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Original Article |

Significance of the Depth of Portal Vein Wall Invasion After Curative Resection for Pancreatic Adenocarcinoma FREE

Saburo Fukuda, MD; Elie Oussoultzoglou, MD; Philippe Bachellier, MD; Edoardo Rosso, MD; Hiroshi Nakano, MD, PhD; Maxime Audet, MD; Daniel Jaeck, MD, PhD, FRCS
[+] Author Affiliations

Author Affiliations: Centre de Chirurgie Visc[[eacute]]rale et de Transplantation, H[[ocirc]]pital de Hautepierre, Universit[[eacute]] Louis Pasteur, Strasbourg, France.


Arch Surg. 2007;142(2):172-179. doi:10.1001/archsurg.142.2.172.
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Published online

Hypothesis  The depth of portal vein (PV) wall invasion is a prognostic factor for survival after curative pancreatic resection for pancreatic ductal adenocarcinoma.

Design  Retrospective clinical study.

Setting  Department of digestive surgery and transplantation.

Patients  From January 1, 1990, through December 31, 2002, 121 patients underwent a curative pancreatic resection for ductal adenocarcinoma of the pancreas. Among these, 37 pancreatic resections combined with PV resection were performed.

Main Outcome Measures  Prognostic factors for survival and predictive factors for the depth of PV wall invasion.

Results  The morbidity and mortality rates did not differ between patients undergoing or not undergoing PV resection (32.4% and 2.7% [1/37], respectively, vs 38.1% and 2.4% [2/84], respectively). The 3-year survival rate after curative pancreatic resection was significantly associated with the depth of PV wall invasion. Indeed, the 3-year overall survival rate was similar for patients with no PV invasion and those with superficial invasion into the tunica adventitia (40.0% vs 32.9%, respectively;  = .85). Deeper PV wall invasion into the tunica media or the tunica intima was associated with a poorer 1-year survival rate similar to that of patients undergoing noncurative resection (21.5% vs 34.4%, respectively; P = .53). Multivariate analysis showed that the depth of PV wall invasion, number of involved lymph nodes, and volume of blood transfusion were independent factors of overall and disease-free survival. Tumor size of 45 mm or more (evaluated by computed tomography) and angiographic type C or D on a portogram were significantly correlated with the depth of PV wall invasion. Patients presenting with both factors simultaneously had poor survival.

Conclusions  The depth of PV wall invasion significantly alters survival after curative pancreatic resection combined with PV resection. However, occasional long-term survival could be observed after curative resection in patients with deep PV wall invasion.

Figures in this Article

Extended pancreatic resection for portal vein (PV) invasion due to locally advanced pancreatic cancer was initially associated with high mortality and morbidity.13 However, during the past decade, the surgical procedure and perioperative care have improved and allowed an extended operation combined with a PV resection to be performed safely.412 According to these reports, perioperative mortality decreased to rates between 0% and 5.4%, and morbidity also decreased to rates between 12% and 41%. In view of these acceptable mortality and morbidity rates, pancreatectomy with PV resection seems justified to achieve curative resection in patients with limited local invasion of the PV. Several studies have suggested that prognosis after pancreatic and PV resections is closely related to the depth of invasion into the PV wall.1316 However, in those series, the authors included patients with various types of pathological findings and patients undergoing noncurative pancreatic resections. Therefore, the real impact of the depth of PV wall invasion as a prognostic factor for survival after a curative pancreatic resection is not fully clarified.

The aim of the present study was to determine the significance of the depth of PV wall invasion on survival in a selected group of patients who underwent a curative pancreatectomy with PV resection for ductal adenocarcinoma of the pancreas. Furthermore, predictive factors of the depth of PV wall invasion were analyzed.

From January 1, 1990, through December 31, 2002, a total of 355 patients underwent pancreatic resection for malignant or benign disease in our department of digestive surgery and transplantation. Among these, 138 patients had ductal adenocarcinoma of the pancreas and underwent a pancreatic resection with or without a PV resection. Curative pancreatic resection was defined as macroscopically and microscopically proved complete surgical removal of the tumor with clear margins of the pancreas, bile duct, PV, and retroperitoneum. According to this clinicopathological definition, 121 patients had a curative resection and 17 patients had a noncurative resection.

