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10.1245/s10434-006-9143-4
Annals of Surgical Oncology 13:1569-1578 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Clinical Implications of Combined Portal Vein Resection as a Palliative Procedure in Patients Undergoing Pancreaticoduodenectomy for Pancreatic Head Carcinoma

Kazuaki Shimada, MD, Tsuyoshi Sano, MD, Yoshihiro Sakamoto, MD and Tomoo Kosuge, MD

Department of Hepatobiliary and Pancreatic Surgery, National Cancer Center Hospital, 5-1-1, Tsukiji, Chuo-ku, Tokyo, 104-0045, Japan

Correspondence: Address correspondence and reprint requests to: Kazuaki Shimada, MD; E-mail: kshimada{at}ncc.go.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The clinical implications of combined portal vein resections are controversial.

Methods: One-hundred and forty-nine consecutive patients underwent macroscopically curative pancreatectomies for pancreatic head carcinoma between January 1, 1996 and December 31, 2004. Portal vein resection was performed in 86 patients (58%). Data on surgical mortality, morbidity, perioperative outcome, pathological factors, initial recurrence site, and survival were retrospectively compared between the patients with and without portal vein resection.

Results: The incidence of postoperative pancreatic fistula was lower among patients who underwent portal vein resection. The median survival period was 14 months for the portal vein resection group and 35 months for the non-portal vein resection group, respectively. Combined portal vein resection was a significant predictor of poor survival using a multivariate analysis. Portal vein resection was strongly associated with larger tumor size, the degree of retropancreatic tissue invasion, the presence of extrapancreatic nerve plexus invasion, lymph node metastases, and positive cancer infiltration at the surgical margins.

Conclusions: Portal vein resection at the time of pancreaticoduodenectomy can be safely performed. However, most of patients requiring portal vein resection do not achieve a potentially curative resection or a favorable survival term. As a result, the aggressive application and the strict selection of portal vein resection might reduce the incidence of positive surgical margins, enabling long-term survival in patients who do not require portal vein resection.

Key Words: Pancreatic cancer • Portal vein resection • Predictive factors • Recurrence pattern • Postoperative complications


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pancreaticoduodenectomy may provide the only chance of a cure for patients with carcinoma of the pancreatic head, and the prognosis of patients with locally advanced disease who undergo non-surgical treatments like systemic chemotherapy and/or radiation is limited.1–2 Currently available high-quality imaging techniques have enabled a precise preoperative assessment of the relationship between local tumor extension and major vessels,3–5 and portal vein or superior mesenteric vein resections have been aggressively performed in the absence of invasion to the superior mesenteric artery or common hepatic artery to increase the resectability rate and the possibility of achieving curative pancreaticoduodenectomies with a negative surgical margin in large series of patients.6–8 Several recent studies concluded that portal vein resection at the time of pancreaticoduodenectomy could be performed with acceptable mortality and morbidity and with a surgical outcome and prognosis comparable to those seen in patients who undergo a pancreaticoduodenectomy without vein resection for the treatment of carcinomas of the pancreatic head.9–13 However, portal vein resection at the time of pancreaticoduodenectomy has not yet been widely recognized as a standard surgical treatment for pancreatic head cancer because of the generally dismal prognosis of patients with this disease and a few reports suggesting that patients undergoing venous resection have a shorter survival period.14–16

To reevaluate the clinical implications and role of portal vein resection, the present study investigated the demographics, operative factors, morbidity, mortality, recurrence pattern, and overall survival of a series of 86 patients with carcinoma of the pancreatic head who underwent portal vein resection during the past 9 years at a single Japanese institution.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between January 1, 1996 and December 31, 2004, a total of 149 consecutive patients with pancreatic adenocarcinoma originating in the head, neck, or uncinate process underwent macroscopic curative pancreatectomy at the National Cancer Center Hospital, Tokyo, Japan. Curative resection was defined as the absence of apparent tumor residue in the operative field and no liver metastases or macroscopic peritoneal dissemination. During the same period, 293 patients did not undergo pancreatic resection because of far advanced locally disease. Patients with lower bile duct carcinoma, ampullary carcinoma, endocrine carcinoma, invasive adenocarcinoma derived from intraductal papillary-mucinous tumors, and other rare pancreatic malignancies were excluded from the present study.

