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10.1245/ASO.2005.02.021
Annals of Surgical Oncology 12:145-151 (2005)
© 2005 Society of Surgical Oncology
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Original Article

The Prognostic Effect of Clinical Staging in Pancreatic Adenocarcinoma

Alessio G. Morganti, MD1, M. Gabriella Brizi, MD2, Gabriella Macchia, MD1, Giuseppina Sallustio, MD3, Guido Costamagna, MD4, Sergio Alfieri, MD5, Gian Carlo Mattiucci, MD6, Vincenzo Valentini, MD6, Luigi Natale, MD2, Francesco Deodato, MD1, Massimiliano Mutignani, MD4, G. Battista Doglietto, MD5 and Numa Cellini, MD6

1 Department of Radiotherapy, Centro di Ricerca e Formazione ad Alta Tecnologia nelle Scienze Biomediche, Universitá Cattolica del S. Cuore, Contrada Tappino, 86100 Campobasso, Italy
2 Department of Radiology, Università Cattolica del S. Cuore, Largo Gemelli 8, 00168 Rome, Italy
3 Department of Radiology, Centro di Ricerca e Formazione ad Alta Tecnologia nelle Scienze Biomediche, Università Cattolica del S. Cuore, Contrada Tappino, 86100 Campobasso, Italy
4 Department of Digestive Endoscopy, Università Cattolica del S. Coure, Largo Gemelli 8, 00168 Rome, Italy
5 Department of Surgery, Università Cattolica del S. Cuore, Largo Gemelli 8, 00168 Rome, Italy
6 Department of Radiotherapy, Universitá Cattolica del S. Cuore, Largo Gemelli 8, 00168 Rome, Italy

Correspondence: Address correspondence and reprint requests to: Gabriella Macchia, MD; E-mail: gmacchia{at}rm.unicatt.it.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The importance of pancreatic cancer staging is uncertain. The aim of this report was to evaluate the accuracy of combined standard imaging techniques in predicting the pathologic stage and to evaluate the prognostic effect of clinical staging to identify patient groups in which laparoscopy and laparotomy could be beneficial.

Methods: Fifty-four patients were included in this analysis. The techniques used for clinical staging were endoscopic retrograde cholangiopancreatography, abdominal computed tomographic scan, and ultrasonography. All patients underwent both clinical and surgical/pathologic staging. A comparison was performed between presurgical stage and surgical/pathologic stage. The prognostic effect of different factors on survival was evaluated with both univariate (log-rank) and multivariate (Cox) analysis.

Results: Sensitivity and specificity for vascular involvement were 73.9% and 96.3%, respectively. Sensitivity and specificity for nodal involvement were 63.6% and 95.4%, respectively. A total of 33.3% of patients showed a higher than expected pathologic stage, and 3.7% showed a lower than expected pathologic stage, by comparing clinical and pathologic evaluation. A highly significant correlation was observed between clinical T stage (P = .0067) and tumor diameter (P = .0037) and patient survival. Maximal prognostic differentiation was observed by dividing patients into two groups based on imaging results: group A (favorable prognosis) and group B (unfavorable prognosis). The median survival was 25.1 and 8.0 months for group A and B, respectively. Five-year survival was 20.1% and 0%, respectively (multivariate analysis: P = .0007).

Conclusions: Integrated standard imaging studies achieved reasonable diagnostic accuracy in our analysis. A single classification based on clinical stage and tumor diameter evaluated by imaging predicts prognosis in patients with pancreatic carcinoma.

Key Words: Pancreatic neoplasms • Imaging • Staging • Prognostic factors • Surgery • Radiotherapy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pancreatic cancer is an aggressive disease with a dismal prognosis. Traditional management of non-metastatic disease consists of surgical exploration followed by pancreatectomy, when feasible, or bypass procedures. The importance of staging, beyond that of "resectable" and "unresectable," is uncertain because state-of-the-art treatments have demonstrated little effect on survival. More recently, a renewed interest in patient stratification, particularly in preoperative staging, is evident.1,2 This is partially due to promising preliminary results of preoperative combined- modality treatments,3–6 which suggested protocols without preliminary surgical exploration. However, to date, most reports on the effect of stage on prognosis are based on surgical/pathologic evaluation. 7,8

