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
Corresponding Author of This Article
Dr. Shao-Liang Han, Department of General Surgery, First Affiliated Hospital of Wenzhou Medical College, Wenzhou 325000, Zhejiang Province, China. email@example.com
Article-Type of This Article
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
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
Shao-Liang Han, Jun Cheng, Hong-Zhong Zhou, Sheng-Cong Guo, Zeng-Rong Jia, Peng-Fei Wang, Department of General Surgery, First Affiliated Hospital of Wenzhou Medical College, Wenzhou 325000, Zhejiang Province, China
ORCID number: $[AuthorORCIDs]
Author contributions: Han SL wrote and revised the manuscript; 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. firstname.lastname@example.org
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
AIM: To evaluate the clinical presentation, treatment and survival of patients with primary malignant tumor of small bowel (PMTSB).
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.
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-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.
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.
Citation: 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
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 11 000 primary GI malignant tumors, Martin 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.
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) was used to classify the extent of adenocarcinoma and carcinoid based on the histopathological and surgical reports. Stage I (T1-2, N0) was defined as tumor extending to muscularis propria, stage II (T3-4, N0) as tumor extending to subserosa, mesentery, and adjacent viscera, stage III (any T, N1) as tumor with regional lymph node metastasis, and stage IV (any T, any N, M1) as tumor with distant metastasis. Adenocarcinoma at stages I-IV was detected in 3, 14, 37 and 7 patients, respectively. Carcinoid at stages I-IV 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. In addition, Ann Arbor staging classification was used to classify the extent of malignant lymphoma. The diagnosis of gastrointestinal stromal tumor (GIST) was made as previously described[14-16].
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.
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).
Table 1 Clinical symptoms and signs of PMTSB patients.
Bowel perforation coexistent peritonitis
Gastrointestinal bleeding and coexistent Shock
Others symptoms: Loss of appetite, diarrhea, anemia and loss of bodyweight. PMTSB: Primary malignant tumor of small bowel.
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.
Table 2 Histopathological type of PMTSB (n = 141).
GIST: Gastrointestinal stromal tumor.
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 (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).
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).
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).
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.
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, 3 leiomyosarcoma patients had a survived time of 15, 39 and 71 mo, respectively. One malignant melanoma patient survived for 18 mo (Table 5).
3 cases of leiomyosarcoma survived (15, 39 and 71 mo, respectively) and 1 case of malignant melanoma survived 18 mo
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 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. 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.
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. If the tumor is located at ileum around the ileocolon junction, ileocolonic resection or right hemi-colectomy is indicated. 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. If the tumor is an adenocarcinoma or a carcinoid, en bloc resection and systemic lymph node dissection are indicated. 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 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.
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 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 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 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 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 also reported that the 5-year survival rate of patients with PMTSB at stage IV is 5%, which is much lower than that of those with PMTSB at stages I-III (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.
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 11 000 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 surgical procedures. The objective of this study was to evaluate the clinical presentation, treatment and survival of PMTSB patients.
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.
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.
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.
Peer reviewer: Rene Lambert, Professor, International Agency for Research on Cancer, 150 Cours Albert Thomas, Lyon 69372 cedex 8, France
S- Editor Wang YR L- Editor Wang XL E- Editor Lin YP
Hatzaras I, Palesty JA, Abir F, Sullivan P, Kozol RA, Dudrick SJ, Longo WE. Small-bowel tumors: epidemiologic and clinical characteristics of 1260 cases from the connecticut tumor registry.Arch Surg. 2007;142:229-235.
Alvarado-Cabrero I, Vázquez G, Sierra Santiesteban FI, Hernández-Hernández DM, Pompa AZ. Clinicopathologic study of 275 cases of gastrointestinal stromal tumors: the experience at 3 large medical centers in Mexico.Ann Diagn Pathol. 2007;11:39-45.
Pătraşcu T, Doran H, Strâmbu V, Vîlcu M. [Small bowel tumors. Clinical course and therapeutic aspects].Chirurgia (Bucur). 2006;101:477-481.
Egberts JH, Scharrer ML, Hinz S, Schafmayer C, Klomp HJ, Faendrich F, Tepel J. Small bowel cancer: single-centre results over a period of 12 years.Hepatogastroenterology. 2007;54:129-134.
Bauer RL, Palmer ML, Bauer AM, Nava HR, Douglass HO Jr. Adenocarcinoma of the small intestine: 21-year review of diagnosis, treatment, and prognosis.Ann Surg Oncol. 1994;1:183-188.
Martin RG. Malignant tumors of the small intestine.Surg Clin North Am. 1986;66:779-785.
Ito H, Perez A, Brooks DC, Osteen RT, Zinner MJ, Moore FD Jr, Ashley SW, Whang EE. Surgical treatment of small bowel cancer: a 20-year single institution experience.J Gastrointest Surg. 2003;7:925-930.
Sutton R, Doran HE, Williams EM, Vora J, Vinjamuri S, Evans J, Campbell F, Raraty MG, Ghaneh P, Hartley M. Surgery for midgut carcinoid.Endocr Relat Cancer. 2003;10:469-481.
Coopersmith CM, Lowell JA. Surgery of the small intestine.Curr Opin Gastroenterol. 1999;15:146-150.
Markogiannakis H, Messaris E, Dardamanis D, Pararas N, Tzertzemelis D, Giannopoulos P, Larentzakis A, Lagoudianakis E, Manouras A, Bramis I. Acute mechanical bowel obstruction: clinical presentation, etiology, management and outcome.World J Gastroenterol. 2007;13:432-437.
