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Figure 1.
Actuarial survival curves of patients undergoing pancreatoduodenectomy, including operative deaths (P = .06) (Cox-Mantel test).

Actuarial survival curves of patients undergoing pancreatoduodenectomy, including operative deaths (P = .06) (Cox-Mantel test).

Figure 2.
Actuarial local control curves of patients undergoing pancreatoduodenectomy, including operative deaths (P<.01) (Cox-Mantel test).

Actuarial local control curves of patients undergoing pancreatoduodenectomy, including operative deaths (P<.01) (Cox-Mantel test).

Table 1. 
Patient Characteristics*
Patient Characteristics*
Table 2. 
Postoperative Complications
Postoperative Complications
Table 3. 
Univariate Analysis of Clinical and Pathological Variables After Curative Resection of Carcinoma of the Pancreatic Head in 46 Patients*
Univariate Analysis of Clinical and Pathological Variables After Curative Resection of Carcinoma of the Pancreatic Head in 46 Patients*
Table 4. 
Independent Prognostic Variables Identified by the Cox Proportional Hazard Model
Independent Prognostic Variables Identified by the Cox Proportional Hazard Model
1.
Parker  SLTong  TBolden  SWingo  PA Cancer statistics, 1996. CA Cancer J Clin. 1996;465- 27Article
2.
Trede  MSchwall  GSaeger  H Survival after pancreaticoduodenectomy: 118 consecutive resections without a mortality. Ann Surg. 1990;221447- 458Article
3.
Gerr  RJBrennan  MF Prognostic indicators for survival after resection of pancreatic adenocarcinoma. Am J Surg. 1993;16568- 73Article
4.
Yeo  CJCameron  JLLillemoe  KD  et al.  Pancreaticoduodenectomy for cancer of the head of pancreas: 201 patients. Ann Surg. 1995;221721- 733Article
5.
Fortner  JGKlimstra  DSSenie  RTMaclean  BJ Tumor size is the primary prognosticator for pancreatic cancer after regional pancreatectomy. Ann Surg. 1996;223147- 153Article
6.
Fuhrman  GMLeach  SDStaley  CA  et al.  Rationale for en bloc vein resection in the treatment of pancreatic adenocarcinoma adherent to the superior mesenteric-portal vein confluence. Ann Surg. 1996;223154- 162Article
7.
Conlon  KCKlimstra  DSBrennan  MF Long-term survival after curative resection for pancreatic ductal adenocarcinoma: clinico-pathologic analysis of 5-year survivors. Ann Surg. 1996;223273- 279Article
8.
Cameron  JLPitt  HAYeo  CJLillimoe  KDKaufman  HSColeman  J One hundred and forty-five consecutive pancreaticoduodenectomies without a mortality. Ann Surg. 1993;217430- 435; discussion 435-438Article
9.
Lillemoe  KD Current management of pancreatic carcinoma. Ann Surg. 1995;221133- 148. ReviewArticle
10.
Andrén-Sandenberg  AIhse  I Factors influencing survival after total pancreatectomy in patients with pancreatic cancer. Ann Surg. 1983;198605- 610Article
11.
Hermanek  PSobin  LHand the International Union Against Cancer (UICC), TNM Classification of Malignant Tumours. 4th ed. 2nd Rev ed. Berlin, Germany Springer1992;
12.
Traverso  LWLongmire  WP Preservation of the pylorus in pancreaticoduodenectomy. Surg Gynecol Obstet. 1978;146959- 962
13.
Mantel  N Evaluation of surgical data and two new rank order statistics arising in its consideration. Cancer Chemother Rep. 1996;50163- 170
14.
Cox  DROakes  D Analysis of Survival Data.  London, England Chapman & Hall1984;
15.
Crucitti  FDoglietto  GBFrontera  D  et al.  Integrated radiosurgical treatment of resectable head carcinoma. Pancreas. 1998;1631- 39Article
16.
Trodella  LMorganti  AGValentini  VDoglietto  GBCellini  NCrucitti  F Carcinoma of the pancreatic head: therapy: intraoperative radiotherapy. Rays. 1995;20316- 325
17.
Nakao  AHorisawa  MKondo  T  et al.  Total pancreatectomy combined with resection of the portal vein employing portal perfusion method. Shujutsu. 1983;371- 6
18.
Crist  DWSitzmann  JVCameron  JL Improved hospital morbidity, mortality, and survival after the Whipple procedure. Ann Surg. 1987;206358- 365Article
