10.1245/ASO.2005.03.009
Annals of Surgical Oncology 12:971-980 (2005)
© 2005 Society of Surgical Oncology
Limitations of Ampullectomy in the Treatment of Nonfamilial Ampullary Neoplasms
Kevin K. Roggin, MD1,
Jen Jen J. Yeh, MD1,
Cristina R. Ferrone, MD1,
Elyn Riedel, MS2,
Hans Gerdes, MD3,
David S. Klimstra, MD4,
David P. Jaques, MD1 and
Murray F. Brennan, MD1
1 Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
2 Department of Biostatistics and Epidemiology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
3 Department of Medicine, Gastroenterology Division, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
4 Department of Pathology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
Correspondence: Address correspondence and reprint requests to: Murray F. Brennan, MD; E-mail: brennanm{at}mskcc.org.
 |
ABSTRACT
|
|---|
Background: Pancreaticoduodenectomy (PD) is the standard surgical management of invasive ampullary neoplasms. A rational plan to use ampullectomy (AMP) for lesions at this location requires careful analysis of preoperative clinical information (comorbidity, lesion size, and histopathology) and intraoperative data (frozen section pathology and clinical impression) to properly select patients for this treatment.
Methods: We identified 140 consecutive cases of nonfamilial ampullary neoplasms from our prospective institutional database over a 7-year period (1996–2003). Preoperative and intraoperative factors were analyzed and related to outcomes.
Results: AMP was planned for 37 patients with small lesions (median, 1.86 cm [range, 0–3 cm] vs. 2.6 cm [range, 0–8 cm] in PD). AMP was converted to PD because of the extent of disease in three and an intraoperative diagnosis of invasive cancer in five patients. Preoperative biopsy had a diagnostic accuracy of 79% (97 of 123) but missed 23 cancers. Intraoperative frozen section had a diagnostic accuracy of 84%; two cases of high-grade dysplasia and invasive cancer were missed. Patients with invasive cancer treated by AMP had a decreased recurrence-free and disease-specific survival compared with those treated by PD. Lymphatic spread of disease was associated with diminished long-term survival. Although both vascular invasion and tumor stage independently predicted lymphatic metastases, both were limited by their sensitivity.
Conclusions: The reduced morbidity and mortality of AMP makes this the preferred treatment for benign lesions of the ampulla. Conversion to PD should be considered when intraoperative or final pathology identifies invasive adenocarcinoma. Refinement of clinicopathologic factors may reduce the occasional PD for benign disease and AMP for malignancy.
Key Words: Ampullectomy • Pancreaticoduodenectomy • Periampullary neoplasms • Adenocarcinoma
|
INTRODUCTION
|
|---|
Periampullary neoplasms are a heterogeneous group of tumors arising from the ampulla of Vater. Adenocarcinomas at this location exhibit more favorable biological behavior than similar tumors of the adjacent pancreas or common bile duct. Standard surgical management of periampullary adenocarcinomas is resection by pancreaticoduodenectomy (PD).1 Advocates claim that adequate tumor clearance, accurate staging, and long-term survival rates as high as 30% to 50% rationalize its use.2,3 These purported advantages are juxtaposed by perioperative morbidity rates that can approach 50%.4,5
Recent paradigms in the treatment of other early-stage cancers (e.g., breast and colorectal malignancies) favor the use of less invasive modalities in place of more radical procedures. Despite inadequate scientific data to support its use, local resection of invasive ampullary cancers by endoscopic mucosal resection or ampullectomy (AMP) is considered by some to be an adequate alternative to PD.6,7 Unfortunately, recent reports indicate that, in most centers, the diagnostic accuracy of preoperative biopsy for periampullary neoplasms may be as low as 40%.8,9 In addition, the inability to address locoregional lymphatic metastases is another major limitation of this procedure.10 This omission may lead to inaccurate staging and inadequate clearance of regional disease, both of which have deleterious effects on optimal cancer care. In lieu of combining AMP with lymphadenectomy, there is no rationale to support its use.
