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| HPB (Oxford). 2005; 7(2): 87–92. doi: 10.1080/13651820510028855. | PMCID: PMC2023930 |
Value of regional lymphadenectomy in pancreatic cancer C. Bassi,  R. Salvia, G. Butturini, S. Marcucci, G. Barugola, and M. Falconi Surgical and Gastroenterological Department, University of Verona, Verona, Italy |
Abstract Radical surgical resection and adjuvant chemotherapy are the goal standard to attempt significant long term survival in patients suffering from ductal pancreatic cancer. The role of extended lymph-node dissection is still a debated issue. In this paper a deep review of the experiences reported in the literature is carried out. Several studies are limited, not randomized and retrospective: generally speaking they seem to suggest a positive role in node dissection. Unfortunately, this trend is not confirmed in the only two trials conducted in a prospective and randomized setting. Moreover the results of these studies are also difficult to compare. At the moment we can say that extended lymphadenectomy does not play a determinant role for long term survival but a positive trend has been shown for node positive patients. |
The only realistic chance of a cure for patients suffering from ductal pancreatic cancer of the pancreas is the radical resection of the tumors. In the past, the disappointing results achieved in the overall long-term survival of resected patients appeared to prompt many surgeons to refrain from surgical intervention 1. What we have actually witnessed over the years is a progressive increase in resection rates, which have steadily risen from around 20% some 15–20 years ago to an average of 35% of cases observed today and which now even exceed 50% in some centers 2. Moreover the tempting results on long-term survival rate recently achieved by adjuvant treatment in a large multi-center randomized study further support the need of aggressive behaviour 3, 4. Today we believe that in cases in which the preoperative staging has ruled out both remote metastases and loco-regional, not resectability, it is ethically mandatory to regard ‘taking it out’ (plus adjuvant chemotherapy!) as the primary aim of curative treatment of carcinoma of the pancreas; this seems to be the suggested and correct policy to use in those centers where the morbidity (around 30%) and mortality rates (<5%) make this a feasible and reasonable proposition. |
Unfortunately the staging of the N factor can be completely clarified only after surgical resection, and the reliability of lymph-node negativity is directly related to the extent of the performed lymphadenectomy and to the pathologist care in the specimen analysis. Moreover, there is a frequent lack of correlation between tumor diameter and lymph-node positivity, which, in some case series, may be present in as many as 50% of cases of small tumors (T <2 cm) 5. The risk of false-negatives also results in the lack of anatomical contiguity in the lymphatic invasion pattern of the pancreatic cancer, with possible positivity in remote lymph-node stations together with negative peripancreatic lymph nodes. The result of this behavior of N factor and the lack of any correlation between N positivity and precise ‘evidence based’ adjuvant options, is that the effective need for a more or less extended lymphadenectomy accompanying the takeout in carcinoma of the pancreas remains a hotly debated issue. Looking at the frequency and pattern of lymph-node involvement in pancreatic cancer, it can be noted that the rate of resected patients with lymph-node involvement is around 70% 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41. The more aggressive approach adopted in Japan might be thought to lead to a generally higher incidence of lymph-node positivity in case series in the Far East. Surprisingly the percentage distribution shows no significant difference on the basis of this parameter: the figure reported by the Japan Pancreas Society (74.6% positivity) 6 is comparable to the