Pancreatic Cancer: 80 Years of Surgery—Percentage and Repetitions

Gudjonsson, Birgir

doi:https://doi.org/10.1155/2016/6839687

HPB Surgery

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Abstract Introduction Methods Discussion and Conclusion Disclosure Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2016 | Article ID 6839687 | https://doi.org/10.1155/2016/6839687

Pancreatic Cancer: 80 Years of Surgery—Percentage and Repetitions

Birgir Gudjonsson¹

Academic Editor: Pablo Ramírez

Received05 Apr 2016

Accepted01 Jun 2016

Published25 Oct 2016

Abstract

Objective. The incidence of pancreatic cancer is estimated to be 48,960 in 2015 in the US and projected to become the second and third leading causes of cancer-related deaths by 2030. The mean costs in 2015 may be assumed to be $79,800 per patient and for each resection $164,100. Attempt is made to evaluate the results over the last 80 years, the number of survivors, and the overall survival percentage. Methods. Altogether 1230 papers have been found which deal with resections and reveal survival information. Only 621 of these report 5-year survivors. Reservation about surgery was first expressed in 1964 and five-year survival of nonresected survivors is well documented. Results. The survival percentage depends not only on the number of survivors but also on the subset from which it is calculated. Since the 1980s the papers have mainly reported the number of resections and survival as actuarial percentages, with or without the actual number of survivors being reported. The actuarial percentage is on average 2.75 higher. Detailed information on the original group (TN), number of resections, and actual number of survivors is reported in only 10.6% of the papers. Repetition occurs when the patients from a certain year are reported several times from the same institution or include survivors from many institutions or countries. Each 5-year survivor may be reported several times. Conclusion. Assuming a 10% resection rate and correcting for repetitions and the life table percentage the overall actual survival rate is hardly more than 0.3%.

1. Introduction

Resections for pancreatic adenocarcinoma which Whipple et al. [1] initiated after earlier attempts by Codivilla [2] and Kausch [3] have now been carried out for 80 years. Opinions still differ as to the results. Some authors claim a survival percentage of up to 22% and are widely quoted and extol the benefits and success of resections [4] while others doubt that anyone survives pancreatic cancer [5].

2. Incidence, Economics

The incidence of pancreatic cancer has been estimated at 48,960 in 2015 in the US and is the fourth leading cause of death from cancer for both sexes [6]. It is projected to increase to 62,000 in the year 2020 and to 88,000 for both sexes in 2030 and to surpass breast, prostate, and colorectal cancers to become the second and third leading causes of cancer-related deaths by 2030 [7].

The cost of treatment of pancreatic cancer is of concern in many countries. O’Neill and colleagues studied the total direct medical cost of patients 66 years and older who were diagnosed from 2000 to 2007 in the US. The mean total direct cost was $65,500, for resectable locoregional disease cost was $134,700, and for unresectable locoregional or distant disease cost was $65,300 and $49,000, respectively [8]. Lea and Stahlgren had earlier pointed out the difference in the cost of resections versus bypass [9].

Assuming 2.5% inflation over 8 years, the mean cost in 2015 would be $79,800, for resections $164,100, for unresectable (or bypasses) disease $79,500, and for distant disease $59,700. With the estimated number of patients in 2015 the overall cost would be close to $4 billion.

3. Methods and Evaluation of Results

There is a growing concern that reports of success in medical research are inflated [10].

Here an attempt is made to evaluate the results over the last 80 years, the number of survivors, and the overall survival percentage.

This author has continued to scrutinize the literature on surgery from the onset, initially using the Index Medicus and then Ovid/PubMed until the end of 2014, with cross-references. Approximately 1230 papers have been found in 15 languages in approximately 200 journals from 44 countries which deal with resections and reveal at least some survival information. A total of 40.5% of the papers originated in the US, 19.3% from Japan, 7.3% from Germany, 5.3% from Italy, and 4% from France and the UK. These have been inserted into a database.

Papers on the surgical aspects of pancreatic cancer differ as to the approach and the composition of the patient group and the method of reporting. A few emphasize only the technical aspects and the mortality with limited or no survival information and indiscriminately cover patients with various malignant and benign pathologies which may require pancreatoduodenal resection, but without clearly separating each pathology group or presenting separate survival information. Only papers with separate pathologic information on patients were selected for analysis for this paper. Analysis of the database reveals that, of these 1230 papers, 609 do not report any 5-year survivors, some seem to be mainly technical, and some report only up to a 3-year survival rate. A total of 621 papers report 5-year survivors and will be examined further in detail in this paper. Special attention has been paid to the origin of each paper, the time period each study covered, patient composition, the subset of patients used for calculations, and the statistical method used.

4. Reservation, Nonresected Survivors

The first reservation about the effect of surgery on this disease was expressed by Glenn and Thorbjarnarson [11] in 1964, again by Gallitano et al. [12] in 1968 whose only 5-year survivor was “nonresected,” and then strongly by Crile Jr. in 1970 [13], whose only survivor was also nonresected. He challenged the value of resection for pancreatic cancer, followed by Shapiro in 1975 [14]. Crile Jr.’s criticism was directed at the then high mortality rate and the survival calculations which were carried out and might count only those who survived the operation and in ignorance of the nonresected survivors.

The presence of nonresected survivors has been disputed [15], but it is a major issue in the debate on survival. It was first pointed out by Cattell and Young in 1957 [16] and, as above, later by Gallitano and Crile Jr. The data were summarized by the present author in a paper in 1995 [17] and a letter in 1996 [18]. In a review by the present author published in 1978 only 65 five-year survivors could be found in the literature, of whom 8 were nonresected [19]. In a review published in 1987, 165 survivors could be found, but 12 of these were nonresected [20]. In this review 41 reports have been found from 31 institutions in 12 countries, many from eminent institutions and renowned authors, thereof 17 from the US, two from Yale [19, 20], two from the University Texas MD Anderson [12, 21], and two from Harvard MGH [22, 23], as well as from the University of Chicago [24], the Dana Farber Cancer Clinic [25], and Thomas Jefferson [26], to mention a few.

Nonresected survival is a fact and should be kept in mind in assessing overall therapeutic results. Initially reports detailed the course of all patients diagnosed at a particular institution but in recent decades reports have concentrated only on resected patients, completely ignoring any nonresected survivors. Nonresected survivors would therefore not be found.

5. Survival Calculations

The survival percentage depends not only on the number of survivors but on the subset from which the number is calculated.

A few earlier studies started by examining the respective tumor registries and disclosed that only about 35–68% of patients in tumor registries had histologic confirmation. Survival calculations have been based on the original number of patients with histologic diagnoses at a particular institution, previously called the total number (TN), the approximately 80% of cases that were surgically explored, the cases that were resected, or location, size, or R status of the tumor, or even only those patients who survived the operation.

Overall survival success must be based on the original group diagnosed with pancreatic cancer (the TN or total number) and the number of survivors and not only on a small subgroup of the cases. Different methods of calculation have been used to enumerate the results, that is, actual versus the actuarial, projected, or estimated percentage.

Initially most papers revealed the TN, the number of resections, and simply the number of survivors, whereas later authors also presented actual percentage figures. In the late 1980s the papers started reporting only the number of resections and survival as actuarial percentages, usually calculated with the Kaplan-Meier method with or without the actual number of survivors being reported [27].

Sir Hill pointed out in his book in 1937 that when a “large number of patients is lost sight of” the outcome might be erroneously high. This warning is reemphasized in later editions [28]. In a frequently quoted paper 11 survivors out of 201 are claimed as proof of 22% survival [4].

As indicated in Table 1 the original number TN of patients studied in a report is only revealed in 90 or 14.5% of the papers and in these the actual number of survivors is stated in only 49. In the remaining 41 with a documented TN and actuarial calculation the actual number of survivors is stated in 17, in addition to life table curves. Detailed information on the original TN group studied, number of resections, and actual number of survivors is therefore reported in only 66 or 10.6% of all papers on pancreatic cancer. In the remaining 89.4% some form of estimate or calculation is required to assess survival percentage. In 531 papers there is no information on the original number of patients from which the number of resections was drawn, although in 102 of these the number of survivors is stated or confirmed by inquiry.

In 424 of these 531 reports with survival calculations by actuarial methods 378 are by the Kaplan-Meier method and 48 by other or unclear methods, though KM is also very likely. The number of survivors is stated in 147 of the reports or 34.6%, but not in the remaining 277 or 65.3%.

A total of 240 inquiries were sent to authors where the actual number of patients was not reported and only 58 replies were obtained. The actual number of survivors with actuarial calculation is therefore known in 205 of the 424 reports or 48.3%. The actuarial and actual percentage figures can therefore be compared, as demonstrated previously [29, 30], and reveal that the actuarial percentage is on average 2.75 higher than the actual percentage. This figure has therefore been used to estimate the number of survivors and the survival percentage in the relevant studies where only the actuarial percentage has been published.