This study was designed to investigate the recent use of AMP at a tertiary referral center that treats a large volume of periampullary malignancies and to compare it with the standard of care (PD). In addition, we sought to characterize the accuracy rates of preoperative and intraoperative biopsies for periampullary neoplasms treated at our institution. Finally, we attempted to identify perioperative clinicopathologic variables that may select appropriate patients for AMP.
|
METHODS
|
|---|
After institutional review board approval was obtained (waiver of authorization WA0253-04), the Memorial Sloan-Kettering Cancer Center (MSKCC) prospective pancreatic cancer database was queried to identify patients with periampullary neoplasms during the study period (January 1, 1996, through December 31, 2003). Since 1983, patients with resected pancreatic neoplasms treated at MSKCC have been entered into and stored in the password-protected computer database. Because this database is primarily used to track invasive cancers, we also searched the MSKCC institutional database by procedure codes for both AMP (Current Procedural Terminology code 48148) and PD (Current Procedural Terminology codes 48150, 48152, 48153, and 48154).
All patients with a diagnosis of familial adenomatous polyposis and nonadenocarcinoma histopathology (i.e., sarcomas, neuroendocrine/carcinoid tumors, and metastatic lesions) were excluded from further analysis. Surgical decision making was independent of protocol. Discretion between AMP and PD was by the operating surgeon, but it seemed that tumor size, perioperative diagnosis of cancer, margin status, and patient comorbidities all influenced the choice of operation. Complications were defined according to strict criteria set forth by surgical secondary events at MSKCC.11
Our database review generated a list of patient medical record numbers, names, and surgery dates. Confidential patient information was encrypted in a password-protected database and used to initiate a complementary chart review. All preoperative pathologic specimens from outside institutions were reviewed by the MSKCC Department of Pathology.
Patient and disease characteristics for each surgical group are presented and were compared by using Fisher’s exact test for categorical data and the Wilcoxon rank sum test for continuous data. To investigate the association of perioperative clinicopathologic variables with lymph node metastases, we used Fisher’s exact test for categorical variables and the Wilcoxon rank sum test for continuous data. The variables included age at operation; symptoms (jaundice and pancreatitis); use of preoperative endoscopic ultrasonography (EUS); whether the mass was discovered on imaging; whether the mass was discovered on EUS; preoperative size, intraoperative size, and site of tumor; vascular invasion; and perineural invasion. Although the pathologic size was not known until operation, we also wanted to investigate whether the actual size of the tumor was associated with nodal status. Those variables (significant at the .10 level) were entered into a multivariate logistic regression model to determine what variables are independent predictors for lymph node status. The analysis for invasive cancer included all 128 patients. The analysis for nodal status included the PD patients with invasive cancer (n = 91) because AMP patients did not have a lymph node dissection.
|
RESULTS
|
|---|
Surgical Management of Periampullary Neoplasms
During the 7-year study period (1996–2003), 128 patients with nonfamilial periampullary neoplasms had definitive surgical treatment at MSKCC. AMP was planned for 37 patients with small periampullary lesions (median, 1.5 cm; range, .4–4.2 cm). Ninety-one patients with larger tumors (median, 2.4 cm; range, 0–7 cm; P = .002 vs. AMP) had PD. A total of eight patients in the AMP group were converted to PD because of the extent of disease in three patients and an intraoperative discovery of invasive cancer in five patients (Table 1
). Overall, 29 patients had AMP and 99 had PD for their periampullary lesions.
Patient and Disease Characteristics by Treatment Group
Preoperative and postoperative clinicopathologic variables for patients who had AMP and PD are listed in Tables 2 and 3. The median age at the time of operation, use of EUS and diagnostic laparoscopy, and final pathologic diagnosis were all statistically different between treatment groups. Compared with the PD group, patients who had AMP were younger and more likely to have had preoperative EUS, and they had diagnostic laparoscopy less often before definitive surgical treatment.