In the last decade, novel imaging techniques have been introduced and tested with the aim of improving staging accuracy: spiral computed tomographic (CT) scan,9,10 multidetector CT angiography,11 endoscopic ultrasonography (EUS),10–12 magnetic resonance cholangiopancreatography,13 positron emission tomography,13–15 and laparoscopic ultrasonography (US).16 However, several questions remain unsolved. Most analyses addressing the role of imaging techniques in predicting tumor resectability have been based on the comparison of different diagnostic modalities, but with no evaluation of the possibility of integrating data from the different techniques. 9,10,12

Furthermore, the role of laparoscopy remains uncertain. Some authors affirm the utility of this technique, considering that it could identify liver, peritoneal, or omental implants in 22% to 48% of patients who have no other evidence of disseminated disease on CT.17 However, on the basis of the observation that the main reason for unresectability is infiltration into the mesenteric axis, which could not be identified laparoscopically, other authors have stated that US and CT are the only diagnostic imaging techniques sufficient for staging pancreatic carcinoma in >95% of patients.18 Moreover, there are few indications about subgroups of patients for whom laparoscopy may be beneficial.2

More generally, the role of surgical exploration as a first treatment modality is debatable, and several studies have confirmed the possibility of downstaging pancreatic carcinoma with preoperative concurrent chemoradiation and of improving tumor resectability and patient outcome.3–6 These studies suggest that further data are necessary to identify patients for whom surgical exploration may be useful and patients for whom different treatment strategies should be tested.

The aim of this study was to evaluate the accuracy of combined standard imaging techniques in predicting the pathologic stage and to evaluate the prognostic effect of clinical staging to identify patients groups in which laparoscopy and laparotomy may be beneficial.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients treated at the radiotherapy departments of our institutions were included in this analysis when they were staged both before surgery and surgically and when they had no metastasis at clinical evaluation. All patients were followed up by the same team of radiologists (M.G.B., G.S., and L.N.), radiation oncologists (A.G.M., V.V., G.M., G.C.M., F.D., and N.C.), and surgeons (G.C., S.A., M.M., and G.B.D.) before, during, and after therapy (follow-up). All patients received surgical exploration followed by curative resection, when feasible, with or without intraoperative radiotherapy, postoperative external beam irradiation, or both. Patients with unresectable tumor received interstitial brachytherapy with implantation in the tumor volume of iodine-125 seeds or postoperative 5-fluorouracil (5-FU)–based chemoradiation. Patients with abdominal metastases detected during surgery or in whom radiotherapy could not be performed received palliative 5-FU–based chemotherapy.

The techniques used for clinical staging were endoscopic retrograde cholangiopancreatography (ERCP), abdominal CT scan, and US. These have been previously described in detail.19 Generally, the same operator (M.G.B.) performed both US and CT examinations in close cooperation with the endoscopist performing ERCP (G.C.). The techniques used for interstitial brachytherapy, intraoperative radiotherapy, postoperative radiotherapy, and concurrent chemoradiation have been previously described.20–22 All patients were staged according to the American Joint Committee on Cancer staging system.23 Survival curves were calculated with the Kaplan-Meier method,24 and differences between curves were analyzed with the log-rank test.25 Multivariate analysis of the prognostic effect of different variables was performed with the Cox proportional hazard method.26


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Fifty-four patients underwent laparotomy and were assessable for this analysis (Table 1Go). The median value of the maximum tumor diameter was 30 mm. Six patients presented with liver metastases at exploration and received palliative 5-FU–based chemotherapy. Seventeen patients had unresectable tumor because of vascular involvement and received interstitial brachytherapy with iodine-125 seed implantation (eight patients) during the same surgical procedure or received postoperative external beam radiotherapy (seven patients; total dose, 40–60 Gy; 1.8 Gy per fraction) with concurrently infused 5-FU (1000 mg/m2/day; continuous intravenous infusion, days 1–4 of radiotherapy) or palliative 5-FU chemotherapy (two patients). The remaining 31 patients received curative tumor resection plus intraoperative radiotherapy (5 patients; 10 Gy with 6-MeV energy electrons), postoperative external beam radiotherapy (1 patient; 50 Gy; 1.8 Gy per fraction), or both (25 patients).