Among the 121 patients with a curative resection, 37 (30.6%) underwent pancreatic and PV resections. Seventy-three patients of the study population have been described in a previous study.12 Patients undergoing the PV resection were selected according to several preoperative and intraoperative criteria as previously reported.12 In brief, after exploration of the abdominal cavity for metastases and mobilization of the pancreatic head by use of the Kocher maneuver, the PV was assessed for invasion. In the case of close macroscopic adhesion with the pancreatic tumor, the PV was considered invaded, and PV resection was performed to avoid tumor rupture and cancer cell seeding. The mean ± SD age of the patients was 64.4 ± 9.7 years (age range, 35-84 years; median age, 66 years). The ratio of men to women was 58:63. Tumor size was evaluated by means of preoperative abdominal computed tomography. Preoperative celiomesenteric angiography was performed in 83 patients in whom vascular invasion was suspected on the basis of computed tomographic and magnetic resonance imaging findings. The angiographic type on the portogram was determined according to the classification by Nakao et al13 and is summarized in Figure 1. Carcinoembryonic antigen and carbohydrate antigen 19-9 tumor markers were available in 108 and 103 patients, respectively, and adjusted as recently reported by Schlieman et al.17 Operative procedures included 101 pancreaticoduodenectomies and 20 total pancreatectomies. The criteria and technique for extended lymphadenectomy and venous resection were previously described.12 The patients received an intraoperative blood transfusion when the hemoglobin level was less than 8 g/dL and according to the intraoperative blood loss, patient age, and associated comorbidities.

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Figure 1.

Subgroups of 83 patients undergoing evaluation with a preoperative arteriogram according to the classification by Nakao et al.13 A, Type A shows a normal portogram (n = 41); B, type B, unilateral narrowing (n = 20); C, type C, bilateral narrowing (n = 18); and D, type D, venous occlusion with collateral circulation (asterisk) (n = 4). PV indicates portal vein; S-MT, splenomesenteric trunk; and SMV, superior mesenteric vein.

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The status of PV wall invasion was pathologically divided into the following 3 subgroups: (1) no invasion, (2) superficial invasion into the tunica adventitia, and (3) deep invasion into the tunica media or the tunica intima.

The clinicopathological variables analyzed included the depth of PV wall invasion. Results are expressed as mean ± SD (median). Statistical analysis was performed using the appropriately unpaired t test, the χ2 test, and the Fisher exact probability test. We calculated survival rates using the Kaplan-Meier method and compared differences in survival curves using the log-rank test. Multivariate analysis was performed using the stepwise forward Cox proportional hazards regression model. Clinicopathological variables associated with the depth of PV wall invasion were determined using a logistic regression model. Differences were considered significant at P<.05.

POSTOPERATIVE OUTCOME

Three of the 121 patients died within 30 days. Among the patients undergoing PV resection, the mortality rate was 2.7% (1/37). Among those who did not undergo PV resection, the mortality rate was 2.4% (2/84) (P = .94). The causes of death were mesenteric venous infarction in the 1 patient after PV resection and sepsis with multiorgan failure due to a pancreatic fistula in the 2 patients with no PV resection. Morbidity rates were 32.4% (12/37) and 38.1% (32/84) in the 2 groups of the patients who did and did not undergo PV resection (P = .46), respectively.

SURVIVAL

The mean ± SD follow-up was 22.0 ± 20.2 months (range, 1.8-104.5 months; median, 13.6 months). Thirty-three of the 121 patients were alive after a mean ± SD follow-up of 33.8 ± 25.3 months (range, 2.6-104.5 months; median, 17 months). Overall survival rates of the patients after curative pancreatic resection with or without PV resection were 47.7% and 63.4%, respectively, at 1 year and 26.8% and 28.4%, respectively, at 3 years (P = .55; Figure 2). The disease-free survival rates of the patients after curative pancreatic resection with or without PV resection were 30.3% and 46.6%, respectively, at 1 year and 16.9% and 17.4%, respectively, at 3 years (P = .61).

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Figure 2.

Comparison of survival curves of patients who underwent pancreatic resection with and without portal vein (PV) resection. No significant difference was found between the 2 groups (P = .55).