EUS was performed on a total of 30 patients: 12 patients in the AMP group and 18 patients in the PD group. None of the AMP patients had evidence of invasion (0 of 12). Eleven patients in the PD group had invasion on EUS; two patients had no invasion, and another five had incomplete endoscopy reports. One of the patients in the PD group (patient 8; Table 1
) initially had an AMP for a subcentimeter tubulovillous adenoma with invasion on EUS at an outside institution. The final pathologic diagnosis (from the AMP) was invasive adenocarcinoma, and she was admitted 2 weeks later to MSKCC for a definitive PD.
PD was associated with a statistically significant difference in perioperative morbidity compared with AMP (Table 3). The rate of surgical complications in the PD group (67%) was more than twice the frequency in the AMP group (31%; P = .001). Complications in the PD group were more severe; the median of the highest-grade complication (scale 0–5) was 3 for PD, compared with 2 for AMP. Five patients died after PD. No postoperative deaths occurred after AMP.
Accuracy of Perioperative Biopsy
Preoperative biopsy results were available in all but five patients; one patient in the AMP group and four in the PD group were operated on without a preoperative diagnosis. Whereas most PD patients had a preoperative diagnosis of invasive adenocarcinoma (70%), only five patients (17%) in the AMP group had a preoperative diagnosis of cancer. Most of the AMP patients (59%) had benign disease (ranging from hyperplasia to adenomas with low-grade dysplasia). Fourteen (70%) of the 20 patients with high-grade dysplasia (HGD) had PD as definitive treatment; 6 were treated by AMP.
Ninety-nine patients (77%) had a postoperative diagnosis of invasive cancer, and preoperative biopsy identified only 72 of these cancers. Four patients with a postoperative diagnosis of invasive cancer had no preoperative biopsy. Eleven patients with a preoperative diagnosis of benign disease and 12 patients with HGD had invasive cancer on final pathologic examination (Table 4). Overall, preoperative biopsy identified 76% (72 of 95) of the patients with malignant lesions and was correct in 79% of all cases (97 of 123).
Intraoperative frozen-section analysis was performed on a total of 26 patients; all but 4 were in the AMP group. Although the frozen-section diagnosis was correct in 22 patients (84%), it failed to diagnose 2 cases of HGD and 2 cases of invasive cancer. In the eight patients with invasive cancer who had an intraoperative biopsy, six cancers were correctly identified (sensitivity, 75%), and four of these cases were subsequently converted to PD. One of the two false-negative results occurred in a patient with a microscopic focus of cancer; the other patient had a pre-operative diagnosis of cancer.
Survival for Treatment Groups
Survival was calculated for the 99 patients with invasive periampullary cancers (Figs. 1 and 2); the median follow-up for the survivors was 18 months. All postoperative deaths were included in the survival calculations. Seven of eight AMP patients experienced recurrent disease at a median of 15 months, and the median recurrence-free survival was not reached for the PD group (91 patients). Two-year estimates of recurrence-free survival were 0% in the AMP group versus 48% (95% confidence interval, 37%–60%). Only one of the eight patients with invasive cancer treated by AMP was alive at last follow-up (median disease-specific survival, 25 months), and 68 of 91 patients in the PD group survived the study period (median disease-specific survival was not reached). The two-year estimated disease-specific survival was 58% in the AMP group (95% confidence interval, 22%–95%) versus 78% in the PD group (95% confidence interval, 68%–88%).