The resection rate has been debatable and varies and can only be assessed accurately if the original group is large and well defined. Tertiary referral centers cannot know the size of the original group from which their resection group is drawn. Of the studies published in the last 5 years, 156 of 161 or 97% report only the number of resections and the percentages. In an earlier study by this author the resection rate was 10.8%. In earlier US studies [31, 32] the rate was, respectively, 8.4% and 12%. In 2 European nationals [33, 34] the rate was from 8% to 12% over the last 5 years. In a recent report from the surgical service at a European university hospital [35] the resection rate was 11.6%. It is therefore practical to assume that the resection rate is 10% in the studies where the original TN of the group is not reported in order to estimate the TN accordingly and divide the percentage by 2.5–3 where the actuarial KM only has been published.

After totaling the numbers in the 621 studies with survivors with the above correction, but without further adjustment, the TN comes to 1,731,834, the number of resected patients comes to 162,207, and the number of survivors comes to 11,300, for an apparent survival percentage of 0.77%.

After totaling the number of patients in all the 1230 reports, the original TN comes to 3,188,543, the number of resected patients to 284,298, and the number of survivors to 11,330. The overall survival percentage would then be only 0.45%.

6. Repetitions

Repetition of reporting the same survivors in different papers was first pointed out in 1978 [17]. It occurs in various ways, such as when papers include survivors from many different institutions or known databases in a specific country or even when a study includes patients from many countries. Thus 92 of the 620 studies with 5-year survivors are from many institutions in a specific country or 14.8% and 10 of these from many countries or 1.6%.

Repetition occurs, though mainly when the patient population and survivors from a certain year are reported several times from the same institution. As can be seen in Figures 1–5, repetition has occurred up to 6–8 times in Germany, Italy, and Japan and up to 20 times in the US.

Examination of reports from a single institution covering the entire study period and stating the number of survivors and then adding up the number of patients from all the studies, including those with an estimated number of survivors, reveals that the total number reported is over 10 times larger than the number reported in the studies with a documented number of survivors.

Each paper may at times reveal some new information but only infrequently is it disclosed that the patients have been reported before.

There is no scientific method to assess the number of repetitions accurately but each reported 5-year survivor and thereby respective resection and the TN seems to be reported 3–5 times. Dividing the number of reported survivors and respective resections and TN by 4, the overall number of 5-year survivors is hardly more than 2,800, the number of resections 40,500, and the original TN number of patients 433,000.

Repetitions occur also in the “no-survivor” group of reports, but not as frequently. It may be assumed that all published reports with or without survivors are drawn from a TN of approx. 1,000,000 patients and with fewer than 3,000 survivors, of whom a significant number were nonresected, meaning that the overall survival rate was no more than approximately 0.3%.

7. Mortality, Positive Margins, and Nodes

Mortality during the first 20 years, 1945–1965, was on average 25.2% with a single report of 62.5%. During the next 20 years or up to 1984 mortality was on average 19.9% with the highest rate at 52%. In 1985–1994 it lowered to 9.8%. In subsequent 5-year periods mortality was reduced to 6.8% and then 4.6% and during the last 5 years 4% with a high of 33%. Aside from the 33%, the average is now 3.7%. The overall mortality rate has therefore greatly reduced.

The majority of surgeons in recent decades have reported the number of positive margins and nodes and numbers over 60–70% frequently quoted [36–38]. It is of great interest that even in the most experienced hands only 16% of cases were both margins and nodes negative [38].

Tumor cells can be found in the bone marrow in up to 50% of cases [39].

8. Discussion and Conclusion

Pancreatic cancer is thus both a costly and devastating disease and has usually spread beyond its boundaries at time of diagnosis and treatment and is thus a systemic disease. The literature on pancreatic surgery, while purporting to report the facts, is nevertheless inaccurate.

The use of actuarial calculation methods exaggerates the percentage and thereby the number of presumed survivors in a particular study.

Reporting the same patients repeatedly without any qualification gives a false impression of success.

Life table curves should be accompanied by the actual number of survivors. The course of nonresected patients should be studied.

Surgical skills are imperative for the care and palliation of pancreatic cancer patients including possible resections, but they have had only a minimal impact on the survival rate.

It is of importance for the medical profession that published results are indisputable.

Disclosure

The paper is based on 45 years of continuous study of the cancer of pancreas with previous communications and papers.

Competing Interests

The author declares that they have no competing interests.

Acknowledgments

The author thanks Terry G. Lacy Ph.D. for reviewing the manuscript.