19.
Grace  PAPitt  HATompkins  RKDenBesten  LLongmire  WP Decreased morbidity and mortality after pancreaticoduodenectomy. Am J Surg. 1986;151141- 149Article
20.
Cameron  JLCrist  DWSitzmann  JV  et al.  Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer. Am J Surg. 1991;161120- 125Article
21.
Nagakawa  TKurachi  MKonishi  KMiyazaki  I Translateral retroperitoneal approach in radical surgery for pancreatic carcinoma. Jpn J Surg. 1982;12229- 233Article
22.
Sato  TSaito  YNoto  TMatsuno  S Follow-up studies of radical resection for pancreaticoduodenal cancer. Ann Surg. 1977;186581- 588Article
23.
The Japan Pancreas Society, The General Rules for Surgical and Pathological Studies on Cancer of the Pancreas.  Tokyo, Japan Kanehara Shuppan1986;
24.
Evans  DAbbruzzese  JLee  JCleary  KRich  T Preoperative chemoradiation and pancreatico-duodenectomy for adenocarcinoma of the pancreas [abstract]. Proc Am Soc Clin Oncol. 1994;226692
25.
Nagakawa  TKonishi  IUeno  K  et al.  Surgical treatment of pancreatic cancer. Int J Pancreatol. 1991;9135- 143
26.
Moossa  AR Surgical treatment of pancreatic cancer. Preece  PECuschieri  ARosin  RDeds.Cancer of the Bile Ducts and Pancreas Philadelphia, Pa WB Saunders Co1989;197- 208
27.
Warren  KWChoe  DSPlaza  JReliham  M Results of radical resection for periampullary cancer. Ann Surg. 1988;208541- 553Article
28.
Kloppel  G Cancer of the pancreas: morphological and biological aspects. Preece  PECuschieri  ARosin  RDeds.Cancer of the Bile Ducts and Pancreas Philadelphia, Pa WB Saunders Co1989;113- 138
29.
Hiraoka  TUchino  RKanemitsu  K  et al.  Combination of intraoperative radiation with resection of cancer of the pancreas. Int J Pancreatol. 1990;7201- 207
30.
Gerard  JPPartensky  CRomestaing  PDe Laroche  GLaasami  R La radiotherapie post-opertorie des cancers resectables du pancreas exocrine: experience Lyonnaise. Bull Cancer Radiother. 1991;7833- 38
31.
Dobelbower  RRBorgelt  BBSuntharalingam  NStrubler  KA Pancreatic carcinoma treated with high-dose small volume irradiation. Cancer. 1978;411087- 1092Article
32.
Kalser  MHEllenberg  SS Pancreatic cancer: adjuvant combined radiation and chemotherapy following curative resection. Arch Surg. 1985;120899- 903Article
33.
Gudjonsson  B Cancer of the pancreas: 50 years of surgery. Cancer. 1987;602284- 2403Article
34.
Dobelbower  RRMerrick  HWKhuder  SBattle  JAHerron  LMPawlicki  T Adjuvant radiation therapy for pancreatic cancer: a 15-year experience. Int J Radiat Oncol Biol Phys. 1997;3931- 37Article
35.
Sindelar  WFKinsella  TJ Randomized trial of intraoperative radiotherapy in resected carcinoma of the pancreas [abstract]. Int J Radiat Oncol Biol Phys. 1986;12(suppl 1)148Article
36.
Gotoh  MMonden  MSakon  M  et al.  Intraoperative irradiation in resected carcinoma of the pancreas and portal vein. Arch Surg. 1992;1271213- 1215Article
37.
Evans  DTermuhlen  PMByrd  DRAmes  FCOchran  TGRich  TA Intraoperative radiation therapy following pancreaticoduodenectomy. Ann Surg. 1993;21854- 60Article
38.
Dobelbower  RRKonshi  AAMerrick  HWBronn  DGSchifeling  DKamen  C Intraoperative electron beam radiation therapy (IOEBRT) for carcinoma of the exocrine pancreas. Int J Radiat Oncol Biol Phys. 1991;20113- 119Article
39.
Zerbi  AFossati  VParolini  D  et al.  Intraoperative radiation therapy adjuvant to resection in the treatment of pancreatic cancer. Cancer. 1994;732930- 2935Article
40.
Whittington  RBryer  MPHaller  DGSolin  LJRosato  EF Adjuvant therapy of resected adenocarcinoma of the pancreas. Int J Radiat Oncol Biol Phys. 1991;211137- 1143Article
41.
Van Heerden  JAReMine  WHWeiland  LHMcIlroth  DCIlstrup  DM Total pancreatectomy for ductal adenocarcinoma of the pancreas. Am J Surg. 1981;142308- 311Article
Original Article
March 2001