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  		TABLE 1. Patient (n = 54) and treatment characteristics
 
At last observation, 8 patients (14.8%) were alive, and 46 patients (85.2%) had died of disease. The overall median and 5-year survival were 11.2months and 8.7%, respectively (Fig. 1Go).



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  		FIG 1. Overall actuarial survival.

 
Diagnostic Accuracy
Clinical versus pT classification, N-classification, and stage classification are shown in Tables 2Go, 3Go, and 4Go, respectively. Four patients were not assessable for pT classification because of early detection of liver metastasis during surgery. Similarly, 10 patients were not assessable for pN classification because of early detection of metastasis or tumor unresectability during surgical exploration. A highly significant correlation was observed between clinical and pT stage in terms of vascular involvement (T1–3 vs. T4, P < .0001). In the prediction of T-classification (pT1–3 vs. pT4 tumors), the sensitivity, specificity, positive predictive value, and negative predictive value of clinical staging were 73.9%, 96.3%, 94.4%, and 81.2%, respectively. The results were similar between smaller tumors (≤30 mm) and larger tumors (>30 mm), except for the negative predictive value (≤30 mm, 90.5%; >30 mm, 63.6%).


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  		TABLE 2. Clinical versus pathologic T staging
 

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  		TABLE 3. Clinical versus pathologic N staging
 

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  		TABLE 4. Clinical versus pathologic staging
 
A highly significant correlation was also observed between clinical and pN stage (N0 vs. N1, P < .0001). In the prediction of N-classification (pN0 vs. pN1), the sensitivity, specificity, positive predictive value, and negative predictive value of clinical staging were 63.6%, 95.4%, 93.3%, and 72.4%, respectively. By comparing the clinical and pathologic stage, 18 (33.3%) of 54 patients showed a higher than expected pathologic stage, and 2(3.7 %) of 54 showed a lower than expected pathologic stage.

Of the 35 of 54 patients who had potentially resectable disease at clinical staging (cT1–3NxM0), 5 patients had pT4 tumor, and 4 patients had pM1 tumor. Twenty-six (74.3%) of 35 patients received curative resection. The correlation between surgical resection and sex, age (≤65 vs. >65 years), cT classification (cT1–3 vs. cT4), cN classification (cN0 vs. cN1), clinical stage (I vs. II vs. III vs. IVA), and tumor diameter (≤30 vs. >30 mm) was evaluated. Only cT classification (P = .0243) and tumor diameter (P = .0132) were significantly correlated with tumor resectability.

By evaluating the distribution of unexpected abdominal metastasis on the basis of maximum tumor diameter (≤30 vs. >30 mm), as measured by imaging, a significant correlation was observed (P = .009; Table 5Go). Particularly, all pM1 tumors were recorded in the group of patients with tumor >30 mm.


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  		TABLE 5. Tumor diameter versus incidence of liver metastasis at laparotomy
 
Prognostic Effect
On univariate analysis, no significant differences in terms of survival were observed according to age (≤65 years [27 patients] vs. >65 years [27 patients]) or cN classification (N0 [34 patients] vs. N1 [20 patients]). Female patients showed significantly higher survival rates (male [30 patients] vs. female [24 patients]: median survival, 9.7 and 19.3 months, respectively; 5-year survival, 3.5% and 15.6%, respectively; P = .0107). A significant effect of cT classification was observed by categorizing patients as cT1–3 (35 patients) and cT4 (19 patients) (median survival, 16.0 and 6.5 months, respectively; 1-year survival, 58.2% and 13.1%, respectively; P = .0067; Fig. 2Go). Pathologic T-, N-, and M-classifications showed a significant effect on survival (P = .0007, P = .0395, and P = .0311, respectively). Both clinical and pathologic stage were significantly correlated with survival (P = .0135 and P = .0001, respectively). Maximum tumor diameter, as evaluated by imaging, significantly affected survival (≤30 mm [27 patients] vs. >30 mm [27 patients]: median survival, 17.2and 8.0 months, respectively; 5-year survival, 15.5% and .0%, respectively; P = .0037; Fig. 3Go). The effect of tumor diameter was also evaluated within the groups of cT3 (30 patients) and cT4 (18 patients) tumors. A significant correlation with survival was observed only in cT3 patients (≤30 vs. >30 mm: median survival, 25.1 and 8.0 months, respectively; 5- year survival, 16.7% and .0%, respectively; P = .0056). On the basis of the worst effect on survival in both cT4 patients and patients with tumor >30 mm, patients were further divided into two groups: group A, cT1–3 and tumor ≤30 mm; and group B, cT4 and/or tumor >30 mm. This prognostic classification showed a highly significant correlation with survival (group A [21 patients] vs. group B [33 patients]: median survival, 25.1 and 8.0 months, respectively; 5- year survival, 20.1% and .0%, respectively; P < .0001; Fig. 4Go). Finally, patients who received curative resection showed a significantly higher survival (tumor resection [31 patients] vs. no resection [23 patients]: median survival, 14.3 and 8.0 months, respectively; 5-year survival, 13.4% and .0%, respectively; P = .0278).