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Survival curves of patients (1) without venous resection, (2) with venous resection but without PV wall invasion, (3) with venous resection and superficial invasion up to the tunica adventitia, (4) with venous resection and deeper invasion into the tunica media or the tunica intima, and (5) with noncurative resection are shown in Figure 3. Survival of the patients with superficial PV invasion up to the tunica adventitia (n = 13) was almost similar to that of the patients without PV resection (n = 84) and that of the patients without PV wall invasion (n = 9). The 1- and 3-year survival rates of the patients with superficial PV wall invasion up to the tunica adventitia were 65.8% and 32.9%, respectively; those of the patients without PV wall invasion were 66.7% and 40.0%, respectively (P = .85). On the other hand, the survival rate of the patients with deeper invasion into the tunica media or the tunica intima (n = 15) and that of the patients undergoing a noncurative resection (n = 17) were lower than those of the other 3 groups with several significant differences, as shown in Figure 3. Survival of the patients with superficial PV wall invasion up to the tunica adventitia was better than that of the patients with deeper invasion into the tunica media or the tunica intima, but the difference was not significant (P = .07). The 1-year survival rate of patients with deeper PV wall invasion was similar to that of patients undergoing a noncurative resection (21.5% vs 34.4%, respectively; P = .53). No 3-year survivor was registered in either group, but 1 patient with deeper PV wall invasion into the tunica intima survived longer than 3 years. The patient is still alive and was disease-free at the last follow-up examination.

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Figure 3.

Cumulative survival curves of patients with no venous resection, no invasion of the portal vein (PV) wall, superficial PV invasion up to the tunica adventitia, deeper invasion into the tunica media or the tunica intima, and noncurative resection. Significant differences were shown between patients with no venous resection and those with deeper invasion into the tunica media or the tunica intima (P = .02), between patients with no venous resection and those with noncurative resection (P<.001), between patients with no PV wall invasion and those with noncurative resection (P<.001), and between patients with superficial invasion up to the tunica adventitia and those with noncurative resection (P = .01).

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PREDICTIVE FACTORS FOR OVERALL SURVIVAL

Univariate analysis for overall survival showed that the volume of blood transfusion, depth of PV wall invasion, and number of involved lymph nodes were significant risk factors for overall survival (Table 1). Moreover, the number of these risk factors present in each patient negatively affected overall survival (Figure 4A). The 1- and 3-year overall survival of the patients without these 3 risk factors (n = 39) were 73.7% and 48.1%, respectively (median, 29 months). In the patients with 1 risk factor (n = 54), the 1- and 3-year overall survival were 56.0% and 20.3%, respectively (median, 14 months). In the patients with 2 or more risk factors (n = 28), the 1- and 3-year overall survival were 43.1% and 10.4%, respectively (median, 12 months).

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Figure 4.

Cumulative survival curves. A, Overall survival curves according to the number of the 3 independent risk factors present in each patient. B, Disease-free survival curves according to the number of the 3 independent risk factors present in each patient.

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Table Graphic Jump LocationTable 1. Univariate Analysis of Potential Predictors of Overall and Disease-Free Survival After Curative Pancreatic Resection*

Multivariate analysis confirmed that the depth of PV wall invasion, number of involved lymph nodes, and blood transfusion were independent prognostic factors for overall survival (Table 2). The highest relative risk among the 3 independent prognostic factors was observed for the depth of PV wall invasion.

Table Graphic Jump LocationTable 2. Multivariate Cox Regression Analysis of Prognostic Factors After Curative Resection
PREDICTIVE FACTORS FOR DISEASE-FREE SURVIVAL

Univariate analysis for disease-free survival showed that the volume of blood transfusion, depth of PV wall invasion, number of involved lymph nodes, and tumor size were significant risk factors (Table 1). Multivariate analysis showed that the number of involved lymph nodes, depth of PV wall invasion, and blood transfusion were also independent factors for disease-free survival (Table 2). The highest relative risk among the 3 independent prognostic factors was observed for the depth of PV wall invasion. The number of these 3 risk factors present in each patient negatively affected disease-free survival (Figure 4B).

The univariate analysis of surgical and pathological variables for intraoperative blood transfusion are given in Table 3. It appears that intraoperative transfusions were significantly associated with more extensive surgery (total pancreatectomy and PV resection), longer operation time, and more advanced disease (deeper PV wall invasion).