All the patients underwent a standardized imaging assessment consisting of ultrasonography, contrast-enhanced computed tomography (CT), magnetic resonance imaging, and angiography examinations. Transarterial portographic CT and hepatic arteriographic CT were routinely performed to examine not only the local tumor invasion to major vessels but also the presence of small hepatic metastases. Pre-operative evaluations for portal vein invasion were mainly based on the results of helical contrast CT scans.5 The extent of venous involvement by the tumor was not a contraindication for operation when there was no CT evidence of tumor extension to the common hepatic or superior mesenteric artery. Multidetectorrow CT (MD-CT) has been applied to estimate tumor invasion to large vessels including portal vein systems since January 2001.

During the laparotomy, local tumor invasion (including portal vein involvement) was further evaluated using intraoperative US. Peritoneal washing cytology specimens were routinely examined. Our principal criteria for performing a pancreatectomy were the absence of hepatic metastases, macroscopic peritoneal seeding, bulky lymph nodal involvements, or cancer invasion to the superior mesenteric or common hepatic artery. Limited invasion to the portal or superior mesenteric vein or a positive washing cytology specimen were not regarded as contraindications for surgery.18 Regional nodes, including the nodes around the common hepatic celiac, the right side of the superior mesenteric arteries, and the paraaortic lymph nodes, were routinely dissected. The area of paraaortic lymph node dissection extended from the celiac trunk to the origin of the inferior mesenteric artery, and from the right margin of the inferior vena cava to the left margin of the left gonadal vein. Of the 149 patients, 143 patients (96%) received a pancreatic head resection and 6 patients (4%) received a total pancreatectomy. Resection of the portal vein was usually performed just before the specimen was delivered. Of the 149 patients, 86 patients (58%) were identified as having clinical involvement of the portal vein or superior mesenteric vein (PV/SMV) or close adherence to these vessels; these patients underwent a pancreatectomy with portal vein resection. When the cause of the adhesion to the portal vein system could not be specified as cancerous invasion or associated inflammatory changes, portal vein resection was aggressively performed. Seventy-seven patients (90%) underwent a segmental resection of the PV/SMV and 9 patients (10%) underwent a wedge excision. Auto-vein interposition using a renal vein graft was performed in one patient (1%). On the other hand, 63 patients (42%) underwent pancreatectomies without portal vein resection. Ninety-eight patients received intraoperative radiation therapy (IORT, 30 Gy of electron beam radiation with an energy of 9 MeV), which was administered to the retroperitoneal fields. This procedure was restricted to patients without contraindications who were under the age of 75 years.19 Twelve patients who were over 75 years did not receive IORT. Thirty-nine patients did not receive IORT because of hospital renovations conducted between 1999 and 2000 and mechanical troubles with the irradiation system, respectively. Eleven of the patients received 5-fluorouracil and cisplatin and 15 received gemcitabine as an adjuvant chemotherapy regimen in a clinical trial setting conducted during the period of the present study.

The demographic and clinical variables of the two groups, including age, sex, symptoms, carbohydrate antigen 19-9 (CA19-9) level, carcinoembryonic antigen (CEA) level, operative procedure, morbidity, mortality, length of postoperative hospital stay, operative time, blood loss, and transfusion requirements, were analyzed and compared. Mortality was defined as the number of operative and in-hospital deaths. Gastric emptying was defined as the inability to resume oral intake within 10 postoperative days. A pancreatic fistula was defined as a persisting secretion of more than 10 ml/day of drainage fluid with a high amylase concentration (>1000 U/ml) for 7 days after the placement of a drain20 or the demonstration of pancreaticojejunal anastomosis leakage on a fistulography.