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  		FIG. 2. Effect of clinical tumor classification on survival (cT2–3 vs. cT4).

 


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  		FIG. 3. Effect of tumor diameter on survival (≤30 vs. >30 mm).

 


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  		FIG. 4. Effect of prognostic group on survival (group A vs. group B).

 
On multivariate analysis, all potential prognostic factors were evaluated (sex, age, tumor diameter, clinical T- and N-classifications, pT and pN classification, tumor resection, and prognostic group). The only parameter significantly correlated with survival was the prognostic group (group A vs. group B, P=.0007).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In our study, the data of 54 patients who underwent laparotomy and subsequent therapy based on pathologic stage were analyzed, and a comparison was performed between presurgical stage and surgical/pathologic stage. By using standard abdominal CT, US, and ERCP as diagnostic modalities, 6 of 54 patients showed undetected liver metastases at surgical exploration. Sensitivity and specificity for vascular involvement were 73.9% and 96.3%, respectively. Sensitivity and specificity for nodal involvement were 63.6% and 95.4%, respectively. One third of the patients (18 of 54; 33.3%) showed a higher than expected pathologic stage, and 2(3.7 %) of 54 showed a lower than expected pathologic stage by comparing clinical and pathologic evaluation. All patients with unexpected metastases had a maximum tumor diameter, as evaluated by imaging, of >30 mm. A highly significant correlation was observed between clinical T-classification and tumor diameter and patient survival. However, at multivariate analysis, these correlations were confirmed only by combining these two factors in a prognostic group. Particularly, patients with cT4 carcinoma, >30-mm tumor diameter, or both had a very unfavorable prognosis: no patient survived >21 months. Therefore, our analysis documented a reasonable diagnostic accuracy and a high prognostic effect of clinical staging in pancreatic carcinoma, despite the standard techniques used.

Recently, novel diagnostic modalities have been evaluated and compared with standard CT-based staging. Particularly, magnetic resonance imaging showed in some studies9,27 a higher diagnostic accuracy in evaluating vascular involvement and, thus, tumor resectability. Another promising technique is EUS. This technique, compared with helical CT scan, showed a higher sensitivity for vascular invasion in the analysis of Tierney et al.12 (100% vs. 62.5%, respectively). Other studies were addressed to evaluate the potential role of this technique as an integration with standard CT-based staging. Tomazic and Pegan28 studied 43 patients operated on for periampullary cancer. Before surgery, all patients were evaluated with US, CT scan, and EUS; the level of carbohydrate antigen 19-9 was assessed. Specificity in predicting tumor resectability was 70.8% on EUS, 45.8% on CT scan, and 12.5% on standard US. The authors observed that a combined use of different diagnostic methods has a higher positive predictive value, and the highest (65.1%) was found in the combination of EUS and carbohydrate antigen 19-9. Similarly, Midwinter et al.10 observed that the combined use of different imaging modalities (EUS and spiral CT) may improve diagnostic accuracy in patients with pancreatic and ampullary tumors. In their analysis, 48 patients with clinical suspicion of a pancreatic or ampullary tumor underwent both spiral CT and EUS; 34 patients had surgical exploration. The authors compared the results of imaging findings with those of operative findings. They observed that EUS demonstrated 33 and spiral CT 26 of the 34 primary lesions and that EUS was particularly useful in the assessment of small resectable tumors missed by spiral CT. Finally, it was observed that the sensitivity and specificity of EUS and spiral CT for detecting involvement by tumor of the superior mesenteric vein, portal vein, and lymph nodes were similar, but EUS was less effective at evaluating the superior mesenteric artery. The authors concluded that EUS is an important additional investigation after spiral CT in patients with a suspected pancreatic or ampullary tumor. Both these reports support our traditional diagnostic management of these neoplasms, based on the integration between different diagnostic modalities.