References

A. O. Whipple, W. B. Parsons, and C. R. Mullins, “Treatment of carcinoma of the ampulla of Vater,” Annals of Surgery, vol. 102, no. 4, pp. 763–776, 1935.
View at: Publisher Site | Google Scholar
J. M. Howard and W. Hess, History of the Pancreas: Mysteries of a Hidden Organ, Kluwer Academic/Plenum Publishers, New York, NY, USA, 2002.
View at: Publisher Site
W. Kausch, “Das Carcinom der Papilla duodeni und seine radikale Entfernung,” Beitrage zur Klinischen Chirurgie, vol. 78, pp. 439–486, 1912.
View at: Google Scholar
C. J. Yeo, J. L. Cameron, K. D. Lillemoe et al., “Pancreaticoduodenectomy for cancer of the head of the pancreas: 201 patients,” Annals of Surgery, vol. 221, no. 6, pp. 721–733, 1995.
View at: Publisher Site | Google Scholar
M. Carpelan-Holmström, S. Nordling, E. Pukkala et al., “Does anyone survive pancreatic ductal adenocarcinoma? A nationwide study re-evaluating the data of the Finnish Cancer Registry,” Gut, vol. 54, no. 3, pp. 385–387, 2005.
View at: Publisher Site | Google Scholar
R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer statistics, 2015,” CA Cancer Journal for Clinicians, vol. 65, no. 1, pp. 5–29, 2015.
View at: Publisher Site | Google Scholar
L. Rahib, B. D. Smith, R. Aizenberg, A. B. Rosenzweig, J. M. Fleshman, and L. M. Matrisian, “Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States,” Cancer Research, vol. 74, no. 11, pp. 2913–2921, 2014.
View at: Publisher Site | Google Scholar
C. B. O'Neill, C. L. Atoria, E. M. O'Reilly, J. Lafemina, M. C. Henman, and E. B. Elkin, “Costs and trends in pancreatic cancer treatment,” Cancer, vol. 118, no. 20, pp. 5132–5139, 2012.
View at: Publisher Site | Google Scholar
M. S. Lea and L. H. Stahlgren, “Is resection appropriate for adenocarcinoma of the pancreas?. A cost-benefit analysis,” The American Journal of Surgery, vol. 154, no. 6, pp. 651–654, 1987.
View at: Publisher Site | Google Scholar
J. P. A. Ioannidis, “Why most published research findings are false,” PLoS Medicine, vol. 2, no. 8, article e124, 2005.
View at: Publisher Site | Google Scholar
F. Glenn and B. Thorbjarnarson, “Carcinoma of the pancreas,” Annals of Surgery, vol. 159, pp. 945–958, 1964.
View at: Publisher Site | Google Scholar
A. Gallitano, H. Fransen, and R. G. Martin, “Carcinoma of the pancreas. Results of treatment,” Cancer, vol. 22, no. 5, pp. 939–944, 1968.
View at: Publisher Site | Google Scholar
G. Crile Jr., “The advantages of bypass operations over radical pancreatoduodenectomy in the treatment of pancreatic carcinoma,” Surgery Gynecology and Obstetrics, vol. 130, no. 6, pp. 1049–1053, 1970.
View at: Google Scholar
T. M. Shapiro, “Adenocarcinoma of the pancreas: a statistical analysis of biliary bypass vs whipple resection in good risk patients,” Annals of Surgery, vol. 182, no. 6, pp. 715–721, 1975.
View at: Publisher Site | Google Scholar
T. A. Gordon and J. L. Cameron, “Management of patients with carcinoma of the pancreas,” Journal of the American College of Surgeons, vol. 181, no. 6, pp. 558–560, 1995.
View at: Google Scholar
R. B. Cattell and W. C. Young, “Long survival in a case of carcinoma of the pancreas,” The Lahey Clinic Bulletin, vol. 10, no. 5, pp. 131–134, 1957.
View at: Google Scholar
B. Gudjonsson, “Carcinoma of the pancreas: critical analysis of costs, results of resections, and the need for standardized reporting,” Journal of the American College of Surgeons, vol. 181, no. 6, pp. 483–503, 1995.
View at: Google Scholar
B. Gudjonsson, “Letter to the editor,” Journal of the American College of Surgeons, vol. 183, pp. 290–291, 1996.
View at: Google Scholar
B. Gudjonsson, E. M. Livstone, and H. M. Spiro, “Cancer of the pancreas. Diagnostic accuracy and survival statistics,” Cancer, vol. 42, no. 5, pp. 2494–2506, 1978.
View at: Publisher Site | Google Scholar
B. Gudjonsson, “Cancer of the pancreas. 50 years of surgery,” Cancer, vol. 60, no. 9, pp. 2284–2303, 1987.
View at: Publisher Site | Google Scholar
M. H. G. Katz, P. W. T. Pisters, D. B. Evans et al., “Borderline resectable pancreatic cancer: the importance of this emerging stage of disease,” Journal of the American College of Surgeons, vol. 206, no. 5, pp. 833–846, 2008.
View at: Publisher Site | Google Scholar
J. Tepper, G. Nardi, and H. Suit, “Carcinoma of the pancreas: review of MGH experience from 1963 to 1973. Analysis of surgical failure and implications for radiation therapy,” Cancer, vol. 37, no. 3, pp. 1519–1524, 1976.
View at: Publisher Site | Google Scholar
I. T. Konstantinidis, A. L. Warshaw, J. N. Allen et al., “Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? What is a “true” R0 resection?” Annals of Surgery, vol. 257, no. 4, pp. 731–736, 2013.
View at: Publisher Site | Google Scholar
F. Michelassi, F. Erroi, P. J. Dawson et al., “Experience with 647 consecutive tumors of the duodenum, ampulla, head of the pancreas, and distal common bile duct,” Annals of Surgery, vol. 210, no. 4, pp. 544–556, 1989.
View at: Publisher Site | Google Scholar
M. K. Krzyzanowska, J. C. Weeks, and C. C. Earle, “Treatment of locally advanced pancreatic cancer in the real world: population-based practices and effectiveness,” Journal of Clinical Oncology, vol. 21, no. 18, pp. 3409–3414, 2003.
View at: Publisher Site | Google Scholar
M. Mohiuddin, F. Rosato, D. Barbot, A. Schuricht, W. Biermann, and R. Cantor, “Long-term results of combined modality treatment with I-125 implantation for carcinoma of the pancreas,” International Journal of Radiation Oncology, Biology, Physics, vol. 23, no. 2, pp. 305–311, 1992.
View at: Publisher Site | Google Scholar
E. L. Kaplan and P. Meier, “Nonparametric estimation from incomplete observations,” Journal of the American Statistical Association, vol. 53, pp. 457–481, 1958.
View at: Publisher Site | Google Scholar | Zentralblatt MATH | MathSciNet
A. B. Hill, Principles of Medical Statistics, The Lancet Limited, London, UK, 1971.
B. Gudjonsson, “Survival statistics gone awry: pancreatic cancer, a case in point,” Journal of Clinical Gastroenterology, vol. 35, no. 2, pp. 180–184, 2002.
View at: Publisher Site | Google Scholar
B. Gudjonsson, “Pancreatic cancer: survival, errors and evidence,” European Journal of Gastroenterology and Hepatology, vol. 21, no. 12, pp. 1379–1382, 2009.
View at: Publisher Site | Google Scholar
T. P. Wade, K. S. Virgo, and F. E. Johnson, “Distal pancreatectomy for cancer: results in U.S. Department of Veterans Affairs Hospitals, 1987–1991,” Pancreas, vol. 11, no. 4, pp. 341–344, 1995.
View at: Publisher Site | Google Scholar
S. B. Edge, R. E. Schmieg Jr., L. K. Rosenlof, and M. C. Wilhelm, “Pancreas cancer resection outcome in American university centers in 1989-1990,” Cancer, vol. 71, no. 11, pp. 3502–3508, 1993.
View at: Publisher Site | Google Scholar
S. W. Nienhuijs, S. A. van den Akker, E. de Vries, I. H. de Hingh, O. Visser, and V. E. Lemmens, “Nationwide improvement of only short-term survival after resection for pancreatic cancer in the netherlands,” Pancreas, vol. 41, no. 7, pp. 1063–1066, 2012.
View at: Publisher Site | Google Scholar
J. K. Bjerregaard, M. B. Mortensen, K. R. Schönnemann, and P. Pfeiffer, “Characteristics, therapy and outcome in an unselected and prospectively registered cohort of pancreatic cancer patients,” European Journal of Cancer, vol. 49, no. 1, pp. 98–105, 2013.
View at: Publisher Site | Google Scholar
J. Kaťuchová, J. Bober, and J. Radoňak, “Postoperative complications and survival rates for pancreatic cancer patients,” Wiener Klinische Wochenschrift, vol. 123, no. 3-4, pp. 94–99, 2011.
View at: Publisher Site | Google Scholar
C. G. Willett, K. Lewandrowski, A. L. Warshaw, J. Efird, and C. C. Compton, “Resection margins in carcinoma of the head of the pancreas: Implications for radiation therapy,” Annals of Surgery, vol. 217, no. 2, pp. 144–148, 1993.
View at: Publisher Site | Google Scholar
V. J. Picozzi, R. A. Kozarek, and L. W. Traverso, “Interferon-based adjuvant chemoradiation therapy after pancreaticoduodenectomy for pancreatic adenocarcinoma,” American Journal of Surgery, vol. 185, no. 5, pp. 476–480, 2003.
View at: Publisher Site | Google Scholar
J. L. Cameron, D. W. Crist, J. V. Sitzmann et al., “Factors influencing survival after pancreaticoduodenectomy for pancreatic cancer,” The American Journal of Surgery, vol. 161, no. 1, pp. 120–125, 1991.
View at: Publisher Site | Google Scholar
