Skip to main content
Top
Published in: Annals of Surgical Oncology 7/2012

01-07-2012 | Endocrine Tumors

Pancreatic Neuroendocrine Tumors: Radiographic Calcifications Correlate with Grade and Metastasis

Authors: George A. Poultsides, MD, MSc, Lyen C. Huang, MD, MPH, Yijun Chen, MD, Brendan C. Visser, MD, Reetesh K. Pai, MD, R. Brooke Jeffrey, MD, Walter G. Park, MD, MSc, Ann M. Chen, MD, Pamela L. Kunz, MD, George A. Fisher, MD, PhD, Jeffrey A. Norton, MD

Published in: Annals of Surgical Oncology | Issue 7/2012

Login to get access

Abstract

Background

Studies to identify preoperative prognostic variables for pancreatic neuroendocrine tumor (PNET) have been inconclusive. Specifically, the prevalence and prognostic significance of radiographic calcifications in these tumors remains unclear.

Methods

From 1998 to 2009, a total of 110 patients with well-differentiated PNET underwent surgical resection at our institution. Synchronous liver metastases present in 31 patients (28%) were addressed surgically with curative intent. Patients with high-grade PNET were excluded. The presence of calcifications in the primary tumor on preoperative computed tomography was recorded and correlated with clinicopathologic variables and overall survival.

Results

Calcifications were present in 16% of patients and were more common in gastrinomas and glucagonomas (50%), but never encountered in insulinomas. Calcified tumors were larger (median size 4.5 vs. 2.3 cm, P = 0.04) and more commonly associated with lymph node metastasis (75 vs. 35%, P = 0.01), synchronous liver metastasis (62 vs. 21%, P < 0.01), and intermediate tumor grade (80 vs. 31%, P < 0.01). On multivariate analysis of factors available preoperatively, calcifications (P = 0.01) and size (P < 0.01) remained independent predictors of lymph node metastasis. Overall survival after resection was significantly worse in the presence of synchronous liver metastasis (5-year, 64 vs. 86%, P = 0.04), but not in the presence of radiographic calcifications.