rates reported in European 7 and American 8 studies (67.5% and 71.6%, respectively). In our own more recent series of 100 patients undergoing pancreaticoduodenoctomy for ductal carcinoma, 67 were lymph-node positive (unpublished data). Particularly interesting, in this connection, are the studies conducted by Cubilla and Fitzgerald 9, which show that the standard Whipple successfully removes 80% of the lymph-node sites most commonly involved. Apart from this study, the literature contains very few reports of pathological analyses of surgical specimens aimed at establishing the topographical distribution of the lymph-node areas affected by the tumor spread 5, 10, 11. In this sector, the Japanese literature is by far the most informative, thanks above all to Nagakawa's study 5, which was planned with the intention to assess, on the basis of quantitative evidence, whether lymphadenectomy should be also extended to the remote lymph nodes: 68.6% of patients presented lymph-node metastases, and 73.7% of these lymph-node-positive subjects showed simultaneous positivity of the resection margin of the posterior lamina. Also looking at our already stressed most recent experience on 100 consecutive patients, the rate of Rl and R2 with N positivity is similar (67.5%). The lymph-node areas most affected are similar too: area 13 (posterior to the head of the pancreas), 17 (anterior to the head of the pancreas) and 14 (radix of the mesenteric area), followed by areas 12 (hepatoduodenal ligament) and 16 (along the abdominal aorta). All other sites are only sporadically affected. In particular, in area 16 the highest incidence is in the interaortocaval region. The extent of lymphatic metastasis tends to increase with tumor diameter, though the finding in two of Nagakawa's cases 5 of small tumors (diameter <2 cm) which had already metastasized to area 16 provided evidence of a poor correlation with bizarre involvement and distribution of the N factor as compared to the T factor. This unpredictability is further confirmed by our own experience: in a study aimed at detecting small tumors of the pancreatic head 12, none of the 4 cases prospectively identified out of 72 consecutive observations were N+. By contrast, 3 out of 7 small tumors identified retrospectively in 56 historical patients were N  + ; even one of the more recent cases with lymph-node positivity had a diameter of 1.5 cm. Taken together all these data would appear to suggest that the pathway of para-aortic metastases passes via a retroperitoneal lymphatic route from area 13 to area 14 before reaching area 16. On the basis of his analysis, Nagakawa concludes that ‘an extensive dissection including areas 14 and 16 is necessary for radical resection’ 5. Non-performance of a standard lymphadenectomy in all patients, in Western series, might be interpreted as the result of both a non-homogeneous surgical approach and definitions used for the standard and extended procedures by the Western surgeons. In actual fact, we surgeons often find ourselves having to operate on patients who, despite the disease, present a major intra-abdominal lipid component of a type which, for anthropomorphic and dietetic reasons, is comparatively rare in Eastern populations. This technical obstacle often proves insurmountable except by prolonging the related operative times and risks, at least in theoretical terms. For this reason, our recent series included only 15 N+ cases potentially capable of providing data on the ill-famed area 16. Two patients presented positivity in this area, both of which in lymph nodes of interaortocaval origin. The similarities to Nagakawa's findings 5, in terms of both frequency and site, are suggestive. In one of our two cases, sequential involvement of areas 13 → 14 → 16 was observed, whereas in the other the area 16 positivity coincided with positivity only of area 13, all the other areas yielding negative findings. The erratic pattern of lymph-node involvement is also confirmed by two cases which were lymph-node negative in area 13, but positive at the level of the hepatoduodenal ligament (area 12): one of these tumors had a diameter of 1.5 cm (the above-mentioned small N + tumor) and the other a diameter of 4 cm. Despite these incongruities, which make any correlation between N and T factors unreliable, in our case series, too, the mean diameter of the N – tumors was less than that of the N+ malignancies (26.3 mm, with a range from 10 mm to 40 mm; and 30.5 mm, with a range from 15 mm to 40, respectively). |