K. Z'graggen, B. A. Centeno, C. Fernandez-Del Castillo, R. E. Jimenez, J. Werner, and A. L. Warshaw, “Biological implications of tumor cells in blood and bone marrow of pancreatic cancer patients,” Surgery, vol. 129, no. 5, pp. 537–546, 2001.
View at: Publisher Site | Google Scholar
D. Henne-Bruns, I. Vogel, J. Lüttges, G. Klöppel, and B. Kremer, “Ductal adenocarcinoma of the pancreas head: survival after regional versus extended lymphadenectomy,” Hepato-Gastroenterology, vol. 45, no. 21, pp. 855–866, 1998.
View at: Google Scholar
D. Henne-Bruns, I. Vogel, J. Lüttges, G. Klöppel, and B. Kremer, “Surgery for ductal adenocarcinoma of the pancreatic head: staging, complications, and survival after regional versus extended lymphadenectomy,” World Journal of Surgery, vol. 24, no. 5, pp. 595–602, 2000.
View at: Publisher Site | Google Scholar
J. Klempnauer, G. J. Ridder, H. Bektas, and R. Pichlmayr, “Surgery for exocrine pancreatic cancer. Who are the 5- and 10-year survivors?” Oncology, vol. 52, no. 5, pp. 353–359, 1995.
View at: Google Scholar
J. Klempnauer, G. J. Ridder, and R. Pichlmayr, “Prognostic factors after resection of ampullary carcinoma: multivariate survival analysis in comparison with ductal cancer of the pancreatic head,” British Journal of Surgery, vol. 82, no. 12, pp. 1686–1691, 1995.
View at: Publisher Site | Google Scholar
J. Klempnauer, G. J. Ridder, H. Bektas, and R. Pichlmayr, “Extended resections of ductal pancreatic cancer-impact on operative risk and prognosis,” Oncology, vol. 53, no. 1, pp. 47–53, 1996.
View at: Google Scholar
F. A. Wenger, F. Peter, J. Zieren, A. Steiert, C. A. Jacobi, and J. M. Müller, “Prognosis factors in carcinoma of the head of the pancreas,” Digestive Surgery, vol. 17, no. 1, pp. 29–35, 2000.
View at: Publisher Site | Google Scholar
H. Wolff and H. Lippert, “Das pankreaskarzinom aus der sicht des chirurgen,” Zbl Chirurgie, vol. 112, pp. 1–11, 1987.
View at: Google Scholar
T. Bottger, J. Zech, W. Weber, K. Sorger, and T. Junginger, “Relevant factors in the prognosis of ductal pancreatic carcinoma,” Acta Chirurgica Scandinavica, vol. 156, no. 11-12, pp. 781–788, 1990.
View at: Google Scholar
T. C. Böttger, S. Störkel, S. Wellek, M. Stöckle, and T. Junginger, “Factors influencing survival after resection of pancreatic cancer. A DNA analysis and a histomorphologic study,” Cancer, vol. 73, no. 1, pp. 63–73, 1994.
View at: Publisher Site | Google Scholar
M. Trede, G. G. Schwall, and H.-D. Saeger, “Survival after pancreatoduodenectomy: 118 consecutive resections without an operative mortality,” Annals of Surgery, vol. 211, no. 4, pp. 447–458, 1990.
View at: Publisher Site | Google Scholar
A. Richter, M. Niedergethmann, D. Lorenz, J. W. Sturm, M. Trede, and S. Post, “Resection for cancers of the pancreatic head in patients aged 70 years or over,” European Journal of Surgery, vol. 168, no. 6, pp. 339–344, 2002.
View at: Publisher Site | Google Scholar
A. Richter, M. Niedergethmann, J. W. Sturm, D. Lorenz, S. Post, and M. Trede, “Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience,” World Journal of Surgery, vol. 27, no. 3, pp. 324–329, 2003.
View at: Publisher Site | Google Scholar
M. Hartel, M. Niedergethmann, M. Farag-Soliman et al., “Benefit of venous resection for ductal adenocarcinoma of the pancreatic head,” European Journal of Surgery, vol. 168, no. 12, pp. 707–712, 2002.
View at: Publisher Site | Google Scholar
M. Trede, “The surgical treatment of pancreatic carcinoma,” Surgery, vol. 97, no. 1, pp. 28–35, 1985.
View at: Google Scholar
F. P. Gall, H. Kessler, and P. Hermanek, “Surgical treatment of ductal pancreatic carcinoma,” European Journal of Surgical Oncology, vol. 17, no. 2, pp. 173–181, 1991.
View at: Google Scholar
F. P. Gall and H. Kessler, “Das Frühcarcinom des exokrinen Pankreas: Diagnose und Prognose,” Der Chirurg, vol. 58, pp. 78–83, 1987.
View at: Google Scholar
A. Tannapfel, C. Wittekind, and G. Hünefeld, “Ductal adenocarcinoma of the pancreas—histopathological features and prognosis,” International Journal of Pancreatology, vol. 12, no. 2, pp. 145–152, 1992.
View at: Publisher Site | Google Scholar
J. Kleeff, M. K. Diener, K. Z'graggen et al., “Distal pancreatectomy: risk factors for surgical failure in 302 consecutive cases,” Annals of Surgery, vol. 245, no. 4, pp. 573–582, 2007.
View at: Publisher Site | Google Scholar
T. Welsch, L. Degrate, S. Zschäbitz, S. Hofer, J. Werner, and J. Schmidt, “The need for extended intensive care after pancreaticoduodenectomy for pancreatic ductal adenocarcinoma,” Langenbeck's Archives of Surgery, vol. 396, no. 3, pp. 353–362, 2011.
View at: Publisher Site | Google Scholar
W. Hartwig, T. Hackert, U. Hinz et al., “Multivisceral resection for pancreatic malignancies. Risk-analysis and long-term outcome,” Annals of Surgery, vol. 250, no. 1, pp. 81–87, 2009.
View at: Publisher Site | Google Scholar
W. Hartwig, T. Hackert, U. Hinz et al., “Pancreatic cancer surgery in the new millennium: better prediction of outcome,” Annals of Surgery, vol. 254, no. 2, pp. 311–319, 2011.
View at: Publisher Site | Google Scholar
O. Strobel, V. Berens, U. Hinz et al., “Resection after neoadjuvant therapy for locally advanced, ‘unresectable’ pancreatic cancer,” Surgery, vol. 152, no. 3, pp. S33–S42, 2012.
View at: Publisher Site | Google Scholar
T. Pausch, W. Hartwig, U. Hinz et al., “Cachexia but not obesity worsens the postoperative outcome after pancreatoduodenectomy in pancreatic cancer,” Surgery, vol. 152, no. 3, pp. S81–S88, 2012.
View at: Publisher Site | Google Scholar
K. Rückert and F. Kümmerle, “Totale duodenopankreatektomie als regeloperation beim pankreazcarcinoma,” Der Chirurg, vol. 49, pp. 162–166, 1978.
View at: Google Scholar
F. Kümmerle and K. Rückert, “Surgical treatment of pancreatic cancer,” World Journal of Surgery, vol. 8, no. 6, pp. 889–894, 1984.
View at: Publisher Site | Google Scholar
F. Kümmerle and K. Rückert, “Role of surgical treatment in pancreatic carcinoma,” Digestive Diseases, vol. 4, no. 1, pp. 33–42, 1986.
View at: Google Scholar
I. M. Civello, D. Frontera, G. Viola, G. Cina, G. Sganga, and F. Crucitti, “Extensive resection in pancreatic cancer: review of the literature and personal experience,” Hepato-Gastroenterology, vol. 45, no. 23, pp. 1877–1893, 1998.
View at: Google Scholar
S. Alfieri, A. G. Morganti, A. Di Giorgio et al., “Improved survival and local control after intraoperative radiation therapy and postoperative radiation therapy: a multivariate analysis of 46 patients undergoing surgery for the pancreatic head,” Archives of Surgery, vol. 136, no. 3, pp. 343–347, 2001.
View at: Google Scholar
P. Magistrelli, A. Antinori, A. Crucitti et al., “Il trattamento chirugico resettivo del carcinoma pancreatico,” Tumori, vol. 85, pp. S22–S26, 1999.
View at: Google Scholar
P. Magistrelli, A. Antinori, A. Crucitti et al., “Prognostic factors after surgical resection for pancreatic carcinoma,” Journal of Surgical Oncology, vol. 74, no. 1, pp. 36–40, 2000.
View at: Publisher Site | Google Scholar
P. Magistrelli, R. Coppola, G. Tonini et al., “Apoptotic index or a combination of Bax/Bcl-2 expression correlate with survival after resection of pancreatic adenocarcinoma,” Journal of Cellular Biochemistry, vol. 97, no. 1, pp. 98–108, 2006.
View at: Publisher Site | Google Scholar
P. Magistrelli, R. Masetti, R. Coppola et al., “Pancreatic resection for periampullary cancer in elderly patients,” Hepato-Gastroenterology, vol. 45, no. 19, pp. 242–247, 1998.
View at: Google Scholar
A. G. Morganti, V. Valentini, G. Macchia et al., “Adjuvant radiotherapy in resectable pancreatic carcinoma,” European Journal of Surgical Oncology, vol. 28, no. 5, pp. 523–530, 2002.
View at: Publisher Site | Google Scholar
G. C. Mattiucci, E. Ippolito, G. R. D'Agostino et al., “Long-term analysis of gemcitabine-based chemoradiation after surgical resection for pancreatic adenocarcinoma,” Annals of Surgical Oncology, vol. 20, no. 2, pp. 423–429, 2013.
View at: Publisher Site | Google Scholar
M. Reni, M. G. Panucci, A. J. M. Ferreri et al., “Effect on local control and survival of electron beam intraoperative irradiation for resectable pancreatic adenocarcinoma,” International Journal of Radiation Oncology Biology Physics, vol. 50, no. 3, pp. 651–658, 2001.
View at: Publisher Site | Google Scholar
V. Dicarlo, G. Balzano, A. Zerbi, and E. Villa, “Pancreatic cancer resection in elderly patients,” British Journal of Surgery, vol. 85, no. 5, pp. 607–610, 1998.
