patients was 20.3 mo. The 1-, 3- and 5-year survival rate
was 75.0% (90/120), 40.0% (48/120) and 20.8% (25/120),
respectively. Adenocarcinoma was detected in 73.7%
(42/57), 21.1% (12/57), and 15.8% (9/57) of the patients,
respectively. GIST was observed in 80.0% (20/25), 72.0%
(18/25) and 36.0% (9/25) of the patients, respectively.
Carcinoid was found in 100.0% (15/15), 80.0% (12/15)
and 46.7% (7/15) of the patients, respectively. Malignant
lymphoma was shown in 69.2% (9/13), 30.8% (4/13)
and 0% (0/13) of the patients, respectively. In addition,

Postoperative complications
Postoperative complications occurred in 21 (14.9%) patients, including pancreatic anastomotic leak in 7 (5.0%),
wound infection in 6 (4.3%), prolonged gastric emptying
in 3 (2.1%), subphrenic abscess in 3 (2.1%), and gastrointestinal bleeding from gastrojejunostomy in 2 (1.4%)
as shown in Table 4. The median hospital stay time of
patients was 13.2 d (range 8-60 d).
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n (%)

Complications

Table 3 Surgical procedure for PMTSB patients

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Han SL et al . Primary malignant tumor of small bowel

Table 5 Survival rate of PMTSB patients n (%)
Histopathological type

Loss of follow-up cases (n )

Adenocarcinoma (n = 61)
GIST (n = 28)
Carcinoid (n = 17)
Lymphoma (n = 14)
Other tumors(n = 21)

4
3
2
1
11

1-yr survival rate

5-yr survival rate

Treatment strategy and surgical procedure

Treatment of PMTSB is mainly based on its histopathological type, location and extent. If the tumor is located
at jejunum or ileum, an aggressive segmental resection
and primary anastomosis are indicated[2]. If the tumor is
located at ileum around the ileocolon junction, ileocolonic
resection or right hemi-colectomy is indicated[3]. The optimal resection extent of duodenal tumor has not been
defined. Some authors advocate pancreaticoduodenectomy (PD) for all patients with malignant tumor of the
duodenum, including those located at the third and fourth
portions to ensure adequate en bloc resection[6]. If the
tumor is an adenocarcinoma or a carcinoid, en bloc resection and systemic lymph node dissection are indicated[7].
If the tumor is a histopathologically proven malignant
lymphoma before operation, systemic chemotherapy is
the first choice of treatment and surgery selection is only
indicated for those with bowel obstruction, perforation
and bleeding[26-29]. The value for routine extensive resection of adenocarcinoma or carcinoid has been recently
challenged[2,3,7,8,26,27]. Others support PD for proximal
duodenal carcinoma, but segmental resection for tumor
of the third and fourth portions[27-29]. In our patients, the
most commonly used surgical procedure was segmental
bowel resection (65.3%), followed by right hemicolectomy
(10.6%), PD (7.1%) and others.
Of the 61 patients (37.7%) who underwent curative
resection, 23 were found to have lymph node metastasis
after surgery, which was not suspected before operation.
It has been shown that laparoscopy can help to stage GI
cancer, thus avoiding unnecessary laparotomies. However, laparoscopy is not appropriate for patients with obstruction or bleeding or for those with no indication for
palliative surgery[24,25]. In this series, 31 (22.0%) patients
required urgent laparotomy for intestinal obstruction,
gastrointestinal bleeding, or perforation.
It has been reported that chemotherapy may be beneficial for PMTSB, but optimal chemotherapy and the
degree of benefit remain to be defined[27,30,31]. Bakaeen
et al [30] showed that chemotherapy with lomustine
(CCNU), 5-FU, either alone or in combination with
other therapies, can considerably improve symptoms and
hormone level, and moderately inhibit tumor regression,
particularly in patients with metastatic gastroenteropancreatic neuroendocrine tumors with minimal adverse
effects[30,31]. In our study, 40 patients (28.4%) received
adjuvant chemotherapy after operation. However, adenocarcinoma and malignant lymphoma were treated with
5-FU and CHOP, respectively.

3 leiomyosarcoma patients had a survived time of 15, 39

and 71 mo, respectively. One malignant melanoma patient
survived for 18 mo (Table 5).

DISCUSSION
Presentation and diagnosis of PMTSB
PMTSB is a rare malignancy. Most PMTSB patients have
nonspecific clinical symptoms and signs[1-6]. In this series, the most frequent symptoms were abdominal pain
(67.4%), abdominal mass (31.2%) and bowel obstruction
(24.1%), followed by hemotochezia (21.3%), jaundice
(16.3%), fever (14.2%), coexistence of bowel perforation
and peritonitis (5.7%), coexistence of gastrointestinal
bleeding and shock (5.0%), and intraabdominal bleeding
(1.4%). The symptoms are similar to the reported findings[1-3,10,11]. The median time of delayed diagnosis in our
series was 2 mo.
Preoperative diagnosis of PMTSB is often difficult. In our series, the preoperative diagnostic rate was
decreased to 91.7% at the duodenum, 70.6% at the jejunum, and 60.3% at the ileum, respectively. The most
commonly used diagnostic techniques were US, CT, upper gastrointestinal radiography and upper endoscopy.
Endoscopic biopsy proved that most duodenal tumors
(91.7%) in our study were malignant before surgery,
suggesting that the more distal the tumor is, the more
difficult the preoperative diagnosis is[16,17]. Since the accuracy of CT staging for small bowel adenocarcinoma is
47%-61%, it is only used in the detection of mesenteric
infiltration and regional lymphadenopathy[16-20].
Hatzaras et al[1] showed that carcinoid tumor is the
most common intestinal cancer, followed by adenocarcinoma. Our data demonstrate that ileum is the most
common site (44.7%), followed by jejunum (30.5%),
duodenum (24.8%), and that the most prevalent histological type is adenocarcinoma (43.3%), followed by GIST
(19.8%), carcinoid (12.1%), malignant lymphoma (9.9%),
leiomyosarcoma (7.1%), malignant melanoma (4.3%), malignant neurilemmoma (2.1%) and fibrosarcoma (1.4%),
indicating that carcinoid tumor is more frequently found
in ileum than adenocarcinoma in duodenum[1,8,21-23].
Laparoscopy can help to stage small bowel malignant
tumor; serosal infiltration, retroperitoneal fixation, lymph
node metastasis and ascites[23]. Laparoscopy can accurately
assess and stage gastric adenocarcinoma[24,25], thus avoiding
unnecessary laparotomy for those with no indication for
palliative surgery. However, laparoscopy is not appropriate
for patients with obstruction or bleeding.
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3-yr survival rate