The ‘N’ factor and the prognosis Despite the generally widespread conviction that the presence of lymph-node metastases is a highly prejudicial factor for the prognosis of pancreatic carcinoma, this is by no means an established fact in the literature 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41; several studies fail to tackle the issue on the basis of multivariate-type analysis, leaving the reader with the suspicion that some other co-factor potentially capable of affecting the prognosis may to some extent blur the real significance of lymph-node positivity. An elegant study by Cameron et al.13 showed, however, that, in multivariate analysis, too, the strongest predictive factor is lymph-node status with a median survival of 55.8 months in N– patients as against 11 inN+ subjects. In 1995, the same group 8 substantially confirmed the findings for lymph-node status, associating it, additionally, with tumor diameter (> 3 cm) and the state of the resection margin, with relative risks of 1.6, 1.7 and 1.4, respectively. In a sub-population of patients who were also studied in terms of tumor DNA status, however, aneuploidy was the element with the highest relative risk (2.7), followed by tumor diameter (2.2), lymph-node status (1.7) and resection margin positivity (1.6). We can therefore reasonably conclude that lymph-node status is an independent factor capable of affecting survival times in patients undergoing resection for pancreatic ductal carcinoma. The N factor also appears to be decisive with regard to long-term survival (beyond 5 years): in a recent study aimed at identifying the characteristics of patients destined to survive for longer periods 14, all the patients surviving for more than 10 years were N –. Finally, in the recent ESPAC trial, stratifying the use of adjuvant chemotherapy according to the N status did not affect the overall treatment result 3, 4. |
Results of extended versus traditional lymphadenectomy Because of the yet unclear pattern of lymph-node involvement and its effective prognostic role in pancreatic cancer, the value of systematic lymph-node dissection is still a much debated issue; this refers to the need, if any, for extending lymph-node removal after pancreatic resection, which involves a proximal lymphadenectomy in itself. Lymphadenectomy in pancreatic cancer, contrary to that in other tumors (breast, stomach and colon), yields no indications of an adjuvant options based on nodes positivity: the advocates of this 'extended' approach can do no more than base their rationale on the intrinsic therapeutic efficacy as such (removal of malignant foci and interruption of lymphatic spread). In 1988, Isikawa et al.15, in a limited number of cases, showed a significant increase in survival. Naga-kawa 16, however, stresses that, if we want to offer the individual patient the maximum chance of survival, we cannot confine ourselves to extended lymphadenectomy alone, but must also remove the retroperitoneal laminar tissue including the celiac nerve plexus. The benefit in terms of survival is questioned by the Japanese authors themselves as these patients are liable to experience devastating diarrhea requiring periods of long hospitalization 17. By contrast, in Western countries few authors suggest more radical approach than a standard resection 18, 19. The concept of ‘radical resection’ was introduced by Fortner at the beginning of 70s 20 with wide vascular removal; nowadays the term radical or extended resection means wide soft tissue resection