The extent of pathological features that might influence prognosis was classified as follows:21 histologically assessed tumor size, serosal invasion (s0, absent; s1, slight invasion; s2, wide invasion; s3, invasion to other organs), retropancreatic tissue invasion (rp0, absent; rp1, slight invasion; rp2, wide invasion; rp3, invasion to other organs), bile duct invasion (ch0, absent; ch1, invasion to bile duct wall but not to mucosal layer, ch2; invasion to mucosal layer, ch3, stenosis or obstruction of bile duct wall), duodenal invasion (du0, absent, du1; invasion to proper muscle layer, du2; invasion to submucosal layer, ch3; invasion to mucosal layer), portal vein invasion (pv0, absent; pv1, invasion to adventitia; pv2, invasion to tunica media; pv3, invasion to tunica intima), extrapancreatic nerve plexus invasion (absent, present), lymph node involvement (n0, absent; n1, regional; n2, peripancreatic; n3, paraaortic involvement), differentiation of the tumor (well, papillary, mucinous/moderately or poorly, adenosquamous), cancer infiltration at surgical margin (absent/present), and peritoneal washing cytology specimen (negative/positive). Histopathologic variables were also compared between the two groups. The tumors were staged according to the TNM system, sixth edition.22

Patients were closely followed up every 1–2 months during the first year after surgery. Each follow-up visit included a physical examination, blood chemistry tests, and a measurement of the serum CA19-9 level. Ultrasound and enhanced CT examinations were performed at 3-month intervals, along with a chest radiography examination. Specific sites of first disease recurrence, and the time until disease recurrence were analyzed. Recurrence was suspected when: 1) a new local or distant metastatic lesion was found on serial images and 2) an increase in the tumor marker level was recognized. Radiologic evidence of tumor recurrence was accepted even if the patients did not undergo a biopsy. When progression of the disease was confirmed by repeated image studies, the dates of the first suspicious radiologic finding were used as the date of initial disease recurrence. One patient who died while undergoing a total pancreatectomy with portal vein resection and two patients requiring a portal vein resection who had an incomplete follow-up were excluded from the follow-up analysis.

The clinicopathological features of the two groups were compared using the chi square test with Yates’ correction. Survival was calculated using the Kaplan-Meier method and was compared between groups using the log-rank test. All variables were dichotomized for analysis. A multivariate analysis using the Cox hazard model was performed to identify independent predictors of survival. All statistical analyses were performed using SPSS for Windows 11.5 software (SPSS, Chicago, IL). P < 0.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A total of 149 patients with pancreatic head carcinoma underwent resections during a 9-year period. The patients consisted of 88 men and 61 women with a median age of 62 (27–86) years. The two treatment groups were similar with respect to sex, age, and other demographic variables (Table 1Go.). As for the operative procedures, standard pancreaticoduonectomy and total pancreatectomy were performed more frequently in the portal vein resection group (Table 2Go). Pancreaticojejunostomy and duct occlusion, which was applied in patients with fragile or normal pancreases using Ethibloc® (Ethicon, GmBH) between 1996 and 2000, were performed in 107 and 36 patients, respectively. No significant difference in the management of the pancreatic remnant was seen between the two groups. The operative time, estimated intraoperative blood loss, and transfusion requirements were significantly larger in the portal vein resection group.


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  		TABLE 1. Demographic characteristics of 149 patients with or without portal vein resection
 

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  		TABLE 2. Operative procedures and findings in 149 patients undergoing pancreaticoduodenectomy with and without portal vein resection
 
The rate of postoperative complications was similar between the two groups, but the incidence of pancreatic fistula was lower in the vein resection group (P = 0.023). One postoperative death occurred in a patient who had undergone a total pancreatectomy with portal vein resection, yielding an in-hospital mortality rate of 1%. The patient had postoperative bleeding, probably originating from a skeltonized hepatic artery on postoperative day 4. Mortality, the reoperation rate, and the postoperative hospital stay were not significantly different between the two groups (Table 3Go).