Conclusions

Calcifications on preoperative computed tomography correlate with intermediate grade and lymph node metastasis in well-differentiated PNET. This information is available preoperatively and supports the routine dissection of regional lymph nodes through formal pancreatectomy rather than enucleation in calcified PNET.
Literature
1.
go back to reference Klimstra DS, Modlin IR, Coppola D, et al. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas. 2010;39:707–12.PubMedCrossRef Klimstra DS, Modlin IR, Coppola D, et al. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas. 2010;39:707–12.PubMedCrossRef
2.
go back to reference Fitzgerald TL, Hickner ZJ, Schmitz M, et al. Changing incidence of pancreatic neoplasms: a 16-year review of statewide tumor registry. Pancreas. 2008;37:134–8.PubMedCrossRef Fitzgerald TL, Hickner ZJ, Schmitz M, et al. Changing incidence of pancreatic neoplasms: a 16-year review of statewide tumor registry. Pancreas. 2008;37:134–8.PubMedCrossRef
3.
go back to reference Buchanan KD, Johnston CF, O’Hare MM, et al. Neuroendocrine tumors. A European view. Am J Med. 1986;81:14–22.PubMedCrossRef Buchanan KD, Johnston CF, O’Hare MM, et al. Neuroendocrine tumors. A European view. Am J Med. 1986;81:14–22.PubMedCrossRef
4.
go back to reference Eriksson B, Oberg K, Skogseid B. Neuroendocrine pancreatic tumors. Clinical findings in a prospective study of 84 patients. Acta Oncol. 1989;28:373–7.PubMedCrossRef Eriksson B, Oberg K, Skogseid B. Neuroendocrine pancreatic tumors. Clinical findings in a prospective study of 84 patients. Acta Oncol. 1989;28:373–7.PubMedCrossRef
5.
go back to reference Halfdanarson TR, McWilliams RR, Donohue JH, et al. A single-institution experience with 491 cases of small bowel adenocarcinoma. Am J Surg. 2010;199:797–803.PubMedCrossRef Halfdanarson TR, McWilliams RR, Donohue JH, et al. A single-institution experience with 491 cases of small bowel adenocarcinoma. Am J Surg. 2010;199:797–803.PubMedCrossRef
6.
go back to reference Halfdanarson TR, Rabe KG, Rubin J, et al. Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol. 2008;19:1727–33.PubMedCrossRef Halfdanarson TR, Rabe KG, Rubin J, et al. Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol. 2008;19:1727–33.PubMedCrossRef
7.
go back to reference Lepage C, Bouvier AM, Phelip JM, et al. Incidence and management of malignant digestive endocrine tumours in a well defined French population. Gut. 2004;53:549–53.PubMedCrossRef Lepage C, Bouvier AM, Phelip JM, et al. Incidence and management of malignant digestive endocrine tumours in a well defined French population. Gut. 2004;53:549–53.PubMedCrossRef
8.
go back to reference Yao JC, Hassan M, Phan A, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–72.PubMedCrossRef Yao JC, Hassan M, Phan A, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–72.PubMedCrossRef
9.
10.
go back to reference Norton JA, Warren RS, Kelly MG, et al. Aggressive surgery for metastatic liver neuroendocrine tumors. Surgery. 2003;134:1057–63.PubMedCrossRef Norton JA, Warren RS, Kelly MG, et al. Aggressive surgery for metastatic liver neuroendocrine tumors. Surgery. 2003;134:1057–63.PubMedCrossRef
11.
go back to reference Norton JA. Surgery for primary pancreatic neuroendocrine tumors. J Gastrointest Surg. 2006;10:327–31.PubMedCrossRef Norton JA. Surgery for primary pancreatic neuroendocrine tumors. J Gastrointest Surg. 2006;10:327–31.PubMedCrossRef
12.
go back to reference Schurr PG, Strate T, Rese K, et al. Aggressive surgery improves long-term survival in neuroendocrine pancreatic tumors: an institutional experience. Ann Surg. 2007;245:273–81.PubMedCrossRef Schurr PG, Strate T, Rese K, et al. Aggressive surgery improves long-term survival in neuroendocrine pancreatic tumors: an institutional experience. Ann Surg. 2007;245:273–81.PubMedCrossRef
13.
go back to reference Akerström G, Hellman P. Surgery on neuroendocrine tumours. Best Pract Res Clin Endocrinol Metab. 2007;21:87–109.PubMedCrossRef Akerström G, Hellman P. Surgery on neuroendocrine tumours. Best Pract Res Clin Endocrinol Metab. 2007;21:87–109.PubMedCrossRef