and retroperitoneal lymphadenectomy. The ‘standard’ means to include anterior and posterior pancreaticoduodenal, pyloric, main bile duct, superior and inferior head and body nodes; the ‘extended’ means to include at the already mentioned nodes stations the liver hilum along the aorta from the diaphragmatic hiatus to the inferior mesenteric artery, celiac trunk, superior mesenteric artery and both renal hili 40. Isikawa 15 showed a 3-year survival rate of 13% versus 38% comparing standard versus radical resection in a historical and prospective group of 37 and 22 patients respectively. Also the retrospective Manabe study involves patients not comparable for tumor staging 21; other reports got surprising morbility and mortality rates 10, 22. The prospective non-randomized study by Henne-Bruns 18 did not show any benefit of radical resection, with a general high mortality and without inclusion of complete removal of hepatoduodenal and celiac origin nodes. The first prospective randomized study reported in the literature comes from Italy by the Multicenter Lymphadenectomy Study Group 23. From March 1991 to March 1994, a total of 83 patients with cancer of the head of the pancreas were recruited by 6 contributing centers. Patients undergoing laparotomy were eligible to enter the trial if the entire macroscopic tumor could be excised. In the course of thorough surgical exploration, the tumor diameter was evaluated and frozen sections of peripancreatic nodes suspected of being metastatic were obtained. Randomization was carried out during laparotomy. If the study inclusion criteria were met, patients were stratified as follows: the first stratum included lymph-node-negative pancreatic tumors measuring less than 4 cm in diameter, while the second stratum comprised all lymph-node-positive pancreatic tumors and node-negative tumors measuring more than 4 cm in diameter. Patients were then allocated to traditional or extended lymphadenectomy. Classic Whipple or pylorus-preserving pancreaticoduodenectomy were performed on the basis of the operating surgeon's preference. Traditional lymphadenectomy included resection of the anterior and posterior pancreaticoduodenal, inferior head, pyloric, common bile duct, superior head, superior mesenteric and superior and inferior pancreatic body nodes. In addition to the latter, extended lymphadenectomy also entailed removal of the hepatic duct, mid-colic, celiac axis and para-aortic region nodes. Forty-two patients were randomized to traditional and 41 to extended lymphadenectomy. Histological specimens were reviewed by two independent pathologists (G. Kloppel and K. Dhaene, from Kiel). Two patients in the traditional lymphadenectomy group were subsequently excluded, one because suffering from an endocrine tumor and the other because of postoperatively histologically proven liver metastasis. The characteristics of the two patient groups were comparable for age, sex, length of follow-up, tumor stage, tumor diameter and grading. The number of lymph nodes removed with the extended procedure was significantly greater than with the traditional one; no adjuvant treatment was given to either group postoperatively. The overall survival was the same in the two groups ( p<0.05) . Neither age, sex, surgical department, pylorus-preserving procedures nor intra-operative radiotherapy influenced survival. Worse survival was observed in patients with high-grade tumors ( p=0.001), tumor diameters >2 cm ( p=0.002) and lymph-node metastases ( p=0.006). Lymph-node-positive patients had significantly better survival after extended than after traditional lymphadenectomy ( p=0.026); moreover, survival was the same in N–patients (whatever the type of lymphadenectomy) and in N+ patients treated with an extensive approach. The most recent prospective and randomized study on the topic was published in 2000 by Yeo et al.24 who admitted 294 patients to the trial. Comparing standard versus radical resection (the latter differs in the extension of nodes dissection from