View larger version (16K):
[in this window]
[in a new window]
|
FIG. 1. Recurrence-free survival in patients with invasive periampullary cancers stratified by procedure. The Kaplan-Meier survival curve for recurrence-free survival is shown with the time (in months) from the date of surgery on the ordinate, and the percentage without recurrence is plotted on the abscissa. The 2-year estimates of recurrence-free survival (95% confidence interval) were 0% for ampullectomy (AMP) and 48% (37%–60%) for pancreaticoduodenectomy (PD). The log-rank P value was .08. The Wilcoxon P value was .38. Tick marks indicate last follow-up.
|
|
View larger version (16K):
[in this window]
[in a new window]
|
FIG. 2. Disease-specific survival in patients with invasive periampullary cancers stratified by procedure. The Kaplan-Meier survival curve for disease-specific survival is shown with the time (in months) from the date of surgery on the ordinate, and the percentage surviving is plotted on the abscissa. The 2-year estimates of disease-specific survival (95% confidence interval) were 58% (22%–95%) for ampullectomy (AMP) and 78% (68%–88%) for pancreaticoduodenectomy (PD). The log-rank P value was .01. The Wilcoxon P value was .21. Tick marks indicate last follow-up.
|
|
Detailed clinical information for the eight patients with invasive cancer treated by AMP is shown in Table 5. Five of the eight patients had conditions diagnosed as invasive cancer on preoperative biopsy; two, on intraoperative biopsy; and one, on final pathology. Complete resection with histologically negative margins was possible in all but three patients. Seven of the eight patients had recurrent disease. Four of the recurrences were locoregional (head of the pancreas or peritoneum), and one patient had both locoregional and distant recurrences (peritoneal and bilobar hepatic metastases). Detailed information was not available on two patients with recurrent disease who were treated at outside hospitals. Salvage PD was attempted in only one patient, whose disease recurred at 19 months after surgery in the head of the pancreas (Table 5; patient 5). Four patients with recurrent locoregional disease had noncurative bypass procedures.
Effect of Lymph Node Involvement on Survival
Lymphatic metastases were present in 44 of the 91 patients in the PD group. Patients in the AMP group were excluded from this analysis because, by definition, lymph nodes were not routinely sampled in this procedure. Both recurrence-free and disease-specific survival were significantly decreased in patients with positive lymph nodes (Figs. 3 and 4). The 2-year estimates of recurrence-free survival were 66% for patients without lymphatic metastases (95% confidence interval, 51%–82%) and 28% for patients with lymphatic metastases (95% confidence interval, 13%–44%). The 2-year estimated disease-specific survival was 90% for patients without lymphatic metastases (95% confidence interval, 80%–99%) and 63% for patients with lymphatic metastases (95% confidence interval, 45%–81%).
View larger version (16K):
[in this window]
[in a new window]
|
FIG. 3. Effect of lymphatic metastasis on recurrence-free survival in patients with invasive cancers treated by pancreaticoduodenectomy (n = 91). The Kaplan-Meier survival curve for recurrence-free survival is shown with the time (in months) from the date of surgery on the ordinate, and the percentage without recurrence is plotted on the abscissa. The 2-year estimates of disease-specific survival (95% confidence interval) were 66% (51%–82%) for patients without lymphatic metastases and 28% (13%–44%) for patients with lymphatic metastases. The log-rank P value was .0002. LN, lymph node status. Tick marks indicate last follow-up.
|
|
View larger version (15K):
[in this window]
[in a new window]
|
FIG. 4. Effect of lymphatic metastasis on disease-specific survival in patients with invasive cancers treated by pancreaticoduodenectomy (n = 99). The Kaplan-Meier survival curve for disease-specific survival is shown with the time (in months) from the date of surgery on the ordinate, and the percentage surviving is plotted on the abscissa. The 2-year estimates of disease-specific survival (95% confidence interval) were 90% (80%–99%) for patients without lymphatic metastases and 63% (45%–81%) for patients with lymphatic metastases. The log-rank P value was .01. LN, lymph node status. Tick marks indicate last follow-up.
|
|
Given the significant effect of lymphatic metastases on both recurrence-free and disease-specific survival, perioperative clinical and pathologic variables were tested as surrogate markers for lymphatic involvement. On univariate analysis, vascular invasion (P < .001), perineural invasion (P = .03), and tumor invasiveness (T stage; P < .001) were all statistically significant (Table 6). Insignificant variables included patient age, symptoms (pancreatitis or jaundice), previous cancer, lesion size, and location in the ampulla (i.e., site). When these variables were analyzed in a logistical regression model, perineural invasion was no longer significantly associated with lymphatic metastases. Only vascular invasion and T stage were independent predictors of lymph node involvement. This statistical correlation was offset by the fact that even in patients without vascular invasion, 18 patients (28%) still had positive lymph nodes. Furthermore, for reasons that are not entirely clear, there was an unusually high rate of lymphatic involvement (42%) in patients with even early-stage tumors.