Improved Survival and Local Control After Intraoperative Radiation Therapy and Postoperative RadiotherapyA Multivariate Analysis of 46 Patients Undergoing Surgery for Pancreatic Head Cancer

Author Affiliations

From the Departments of Digestive Surgery (Drs Alfieri, Di Giorgio, Bossola, and Doglietto) and Radiotherapy (Drs Morganti, Valentini, Trodella, and Cellini), Catholic University, Gemelli Hospital, Rome, Italy.

Arch Surg. 2001;136(3):343-347. doi:10.1001/archsurg.136.3.343
Abstract

Hypothesis  Despite aggressive approaches, locoregional tumor control and survival rates for patients with cancer of the pancreatic head remain disappointing. In the present study, we address whether intraoperative and adjuvant radiotherapy may improve the prognosis for these patients.

Design  A retrospective study.

Setting  University hospital.

Patients  From February 1985 to December 1995, 46 patients with an adenocarcinoma of the pancreatic head underwent pancreatic resection. The last 26 patients also received intraoperative radiotherapy (except 5 patients) and adjuvant external beam radiation therapy.

Main Outcome Measures  Demographic data, tumor characteristics, surgical procedures, 5-year survival, and local control of disease were analyzed retrospectively.

Results  The morbidity rate was not increased by adjuvant radiation therapy; it was 43% in patients treated with surgery alone and 57% in patients treated with surgery and radiotherapy (P = .1); operative mortality was 8% (n = 2) and 9% (n = 2), respectively (P = .8). Overall 5-year survival and local control were 13% and 48.6%, respectively. The mean ± SD 5-year survival was 5.5% ± 5.3% (median, 10.8 months) in the surgery-alone group and 15.7% ± 8.6% (median, 14.3 months) in the surgery plus radiotherapy group (P = .06); local control at 5 years was 29.8% ± 16.9% and 58.4% ± 19.9%, respectively (P<.01). Median metastasis-free survival was 8 and 9 months, respectively (P = .52). Multivariate analysis showed that adjuvant radiotherapy was an independent prognostic factor for survival (P<.01) and local control of the disease (P = .03).

Conclusion  The present study supports the role of radiotherapy combined with pancreatoduodenectomy for treatment of cancer of the pancreatic head because even if the improvement in overall survival is moderate, it is effective in improving the local control of the tumor.