View at: Publisher Site | Google Scholar
V. Di Carlo, A. Zerbi, G. Balzano, and V. Corso, “Pylorus-preserving pancreaticoduodenectomy versus conventional Whipple operation,” World Journal of Surgery, vol. 23, no. 9, pp. 920–925, 1999.
View at: Publisher Site | Google Scholar
A. M. Taschieri, M. Elli, M. Cristaldi, G. Montecamozzo, T. Porretta, and P. G. Danelli, “Pancreasectomia totale vs pancreasectomia parziale nel trattamento chirurgico del carcinoma della testa del pancreas,” Chirurgia Italiana, vol. 46, pp. 44–50, 1994.
View at: Google Scholar
A. M. Taschieri, M. Elli, M. Rovati et al., “Surgical treatment of pancreatic tumors invading the spleno-mesenteric-portal vessels. An Italian multicenter survey,” Hepato-Gastroenterology, vol. 46, no. 25, pp. 492–497, 1999.
View at: Google Scholar
G. Serio, C. Icono, G. Prati, E. Facci, G. Falezza, and A. Gorla, “La chirurgia resettiva per neoplasie pancreatiche negli ultimi venti anni,” Chirurgia Italiana, vol. 46, pp. 1–10, 1994.
View at: Google Scholar
S. Crippa, S. Partelli, G. Zamboni et al., “Poorly differentiated resectable pancreatic cancer: is upfront resection worthwhile?” Surgery, vol. 152, no. 3, pp. S112–S119, 2012.
View at: Publisher Site | Google Scholar
G. Malleo, G. Marchegiani, R. Salvia, G. Butturini, P. Pederzoli, and C. Bassi, “Pancreaticoduodenectomy for pancreatic cancer: the verona experience,” Surgery Today, vol. 41, no. 4, pp. 463–470, 2011.
View at: Publisher Site | Google Scholar
C. Iacono, S. Accordini, L. Bortolasi et al., “Results of pancreaticoduodenectomy for pancreatic cancer: extended versus standard procedure,” World Journal of Surgery, vol. 26, no. 11, pp. 1309–1314, 2002.
View at: Publisher Site | Google Scholar
G. Barugola, S. Partelli, S. Marcucci et al., “Resectable pancreatic cancer: who really benefits from resection?” Annals of Surgical Oncology, vol. 16, no. 12, pp. 3316–3322, 2009.
View at: Publisher Site | Google Scholar
G. Barugola, S. Partelli, S. Crippa et al., “Outcomes after resection of locally advanced or borderline resectable pancreatic cancer after neoadjuvant therapy,” American Journal of Surgery, vol. 203, no. 2, pp. 132–139, 2012.
View at: Publisher Site | Google Scholar
F. Mosca, P. C. Giulianotti, T. Balestracci et al., “La duodenocefalopancreasectomia con conservazione del piloro (PPPD) nel carcinoma pancreatico e periampollare,” Chirurgia Italiana, vol. 46, pp. 59–67, 1994.
View at: Google Scholar
F. Mosca, P. C. Giulianotti, T. Balestracci et al., “Long-term survival in pancreatic cancer: pylorus-preserving versus Whipple pancreatoduodenectomy,” Surgery, vol. 122, no. 3, pp. 553–566, 1997.
View at: Publisher Site | Google Scholar
S. Pedrazzoli, C. Sperti, and C. Pasquali, “Previsione della resecabilita e del rischio chirurgico del carcinoma pancreatic; fattori che condizionano la sopravivenza dopo intervento resettivo,” Chirurgia Italiana, vol. 46, pp. 30–38, 1994.
View at: Google Scholar
C. Sperti, B. Bonadimani, C. Pasquali et al., “Ductal adenocarcinoma of the pancreas. Clinicopathological features and survival,” Tumori, vol. 79, no. 5, pp. 325–330, 1993.
View at: Google Scholar
C. Sperti, C. Pasquali, A. Piccoli, and S. Pedrazzoli, “Survival after resection for ductal adenocarcinoma of the pancreas,” British Journal of Surgery, vol. 83, no. 5, pp. 625–631, 1996.
View at: Publisher Site | Google Scholar
C. Sperti, C. Pasquali, A. Piccoli, and S. Pedrazzoli, “Recurrence after resection for ductal adenocarcinoma of the pancreas,” World Journal of Surgery, vol. 21, no. 2, pp. 195–200, 1997.
View at: Publisher Site | Google Scholar
C. Sperti, C. Pasquali, and S. Pedrazzoli, “Ductal adenocarcinoma of the body and tail of the pancreas,” Journal of the American College of Surgeons, vol. 185, no. 3, pp. 255–259, 1997.
View at: Publisher Site | Google Scholar
Y. Murakami, K. Uemura, T. Sudo et al., “Postoperative adjuvant chemotherapy improves survival after surgical resection for pancreatic carcinoma,” Journal of Gastrointestinal Surgery, vol. 12, no. 3, pp. 534–541, 2008.
View at: Publisher Site | Google Scholar
Y. Murakami, K. Uemura, T. Sudo et al., “Number of metastatic lymph nodes, but not lymph node ratio, is an independent prognostic factor after resection of pancreatic carcinoma,” Journal of the American College of Surgeons, vol. 211, no. 2, pp. 196–204, 2010.
View at: Publisher Site | Google Scholar
Y. Murakami, K. Uemura, T. Sudo, Y. Hashimoto, Y. Yuasa, and T. Sueda, “Prognostic impact of para-aortic lymph node metastasis in pancreatic ductal adenocarcinoma,” World Journal of Surgery, vol. 34, no. 8, pp. 1900–1907, 2010.
View at: Publisher Site | Google Scholar
Y. Murakami, K. Uemura, T. Sudo et al., “Long-term results of adjuvant gemcitabine plus S-1 chemotherapy after surgical resection for pancreatic carcinoma,” Journal of Surgical Oncology, vol. 106, no. 2, pp. 174–180, 2012.
View at: Publisher Site | Google Scholar
Y. Murakami, K. Uemura, T. Sudo et al., “Benefit of portal or superior mesenteric vein resection with adjuvant chemotherapy for patients with pancreatic head carcinoma,” Journal of Surgical Oncology, vol. 107, no. 4, pp. 414–421, 2013.
View at: Publisher Site | Google Scholar
M. Kayahara, T. Nagakawa, K. Ueno et al., “Distal pancreatectomy. Does it have a role for pancreatic body and tail cancer,” Hepato-Gastroenterology, vol. 45, no. 21, pp. 827–832, 1998.
View at: Google Scholar
T. Nagakawa, I. Konishi, K. Ueno et al., “Surgical treatment of pancreatic cancer-the japanese experience,” International Journal of Pancreatology, vol. 9, no. 1, pp. 135–143, 1991.
View at: Google Scholar
M. Kayahara, T. Nagakawa, K. Ueno, T. Ohta, Y. Tsukioka, and I. Miyazaki, “Surgical strategy for carcinoma of the pancreas head area based on clinicopathologic analysis of nodal involvement and plexus invasion,” Surgery, vol. 117, no. 6, pp. 616–623, 1995.
View at: Publisher Site | Google Scholar
T. Nagakawa, M. Nagamori, F. Futakami et al., “Results of extensive surgery for pancreatic carcinoma,” Cancer, vol. 77, no. 4, pp. 640–645, 1996.
View at: Publisher Site | Google Scholar
T. Nagakawa, I. Konishi, K. Ueno, T. Ohta, M. Kayahara, and I. Miyazaki, “Extended radical pancreatectomy for carcinoma of the head of the pancreas,” Hepato-Gastroenterology, vol. 45, no. 21, pp. 849–854, 1998.
View at: Google Scholar
T. Nagakawa, H. Sanada, M. Inagaki et al., “Long-term survivors after resection of carcinoma of the head of the pancreas: significance of histologically curative resection,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 11, no. 6, pp. 402–408, 2004.
View at: Publisher Site | Google Scholar
T. Nagakawa, K. Ueno, T. Ohta et al., “Evaluation of long-term survivors after pancreatoduodenectomy for pancreatoduodenal carcinoma,” Hepato-Gastroenterology, vol. 42, no. 2, pp. 117–122, 1995.
View at: Google Scholar
T. Hiraoka, R. Uchino, K. Kanemitsu et al., “Combination of intraoperative radiation with resection of cancer of the pancreas,” International Journal of Pancreatology, vol. 7, no. 1–3, pp. 201–207, 1990.
View at: Publisher Site | Google Scholar
T. Hiraoka and K. Kanemitsu, “Value of extended resection and intraoperative radiotherapy for resectable pancreatic cancer,” World Journal of Surgery, vol. 23, no. 9, pp. 930–936, 1999.
View at: Publisher Site | Google Scholar
H. Takamori, T. Hiraoka, K. Kanemitsu, and T. Tsuji, “Pancreatic liver metastases after curative resection combined with intraoperative radiation for pancreatic cancer,” Hepato-Gastroenterology, vol. 51, no. 59, pp. 1500–1503, 2004.
View at: Google Scholar
H. Takamori, T. Hiraoka, K. Kanemitsu, T. Tsuji, C. Hamada, and H. Baba, “Identification of prognostic factors associated with early mortality after surgical resection for pancreatic cancer—under-analysis of cumulative survival curve,” World Journal of Surgery, vol. 30, no. 2, pp. 213–218, 2006.
View at: Publisher Site | Google Scholar
H. Takamori, T. Hiraoka, K. Kanemitsu et al., “Long-term outcomes of extended radical resection combined with intraoperative radiation therapy for pancreatic cancer,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 15, no. 6, pp. 603–607, 2008.
View at: Publisher Site | Google Scholar