Table Graphic Jump LocationTable 3. Clinicopathological Factors Associated With the Volume of Intraoperative Transfusion*
PREDICTIVE FACTORS FOR THE DEPTH OF PV WALL INVASION

The univariate analysis of clinicopathological variables showed that tumor size, angiographic type on the portogram, and tumor differentiation were significantly associated with the depth of PV wall invasion (Table 4). Table 4 shows that deep PV wall invasion was significantly associated with larger tumors compared with patients presenting with no invasion or with superficial invasion of the PV (tumor size of ≥45 mm, 66.7% vs 22.7%, respectively; P = .001). According to the angiographic type, among the 15 patients with deep PV wall invasion, 5 portograms were classified as type B and 9 as type C or type D (35.7% and 64.3%, respectively; P<.001). Moreover, deep PV wall invasion was significantly associated with poor tumor differentiation (40.0% vs 15.1%; P = .02). There were 10 patients with tumors larger than 45 mm and in whom the portographic pattern was type C or type D. Six of the 15 patients with deeper PV wall invasion into the tunica media or the tunica intima fulfilled these 2 factors. Survival of these patients was extremely poor; all of them died within 20 months.

Table Graphic Jump LocationTable 4. Comparison of Clinicopathological Features of Patients According to Depth of PV Wall Invasion

The performance of portography for the diagnosis of PV wall invasion was assessed statistically. The sensitivity, specificity, and positive and negative predictive values for the absence of PV wall invasion were 100.0%, 59.4%, 33.3%, and 100.0%, respectively (Table 4).

The present study showed that PV involvement is not by itself an important prognostic factor in patients with pancreatic duct adenocarcinoma. Indeed, survival of the patients with superficial PV invasion up to the tunica adventitia was almost similar to survival of the patients without PV resection and of those without PV wall invasion. However, survival of the patients with deeper invasion into the tunica media or tunica intima was almost similar to that of the patients undergoing a noncurative resection. These results indicate that pancreaticoduodenectomy with PV resection can be the only potential cure for patients with pancreatic duct adenocarcinoma who present with PV involvement.

Several reports in the literature underlined the deleterious effect of PV wall invasion on the long-term survival of patients after pancreatic resection for carcinomas.1316 However, it is still unclear whether curative pancreatic resection with PV resection will offer a better chance of long-term survival for patients with PV wall invasion. In fact, reports included some bias because they considered together various types of primary tumor and/or included curative and noncurative resections.14,15,18 To the best of our knowledge, no report analyzed the significance of the depth of PV wall invasion after curative pancreatic resection. For this reason, this study focused only on patients with pancreatic duct adenocarcinoma who underwent a macroscopically complete and a microscopically proved curative resection to allow more accurate evaluation of the effect of depth of PV wall invasion on survival.

Numerous series have shown that the early postoperative outcome did not differ between patients who underwent PV resection and those who did not.412 Our results are in accordance with these previous reports.

The number of involved lymph nodes and tumor size were recognized in previous reports to be prognostic factors.1931 With regard to the depth of PV wall invasion, several investigators demonstrated that PV wall invasion itself was a negative prognostic factor.1,1316,18 However, only a few reports have described in detail the correlation between the depth of PV wall invasion and survival.13,14 In the present study, multivariate analysis showed that the depth of PV wall invasion (to the tunica media or tunica intima vs no invasion or to the tunica adventitia only), the number of involved lymph nodes (≥2 vs <2) and the volume of blood transfusion (≥3 vs ≤2 U) were independent factors for long-term and disease-free survival. Remarkably, the 3-year survival in the case of superficial PV wall invasion was similar to that of patients who did not require PV resection. Conversely, in the case of deep PV wall invasion, survival was dismal. However, overall survival, as shown by multivariate analysis, was also affected by the volume of blood transfusion and the number of lymph node metastases. In the case of absence of any risk factor, 1- and 3-year survival rates were favorable (73.7% and 48.1%, respectively), whereas the presence of a single risk factor significantly reduced the survival rate. However, even in that case, the 3-year survival rate remained 20.3%, which may justify an aggressive surgical approach. Therefore, deep PV wall invasion should not be considered an absolute contraindication to pancreatic resection when it constitutes the only risk factor. In such cases, an acceptable survival can be expected. The present study has indicated that the depth of PV wall invasion was a more important prognostic factor than the presence or absence of the number of lymph node metastases. Indeed, if PV wall invasion was remaining superficial, it did not affect the recurrence rate and long-term survival could be expected. Moreover, even in case of deep PV wall invasion over the tunica media, long-term survival might occasionally occur. Indeed, Leach et al6 reported that PV involvement is dependent on tumor size and location and that it is not an indicator of aggressive tumor biology. This concept could not be confirmed in our study. The probability of tumor dissemination might increase when the tumor invades the tunica media or the tunica intima. Finally, the present study showed that the volume of blood transfusion was an independent prognostic factor for survival. Indeed, in our series, the volume of blood transfusion was associated with more advanced disease. However, the immunosuppressive effect of blood transfusion on survival cannot be excluded.