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  		TABLE 3. Surgical morbidity in 149 patients undergoing pancreaticoduodenectomy with or without portal vein resection
 
The median follow-up period was 18 months (range, 3–84 months). The overall median survival period for the 149 patients was 18 months, and the 5-year survival rate was 27%. The median survival period and the 5-year survival rate were 14 months and 12%, respectively, for the portal vein resection group and 35 months and 46%, respectively, for the non-portal vein resection group (Fig. 1Go). Combined portal vein resection was a significant predictor of poor survival (P = 0.006). Sixteen other clinicopathological variables were investigated to determine whether they were of prognostic significance. The results of the log-lank test are shown in Table 4Go. In the univariate analysis, the indicators of an unfavorable prognosis included a CA19-9 value higher than 240 U/ml (P = 0.0048); a tumor size larger than 35 mm (P = 0.0021); the presence of serosal invasion (s1, s2 and s3) (P = 0.0011), duodenal invasion (du2 and du3) (P = 0.0096), portal vein invasion (pv1, pv2, and pv3) (P = 0.0303), extrapancreatic nerve plexus invasion (P = 0.0077), or lymph node metastases (n2 and n3) (P = 0.0019); cancer infiltration at the surgical margins (P = 0.0329); and the application of IORT (P = 0.0357). When the significant prognostic factors identified by the univariate analysis were assessed using a multivariate analysis, the following factors were found to be independently associated with a poor prognosis: combined portal vein resection, presence of duodenal invasion, and a CA19-9 value higher than 240 U/ml, with hazard ratios (95% confidence intervals) of 2.246 (1.092–3.624), 1.705 (1.092–2.661), and 1.690 (1.074–2.659), respectively. Patients were staged according to the TNM system, sixth edition, as follows: stage IA (patients without portal vein resection, n = 1 [2%]/patients with portal vein resection, n = 0), stage IB (n = 1 [2%]/n = 0), stage IIA (n = 15 [24%]/n = 9 [11%]), stage IIB (n = 31 [49%]/n = 38 [44%]), stage III (n = 0/n = 0), and stage IV (n = 15 [24%]/n = 39 [45%]).


Figure 1
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  		FIG. 1. Actuarial 5-year survival curve (Kaplan-Meier) for 149 patients who underwent pancreatectomies for pancreatic head carcinomas with portal vein resection (n = 86) or without portal vein resection (n = 63). The differences were statistically significant (P = 0.0006).

 

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  		TABLE 4. Univariate analysis of predictors of survival
 
A comparison of the clinicopathologic features of the two groups is shown in Table 5Go. Portal vein resection was strongly associated with tumor size (P = 0.013), retropancreatic tissue invasion (P = 0.001), extrapancreatic nerve plexus invasion (P < 0.001), lymph node metastases (P = 0.009), cancer infiltration at the surgical margins (P = 0.002), and IORT (P = 0.014).


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  		TABLE 5. Clinicopathologic comparison of 149 patients with or without portal vein resection
 
The degree of histological portal vein invasion was assessed among 86 patients with portal vein resection. The degree of histological portal vein invasion (pvp0 = 28, 33%; pvp1 = 11, 13%; pvp2 = 28, 33%; and pvp3 = 19, 21%) was not significantly different, but none of the 58 patients with histological portal vein invasion (pv1–3) survived for 5 years (Fig. 2Go). A tumor size (>35mm) (P = 0.0087) and a Ca19-9 value (>240 U/ml) (P = 0.0175) were unfavorable prognostic factors assessed in 16 clinicopathologic factors among 86 patients undergoing portal vein resection.