14.
go back to reference Pitt SC, Pitt HA, Baker MS, et al. Small pancreatic and periampullary neuroendocrine tumors: resect or enucleate? J Gastrointest Surg. 2009;13:1692–8.PubMedCrossRef Pitt SC, Pitt HA, Baker MS, et al. Small pancreatic and periampullary neuroendocrine tumors: resect or enucleate? J Gastrointest Surg. 2009;13:1692–8.PubMedCrossRef
15.
go back to reference Ballian N, Loeffler AG, Rajamanickam V, et al. A simplified prognostic system for resected pancreatic neuroendocrine neoplasms. HPB. 2009;11:422–8.PubMedCrossRef Ballian N, Loeffler AG, Rajamanickam V, et al. A simplified prognostic system for resected pancreatic neuroendocrine neoplasms. HPB. 2009;11:422–8.PubMedCrossRef
16.
go back to reference Bilimoria KY, Tomlinson JS, Merkow RP, et al. Clinicopathologic features and treatment trends of pancreatic neuroendocrine tumors: analysis of 9,821 patients. J Gastrointest Surg. 2007;11:1460–9.PubMedCrossRef Bilimoria KY, Tomlinson JS, Merkow RP, et al. Clinicopathologic features and treatment trends of pancreatic neuroendocrine tumors: analysis of 9,821 patients. J Gastrointest Surg. 2007;11:1460–9.PubMedCrossRef
17.
go back to reference Bloomston M, Muscarella P, Shah MH, et al. Cytoreduction results in high perioperative mortality and decreased survival in patients undergoing pancreatectomy for neuroendocrine tumors of the pancreas. J Gastrointest Surg. 2006;10:1361–70.PubMedCrossRef Bloomston M, Muscarella P, Shah MH, et al. Cytoreduction results in high perioperative mortality and decreased survival in patients undergoing pancreatectomy for neuroendocrine tumors of the pancreas. J Gastrointest Surg. 2006;10:1361–70.PubMedCrossRef
18.
go back to reference Ekeblad S, Skogseid B, Dunder K, et al. Prognostic factors and survival in 324 patients with pancreatic endocrine tumor treated at a single institution. Clin Cancer Res. 2008;14:7798–803.PubMedCrossRef Ekeblad S, Skogseid B, Dunder K, et al. Prognostic factors and survival in 324 patients with pancreatic endocrine tumor treated at a single institution. Clin Cancer Res. 2008;14:7798–803.PubMedCrossRef
19.
go back to reference Ferrone CR, Tang LH, Tomlinson J, et al. Determining prognosis in patients with pancreatic endocrine neoplasms: can the WHO classification system be simplified? J Clin Oncol. 2007;25:5609–15.PubMedCrossRef Ferrone CR, Tang LH, Tomlinson J, et al. Determining prognosis in patients with pancreatic endocrine neoplasms: can the WHO classification system be simplified? J Clin Oncol. 2007;25:5609–15.PubMedCrossRef
20.
go back to reference Fischer L, Kleeff J, Esposito I, et al. Clinical outcome and long-term survival in 118 consecutive patients with neuroendocrine tumours of the pancreas. Br J Surg. 2008;95:627–35.PubMedCrossRef Fischer L, Kleeff J, Esposito I, et al. Clinical outcome and long-term survival in 118 consecutive patients with neuroendocrine tumours of the pancreas. Br J Surg. 2008;95:627–35.PubMedCrossRef
21.
go back to reference Franko J, Feng W, Yip L, et al. Non-functional neuroendocrine carcinoma of the pancreas: incidence, tumor biology, and outcomes in 2,158 patients. J Gastrointest Surg. 2010;14:541–8.PubMedCrossRef Franko J, Feng W, Yip L, et al. Non-functional neuroendocrine carcinoma of the pancreas: incidence, tumor biology, and outcomes in 2,158 patients. J Gastrointest Surg. 2010;14:541–8.PubMedCrossRef
22.
go back to reference Hochwald SN, Zee S, Conlon KC, et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol. 2002;20:2633–42.PubMedCrossRef Hochwald SN, Zee S, Conlon KC, et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol. 2002;20:2633–42.PubMedCrossRef
23.
go back to reference Ito H, Abramson M, Ito K, et al. Surgery and staging of pancreatic neuroendocrine tumors: a 14-year experience. J Gastrointest Surg. 2010;14:891–8.PubMedCrossRef Ito H, Abramson M, Ito K, et al. Surgery and staging of pancreatic neuroendocrine tumors: a 14-year experience. J Gastrointest Surg. 2010;14:891–8.PubMedCrossRef
24.