Preoperative estimation of the depth of PV seems to be a key factor for management of pancreatic adenocarcinoma. Several investigations have been proposed to assess PV wall invasion, including endoscopic ultrasonography, intraoperative intraportal endovascular ultrasonography, laparoscopic ultrasonography, and percutaneous transhepatic portography with intravascular ultrasonography.3235 Some of these technologies are invasive, and not all are available in most centers. Currently, computed tomography with 3-dimensional reconstruction and angiographic magnetic resonance imaging were introduced as less invasive alternatives to assess PV wall invasion. In many centers, preoperative angiography with a portogram is still commonly used to evaluate vascular involvement. Nakao et al13 was the first to report the correlation between angiographic type on portogram findings and the pathological grade of carcinoma invasion into the PV. Similarly, the present study confirms the existence of a correlation between angiographic type on the portogram and the depth of PV wall invasion. Rösch et al36 reported that endoscopic ultrasonography is a reliable investigation to demonstrate the absence of vascular involvement. However, Aslanian et al37 recently reported that endoscopic ultrasonography has poor sensitivity, specificity, and positive diagnostic value for the diagnosis of venous involvement by pancreatic cancer. The present study showed that angiographic type on the portogram seems to be an accurate investigation to demonstrate the absence of venous involvement. In consideration of its low specificity, portography cannot be considered an accurate method to diagnose vascular involvement and cannot be recommended as a routine preoperative investigation to assess venous involvement before pancreatic resection for pancreatic adenocarcinoma.

Preoperative diagnosis of the depth of PV wall invasion remains a major concern. We tried to identify predictive factors of the depth of PV wall invasion by comparing the clinicopathological variables between patients presenting with no invasion or with superficial PV wall invasion to the tunica adventitia and those with deep PV wall invasion over the tunica media. Schlieman et al17 described that the adjusted carbohydrate antigen 19-9 level is useful to evaluate the resectability of pancreatic cancer, but the adjusted carbohydrate antigen 19-9 level in our study did not differ between patients presenting with superficial or deep PV wall invasion. In the case of a large tumor (≥45 mm) and an angiographic image obviously in favor of type C or type D venous invasion, the probability of deep PV wall invasion is high and a long-term survival cannot be expected. In such cases, it might be useful to combine resection with multimodality treatment that includes postoperative intra-arterial adjuvant chemotherapy.3840

The results after PV resection should be evaluated for long-term survival but also for quality of life. Invalidating pain, obstructive jaundice, and duodenal obstruction are frequent complications of pancreatic cancer. Pancreatic resection has been advocated as the best palliation of all these complications.41,42 Currently, a palliative resection for patients with pancreatic carcinoma can be performed safely with low mortality and acceptable morbidity in large-volume centers.41,43,44 Our results showed that perioperative mortality and morbidity were not different in patients with or without PV resection and similar to the results reported after stent palliation or surgical bypass.31,43,45 Therefore, pancreatic resection, even in the case of PV wall invasion, could be an alternative for palliative treatment of pancreatic cancer.

In conclusion, pancreatic resection with PV resection can be safely performed without increasing morbidity and mortality. However, the depth of PV wall invasion carries a deleterious effect on survival and recurrence rates, as do tumor size, the number of involved lymph nodes, and the volume of blood transfusion. To predict the depth of PV wall invasion preoperatively, tumor size and angiographic type on the portogram appeared to be useful indicators.

Correspondence: Daniel Jaeck, MD, PhD, FRCS, Centre de Chirurgie Viscérale et de Transplantation, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, Université Louis-Pateur, Avenue Molière, 67098 Strasbourg CEDEX, France (Daniel.Jaeck@chru-strasbourg.fr).