Figure 2
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  		FIG. 2. Actuarial 5-year survival curve (Kaplan-Meier) for 86 patients who underwent pancreatectomies with portal vein resection, according to pathological portal vein involvement: pv0 (absent), n = 28; pv1 (invasion to adventitia), n = 11; pv2 (invasion to tunica media), n = 18; pv3 (invasion to tunica intima), n = 19. The differences were not statistically significant (P = 0.8178).

 
Table 6Go shows the anatomic locations of all the initial recurrences. Initial recurrence at a single site occurred in 28 patients (72%) without portal vein resection and in 53 patients (75%) with portal vein resection. Initial recurrence at two or more sites occurred in 11 patients (28%) without portal vein resection and in 18 patients (25%) with portal vein resection. The leading recurrence site was the liver, in 34 patients (34%). Local recurrence at the primary site without apparent distant metastases occurred in 3 patients (11%) without portal vein resection and in 10 (19%) patients with portal vein resection. The recurrence patterns and sites were similar between the two groups.


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  		TABLE 6. Recurrence pattern and sites in 146 patients with or without portal vein resection
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Portal vein resection at the time of pancreaticoduodenectomy was more common in the current study than in previous reports (with more than 30 patients undergoing portal vein resection) (Table 7Go). Previously, angiographic findings were used to determine whether a combined vein resection was indicated,3 but helical CT images can now be used to precisely evaluate the relationship between the tumors and the portal and/or superior mesenteric vein without major arterial invasions, not only allowing the preoperative identification of unresectable advanced disease, but also increasing the incidence of vein resection to achieve a wider retroperitoneal surgical margins.4,5 In addition, portal vein resection during pancreaticoduodenectomy has now been established as a standard operative procedure,10,13,14 encouraging the use of vein resection even if tumor involvement of the portal vein is only suspected or if the tumor is only located adjacent to the portal vein, with concomitant obstructive pancreatitis.


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  		TABLE 7. Large series (n > 30) examining portal vein resection for pancreatic carcinoma, conducted between 1994 and 2004
 
Portal vein resections during pancreaticoduodenectomy have been safely performed with acceptable mortality and morbidity in the present study as well as in previous large series.8–17 The postoperative complications rate was similar between patients who underwent portal vein resection and those who did not, but pancreatic fistulas were less common in patients with portal vein resection. Patients with vein resection associated with large tumors probably had a high incidence of obstructive pancreatitis with pancreatic duct dilation, possibly reducing the formation of postoperative pancreatic fistulas.23 Patients undergoing portal vein resection might recover promptly after resection because of lower incidence of pancreatic fistula and could receive adjuvant chemotherapy with safe. Careful attention should be paid to patients with portal vein resection who have fragile pancreases and pancreatic ducts that are not dilated. The portal vein resection group had a longer operative time, much more blood loss, more blood transfusions, and a higher use of combined gastrectomies (Whipple procedure). Such intraoperative factors could be gradually improved by a team of well-trained and experienced pancreatic surgeons, since the complexity and magnitude of the operative procedure does not enhance postoperative severe complications.10,14 The prolonged hospital stay not only after pancreaticoduodenectomy but also other surgical resections has been a serious problem in Japan. One of the major causes of the prolonged hospital stay in the present series might be due to the higher occurrence of pancreatic fistula or gastric empty. However, Japanese patients generally tend to stay in the hospital until all drains and/or tubes are pulled out and they feel completely well, even if no complications occurred. Recently, we pull out drains or tubes at the out-patient clinic when their postoperative course is uneventful, and the hospital stay period has been remarkably reduced.