A. Nakase, Y. Matsumoto, K. Uchida, and I. Honjo, “Surgical treatment of cancer of the pancreas and the periampullary region: cumulative results in 57 institutions in Japan,” Annals of Surgery, vol. 185, no. 1, pp. 52–57, 1977.
View at: Publisher Site | Google Scholar
T. Manabe, G. Ohshio, N. Baba et al., “Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas,” Cancer, vol. 64, no. 5, pp. 1132–1137, 1989.
View at: Publisher Site | Google Scholar
T. Manabe and T. Tobe, “Progress in the diagnosis and treatment of pancreatic cancer—The Kyoto University experience,” Hepato-Gastroenterology, vol. 36, no. 6, pp. 431–436, 1989.
View at: Google Scholar
T. Manabe, G. Ohshio, N. Baba, and T. Tobe, “Factors influencing prognosis and indications for curative pancreatectomy for ductal adenocarcinoma of the head of the pancreas,” International Journal of Pancreatology, vol. 7, no. 1–3, pp. 187–193, 1990.
View at: Publisher Site | Google Scholar
M. Kokubo, Y. Nishimura, Y. Shibamoto et al., “Analysis of the clinical benefit of intraoperative radiotherapy in patients undergoing macroscopically curative resection for pancreatic cancer,” International Journal of Radiation Oncology Biology Physics, vol. 48, no. 4, pp. 1081–1087, 2000.
View at: Publisher Site | Google Scholar
M. Imamura, R. Hosotani, and M. Kogire, “Rationale of the so-called extended resection for pancreatic invasive ductal carcinoma,” Digestion, vol. 60, no. 1, pp. 126–129, 1999.
View at: Publisher Site | Google Scholar
R. Hosotani, M. Kogire, S. Arii, Y. Nishimura, M. Hiraoka, and M. Imamura, “Results of pancreatectomy with radiation therapy for pancreatic cancer,” Hepato-Gastroenterology, vol. 44, no. 18, pp. 1528–1535, 1997.
View at: Google Scholar
R. Doi, H. Ikeda, H. Kobayashi, M. Kogire, and M. Imamura, “Carcinoma in the remnant pancreas after distal pancreatectomy for carcinoma,” European Journal of Surgery, Supplement, vol. 168, no. 588, pp. 62–65, 2003.
View at: Google Scholar
R. Doi, M. Imamura, R. Hosotani et al., “Surgery versus radiochemotherapy for resectable locally invasive pancreatic cancer: final results of a randomized multi-institutional trial,” Surgery Today, vol. 38, no. 11, pp. 1021–1028, 2008.
View at: Publisher Site | Google Scholar
R. Tsuchiya, T. Oribe, and T. Noda, “Size of the tumor and other factors influencing prognosis of carcinoma of the head of the pancreas,” American Journal of Gastroenterology, vol. 80, no. 6, pp. 459–462, 1985.
View at: Google Scholar
R. Tsuchiya, T. Noda, N. Harada et al., “Collective review of small carcinomas of the pancreas,” Annals of Surgery, vol. 203, no. 1, pp. 77–81, 1986.
View at: Publisher Site | Google Scholar
R. Tsuchiya, N. Harada, T. Tsunoda, T. Miyamoto, and K. Ura, “Long-term survivors after operation on carcinoma of the pancreas,” International Journal of Pancreatology, vol. 3, no. 6, pp. 491–496, 1988.
View at: Publisher Site | Google Scholar
R. Tsuchiya, T. Tsunoda, and T. Yamaguchi, “Operation of choice for resectable carcinoma of the head of the pancreas,” International Journal of Pancreatology, vol. 6, no. 4, pp. 295–306, 1990.
View at: Publisher Site | Google Scholar
A. Nanashima, S. Tobinaga, T. Abo et al., “Evaluation of surgical resection for pancreatic carcinoma at a Japanese single cancer institute,” Hepato-Gastroenterology, vol. 59, no. 115, pp. 911–915, 2012.
View at: Publisher Site | Google Scholar
Y. Nimura, M. Nagino, S. Takao et al., “Standard versus extended lymphadenectomy in radical pancreatoduodenectomy for ductal adenocarcinoma of the head of the pancreas,” Journal of Hepato-Biliary-Pancreatic Sciences, vol. 19, no. 3, pp. 230–241, 2012.
View at: Publisher Site | Google Scholar
A. Nakao, “Debate: extended resection for pancreatic cancer; the affirmative case,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 10, no. 1, pp. 57–60, 2003.
View at: Google Scholar
A. Nakao, S. Takeda, M. Sakai et al., “Extended radical resection versus standard resection for pancreatic cancer: the rationale for extended radical resection,” Pancreas, vol. 28, no. 3, pp. 289–292, 2004.
View at: Publisher Site | Google Scholar
A. Nakao, S. Takeda, S. Inoue et al., “Indications and techniques of extended resection for pancreatic cancer,” World Journal of Surgery, vol. 30, no. 6, pp. 976–982, 2006.
View at: Publisher Site | Google Scholar
S. Yamada, T. Fujii, A. Nakao et al., “Aggressive surgery for borderline resectable pancreatic cancer: evaluation of national comprehensive cancer network guidelines,” Pancreas, vol. 42, no. 6, pp. 1004–1010, 2013.
View at: Publisher Site | Google Scholar
O. Ishikawa, H. Ohigashi, S. Imaoka et al., “Minute carcinoma of the pancreas measuring 1 cm or less in diameter—collective review of Japanese case reports,” Hepato-Gastroenterology, vol. 46, no. 25, pp. 8–15, 1999.
View at: Google Scholar
Y. Matsui, Y. Aoki, O. Ishikawa et al., “Ductal carcinoma of the pancreas. Rationales for total pancreatectomy,” Archives of Surgery, vol. 114, no. 6, pp. 722–726, 1979.
View at: Publisher Site | Google Scholar
M. Miyata, K. Nakao, T. Takao et al., “An appraisal of pancreatectomy for advanced cancer of the pancreas based on survival rate and postoperative physical performance,” Journal of Surgical Oncology, vol. 45, no. 1, pp. 33–39, 1990.
View at: Publisher Site | Google Scholar
K. Satake, H. Nishiwaki, H. Yokomatsu et al., “Surgical curability and prognosis for standard versus extended resection for T1 carcinoma of the pancreas,” Surgery Gynecology and Obstetrics, vol. 175, no. 3, pp. 259–265, 1992.
View at: Google Scholar
O. Ishikawa, “Surgical technique, curability and postoperative quality of life in an extended pancreatectomy for adenocarcinoma of the pancreas,” Hepato-Gastroenterology, vol. 43, no. 8, pp. 320–325, 1996.
View at: Google Scholar
O. Ishikawa, H. Ohigashi, Y. Sasaki et al., “Adjuvant therapies in extended pancreatectomy for ductal adenocarcinoma of the pancreas,” Hepato-Gastroenterology, vol. 45, no. 21, pp. 644–650, 1998.
View at: Google Scholar
O. Ishikawa, H. Ohigashi, S. Imaoka et al., “Preoperative indications for extended pancreatectomy for locally advanced pancreas cancer involving the portal vein,” Annals of Surgery, vol. 215, no. 3, pp. 231–236, 1992.
View at: Publisher Site | Google Scholar
O. Ishikawa, H. Ohigashi, S. Imaoka et al., “Is the long-term survival rate improved by preoperative irradiation prior to Whipple's procedure for adenocarcinoma of the pancreatic head?” Archives of Surgery, vol. 129, no. 10, pp. 1075–1080, 1994.
View at: Publisher Site | Google Scholar
H. Ohigashi, O. Ishikawa, H. Eguchi et al., “Feasibility and efficacy of combination therapy with preoperative full-dose gemcitabine, concurrent three-dimensional conformal radiation, surgery, and postoperative liver perfusion chemotherapy for T3-pancreatic cancer,” Annals of Surgery, vol. 250, no. 1, pp. 88–95, 2009.
View at: Publisher Site | Google Scholar
H. Ohigashi, O. Ishikawa, H. Eguchi et al., “Feasibility and efficacy of combination therapy with preoperative and postoperative chemoradiation, extended pancreatectomy, and postoperative liver perfusion chemotherapy for locally advanced cancers of the pancreatic head,” Annals of Surgical Oncology, vol. 12, no. 8, pp. 629–636, 2005.
View at: Publisher Site | Google Scholar
H. Takahashi, H. Ohigashi, O. Ishikawa et al., “Perineural invasion and lymph node involvement as indicators of surgical outcome and pattern of recurrence in the setting of preoperative gemcitabine-based chemoradiation therapy for resectable pancreatic cancer,” Annals of Surgery, vol. 255, pp. 95–102, 2012.
View at: Google Scholar
H. Takahashi, H. Ohigashi, K. Gotoh et al., “Preoperative gemcitabine-based chemoradiation therapy for resectable and borderline resectable pancreatic cancer,” Annals of Surgery, vol. 258, no. 6, pp. 1040–1050, 2013.
View at: Publisher Site | Google Scholar
F. Motoi, T. Rikiyama, Y. Katayose, S.-I. Egawa, and M. Unno, “Retrospective evaluation of the influence of postoperative tumor marker status on survival and patterns of recurrence after surgery for pancreatic cancer based on RECIST guidelines,” Annals of Surgical Oncology, vol. 18, no. 2, pp. 371–379, 2011.
View at: Publisher Site | Google Scholar
T. Sato, Y. Saitoh, N. Noto, and S. Matsuno, “Follow up studies of radical resection for pancreaticoduodenal cancer,” Annals of Surgery, vol. 186, no. 5, pp. 581–588, 1977.
View at: Publisher Site | Google Scholar