Neugut AI, Marvin MR, Rella VA, Chabot JA. An overview of adenocarcinoma of the small intestine.Oncology (Williston Park). 1997;11:529-536; discussion 545, 549-550.
Neugut AI. AJCC Cancer Staging Manual. 6th edition. New York: NY: Springer; 2002;107-110.
Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, Lister TA, Bloomfield CD. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting-Airlie House, Virginia, November 1997.J Clin Oncol. 1999;17:3835-3849.
Miettinen M, Majidi M, Lasota J. Pathology and diagnostic criteria of gastrointestinal stromal tumors (GISTs): a review.Eur J Cancer. 2002;38 Suppl 5:S39-S51.
Woodall CE 3rd, Brock GN, Fan J, Byam JA, Scoggins CR, McMasters KM, Martin RC 2nd. An evaluation of 2537 gastrointestinal stromal tumors for a proposed clinical staging system.Arch Surg. 2009;144:670-678.
Xiang Y, Gao Y. [Grouped Cox regression model and its application in study of prognostic factors on cancer].Zhonghua Liuxingbingxue Zazhi. 1994;15:46-50.
Gore RM, Mehta UK, Berlin JW, Rao V, Newmark GM. Diagnosis and staging of small bowel tumours.Cancer Imaging. 2006;6:209-212.
Brücher BL, Stein HJ, Roder JD, Busch R, Fink U, Werner M, Siewert JR. New aspects of prognostic factors in adenocarcinomas of the small bowel.Hepatogastroenterology. 2001;48:727-732.
Dudiak KM, Johnson CD, Stephens DH. Primary tumors of the small intestine: CT evaluation.AJR Am J Roentgenol. 1989;152:995-998.
Buckley JA, Siegelman SS, Jones B, Fishman EK. The accuracy of CT staging of small bowel adenocarcinoma: CT/pathologic correlation.J Comput Assist Tomogr. 1997;21:986-991.
Agrawal S, McCarron EC, Gibbs JF, Nava HR, Wilding GE, Rajput A. Surgical management and outcome in primary adenocarcinoma of the small bowel.Ann Surg Oncol. 2007;14:2263-2269.
Wu TJ, Yeh CN, Chao TC, Jan YY, Chen MF. Prognostic factors of primary small bowel adenocarcinoma: univariate and multivariate analysis.World J Surg. 2006;30:391-398; discussion 399.
Asencio F, Aguiló J, Salvador JL, Villar A, De la Morena E, Ahamad M, Escrig J, Puche J, Viciano V, Sanmiguel G. Video-laparoscopic staging of gastric cancer. A prospective multicenter comparison with noninvasive techniques.Surg Endosc. 1997;11:1153-1158.
Burke EC, Karpeh MS, Conlon KC, Brennan MF. Laparoscopy in the management of gastric adenocarcinoma.Ann Surg. 1997;225:262-267.
Karatzas G, Kouskos E, Kouraklis G, Mantas D, Papachristodoulou A. Gastrointestinal carcinoid tumors: 10-year experience of a general surgical department.Int Surg. 2004;89:21-26.
Czaykowski P, Hui D. Chemotherapy in small bowel adenocarcinoma: 10-year experience of the British Columbia Cancer Agency.Clin Oncol (R Coll Radiol). 2007;19:143-149.
Kaklamanos IG, Bathe OF, Franceschi D, Camarda C, Levi J, Livingstone AS. Extent of resection in the management of duodenal adenocarcinoma.Am J Surg. 2000;179:37-41.
Dabaja BS, Suki D, Pro B, Bonnen M, Ajani J. Adenocarcinoma of the small bowel: presentation, prognostic factors, and outcome of 217 patients.Cancer. 2004;101:518-526.
Bakaeen FG, Murr MM, Sarr MG, Thompson GB, Farnell MB, Nagorney DM, Farley DR, van Heerden JA, Wiersema LM, Schleck CD. What prognostic factors are important in duodenal adenocarcinoma.Arch Surg. 2000;135:635-641; discussion 641-642.
Howe JR, Karnell LH, Menck HR, Scott-Conner C. The American College of Surgeons Commission on Cancer and the American Cancer Society. Adenocarcinoma of the small bowel: review of the National Cancer Data Base, 1985-1995.Cancer. 1999;86:2693-2706.
Nikou GC, Lygidakis NJ, Toubanakis C, Pavlatos S, Tseleni-Balafouta S, Giannatou E, Mallas E, Safioleas M. Current diagnosis and treatment of gastrointestinal carcinoids in a series of 101 patients: the significance of serum chromogranin-A, somatostatin receptor scintigraphy and somatostatin analogues.Hepatogastroenterology. 2005;52:731-741.
Stang A, Stegmaier C, Eisinger B, Stabenow R, Metz KA, Jöckel KH. Descriptive epidemiology of small intestinal malignancies: the German Cancer Registry experience.Br J Cancer. 1999;80:1440-1444.
Kaltsas GA, Mukherjee JJ, Isidori A, Kola B, Plowman PN, Monson JP, Grossman AB, Besser GM. Treatment of advanced neuroendocrine tumours using combination chemotherapy with lomustine and 5-fluorouracil.Clin Endocrinol (Oxf). 2002;57:169-183.
Locher C, Malka D, Boige V, Lebray P, Elias D, Lasser P, Ducreux M. Combination chemotherapy in advanced small bowel adenocarcinoma.Oncology. 2005;69:290-294.