TREATMENT FOR pancreatic cancer still remains a therapeutic challenge to surgeons. When curative resection is performed, the median and 5-year survival rates remain disappointing.1 Local recurrence of the tumor and liver metastases are the main causes of treatment failures after surgery.27 Therefore, several authors have suggested that further improvements in long-term survival may be achieved with adjuvant therapies.810 The aim of the present study is to report results in terms of survival and local control of disease in a consecutive series of 46 patients undergoing combined radiation therapy and surgery or surgery alone for carcinoma of the pancreatic head over a 10-year period in our department.

SUBJECTS AND METHODS

A retrospective cohort study was carried out on 46 patients with localized carcinoma of the pancreatic head who underwent resection between February 1985 and December 1995. In all patients ductal adenocarcinoma was diagnosed from cytologic or histologic examination findings and staged according to the Union Internationale Contre le Cancer (UICC) classification system.11

Twenty patients underwent pancreatic resection with no adjuvant therapy in the first part of our series (1985-1991); the other 26 patients underwent combined surgery and radiation therapy (1992-1995): duodenopancreatectomy, intraoperative radiation therapy (IORT), and adjuvant external beam radiation therapy (EBRT). Five patients treated with adjuvant EBRT did not receive IORT because of inavailability of the linear accelerator. The operation was always performed by the same team.

At laparotomy, if the abdominal exploration excluded metastases or locally advanced pancreatic cancer, a subtotal pancreatoduodenectomy (resection of the pancreatic head and body up to the left margin of the aorta) was performed; if possible, the entire stomach and the pylorus were preserved according to Traverso-Longmire technique.12 Pancreatic resection was always associated with lymphadenectomy extended to the hepatic portal, the common hepatic artery, the celiac trunk, the splenic vessels, the mesentericoportal trunk, and the inferior mesenteric artery.

After surgical resection, patients treated with radiation therapy had a cone of an appropriate size selected by the radiotherapist. The patients were then transferred to the linear accelerator suite. A dose of 10 Gy was delivered with a 6-MeV electron beam to the tumor bed, including the portal vein, the splenomesenteric confluence, the superior mesenteric vein up to its branches, the celiac trunk, the hepatic artery up to its division, the proximal splenic vessels, the suprarenal aorta, and the caval vein.

Four to 6 weeks postoperatively or after complete recovery, EBRT was started. A 9-mV photon beam was delivered using a box or 3-beam technique. The total dose of 50.4 Gy (International Commission on Radiological Units and Measurements, 50), subdivided into 1.8 Gy daily fractions for 5 days per week, was delivered to a target volume that included the tumor and nodal bed.

EVALUATION OF OUTCOME

In all patients, tumor-free margins in the resection specimen, depth of invasion, and regional lymph node involvement were recorded. The operative time, intraoperative blood loss, postoperative morbidity rate, hospital mortality, and overall and disease-free 5-year survival after curative resection were recorded.

At treatment completion and at 3-month intervals thereafter, patients were assessed using findings from complete medical history, physical examination, performance status, complete blood cell count, blood chemistry analysis, and abdominal ultrasound. At 6-month intervals, a chest radiograph and abdominal computed tomographic scan with contrast were also obtained.

STATISTICS

The survival rate was assessed, including operative deaths, from the date of laparotomy to the date of death or last follow-up. Survival curves were constructed according to the actuarial life table method. Differences between the curves were assessed using the log-rank test.13 The Fisher exact test was used when appropriate. Differences were considered significant at P<.05. All statistical computations were performed using a computer program (SPSS version 7.01; BMDP Statistical Software, Los Angeles, Calif).