T. Sato, Y. Saitoh, N. Noto, and S. Matsuno, “Factors influencing the late results of operation for carcinoma of the pancreas,” The American Journal of Surgery, vol. 136, no. 5, pp. 582–586, 1978.
View at: Publisher Site | Google Scholar
S. Matsuno and T. Sato, “Surgical treatment for carcinoma of the pancreas. Experience in 272 patients,” The American Journal of Surgery, vol. 152, no. 5, pp. 499–503, 1986.
View at: Publisher Site | Google Scholar
C. Shibata, M. Kobari, T. Tsuchiya et al., “Pancreatectomy combined with superior mesenteric-portal vein resection for adenocarcinoma in pancreas,” World Journal of Surgery, vol. 25, no. 8, pp. 1002–1005, 2001.
View at: Publisher Site | Google Scholar
N. Sata, K. Kurashina, H. Nagai et al., “The effect of adjuvant and neoadjuvant chemo(radio)therapy on survival in 1,679 resected pancreatic carcinoma cases in Japan: report of the national survey in the 34th annual meeting of Japanese Society of Pancreatic Surgery,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 16, no. 4, pp. 485–492, 2009.
View at: Publisher Site | Google Scholar
K. Yoshizawa, H. Nagai, K. Kurihara, N. Sata, T. Kawai, and K. Saito, “Long-term survival after surgical resection for pancreatic cancer,” Hepato-Gastroenterology, vol. 48, no. 40, pp. 1153–1156, 2001.
View at: Google Scholar
S. Hishinuma, Y. Ogata, M. Tomikawa, I. Ozawa, K. Hirabayashi, and S. Igarashi, “Patterns of recurrence after curative resection of pancreatic cancer, based on autopsy findings,” Journal of Gastrointestinal Surgery, vol. 10, no. 4, pp. 511–518, 2006.
View at: Publisher Site | Google Scholar
S. Hishinuma, Y. Ogata, M. Tomikawa, and I. Ozawa, “Stomach-preserving distal pancreatectomy with combined resection of the celiac artery: radical procedure for locally advanced cancer of the pancreatic body,” Journal of Gastrointestinal Surgery, vol. 11, no. 6, pp. 743–749, 2007.
View at: Publisher Site | Google Scholar
Y. Ogata and S. Hishinuma, “The impact of pylorus-preserving pancreatoduodenectomy on surgical treatment for cancer of the pancreatic head,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 9, no. 2, pp. 223–232, 2002.
View at: Publisher Site | Google Scholar
H. Ozaki, T. Kinoshita, T. Kosuge et al., “An aggressive therapeutic approach to carcinoma of the body and tail of the pancreas,” Cancer, vol. 77, no. 11, pp. 2240–2245, 1996.
View at: Publisher Site | Google Scholar
K. Shimada, Y. Sakamoto, S. Nara, M. Esaki, T. Kosuge, and N. Hiraoka, “Analysis of 5-year survivors after a macroscopic curative pancreatectomy for invasive ductal adenocarcinoma,” World Journal of Surgery, vol. 34, no. 8, pp. 1908–1915, 2010.
View at: Publisher Site | Google Scholar
K. Shimada, Y. Sakamoto, T. Sano, T. Kosuge, and N. Hiraoka, “Reappraisal of the clinical significance of tumor size in patients with pancreatic ductal carcinoma,” Pancreas, vol. 33, no. 3, pp. 233–239, 2006.
View at: Publisher Site | Google Scholar
S. Yachida, N. Fukushima, M. Sakamoto, Y. Matsuno, T. Kosuge, and S. Hirohashi, “Implications of peritoneal washing cytology in patients with potentially resectable pancreatic cancer,” British Journal of Surgery, vol. 89, no. 5, pp. 573–578, 2002.
View at: Publisher Site | Google Scholar
K. Shimada, Y. Sakamoto, T. Sano, and T. Kosuge, “Prognostic factors after distal pancreatectomy with extended lymphadenectomy for invasive pancreatic adenocarcinoma of the body and tail,” Surgery, vol. 139, no. 3, pp. 288–295, 2006.
View at: Publisher Site | Google Scholar
K. Shimada, Y. Sakamoto, T. Sano, and T. Kosuge, “The role of paraaortic lymph node involvement on early recurrence and survival after macroscopic curative resection with extended lymphadenectomy for pancreatic carcinoma,” Journal of the American College of Surgeons, vol. 203, no. 3, pp. 345–352, 2006.
View at: Publisher Site | Google Scholar
S. Oguro, K. Shimada, Y. Kishi, S. Nara, M. Esaki, and T. Kosuge, “Perioperative and long-term outcomes after pancreaticoduodenectomy in elderly patients 80 years of age and older,” Langenbeck's Archives of Surgery, vol. 398, no. 4, pp. 531–538, 2013.
View at: Publisher Site | Google Scholar
E. M. Miller and O. T. Clagett, “Survival five years after radical pancreatoduodenectomy for carcinoma of the head of the pancreas,” Annals of Surgery, vol. 134, no. 6, pp. 1013–1017, 1951.
View at: Publisher Site | Google Scholar
J. J. Monge, E. S. Judd, and R. P. Gage, “Radical pancreatoduodenectomy: a 22-year experience with the complications, mortality rate and survival rate,” Annals of Surgery, vol. 160, pp. 711–722, 1964.
View at: Publisher Site | Google Scholar
W. H. ReMine, J. T. Priestley, E. S. Judd, and J. N. King, “Total pancreatectomy,” Annals of Surgery, vol. 172, no. 4, pp. 595–604, 1970.
View at: Publisher Site | Google Scholar
M. B. Pliam and W. H. ReMine, “Further evaluation of total pancreatectomy,” Archives of Surgery, vol. 110, no. 5, pp. 506–512, 1975.
View at: Publisher Site | Google Scholar
A. J. Edis, P. D. Kiernan, and W. F. Taylor, “Attempted curative resection of ductal carcinoma of the pancreas. Review of Mayo Clinic experience, 1951–1975,” Mayo Clinic Proceedings, vol. 55, no. 9, pp. 531–536, 1980.
View at: Google Scholar
J. A. van Heerden, W. H. ReMine, L. H. Weiland, D. C. McIlrath, and D. M. Ilstrup, “Total pancreatectomy for ductal adenocarcinoma of the pancreas. Mayo clinic experience,” The American Journal of Surgery, vol. 142, no. 3, pp. 308–311, 1981.
View at: Publisher Site | Google Scholar
J. A. Van Heerden, D. C. McIlrath, D. M. Ilstrup, and L. H. Weiland, “Total pancreatectomy for ductal adenocarcinoma of the pancreas: an update,” World Journal of Surgery, vol. 12, no. 5, pp. 658–661, 1988.
View at: Publisher Site | Google Scholar
R. R. Dalton, M. G. Sarr, J. A. Van Heerden, and T. V. Colby, “Carcinoma of the body and tail of the pancreas: is curative resection justified?” Surgery, vol. 111, no. 5, pp. 489–494, 1992.
View at: Google Scholar
J. A. Van Heerden, “Pancreatic resection for carcinoma of the pancreas: whipple versus total pancreatectomy-an institutional perspective,” World Journal of Surgery, vol. 8, no. 6, pp. 880–888, 1984.
View at: Publisher Site | Google Scholar
M. L. Foo, L. L. Gunderson, D. M. Nagorney et al., “Patterns of failure in grossly resected pancreatic ductal adenocarcinoma treated with adjuvant irradiation ± 5 fluorouracil,” International Journal of Radiation Oncology, Biology, Physics, vol. 26, no. 3, pp. 483–489, 1993.
View at: Publisher Site | Google Scholar
T. Schnelldorfer, A. L. Ware, M. G. Sarr et al., “Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible?” Annals of Surgery, vol. 247, no. 3, pp. 456–462, 2008.
View at: Publisher Site | Google Scholar
J. Fatima, T. Schnelldorfer, J. Barton et al., “Pancreatoduodenectomy for ductal adenocarcinoma: implications of positive margin on survival,” Archives of Surgery, vol. 145, no. 2, pp. 167–172, 2010.
View at: Publisher Site | Google Scholar
S. Khan, G. Sclabas, K. Reid-Lombardo et al., “Does body mass index/morbid obesity influence outcome in patients who undergo pancreatoduodenectomy for pancreatic adenocarcinoma?” Journal of Gastrointestinal Surgery, vol. 14, no. 11, pp. 1820–1825, 2010.
View at: Publisher Site | Google Scholar
S. Khan, G. Sclabas, K. R. Lombardo et al., “Pancreatoduodenectomy for ductal adenocarcinoma in the very elderly; is it safe and justified?” Journal of Gastrointestinal Surgery, vol. 14, no. 11, pp. 1826–1831, 2010.
View at: Publisher Site | Google Scholar
S. S. Nitecki, M. G. Sarr, T. V. Colby, and J. A. Van Heerden, “Long-term survival after resection for ductal adenocarcinoma of the pancreas: is it really improving?” Annals of Surgery, vol. 221, no. 1, pp. 59–66, 1995.
View at: Publisher Site | Google Scholar
M. P. Spencer, M. G. Sarr, and D. M. Nagorney, “Radical pancreatectomy for pancreatic cancer in the elderly: is it safe and justified?” Annals of Surgery, vol. 212, no. 2, pp. 140–143, 1990.
View at: Publisher Site | Google Scholar
B. J. Billings, J. D. Christein, W. S. Harmsen et al., “Quality-of-life after total pancreatectomy: is it really that bad on long-term follow-up?” Journal of Gastrointestinal Surgery, vol. 9, no. 8, pp. 1059–1067, 2005.
View at: Publisher Site | Google Scholar
C. C. Hsu, J. M. Herman, M. M. Corsini et al., “Adjuvant chemoradiation for pancreatic adenocarcinoma: The Johns Hopkins Hospital-Mayo Clinic collaborative study,” Annals of Surgical Oncology, vol. 17, no. 4, pp. 981–990, 2010.