Another debated issue in patient selection is the role of laparoscopy. Several analyses have addressed the potential efficacy of this method of patient evaluation. 1,2 However, the role of laparoscopy in patients with pancreatic carcinoma is debated. Our data suggest that a simple and potentially effective way to select patients for laparoscopy could be by maximum tumor diameter at CT/US. In fact, no patient with a tumor diameter ≤30 mm showed abdominal metastasis, whereas 6 (22.2%) of 27 patients with tumor diameter >30 mm had liver metastases undetected at CT/US examination (P = .009).

In conclusion, integrated standard imaging studies achieved reasonable diagnostic accuracy in our analysis. Further studies are necessary to explore these results, particularly for N-stage, for which the sensitivity of current imaging techniques is poor.9 Use of selective laparoscopy should be tried, on the basis of the correlation of tumor stage and diameter with the rate of undetected abdominal metastases. Furthermore, newer procedures of patient stratification should be tested to integrate and improve the present possibility of patient selection by modern imaging techniques, such as tumor marker (carbohydrate antigen 19-9) determination and evaluation of genetic parameters (p53 and ras oncogene expression).29

In terms of prognostic effects, clinical staging showed a close correlation with patient survival. On the basis of these data, future clinical trials should use preoperative staging for patient stratification, thus avoiding the time and costs related to unnecessary "staging" laparotomy, in candidates for preoperative treatments.