Variables shown to be prognostically significant by univariate analysis were entered into a multivariate model. Multivariate analysis was applied using to the Cox regression proportional hazard model.14

RESULTS

The demographic data, tumor characteristics, and surgical procedures are given in Table 1. No significant differences were observed between patients treated with or without radiation therapy in terms of age, sex, tumor classification, node classification, UICC stage, and status of resection margins. Patients treated with surgery plus radiotherapy showed a significantly greater tumor diameter (P = .0097). Preliminary results concerning the IORT procedure have been reported elsewhere.15,16

The mean ± SD operative time was 414 ± 183 minutes for patients treated with surgery alone and 586 ± 118 minutes for patients also receiving IORT (P = .03). The mean ± SD intraoperative blood transfusion was 816 ± 777 mL and 1073 ± 642 mL, respectively (P = .20). The average postoperative hospital stay was 23.4 ± 16.6 days and 26.8 ± 14.3 days, respectively (P = .21).

MORBIDITY AND MORTALITY RATE

The incidence of postoperative complications was similar in patients treated with surgery alone and in those also receiving IORT (43% vs 57%) (P = .1) (Table 2). Seven patients (15%) required reoperation (2 in the surgery-alone group and 5 in the surgery plus radiotherapy group): 3 for bleeding (1 in the surgery-alone group and 2 in the surgery plus radiotherapy group), 1 for pancreatojejunostomy leakage (surgery-alone group), 1 for intra-abdominal abscess (surgery-alone group), and 2 for fascial dehiscence (surgery plus radiotherapy group). The hospital mortality rate was 8% (n = 2) after pancreatic resection alone and 9% (n = 2) when associated to IORT (P = .8).

SURVIVAL

Survival after curative resection was evaluated in all patients. None were lost to follow-up. The median follow-up was 82 months. Thirty-eight patients (82.6%) died. Thirty-six (78.3%) patients developed some form of recurrence. Local recurrence developed in 9 patients (19.6%): 6 (30%) in the surgery-alone group and 3 (11.5%) in the surgery plus radiotherapy group. Distant metastases were observed in 30 patients (65.2%): 12 (60%) in the surgery-alone group and 18 (69%) in the surgery plus radiotherapy group.

The overall 5-year survival rate was 13% ± 5.4% (median, 12.5 months); 5.5% ± 5.3% (median, 10.8 months) in the surgery-alone group and 15.7% ± 8.6% (median, 14.3 months) in patients receiving adjuvant radiotherapy (P = .06) (Figure 1). Overall, local control at 5 years was 48.6% ± 14.5% (median, 41.4 months); 29.8% ± 16.9% in the surgery-alone group and 58.4% ± 19.9% in the adjuvant therapy group (P<.01) (Figure 2). Median metastasis-free survival was 8 and 9 months, respectively (P = .52).

Univariate analysis showed that the poor survival rate was closely related with lymph node involvement, tumor extension, a tumor diameter greater than or equal to 2.5 cm, and male sex. In contrast, no significant differences were found in relation to age and blood transfusion as well as to the kind of therapy adopted, even if a relationship was shown between adjuvant radiotherapy and survival (Table 3). Of the factors found to be prognostically significant by univariate analysis, the Cox multivariate model confirmed not only that sex, nodal involvement, and tumor diameter were independent predictors of death, but most important, that adjuvant radiotherapy had a role in predicting survival (Table 4). As for local control, multivariate analysis demonstrated a higher risk of local recurrence in patients who did not receive radiotherapy and in those with lymph node involvement (Table 4).

COMMENT

In recent years pancreatic surgery has become safer, and indications for resection have increased.17 Hospital mortality has decreased18,19 with improvements in intensive care, nutritional support, and gained experience, which resulted in a decreased operative time and blood loss.20 However, efforts to extend the operative procedure to achieve wider safety margins thus far have failed to improve survival rates for patients with cancer of the pancreatic head; in fact, the 5-year survival rate is still disappointing, ranging from 2% to 19%.2123 Microscopic residual tumor, located at the site of the original tumor, and distant metastases (liver, peritoneum) are the main causes of treatment failure after pancreatoduodenectomy for pancreatic carcinoma.24