View this table:
[in this window]
[in a new window]
|
TABLE 6. Clinicopathologic factors associated with lymphatic metastases in patients having pancreaticoduodenectomy (n = 99)
|
|
|
DISCUSSION
|
|---|
Since Halsted’s seminal incorporation of AMP into the surgical armamentarium for periampullary neoplasms in 1898,12 surgeons have struggled to effectively use this less radical alternative to PD. Despite high rates of perioperative morbidity, PD remains the standard of care because it effectively removes the primary tumor, provides tissue for accurate locoregional staging, and offers a 30% to 50% chance of long-term survival.2,3 The allure of AMP stems from the theoretical advantage of being able to extirpate early periampullary malignancies without the deleterious consequences of PD. Furthermore, similar treatment paradigms have been used with varying degrees of success in other areas of surgical oncology (e.g., transanal excision of T1 rectal cancers13). Although most would agree that AMP is a safe alternative to PD, few believe that there is evidence-based justification for its use.
Uniform indications for AMP have not been widely accepted. A 1996 report of 27 patients with protean histopathology is the foundation for currently accepted indications for AMP.7 On the basis of this small, heterogeneous population of patients, the authors concluded that small (<3-cm) benign periampullary lesions, neuroendocrine tumors, and early-stage (T1) ampullary invasive cancers could all be effectively treated by AMP.7 Despite a paucity of data supporting its use, local resection has been reported by several centers over the last decade.14–18 Because lymphatic metastases from periampullary cancers are independently associated with decreased long-term survival after PD,1,19 failure to address the locoregional draining basins with AMP constitutes suboptimal oncological therapy.20,21 Concern over the liberal use of AMP is justified by reports of lymphatic metastases in pathologic T1 periampullary cancers in almost 25% of patients10 and microscopic lymphatic invasion in up to 50% of patients.19,20
Our intent was to describe the recent use of AMP at a large-volume tertiary cancer center with expertise in the management of periampullary neoplasms. We sought to report our recent experience with AMP and compare it with the standard of care (PD). AMP was associated with significantly lower perioperative morbidity and mortality rates compared with PD. This short-term benefit was offset by the statistically significant adverse effect on recurrence-free and disease-specific survival in patients with invasive cancers. Although the number of patients in the AMP group with invasive cancer was small and follow-up was limited, at least in our series, all but one patient experienced disease recurrence and eventually died of their disease. It seemed that because most deaths occurred from locoregional recurrence, AMP may have neglected disease that had already spread to draining lymphatic basins. Although we were able to identify both vascular invasion and tumor invasiveness as independent predictors of lymph node involvement, neither was sensitive enough to be used without an unacceptable margin of error. Proper use of AMP as definitive treatment for invasive cancers requires further refinement of clinicopathologic risk factors to identify tumors with aggressive biology and a propensity for lymphatic metastases. Molecular analysis of primary tumor characteristics at either the gene or protein level may elucidate the true biologic behavior of these uncommon, but potentially treatable, neoplasms. With an improved understanding of these tumors, perhaps we can maximize survival after appropriate surgical resection.