go back to reference Martin RCG, Kooby DA, Weber SM, et al. Analysis of 6,747 pancreatic neuroendocrine tumors for a proposed staging system. J Gastrointest Surg. 2011;15:175–83.PubMedCrossRef Martin RCG, Kooby DA, Weber SM, et al. Analysis of 6,747 pancreatic neuroendocrine tumors for a proposed staging system. J Gastrointest Surg. 2011;15:175–83.PubMedCrossRef
25.
go back to reference Bilimoria KY, Talamonti MS, Tomlinson JS, et al. Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors. Ann Surg. 2008;247:490–500.PubMedCrossRef Bilimoria KY, Talamonti MS, Tomlinson JS, et al. Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors. Ann Surg. 2008;247:490–500.PubMedCrossRef
26.
go back to reference Gullo L, Migliori M, Falconi M, et al. Nonfunctioning pancreatic endocrine tumors: a multicenter clinical study. Am J Gastroenterol. 2003;98:2435–9.PubMedCrossRef Gullo L, Migliori M, Falconi M, et al. Nonfunctioning pancreatic endocrine tumors: a multicenter clinical study. Am J Gastroenterol. 2003;98:2435–9.PubMedCrossRef
27.
go back to reference Phan GQ, Yeo CJ, Hruban RH, et al. Surgical experience with pancreatic and peripancreatic neuroendocrine tumors: review of 125 patients. J Gastrointest Surg. 1998;2:473–82.PubMedCrossRef Phan GQ, Yeo CJ, Hruban RH, et al. Surgical experience with pancreatic and peripancreatic neuroendocrine tumors: review of 125 patients. J Gastrointest Surg. 1998;2:473–82.PubMedCrossRef
28.
go back to reference Tomassetti P, Campana D, Piscitelli L, et al. Endocrine pancreatic tumors: factors correlated with survival. Ann Oncol. 2005;16:1806–10.PubMedCrossRef Tomassetti P, Campana D, Piscitelli L, et al. Endocrine pancreatic tumors: factors correlated with survival. Ann Oncol. 2005;16:1806–10.PubMedCrossRef
29.
go back to reference Imhof H, Frank P. Pancreatic calcifications in malignant islet cell tumors. Radiology. 1977;122:333–7.PubMed Imhof H, Frank P. Pancreatic calcifications in malignant islet cell tumors. Radiology. 1977;122:333–7.PubMed
30.
go back to reference Rodallec M, Vilgrain V, Couvelard A, et al. Endocrine pancreatic tumours and helical CT: contrast enhancement is correlated with microvascular density, histoprognostic factors and survival. Pancreatology. 2006;6:77–85.PubMedCrossRef Rodallec M, Vilgrain V, Couvelard A, et al. Endocrine pancreatic tumours and helical CT: contrast enhancement is correlated with microvascular density, histoprognostic factors and survival. Pancreatology. 2006;6:77–85.PubMedCrossRef
31.
go back to reference Norton JA. Intraoperative methods to stage and localize pancreatic and duodenal tumors. Ann Oncol. 1999;10(Suppl 4):182–4.PubMedCrossRef Norton JA. Intraoperative methods to stage and localize pancreatic and duodenal tumors. Ann Oncol. 1999;10(Suppl 4):182–4.PubMedCrossRef
32.
go back to reference Norton JA, Alexander HR, Fraker DL, et al. Does the use of routine duodenotomy (DUODX) affect rate of cure, development of liver metastases, or survival in patients with Zollinger-Ellison syndrome? Ann Surg. 2004;239:617–25.PubMedCrossRef Norton JA, Alexander HR, Fraker DL, et al. Does the use of routine duodenotomy (DUODX) affect rate of cure, development of liver metastases, or survival in patients with Zollinger-Ellison syndrome? Ann Surg. 2004;239:617–25.PubMedCrossRef
33.
go back to reference Norton JA, Doppman JL, Jensen RT. Curative resection in Zollinger-Ellison syndrome. Results of a 10-year prospective study. Ann Surg. 1992;215:8–18.PubMedCrossRef Norton JA, Doppman JL, Jensen RT. Curative resection in Zollinger-Ellison syndrome. Results of a 10-year prospective study. Ann Surg. 1992;215:8–18.PubMedCrossRef
34.
go back to reference Norton JA, Fraker DL, Alexander HR, et al. Surgery to cure the Zollinger-Ellison syndrome. N Engl J Med. 1999;341:635–44.PubMedCrossRef Norton JA, Fraker DL, Alexander HR, et al. Surgery to cure the Zollinger-Ellison syndrome. N Engl J Med. 1999;341:635–44.PubMedCrossRef
35.