Nagakawa et al25 deem that an extensive dissection of the retroperitoneum and extrapancreatic nerve plexus is necessary for curative resection of cancer of the pancreas, and local recurrence rate of pancreatic bed often involved by tumor extension can be lower.2628 However, single cancer cells and cancer cell clumps cannot always be eradicated by surgery alone, and serious nutritional disorders (diarrhea) have appeared following this procedure.29

For these reasons, the use of adjuvant treatment such as chemotherapy, IORT, and postoperative EBRT has been proposed.3032 The standard adjuvant therapy of pancreatic adenocarcinoma treated with curative resection is still controversial. The role of radiotherapy with or without chemotherapy in resectable pancreatic cancer has yielded interesting results.15,30,32 Studies by the Gastrointestinal Tumor Study Group have shown improvement in survival with a combination of EBRT and fluorouracil chemotherapy, reporting a median survival of 18 months.33 To increase survival, the use of IORT with postoperative EBRT was also evaluated with controversial results.3439 In this case, IORT represents a "boost" dose to the subsequent external radiotherapy. Postoperative EBRT is delivered to a larger volume to destroy possible microscopic neoplastic residuals in the pancreatic stump and peripancreatic lymphatic tissues.

As demonstrated in our experience, the combination of IORT and EBRT as adjuvant therapy can be delivered safely to patients as part of a planned combined modality approach for radical resection of carcinoma of the head of the pancreas.15,40 Moreover, in this study morbidity and mortality rates in patients who received IORT were similar to those who underwent surgery alone.

In the attempt to identify important factors in predicting long-term survival, multiple variables were evaluated. Age, type of resection, and blood transfusion did not influence survival. On the contrary, in patients with tumors 2.5 cm or less in diameter, no lymph node involvement, and stage T1 and T2 tumors, the survival was significantly prolonged. As given in Table 3, women surviving the operation seemed to have a somewhat better prognosis than men (P<.01). Similar observations were made in other series10,41 reporting a correlation between female sex and a less-advanced stage of the tumor, but similar findings were not confirmed in the present study. The absence of statistical correlation between status of tumor margins and outcome is probably due to the small number of patients with microscopic residual disease.

Although use of adjuvant radiotherapy was not shown to be statistically significant by the univariate analysis, there was a trend toward a longer survival period in patients who received combined radiosurgical treatment. The adjuvant treatment group had a longer median overall survival (14.3 months) than patients who received surgery alone (10.8 months), and the 5-year survival in the surgery plus radiotherapy group was 3 times (15.7%) as high as that of the surgery-alone group (5.5%). The local control rate in the surgery plus radiotherapy group was significantly higher than in surgery-alone group (58.4% vs 29.8%, P<.009), while the metastasis-free survival remained low in both (P = .52). Adjuvant radiotherapy was confirmed to be a major determinant of survival and local control of the disease when evaluated by the Cox proportional hazard model.

In summary, the present study was not randomized; therefore, far-reaching conclusions cannot be drawn. However, our results support the utility of radiation therapy following pancreaticoduodenectomy in the treatment of pancreatic cancer because the findings represent an effective way to improve local control of tumor and, most likely, survival. Other therapeutic options such as neoadjuvant and adjuvant chemoradiotherapy might further increase survival after pancreatoduodenectomy, reducing the incidence of distant metastases.

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Article Information

Corresponding author and reprints: Sergio Alfieri, MD, Department of Digestive Surgery, Istituto Clinica Chirurgica, Catholic University–Gemelli Hospital, L.go A. Gemelli, 8, 00168 Roma, Italy (e-mail: sergioalfieri@yahoo.it).