The accuracy rates of preoperative biopsies for periampullary neoplasms can be as low as 40% to 60%.8,9 In our series, preoperative and intraoperative biopsies were correct in at least 75% of cases. Both techniques were highly sensitive in the detection of invasive cancer. We believe that our diagnostic precision can be at least partially explained by a dedicated policy of reviewing all non-MSKCC biopsy specimens by a dedicated, organ-specific team of expert pathologists. Furthermore, most patients had creased the rate of sampling error. In our hands, frozen sectioning identified six previously occult cancers that altered the operative management from AMP to PD in four patients. In addition, just over 25% of patients with a final diagnosis of invasive cancer had "benign" preoperative biopsy results. Therefore, when AMP is considered for periampullary neoplasms, our data indicate that routine intraoperative frozen section should be performed.
Our current approach to the surgical management of nonfamilial periampullary neoplasms is summarized in a treatment algorithm (Fig. 5). Periampullary neoplasms should be thoroughly investigated before surgery by a comprehensive history and physical examination, high-quality cross-sectional imaging (with helical computed tomography or magnetic resonance imaging), and invasive upper gastrointestinal endoscopy with EUS. Dedicated review of all preoperative biopsy samples by an experienced pathologist is essential to improve diagnostic accuracy. Intraoperative assessment, whether by diagnostic laparoscopy or celiotomy, may help planning of the appropriate surgical procedure. If the disease remains localized to the periampullary region, then pathologic characteristics should dictate the choice of operations. Although AMP may be suitable for benign disease, our data support the use of PD for invasive periampullary adenocarcinoma. If AMP is attempted for either benign disease or HGD, the surgeon should perform an intraoperative frozen section to rule out adenocarcinoma. Should the intraoperative frozen section reveal cancer, we recommend conversion to PD. In the unlikely event that after AMP the final pathology report reveals an occult adenocarcinoma, then strong consideration should be made for an interval PD. The appropriate surgical management of HGD remains controversial and should be dictated by balancing patient comorbidities with the radicality of the operative procedure.
View larger version (24K):
[in this window]
[in a new window]
|
FIG. 5. Summary treatment algorithm for periampullary neoplasms. Appropriate surgical management of periampullary neoplasms requires a thorough preoperative diagnostic workup, accurate histopathologic diagnosis, and meticulous intraoperative assessment. Ampullectomy may be suitable for benign disease after intraoperative frozen section. The appropriate surgical management of HGD remains controversial and should be dictated by balancing patient comorbidities with the radicality of the operative procedure. Pancreaticoduodenectomy is indicated for the treatment of all invasive periampullary cancers. HGD, high-grade dysplasia; CA, cancer.
|
|
This study was designed to report our recent use of and outcomes associated with AMP for periampullary neoplasms. Our data indicate that the reduced morbidity and mortality of AMP make this the preferred treatment for benign lesions of the ampulla. Conversion to PD should be considered when intraoperative or final pathologic examination identifies invasive adenocarcinoma. Despite higher rates of perioperative complications and death, PD is associated with improved long-term survival for invasive periampullary neoplasms. On the basis of these data, it seems that further refinement of clinicopathologic factors may reduce the occasional PD for benign disease and AMP for malignancy.
|
FOOTNOTES
|
|---|
Presented at the 58th Annual Cancer Symposium of the Society of Surgical Oncology, Atlanta, Georgia, May 3–6, 2005.
Received for publication March 3, 2005.
Accepted for publication July 29, 2005.