other prospective studies 18, 22) there were no significant differences neither in 1-, 3- and 5-year survival (80% versus 77%, 44% versus 44% and 23% versus 29% respectively) nor in median survival (30 versus 28 months). These negative data on the role of extended nodes resection in pancreatic cancer seem to be confirmed in a still not published study coming from Majo Clinic 25. Last, a further concept of radical surgery includes the segmental resection of the mesenteric-portal vein. Also in this area the data coming from the literature are conflicting and mainly derived from retrospective or not randomized experiences 26, 27, 28, 29, 30, 31, 32, 33, 34. Tables I, II and III report the main data on extended versus standard surgery for pancreatic cancer coming from retrospective, prospective non-randomized and randomized studies respectively.
 | Table I. Reports of standard versus extended surgery in pancreatodudodenectomy for pancreatic ductal cancer |
| Table II.Reports of standard versus extended surgery in pancreatodudodenectomy for pancreatic ductal cancer |
| Table III.Reports of standard versus extended surgery in pancreatodudodenectomy for pancreatic ductal cancer |
Looking at safety, there are no significant differences in postoperative morbidity and mortality in the patient groups undergoing classic lymphadenectomy as compared to those undergoing the extended procedure 21, 23, 26. In our experience 23, both the number of transfusion recipients and blood units used showed no significant difference between the two treatment groups; also the post-operative hospitalization was comparable and, as regards operative times, extended lymphadenectomy took on average about 30 min longer to perform than the classic operation. In the Yeo study 24 the final results 35 confirm the similar mortality rate between extended and standard procedures (2% and 4% respectively) but increased morbidity in the radical resection, mainly due to a higher rate of delayed gastric empting (16% versus 6%) and pancreatic fistula (13% versus 6%). Last but not least, in long-term survivors, no differences in quality of life have been reported in a very recent study 36. |
How meaningful, then, today is a lymphadenectomy procedure involving a greater measure of radicality? The only controlled data provided by two prospective, randomized studies 23, 24 would appear to suggest that extended lymphadenectomy is not capable of favorably affecting prognosis, at least in the population of resected patients as a whole. Unfortunately, the results of these two studies are difficult to compare and both underpowered; because of the small difference in survival rate between the two different procedures, in order to detect a significant result, it should be necessary to admit at least 1000 patients for an adequately powered trial! All the others' experiences are limited, not randomized and mainly retrospective 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41. At the moment we can state that extended lymphadenectomy does not play a determinant role for long-term survival in pancreatic cancer, but a positive tendency should be deserved for node positive patients 23. Preoperative recognition of positive nodes patients and potentially R0 resections seem to be the up-to-date clinical challenges together with the further understanding of the role of adjuvant treatment 3, 4, 37, 38. |
References 1. Gudjonson, B. Carcinoma of the pancreas: critical analysis of costs, results of resections and the need of standardized reporting. J Am Coll Surg. 1995;181:483–503. [PubMed]2. Dervenis, C; Bassi, C. Thieme-Verlag; Stutgard: 2000. Pancreatic Tumors. 3. Neoptolemos, JP; , Dunn, JA; , Stocken, D; , Almond, J; , Link, K; , Beger, H; , Bassi, C; , Falconi, M; , Pederzoli, P; , Dervenis, C; , et al. ., for the members of the European Study Group for Pancreatic Cancer; . Adjuvant chemoradiotherapy and chemotherapy in resectable pancreatic cancer: a randomized controlled trial. The Lancet2001. ;358:1576–85. 