Received for publication February 18, 2004. Accepted for publication October 28, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Jimenez RE, Warshaw AL, Rattner DW, Willett CG, McGrath D, Fernandez-del Castillo C. Impact of laparoscopic staging in the treatment of pancreatic cancer. Arch Surg 2000;135:409–14.[Abstract/Free Full Text]
  2. Saldinger PF, Reilly M, Reynolds K, et al. Is CT angiography sufficient for prediction of resectability of periampullary neoplasms? J Gastrointest Surg 2000;4:233–7.[CrossRef][Medline]
  3. Spitz FR, Abruzzese JL, Lee JE, et al. Preoperative and postoperative chemoradiation strategies in patients treated with pancreaticoduodenectomy for adenocarcinoma of the pancreas. J Clin Oncol 1997;15:928–37.[Abstract/Free Full Text]
  4. Wanebo HJ, Glicksmann AS, Vezeridis MP, et al. Preoperative chemotherapy, radiotherapy, and surgical resection of locally advanced pancreatic cancer. Arch Surg 2000;135:81–7.[Abstract/Free Full Text]
  5. Snady H, Bruckner H, Cooperman A, Paradiso J, Kiefer L. Survival advantage of combined chemoradiotherapy compared with resection as the initial treatment of patients with regional pancreatic carcinoma An outcomes trial. Cancer 2000;89:314–27.[CrossRef][Medline]
  6. Kamthan AG, Morris JC, Dalton J, et al. Combined modality therapy for stage II and stage III pancreatic carcinoma. J Clin Oncol 1997;15:2920–7.[Abstract]
  7. Delcore R, Rodriguez FJ, Forster J, Hermreck AS, Thomas JH. Significance of lymph node metastases in patients with pancreatic cancer undergoing curative resection. Am J Surg 1996;172:463–8.[CrossRef][Medline]
  8. Tannapfel A, Wittekind C, Hunefeld G. Ductal adenocarcinoma of the pancreas. Histopathological features and prognosis. Int J Pancreatol 1992;12:145–52.[Medline]
  9. Gorelick AB, Scheiman JM, Fendrick AM. Identification of patients with resectable pancreatic cancer: at what stage are we? Am J Gastroenterol 1998;93:1995–6.[Medline]
  10. Midwinter MJ, Beveridge CJ, Wilsdon JB, Bennett MK, Baudouin CJ, Charnley RM. Correlation between spiral computed tomography, endoscopic ultrasonography and findings at operation in pancreatic and ampullary tumours. Br J Surg 1999;86:189–93.[CrossRef][Medline]
  11. Fishman EK, Horton KM, Urban BA. Multidetector CT angiography in the evaluation of pancreatic carcinoma: preliminary observations. J Comput Assist Tomogr 2000;24:849–53.[CrossRef][Medline]
  12. Tierney WM, Francis IR, Eckhauser F, Elta G, Nostrant TT, Scheiman JM. The accuracy of EUS and helical CT in the assessment of vascular invasion by periampullary malignancy. Gastrointest Endosc 2001;53:182–8.[CrossRef][Medline]
  13. Freeny PC. Pancreatic carcinoma: imaging update 2001. Dig Dis 2001;19:37–46.[CrossRef][Medline]
  14. Mertz HR, Sechopoulos P, Delbeke D, Leach SD. EUS, PET, and CT scanning for evaluation of pancreatic adenocarcinoma. Gastrointest Endosc 2000;52:367–71.[CrossRef][Medline]
  15. Diederichs CG, Staib L, Vogel J, et al. Values and limitations of 18F-fluorodeoxyglucose-positron-emission tomography with preoperative evaluation of patients with pancreatic masses. Pancreas 2000;20:109–16.[Medline]
  16. Minnard EA, Conlon KC, Hoos A, Dougherty EC, Hann LE, Brennan MF. Laparoscopic ultrasound enhances standard laparoscopy in the staging of pancreatic cancer. Ann Surg 1998;228:182–7.[CrossRef][Medline]
  17. Fernandez-del Castillo CL, Warshaw AL Pancreatic cancer. Laparoscopic staging and peritoneal cytology. Surg Oncol Clin North Am 1998;7:135–42.[Medline]
  18. Bottger TC, Boddin J, Duber C, Heintz A, Kuchle R, Junginger T. Diagnosing and staging of pancreatic carcinoma—what is necessary? Oncology 1998;55:122–9.[CrossRef][Medline]
  19. Marano P, Brizi MG, Cellini N, et al. Diagnostic and therapeutic integration in ductal carcinoma of the head of the pancreas. Preliminary note. Radiol Med 1993;85:615–24.
  20. Montemaggi P, Dobelbower R Jr, Crucitti F, et al. Interstitial brachytherapy for pancreatic cancer: report of seven cases treated with 125-I and a review of the literature. Int J Radiat Oncol Biol Phys 1991;21:451–7.[Medline]
  21. Crucitti F, Doglietto GB, Frontera D, et al. Integrated radiosurgical treatment of resectable pancreatic head carcinoma. Pancreas 1998;16:31–9.[Medline]
  22. Morganti AG, Valentini V, Macchia G, et al. 5-FU-based chemoradiation in unresectable pancreatic carcinoma: a phase II dose escalation study. Int J Radiat Oncol Biol Phys 2004;54:1454–60.[CrossRef]
  23. Exocrine pancreas. In: American Joint Committee on Cancer: AJCC Cancer Staging Manual. 5th ed. Lippincott-Raven, Philadelphia, 1997; pp 121–6.
  24. Kaplan FL, Meier P. In: Nonparametric estimation from incomplete observations. Am J Stat Assoc 1958;53:457–81.[CrossRef]
  25. Peto R, Peto J. Asymptotically efficient rank invariant procedures. J R Stat Soc 1972;135:185–207.
  26. Cox DR. Regression model and life tables. J R Stat Soc B 1972;34:187–220.
  27. Sheridan MB, Ward J, Guthrie JA, et al. Dynamic contrast-enhanced MR imaging and dual-phase helical CT in the preoperative assessment of suspected pancreatic cancer: a comparison study with receiver operating characteristics analysis. AJR Am J Roentgenol 1999;173:583–9.[Abstract/Free Full Text]
  28. Tomazic A, Pegan V. Preoperative staging of periampullar cancer with US, CT, EUS and Ca19-9. Hepatogastroenterology 2000;47:1135–7.[Medline]
  29. Riker A, Libutti SK, Bartlett DL. Advances in the early detection, diagnosis, and staging of pancreatic cancer. Surg Oncol 1997;6:157–69.[CrossRef][Medline]



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