References
1.
Parker  SLTong  TBolden  SWingo  PA Cancer statistics, 1996. CA Cancer J Clin. 1996;465- 27Article
2.
Trede  MSchwall  GSaeger  H Survival after pancreaticoduodenectomy: 118 consecutive resections without a mortality. Ann Surg. 1990;221447- 458Article
3.
Gerr  RJBrennan  MF Prognostic indicators for survival after resection of pancreatic adenocarcinoma. Am J Surg. 1993;16568- 73Article
4.
Yeo  CJCameron  JLLillemoe  KD  et al.  Pancreaticoduodenectomy for cancer of the head of pancreas: 201 patients. Ann Surg. 1995;221721- 733Article
5.
Fortner  JGKlimstra  DSSenie  RTMaclean  BJ Tumor size is the primary prognosticator for pancreatic cancer after regional pancreatectomy. Ann Surg. 1996;223147- 153Article
6.
Fuhrman  GMLeach  SDStaley  CA  et al.  Rationale for en bloc vein resection in the treatment of pancreatic adenocarcinoma adherent to the superior mesenteric-portal vein confluence. Ann Surg. 1996;223154- 162Article
7.
Conlon  KCKlimstra  DSBrennan  MF Long-term survival after curative resection for pancreatic ductal adenocarcinoma: clinico-pathologic analysis of 5-year survivors. Ann Surg. 1996;223273- 279Article
8.
Cameron  JLPitt  HAYeo  CJLillimoe  KDKaufman  HSColeman  J One hundred and forty-five consecutive pancreaticoduodenectomies without a mortality. Ann Surg. 1993;217430- 435; discussion 435-438Article
9.
Lillemoe  KD Current management of pancreatic carcinoma. Ann Surg. 1995;221133- 148. ReviewArticle
10.
Andrén-Sandenberg  AIhse  I Factors influencing survival after total pancreatectomy in patients with pancreatic cancer. Ann Surg. 1983;198605- 610Article
11.
Hermanek  PSobin  LHand the International Union Against Cancer (UICC), TNM Classification of Malignant Tumours. 4th ed. 2nd Rev ed. Berlin, Germany Springer1992;
12.
Traverso  LWLongmire  WP Preservation of the pylorus in pancreaticoduodenectomy. Surg Gynecol Obstet. 1978;146959- 962
13.
Mantel  N Evaluation of surgical data and two new rank order statistics arising in its consideration. Cancer Chemother Rep. 1996;50163- 170
14.
Cox  DROakes  D Analysis of Survival Data.  London, England Chapman & Hall1984;
15.
Crucitti  FDoglietto  GBFrontera  D  et al.  Integrated radiosurgical treatment of resectable head carcinoma. Pancreas. 1998;1631- 39Article
16.
Trodella  LMorganti  AGValentini  VDoglietto  GBCellini  NCrucitti  F Carcinoma of the pancreatic head: therapy: intraoperative radiotherapy. Rays. 1995;20316- 325
17.
Nakao  AHorisawa  MKondo  T  et al.  Total pancreatectomy combined with resection of the portal vein employing portal perfusion method. Shujutsu. 1983;371- 6
18.
Crist  DWSitzmann  JVCameron  JL Improved hospital morbidity, mortality, and survival after the Whipple procedure. Ann Surg. 1987;206358- 365Article
19.
Grace  PAPitt  HATompkins  RKDenBesten  LLongmire  WP Decreased morbidity and mortality after pancreaticoduodenectomy. Am J Surg. 1986;151141- 149Article
20.
Cameron  JLCrist  DWSitzmann  JV  et al.  Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer. Am J Surg. 1991;161120- 125Article
21.
Nagakawa  TKurachi  MKonishi  KMiyazaki  I Translateral retroperitoneal approach in radical surgery for pancreatic carcinoma. Jpn J Surg. 1982;12229- 233Article
22.