View at: Publisher Site | Google Scholar
J. D. Christein, M. L. Kendrick, C. W. Iqbal, D. M. Nagorney, and M. B. Farnell, “Distal pancreatectomy for resectable adenocarcinoma of the body and tail of the pancreas,” Journal of Gastrointestinal Surgery, vol. 9, no. 7, pp. 922–927, 2005.
View at: Publisher Site | Google Scholar
M. B. Farnell, R. K. Pearson, M. G. Sarr et al., “A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma,” Surgery, vol. 138, no. 4, pp. 618–630, 2005.
View at: Publisher Site | Google Scholar
M. Al-Haddad, J. K. Martin, J. Nguyen et al., “Vascular resection and reconstruction for pancreatic malignancy: a single center survival study,” Journal of Gastrointestinal Surgery, vol. 11, no. 9, pp. 1168–1174, 2007.
View at: Publisher Site | Google Scholar
J. G. Barton, T. Schnelldorfer, C. M. Lohse et al., “Patterns of pancreatic resection differ between patients with familial and sporadic pancreatic cancer,” Journal of Gastrointestinal Surgery, vol. 15, no. 5, pp. 836–842, 2011.
View at: Publisher Site | Google Scholar
K. P. Croome, M. B. Farnell, F. G. Que et al., “Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. Oncologic advances over open approaches,” Annals of Surgery, vol. 260, no. 4, pp. 633–640, 2014.
View at: Publisher Site | Google Scholar
D. W. Crist, J. V. Sitzmann, and J. L. Cameron, “Improved hospital morbidity, mortality, and survival after the Whipple procedure,” Annals of Surgery, vol. 206, no. 3, pp. 358–365, 1987.
View at: Publisher Site | Google Scholar
D. W. Crist and J. L. Cameron, “Current status of pancreaticoduodenectomy for periampullary carcinoma,” Hepato-Gastroenterology, vol. 36, no. 6, pp. 478–485, 1989.
View at: Google Scholar
J. L. Cameron, T. S. Riall, J. Coleman, and K. A. Belcher, “One thousand consecutive pancreaticoduodenectomies,” Annals of Surgery, vol. 244, no. 1, pp. 10–15, 2006.
View at: Publisher Site | Google Scholar
C. J. Yeo, T. A. Sohn, J. L. Cameron, R. H. Hruban, K. D. Lillemoe, and H. A. Pitt, “Periampullary adenocarcinoma: analysis of 5-year survivors,” Annals of Surgery, vol. 227, no. 6, pp. 821–831, 1998.
View at: Publisher Site | Google Scholar
J. A. DiGiuseppe, C. J. Yeo, and R. H. Hruban, “Molecular biology and the diagnosis and treatment of adenocarcinoma of the pancreas,” Advances in Anatomic Pathology, vol. 3, no. 3, pp. 139–155, 1996.
View at: Publisher Site | Google Scholar
T. S. Riall, J. L. Cameron, K. D. Lillemoe et al., “Resected periampullary adenocarcinoma: 5-year survivors and their 6- to 10-year follow-up,” Surgery, vol. 140, no. 5, pp. 764–772, 2006.
View at: Publisher Site | Google Scholar
M. A. Makary, J. M. Winter, J. L. Cameron et al., “Pancreaticoduodenectomy in the very elderly,” Journal of Gastrointestinal Surgery, vol. 10, no. 3, pp. 347–356, 2006.
View at: Publisher Site | Google Scholar
J. M. Winter, J. L. Cameron, K. A. Campbell et al., “1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience,” Journal of Gastrointestinal Surgery, vol. 10, no. 9, pp. 1199–1211, 2006.
View at: Publisher Site | Google Scholar
S. Reddy, C. L. Wolfgang, J. L. Cameron et al., “Total pancreatectomy for pancreatic adenocarcinoma: evaluation of morbidity and long-term Survival,” Annals of Surgery, vol. 250, no. 2, pp. 282–287, 2009.
View at: Publisher Site | Google Scholar
I. H. Nordback, R. H. Hruban, J. K. Boitnott, H. A. Pitt, and J. L. Cameron, “Carcinoma of the body and tail of the pancreas,” The American Journal of Surgery, vol. 164, no. 1, pp. 26–31, 1992.
View at: Publisher Site | Google Scholar
D. C. Allison, K. K. Bose, R. H. Hruban et al., “Pancreatic cancer cell DNA content correlates with long-term survival after pancreatoduodenectomy,” Annals of Surgery, vol. 214, no. 6, pp. 648–656, 1991.
View at: Publisher Site | Google Scholar
D. C. Allison, S. Piantadosi, R. H. Hruban et al., “DNA content and other factors associated with ten-year survival after resection of pancreatic carcinoma,” Journal of Surgical Oncology, vol. 67, no. 3, pp. 151–159, 1998.
View at: Publisher Site | Google Scholar
J. He, B. H. Edil, J. L. Cameron et al., “Young patients undergoing resection of pancreatic cancer fare better than their older counterparts,” Journal of Gastrointestinal Surgery, vol. 17, no. 2, pp. 339–344, 2013.
View at: Publisher Site | Google Scholar
G. E. McGuire, H. A. Pitt, K. D. Lillemoe, J. E. Niederhuber, C. J. Yeo, and J. L. Cameron, “Reoperative surgery for periampullary adenocarcinoma,” Archives of Surgery, vol. 126, no. 10, pp. 1205–1212, 1991.
View at: Publisher Site | Google Scholar
J. W. Lin, J. L. Cameron, C. J. Yeo, T. S. Riall, and K. D. Lillemoe, “Risk factors and outcomes in postpancreaticoduodenectomy pancreaticocutaneous fistula,” Journal of Gastrointestinal Surgery, vol. 8, no. 8, pp. 951–959, 2004.
View at: Publisher Site | Google Scholar
T. A. Sohn, C. J. Yeo, J. L. Cameron et al., “Resected adenocarcinoma of the pancreas—616 patients: results, outcomes, and prognostic indicators,” Journal of Gastrointestinal Surgery, vol. 4, no. 6, pp. 567–579, 2000.
View at: Publisher Site | Google Scholar
K. D. Lillemoe, J. L. Cameron, C. J. Yeo et al., “Pancreaticoduodenectomy: does it have a role in the palliation of pancreatic cancer?” Annals of Surgery, vol. 223, no. 6, pp. 718–728, 1996.
View at: Publisher Site | Google Scholar
C. J. Yeo, J. L. Cameron, T. A. Sohn et al., “Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes,” Annals of Surgery, vol. 226, no. 3, pp. 248–260, 1997.
View at: Publisher Site | Google Scholar
T. A. Sohn, K. D. Lillemoe, J. L. Cameron, J. J. Huang, H. A. Pitt, and C. J. Yeo, “Surgical palliation of unresectable periampullary adenocarcinoma in the 1990s,” Journal of the American College of Surgeons, vol. 188, no. 6, pp. 658–669, 1999.
View at: Publisher Site | Google Scholar
B. Hristov, S. Reddy, S. H. Lin et al., “Outcomes of adjuvant chemoradiation after pancreaticoduodenectomy with mesenterico-portal vein resection for adenocarcinoma of the pancreas,” International Journal of Radiation Oncology Biology Physics, vol. 76, no. 1, pp. 176–180, 2010.
View at: Publisher Site | Google Scholar
A. L. Gleisner, L. Assumpcao, J. L. Cameron et al., “Is resection of periampullary or pancreatic adenocarcinoma with synchronous hepatic metastasis justified?” Cancer, vol. 110, no. 11, pp. 2484–2492, 2007.
View at: Publisher Site | Google Scholar
B. Asiyanbola, A. Gleisner, J. M. Herman et al., “Determining pattern of recurrence following pancreaticoduodenectomy and adjuvant 5-flurouracil-based chemoradiation therapy: effect of number of metastatic lymph nodes and lymph node ratio,” Journal of Gastrointestinal Surgery, vol. 13, no. 4, pp. 752–759, 2009.
View at: Publisher Site | Google Scholar
S. Tsai, M. A. Choti, L. Assumpcao et al., “Impact of obesity on perioperative outcomes and survival following pancreaticoduodenectomy for pancreatic cancer: a large single-institution study,” Journal of Gastrointestinal Surgery, vol. 14, no. 7, pp. 1143–1150, 2010.
View at: Publisher Site | Google Scholar
C. J. Yeo, J. L. Cameron, K. D. Lillemoe et al., “Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality,” Annals of Surgery, vol. 236, no. 3, pp. 355–368, 2002.
View at: Publisher Site | Google Scholar
C. J. Yeo, “The whipple operation: is a radical resection of benefit?” Advances in Surgery, vol. 37, pp. 1–27, 2003.
View at: Google Scholar
T. S. Riall, J. L. Cameron, K. D. Lillemoe et al., “Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma-part 3: update on 5-year survival,” Journal of Gastrointestinal Surgery, vol. 9, no. 9, pp. 1191–1206, 2005.
View at: Publisher Site | Google Scholar
D. M. Emick, T. S. Riall, J. L. Cameron et al., “Hospital readmission after pancreaticoduodenectomy,” Journal of Gastrointestinal Surgery, vol. 10, no. 9, pp. 1243–1253, 2006.
View at: Publisher Site | Google Scholar
H. Nathan, C. L. Wolfgang, B. H. Edil et al., “Peri-operative mortality and long-term survival after total pancreatectomy for pancreatic adenocarcinoma: a population-based perspective,” Journal of Surgical Oncology, vol. 99, no. 2, pp. 87–92, 2009.
View at: Publisher Site | Google Scholar

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Copyright © 2016 Birgir Gudjonsson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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