In the present study, the median survived period was 14 months in patients with portal vein resection, and 35 month with non-portal vein resection, respectively. A significant reduced survival was recognized in patients undergoing portal vein resection. Recent studies have reported a median survival period ranging from 12 to 23 months in patients with pancreatic carcinoma who underwent portal vein resection.6–9,11,12,14,17 In most of the reports, survival did not differ between patients who did and those who did not undergo portal vein resections.9–14 Fuhrman et al.13 suggested that venous involvement was a function of tumor location, rather than an indication of aggressive tumor biology, since no difference in size, nodal positivity, or tumor DNA content were observed between patients with and without vein resections. Tseng et al. confirmed their early experience in a large series, but the incidence of positive surgical margins was higher and the rate of histopathologic vein invasion was 61% (n = 38) in patients who required vascular resection in their recent study.14 On the contrary, the present study showed that portal vein resection was one of the most unfavorable predictors, when analyzed using a multivariate analysis. Portal vein resection was strongly associated with a larger tumor size, extensive retro-pancreatic tissue invasion, the presence of extrapancreatic nerve plexus invasion, lymph node metastases, and cancer infiltration at the surgical margins. The present data suggested that patients requiring vein resection had more aggressive cancers and were less likely to be cured, even if precise preoperative and intraoperative assessments suggested a curative resection. As a result, the aggressive application and the strict selection of portal vein resection might reduce the incidence of positive surgical margins, enabling long-term survival similar to that of patients who do not require portal vein resection. Ishikawa et al.24 reported that large tumors and retroperitoneal invasion were risk factors for death from distant metastases.

Portal vein resection is important for local macroscopic cancer control to reduce the incidence of positive retroperitoneal surgical margins, but portal vein resection on its own cannot achieve a favorable survival term in most patients requiring portal vein resection because distant recurrences are common.

Histological vein involvement was reported to be an important factor determining survival.12,25 Extensive invasion to the portal vein wall seems to be a characteristic of aggressive cancers, but extensive retroperitoneal cancer infiltration sometimes occurs in patients requiring portal vein resection even if histological evidence of tumor invasion to the vein wall is not present, resulting in a dismal outcome similar to that of patients with histological vein involvement.24–26 The presence of histological invasion in 39% (n = 58) of the patients was an unfavorable predictor according to univariate analysis, but not according to a multivariate analysis.

Another reason for these similar survival results might be suggested by Ishikawa’s report,27 which described positive intraoperative cytology findings in several patients who underwent pancreatectomies without evidence of macroscopic vein involvement and in which additional resection of the portal vein confirmed cancer invasion in most of the cases. Their results suggest that a precise assessment of venous involvement is difficult and that venous involvement may exist in patients who are not thought to require vein resections.

In spite of limitation of various preoperative imaging studies, intra-operative ultrasonography is another useful tool not only to evaluate tumor invasion to the portal vein, but also to confirm the presence of invasion to the common hepatic or superior mesenteric artery and tiny hepatic metastases. Recently, intravascular ultrasonography seems to be more effective to evaluate the precise extension of portal vein invasion or to estimate the degree of histologic portal vein invasion.28

It is extremely important to determine a subgroup that might derive most benefit from portal vein resection. A smaller tumor size and a lower Ca19-9 value were favorable prognostic factors in 86 patients undergoing portal vein resection. Nakagohri et al.12 reported that negative microscopic invasion to the portal vein was associated with longer survival. In the present study, none of the 58 patients with histological portal vein invasion survived for more than 5 years, but there was no significant survival difference among the 86 patients when analyzed according to the degree of histologic portal vein invasion. Histological vein involvement has also been reported to be a significant risk factor for liver metastases,29 but no clear relationship between portal vein involvement and liver metastases was observed.

In conclusion, the results of the present study show that a combined pancreaticoduodenectomy and portal vein resection can be safely performed with a low incidence of postoperative pancreatic fistula formation. However, combined portal vein resections might only be required for aggressive tumors with extensive retroperitoneal invasion. Additional systemic chemotherapy should be mandatory in patients requiring portal vein resection during pancreaticoduodenectomy with a curative intent since retroperitoneal positive surgical margins and lymph node metastases are common and distant recurrences might be inevitable.


   ACKNOWLEDGMENTS
 
This study was supported by a Grant-in-Aid for cancer research from the Ministry of Health, Labor and Welfare of Japan.

Received for publication November 11, 2005. Accepted for publication April 5, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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