Accepted for Publication: December 12, 2005.

Author Contributions:Study concept and design: Oussoultzoglou. Acquisition of data: Fukuda and Rosso. Analysis and interpretation of data: Bachellier, Nakano, Audet, and Jaeck. Drafting of the manuscript: Fukuda and Oussoultzoglou. Critical revision of the manuscript for important intellectual content: Bachellier, Rosso, Nakano, Audet, and Jaeck. Statistical analysis: Fukuda, Oussoultzoglou, and Rosso. Study supervision: Bachellier and Jaeck.

Financial Disclosure: None reported.

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Lygidakis  NJSgourakis  GGeorgia  DVlachos  LRaptis  S Regional targeting chemoimmunotherapy in patients undergoing pancreatic resection in an advanced stage of their disease: a prospective randomized study. Ann Surg 2002;236806- 813
PubMed
Lillemoe  KDCameron  JLYeo  CJ  et al.  Pancreaticoduodenectomy: does it have a role in the palliation of pancreatic cancer? Ann Surg 1996;223718- 725
PubMed
Huguier  MNicholas  P Treatment of cancer of the exocrine pancreas. Am J Surg 1999;177257- 265
PubMed
Okamoto  ATsuruta  KKarasawa  K  et al.  Resection versus palliation: treatment of stage III and IVA carcinomas of the pancreas employing intraoperative radiation. World J Surg 2003;27599- 605
PubMed
Oussoultzoglou  EBachellier  PBigourdan  JMWeber  JCNakano  HJaeck  D Pancreaticogastrostomy decreased relaparotomy caused by pancreatic fistula after pancreaticoduodenectomy compared with pancreaticojejunostomy. Arch Surg 2004;139327- 335
PubMed
Martin  DFEngland  RETweedle  DE Radiological intervention in pancreatic cancer. Eur Radiol 1998;89- 15
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Subgroups of 83 patients undergoing evaluation with a preoperative arteriogram according to the classification by Nakao et al.13 A, Type A shows a normal portogram (n = 41); B, type B, unilateral narrowing (n = 20); C, type C, bilateral narrowing (n = 18); and D, type D, venous occlusion with collateral circulation (asterisk) (n = 4). PV indicates portal vein; S-MT, splenomesenteric trunk; and SMV, superior mesenteric vein.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Comparison of survival curves of patients who underwent pancreatic resection with and without portal vein (PV) resection. No significant difference was found between the 2 groups (P = .55).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Cumulative survival curves of patients with no venous resection, no invasion of the portal vein (PV) wall, superficial PV invasion up to the tunica adventitia, deeper invasion into the tunica media or the tunica intima, and noncurative resection. Significant differences were shown between patients with no venous resection and those with deeper invasion into the tunica media or the tunica intima (P = .02), between patients with no venous resection and those with noncurative resection (P<.001), between patients with no PV wall invasion and those with noncurative resection (P<.001), and between patients with superficial invasion up to the tunica adventitia and those with noncurative resection (P = .01).

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.

Cumulative survival curves. A, Overall survival curves according to the number of the 3 independent risk factors present in each patient. B, Disease-free survival curves according to the number of the 3 independent risk factors present in each patient.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Univariate Analysis of Potential Predictors of Overall and Disease-Free Survival After Curative Pancreatic Resection*
Table Graphic Jump LocationTable 2. Multivariate Cox Regression Analysis of Prognostic Factors After Curative Resection
Table Graphic Jump LocationTable 3. Clinicopathological Factors Associated With the Volume of Intraoperative Transfusion*
Table Graphic Jump LocationTable 4. Comparison of Clinicopathological Features of Patients According to Depth of PV Wall Invasion

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PubMed
Lillemoe  KDCameron  JLYeo  CJ  et al.  Pancreaticoduodenectomy: does it have a role in the palliation of pancreatic cancer? Ann Surg 1996;223718- 725
PubMed
Huguier  MNicholas  P Treatment of cancer of the exocrine pancreas. Am J Surg 1999;177257- 265
PubMed
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PubMed
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PubMed
Martin  DFEngland  RETweedle  DE Radiological intervention in pancreatic cancer. Eur Radiol 1998;89- 15
PubMed

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