42 (73.7)
12 (21.0)
9 (15.8)
20 (80.0)
18 (72.0)
9 (36.0)
15 (100.0)
12 (80.0)
7 (46.7)
9 (9.25)
4 (30.8)
0
3 cases of leiomyosarcoma survived (15, 39 and 71 mo, respectively) and 1 case of malignant
melanoma survived 18 mo

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Han SL et al . Primary malignant tumor of small bowel

Surgical outcome
It has been reported that the 5-year survival rate of PMTSB
patients after curative resection is 32%-47%[1,20-22,32,33]. Howe
et al[31] have reported that the 5-year survival rate of patients after curative resection of localized, regional and distant metastatic PMTSB is 47.6%, 31% and 3.9%, respectively, which is similar to that of our patients. The median
survival time of the 141 PMTSB patients was 20.3 mo.
The 1-, 3- and 5-year survival rate was 75.0%, 40.0%
and 20.8%, respectively. Adenocarcinoma was detected
in 73.7%, 21.1% and 15.8% of the patients, respectively.
GIST was found in 80.0%, 72.0% and 36.0% of the patients, respectively. Carcinoid was observed in 100.0%,
80.0% and 46.7% of the patients, respectively. Malignant
lymphoma was demonstrated in 69.2%, 30.8% and 0% of
the patients, respectively.
The site, clinical stage, and histological type do not
influence the survival time of PMTSB patients. Howe
et al[31] reported that the median survival time of patients
with tumors of duodenum, jejunum and ileum is 16.9
and 28-31 mo, respectively. In our study, 32 of 104 patients (22.7%) had distant metastasis or intra-abdominal
carcinomatosis at presentation, which is consistent with
the reported findings[1,5,7,11,26]. Ito et al[7] reported that the
5-year survival rate of T1/T2 and T3/T4 tumor patients
is 82% and 58%, respectively (P < 0.05). In contrast,
Bakaeen et al[30] found that T stage can not predict the
survival time of PMTSB patients. Curative resection,
however, may not be possible owing to the late diagnosis
of PMTSB. Dabaja et al[29] also reported that the 5-year
survival rate of patients with PMTSB at stage is 5%,
which is much lower than that of those with PMTSB at
stages- (36%). Although carcinoid is usually silent
and diagnosed at its advanced stage, carcinoid patients
have a good prognosis and a long survival time after effective treatment[2,5,7,34,35].
In summary, en bloc resection is the principal procedure for most PMTSB patients and chemotherapy is the
important treatment modality for malignant lymphoma
and other small bowel malignant tumors with no indication for radical resection.

surgical procedures. The objective of this study was to evaluate the clinical
presentation, treatment and survival of PMTSB patients.

Research frontiers

How to improve the early diagnosis and treatment of PMTSB is a hotspot in

recent studies.

Innovations and breakthroughs

This study evaluated the clinical presentation, treatment and survival time of
PMTSB patients.

Applications

The retrospective analysis of the clinical presentation, treatment and survival

time of PMTSB patients showed that PMTSB can be made early diagnosed and
can thus be rationally treated.

Peer review

This is a rather large series of PMTSB patients from a single center. The data
provided in this study contribute to the early diagnosis and treatment of PMTSB.

REFERENCES
1

3
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6
7

ACKNOWLEDGMENTS

10

The authors thank Professor Sou-Rong Ji, Department

of Foreign Languages, Wenzhou University, for polishing
the English.

11

COMMENTS
COMMENTS

12

Background

Although small bowel is considerably long and exposed to a wide variety of

potentially noxious substances, it is relatively resistant to carcinogenesis. Primary
malignant tumor of the small bowel (PMTSB) accounts for 2% of gastrointestinal
(GI) tumors and 1% of gastrointestinal tract cancer- related deaths. In a review
of over 11000 primary GI malignant tumors, Martin found that only 2.4%, 10.8%,
16.4% and 16.4% are originated from the small bowel, esophagus, stomach, and
colorectum, respectively. However, the diagnosis of PMTSB is difficult, because
its symptoms and signs are nonspecific at presentation. Therefore, PMTSB is
usually discovered at its advanced stage and often needs surgical intervention
due to acute complications. Sometimes, it is occasionally found during other

WJG|www.wjgnet.com

13

14
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S- Editor Wang YR L- Editor Wang XL E- Editor Lin YP

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March 28, 2010|Volume 16|Issue 12|