4. Neoptolemos, JP; Stocken, DD; Friess, H; Bassi, C; Dunn, JA; Hickey, H; Beger, H; Fernandez-Cruz, L; Dervenis, C; Lacaine, F, et al. European Study Group for Pancreatic Cancer. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med. 2004;350:1200–10. [PubMed]5. Nagakawa, T; Kobayashi, H; Ueno, K; Ohta, T; Kayahara, M; Mori, K; Nakano, T; Takeda, T; Konishi, I; Miyazaki, I. The pattern of lymph node involvement in carcinoma of the head of the pancreas. Int J Pancreatol. 1993;13:15–22. [PubMed]6. Japan Pancreas Society; . Classification of Pancreatic Carcinoma. (English edition). Tokio: Kanehara; 1996 . 7. Kockerling, F; Kessler, H; Hermanek, P; Gall, FP. Beger, HG; Buchler, M; Schoenberg, MH. Universitätsverlag Ulm; UlmGermany: 1996. The role of lymph node dissection in the treatment of ductal carcinoma of the pancreas, Cancer of The Pancreas; pp. 403–08. 8. Yeo, CJ; Cameron, JL; Lillemoe, KD; Sitzmann, JV; Hruban, RH; Goodman, SN; Dooley, WC; Coleman, J; Pitt, HA. Pancreaticoduodenectomy for cancer of the head of the pancreas. Ann Surg. 1995;221:721–33. [PubMed]9. Cubilla, AL; Fitzgerald, PJ. Moossa, AR. Williams & Wilkins; Baltimore: 1980. Surgical Pathology of tumors of esocrine pancreas, Tumors of the Pancreas; pp. 159–93. 10. Nagakawa, T; Kobayashi, H; Ueno, T; Kayahara, I; Miyazaki, I. Clinical study on lymphatic flow to the paraortic lymph nodes in carcinoma of the head of the pancreas. Cancer. 1994;73:1155–62. [PubMed]11. Kawarada, Y; Yanigisawa, K; Isaji, S; Mizumoto, R. The prevalence of pancreatic cancer lymph node metastasis in Japan and pancreatic cancer categories. Int J Pancreatol. 1994;16:101–04. 12. Bassi, C; Falconi, M; Talamini, G; Salvia, R; Caldiron, E; De Santis, L; Bonora, A; Butturini, G; Sartori, N; Procacci, C, et al. Prospective study of the detection and treatment of Small tumors of the head of the pancreas. J Hep Bil Pancr Surg. 1995;2:347–51. 13. Cameron, JP; Pitt, HA; Yeo, CJ; Lillemoe, KD; Kaufmann, HS; Coleman, J. One hundred and forty five consecutive pancreaticoduodenectomies without mortality. Ann Surg. 1993;217:430–8. [PubMed]14. Klempnauer, J; Ridder, GJ; Bektas, H; Pichmayr, R. Surgery for exocrine pancreatic cancer: who are the five and ten year survivors? Oncology. 1995;52:353–9. [PubMed]15. Isikawa, O; Ohhigashi, K; Sasaky, J, et al. Practical usefulness of lymphatic and connective tissue clearance for the carcinoma of pancreas head. Ann Surg. 1988;208:215–20. [PubMed]16. Nagakawa, T; Konishi, I; Ohta, T, et al. The results and problems of extensive radical surgery for carcinoma of the head of the pancreas. Jpn J Surg. 1991;21:262–7. [PubMed]17. Osaki, H. Modern surgical treatment of pancreatic cancer. Int J Pancreatol. 1994;16:121–9. [PubMed]18. Henne-Bruns, D; Vogel, I; Luttges, J; Kloppel, G; Kremer, B. Surgery for ductal adenocarcinoma of the pancreatic head: staging, complications, and survival after regional versus extended lyphadenectomy. World J Surg. 2000;24:595–601. [PubMed]19. Mcfadden, DW; Reber, HA. Cancer of the pancreas: radical resection-supporting view. Adv Surg. 1994;27:257–72. [PubMed]20. Fortner, JG. Regional resection of cancer of the pancreas: a new surgical approach. Surgery. 1973;73:307–20. [PubMed]21. Manabe, T; Ohshio, G; Baba, N; Miyashita, T; Asano, N; Tamura, K; Yamaki, K; Nonaka, A; Tobe, T. Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas. Cancer. 1989;64:1132–7. [PubMed]22. Sindelar, WF. Clinical experience with regional pancreatectomy for adenocarcinoma of the pancreas. Arch Surg. 1989;124:127–32. [PubMed]23. Pedrazzoli, S; Di Carlo, V; Dionigi, R; Mosca, F; Pederzoli, P; Pasquali, C; Klöppel, G; Dheane, K; Michelassi, F; Sperti, C, et al. Standard Versus Extended Lymphadenectomy Associated with Pancreatoduodenectomy in the Surgical Treatment of Adenocarcinoma of the Head of the Pancreas: a multicenter, prospective, randomized study. Ann Surg. 1998;228:508–17. [PubMed]24. Yeo, CJ; Cameron, JL; Sohn, TA; Coleman, J; Sauter, PK; Hruban, RH; Pitt, HA; Lillemoe, KD. Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg. 1999;229:613–22. [PubMed]25. Farnell, MB.; . Presentation to The Pancreas Cancer Conference. Tirrenia, Italy, April2004 . 26. Fuhrman, GM; Leach, SD; Staley, CA; Cusak, JC; Charnsangavej, C; Cleary, KR; El Naggar, AK; Fenoglio, CJ; Lee, JE; Evans, DB. Rationale for en bloc vein resection in the treatment of pancreatic adenocarcinoma adherent to the superior mesenteric-portal vein confluence. Pancreatic Tumor Study Group. Ann Surg. 1996;223:154–62. 27. Harrison, LE; Brenner, MF. Portal vein involvement in pancreatic cancer: a sign of unresectabily? Adv Surg. 1997;31:375–94. [PubMed]28. Van Green, RC; Ten Kate, FJ; De Wit, LT; Van Gulik, TM; Obertop, H; Gouma, DJ. Segmental resection and wedge excision of the portal or superior mesenteric vein during pancreatoduodenectomy. Surgery. 2001;129:158–63. [PubMed]29. Hartel, M; Niedergethmann, M; Farag-Soliman, M; Sturm, JW; Ricther, A; Trede, M; Post, S. Benefit of venous resection for ductal adenocarcinoma of the pancreatic head. Eur J Surg. 2002;168:707–12. [PubMed]30. Keck, H; Knoop, M; Langrehr, JM; Henneken, V; Neuhaus, P. [Extended partial Kausch-Whipple duodenopancreatectomy by resection of tumor infiltrated vascular segments]. Zentralbl Chir. 1995;120:809–14. [PubMed]31. Klempnauer, J; Ridder, GJ; Bektas, H; Pichlmayr, R. Extended resections of ductal pancreatic cancer-impact on operative risk and prognosis. Oncology. 1996;53:4–53. [PubMed]32. Roder, JD; Stein, HJ; Siewert, JR. Carcinoma of the periampullaryregion: who benefits from portal vein resection? Am J Surg. 1996;171:170–4. [PubMed]33. Shibata, C; Kobari, M; Tsuchiya, T; Arai, K; Anzai, R; Takahashi, M; Uzuki, M; Sawai, T; Yamazaki, T. Pancreatectomy combined with superior mesenteric-portal vein resection for adenocarcinoma in pancreas. World J Surg. 2001;25:1002–05. [PubMed]34. Takahashi, S; Ogata, Y; Tsuzuki, T. Combined resection of the pancreas and portal vein for pancreatic cancer. Br J Surg. 1994;81:1190–3. [PubMed]35. Yeo, CJ; Cameron, JL; Lillemoe, KD; Sohn, TA; Campbell, KA; Sauter, PK; Coleman, J; Abrams, RA; Hruban, RH. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Ann Surg. 2002;236:355–66. [PubMed]36. Nguyen, TC; Sohn, TA; Cameron, JL; Lillemoe, KD; Campbell, KA; Coleman, J; Sauter, PK; Abrams, RA; Hruban, RH; Yeo, CJ. Standard versus Radical pancreaticoduodenectomy for periampullary adenocarcinoma: a prospective, randomized trial evaluating quality of life in pancreaticoduodenectomy survivors. J Gastrointest Surg. 2003;7:1–9. [PubMed]37. Falconi, M; Mantovani, W; Bettini, R; Talamini, G; Bassi, C; Cascinu, S; Oliani, C; Pederzoli, P. Carcinoma of pancreatic body and tail: are there improvements in diagnosis and treatment modalities over the past decade? Dig Liver Dis. 2003;35:421–7. [PubMed]38. Neoptolemos, JP; , Moffitt, DD; , Dunn, JA; , Almond, J; , Beger, HG; , Pederzoli, P; , Bassi, C; , Dervenis, C; , Fernandez-Cruz, L; , Lacaine, F; , et al. ., for the members of the European Study Group for Pancreatic Cancer; . The influence of resection margin on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy within the ESPAC-1 randomized controlled trial. Ann Surg2001. ;234: 758–68. 39. Capussotti, L; Massucco, P; Ribero, D; Vigano, L; Muratore, A; Clgaro, C. Extended limphadenectomy and vein resection for pancreatic cancer: outcomes and implications for therapy. Arch Surg. 2003;138:1316–22. [PubMed]40. Pedrazzoli, S; Beger, HG; Obertop, H; Andren-Sandberg, A; Fernandez-Cruz, L; Henne-Bruns, D; Luttges, J; Neoptolemos, J. A surgical and pathological based classification of resective treatment of pancreatic cancer. Summary of an international workshop on surgical procedures in pancreatic cancer. Dig Surg. 1999;16:337–45. [PubMed]41. Satake, K; Nishivaki, H; Yokomatsu, H; Kim, K; Haku, A; Umeyama, K; Miyaazaki, I. Surgical curability and prognosis for standard versus extended resection for Tl carcinoma of the pancreas. Surg Gynecol Obstet. 1992;175:259–65. [PubMed] |
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