|
REFERENCES
|
|---|
- Howe JR, Klimstra DS, Moccia RD, Conlon KC, Brennan MF. Factors predictive of survival in ampullary carcinoma. Ann Surg 1998;228:87–94.[CrossRef][Medline]
- Cameron JL, Crist DW, Sitzmann JV, et al. Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer. Am J Surg 1991;161:120–4; discussion 124–5.[CrossRef][Medline]
- Trede M, Schwall G. The complications of pancreatectomy. Ann Surg 1988;207:39–47.[Medline]
- Schmidt CM, Powell ES, Yiannoutsos CT, et al. Pancreaticoduodenectomy: a 20-year experience in 516 patients. Arch Surg 2004;139:718–25; discussion 725–7.[Abstract/Free Full Text]
- Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas—616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000;4:567–79.[CrossRef][Medline]
- Tokunaga Y, Hosogi H, Hoppou T, Nakagami M, Tokuka A, Ohsumi K. A case of ampullary carcinoma successfully managed with endoscopic snare resection. Surg Laparosc Endosc Percutan Tech 2002;12:273–6; discussion 276–8.[Medline]
- Rattner DW, Fernandez-del Castillo C, Brugge WR, Warshaw AL. Defining the criteria for local resection of ampullary neoplasms. Arch Surg 1996;131:366–71.[Abstract]
- Ryan DP, Schapiro RH, Warshaw AL. Villous tumors of the duodenum. Ann Surg 1986;203:301–6.[Medline]
- Komorowski RA, Beggs BK, Geenan JE, Venu RP. Assessment of ampulla of Vater pathology. An endoscopic approach. Am J Surg Pathol 1991;15:1188–96.[Medline]
- Beger HG, Treitschke F, Gansauge F, Harada N, Hiki N, Mattfeldt T. Tumor of the ampulla of Vater: experience with local or radical resection in 171 consecutively treated patients. Arch Surg 1999;134:526–32.[Abstract/Free Full Text]
- Martin RC II, Brennan MF, Jaques DP. Quality of complication reporting in the surgical literature. Ann Surg 2002;235: 803–13.[CrossRef][Medline]
- Finney JMT. A personal appreciation of Dr. Halsted. Bull Johns Hopkins Hosp 1923;36:28.3.
- Stipa F, Lucandri G, Ferri M, Casula G, Ziparo V. Local excision of rectal cancer with transanal endoscopic microsurgery (TEM). Anticancer Res 2004;24:1167–72.[Medline]
- Farouk M, Niotis M, Branum GD, Cotton PB, Meyers WC. Indications for and the technique of local resection of tumors of the papilla of Vater. Arch Surg 1991;126: 650–2.[Abstract]
- Isaksson G, Ihse I, Andren-Sandberg A, Evander A, Lofgren B, Millbourn E. Local excision for ampullary carcinoma. An alternative treatment for patients unfit for pancreatectomy. Acta Chir Scand 1982;148:163–5.[Medline]
- Chiappetta A, Sperti C, Bonadimani B, et al. Surgical experience with adenocarcinoma of the ampulla of Vater. Am Surg 1986;52:603–6.[Medline]
- Robertson JF, Imrie CW. Local excision of ampullary carcinoma. Acta Chir Scand 1986;152:537–9.[Medline]
- Goldberg M, Zamir O, Hadary A, Nissan S. Wide local excision as an alternative treatment for periampullary carcinoma. Am J Gastroenterol 1987;82:1169–71.[Medline]
- Talamini MA, Moesinger RC, Pitt HA, et al. Adenocarcinoma of the ampulla of Vater. A 28-year experience. Ann Surg 1997;225:590–9; discussion 599–600.[CrossRef][Medline]
- Monson JR, Donohue JH, McEntee GP, et al. Radical resection for carcinoma of the ampulla of Vater. Arch Surg 1991;126:353–7.[Abstract]
- Bottger T, Boddin J, Kuchle R, Junginger T. Does the extent of lymph node dissection have an effect on morbidity and prognosis after resection of the head of the pancreas for ductal or periampullary pancreatic carcinoma (in German)? Langenbecks Arch Chir 1997;382:209–15.[Medline]
This article has been cited by other articles:
|
|
|
|
 
M. Falconi, S. Crippa, I. Dominguez, G. Barugola, P. Capelli, S. Marcucci, S. Beghelli, A. Scarpa, C. Bassi, and P. Pederzoli
Prognostic Relevance of Lymph Node Ratio and Number of Resected Nodes after Curative Resection of Ampulla of Vater Carcinoma
Ann. Surg. Oncol.,
November 1, 2008;
15(11):
3178 - 3186.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
ABSTRACT
INTRODUCTION