Sato  TSaito  YNoto  TMatsuno  S Follow-up studies of radical resection for pancreaticoduodenal cancer. Ann Surg. 1977;186581- 588Article
23.
The Japan Pancreas Society, The General Rules for Surgical and Pathological Studies on Cancer of the Pancreas.  Tokyo, Japan Kanehara Shuppan1986;
24.
Evans  DAbbruzzese  JLee  JCleary  KRich  T Preoperative chemoradiation and pancreatico-duodenectomy for adenocarcinoma of the pancreas [abstract]. Proc Am Soc Clin Oncol. 1994;226692
25.
Nagakawa  TKonishi  IUeno  K  et al.  Surgical treatment of pancreatic cancer. Int J Pancreatol. 1991;9135- 143
26.
Moossa  AR Surgical treatment of pancreatic cancer. Preece  PECuschieri  ARosin  RDeds.Cancer of the Bile Ducts and Pancreas Philadelphia, Pa WB Saunders Co1989;197- 208
27.
Warren  KWChoe  DSPlaza  JReliham  M Results of radical resection for periampullary cancer. Ann Surg. 1988;208541- 553Article
28.
Kloppel  G Cancer of the pancreas: morphological and biological aspects. Preece  PECuschieri  ARosin  RDeds.Cancer of the Bile Ducts and Pancreas Philadelphia, Pa WB Saunders Co1989;113- 138
29.
Hiraoka  TUchino  RKanemitsu  K  et al.  Combination of intraoperative radiation with resection of cancer of the pancreas. Int J Pancreatol. 1990;7201- 207
30.
Gerard  JPPartensky  CRomestaing  PDe Laroche  GLaasami  R La radiotherapie post-opertorie des cancers resectables du pancreas exocrine: experience Lyonnaise. Bull Cancer Radiother. 1991;7833- 38
31.
Dobelbower  RRBorgelt  BBSuntharalingam  NStrubler  KA Pancreatic carcinoma treated with high-dose small volume irradiation. Cancer. 1978;411087- 1092Article
32.
Kalser  MHEllenberg  SS Pancreatic cancer: adjuvant combined radiation and chemotherapy following curative resection. Arch Surg. 1985;120899- 903Article
33.
Gudjonsson  B Cancer of the pancreas: 50 years of surgery. Cancer. 1987;602284- 2403Article
34.
Dobelbower  RRMerrick  HWKhuder  SBattle  JAHerron  LMPawlicki  T Adjuvant radiation therapy for pancreatic cancer: a 15-year experience. Int J Radiat Oncol Biol Phys. 1997;3931- 37Article
35.
Sindelar  WFKinsella  TJ Randomized trial of intraoperative radiotherapy in resected carcinoma of the pancreas [abstract]. Int J Radiat Oncol Biol Phys. 1986;12(suppl 1)148Article
36.
Gotoh  MMonden  MSakon  M  et al.  Intraoperative irradiation in resected carcinoma of the pancreas and portal vein. Arch Surg. 1992;1271213- 1215Article
37.
Evans  DTermuhlen  PMByrd  DRAmes  FCOchran  TGRich  TA Intraoperative radiation therapy following pancreaticoduodenectomy. Ann Surg. 1993;21854- 60Article
38.
Dobelbower  RRKonshi  AAMerrick  HWBronn  DGSchifeling  DKamen  C Intraoperative electron beam radiation therapy (IOEBRT) for carcinoma of the exocrine pancreas. Int J Radiat Oncol Biol Phys. 1991;20113- 119Article
39.
Zerbi  AFossati  VParolini  D  et al.  Intraoperative radiation therapy adjuvant to resection in the treatment of pancreatic cancer. Cancer. 1994;732930- 2935Article
40.
Whittington  RBryer  MPHaller  DGSolin  LJRosato  EF Adjuvant therapy of resected adenocarcinoma of the pancreas. Int J Radiat Oncol Biol Phys. 1991;211137- 1143Article
41.
Van Heerden  JAReMine  WHWeiland  LHMcIlroth  DCIlstrup  DM Total pancreatectomy for ductal adenocarcinoma of the pancreas. Am J Surg. 1981;142308- 311Article
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