go back to reference Sugg SL, Norton JA, Fraker DL, et al. A prospective study of intraoperative methods to diagnose and resect duodenal gastrinomas. Ann Surg. 1993;218:138–44.PubMedCrossRef Sugg SL, Norton JA, Fraker DL, et al. A prospective study of intraoperative methods to diagnose and resect duodenal gastrinomas. Ann Surg. 1993;218:138–44.PubMedCrossRef
36.
go back to reference Arnold WS, Fraker DL, Alexander HR, et al. Apparent lymph node primary gastrinoma. Surgery. 1994;116:1123–9.PubMed Arnold WS, Fraker DL, Alexander HR, et al. Apparent lymph node primary gastrinoma. Surgery. 1994;116:1123–9.PubMed
37.
go back to reference Norton JA, Alexander HR, Fraker DL, et al. Possible primary lymph node gastrinoma: occurrence, natural history, and predictive factors: a prospective study. Ann Surg. 2003;237:650–7.PubMed Norton JA, Alexander HR, Fraker DL, et al. Possible primary lymph node gastrinoma: occurrence, natural history, and predictive factors: a prospective study. Ann Surg. 2003;237:650–7.PubMed
38.
go back to reference Norton JA, Doherty GM, Fraker DL, et al. Surgical treatment of localized gastrinoma within the liver: a prospective study. Surgery. 1998;124:1145–52.PubMedCrossRef Norton JA, Doherty GM, Fraker DL, et al. Surgical treatment of localized gastrinoma within the liver: a prospective study. Surgery. 1998;124:1145–52.PubMedCrossRef
39.
go back to reference Norton JA, Kivlen M, Li M, et al. Morbidity and mortality of aggressive resection in patients with advanced neuroendocrine tumors. Arch Surg. 2003;138:859–66.PubMedCrossRef Norton JA, Kivlen M, Li M, et al. Morbidity and mortality of aggressive resection in patients with advanced neuroendocrine tumors. Arch Surg. 2003;138:859–66.PubMedCrossRef
40.
go back to reference Rindi G, Klöppel G, Alhman H, et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Archiv. 2006;449:395–401.PubMedCrossRef Rindi G, Klöppel G, Alhman H, et al. TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Archiv. 2006;449:395–401.PubMedCrossRef
41.
go back to reference Hiramoto JS, Feldstein VA, LaBerge JM, et al. Intraoperative ultrasound and preoperative localization detects all occult insulinomas. Arch Surg. 2001;136:1020–5.PubMedCrossRef Hiramoto JS, Feldstein VA, LaBerge JM, et al. Intraoperative ultrasound and preoperative localization detects all occult insulinomas. Arch Surg. 2001;136:1020–5.PubMedCrossRef
42.
go back to reference Fishbeyn VA, Norton JA, Benya RV, et al. Assessment and prediction of long-term cure in patients with the Zollinger-Ellison syndrome: the best approach. Ann Intern Med. 1993;119:199–206.PubMed Fishbeyn VA, Norton JA, Benya RV, et al. Assessment and prediction of long-term cure in patients with the Zollinger-Ellison syndrome: the best approach. Ann Intern Med. 1993;119:199–206.PubMed
43.
go back to reference Roy PK, Venzon DJ, Feigenbaum KM, et al. Gastric secretion in Zollinger-Ellison syndrome. Correlation with clinical expression, tumor extent and role in diagnosis—a prospective NIH study of 235 patients and a review of 984 cases in the literature. Medicine (Baltimore). 2001;80:189–222. Roy PK, Venzon DJ, Feigenbaum KM, et al. Gastric secretion in Zollinger-Ellison syndrome. Correlation with clinical expression, tumor extent and role in diagnosis—a prospective NIH study of 235 patients and a review of 984 cases in the literature. Medicine (Baltimore). 2001;80:189–222.
44.
go back to reference Roy PK, Venzon DJ, Shojamanesh H, et al. Zollinger-Ellison syndrome. Clinical presentation in 261 patients. Medicine (Baltimore). 2000;79:379–411. Roy PK, Venzon DJ, Shojamanesh H, et al. Zollinger-Ellison syndrome. Clinical presentation in 261 patients. Medicine (Baltimore). 2000;79:379–411.
45.
go back to reference Norton JA, Kahn CR, Schiebinger R, et al. Amino acid deficiency and the skin rash associated with glucagonoma. Ann Intern Med. 1979;91:213–5.PubMed Norton JA, Kahn CR, Schiebinger R, et al. Amino acid deficiency and the skin rash associated with glucagonoma. Ann Intern Med. 1979;91:213–5.PubMed
46.
go back to reference Alexiev BA, Darwin PE, Goloubeva O, et al. Proliferative rate in endoscopic ultrasound fine-needle aspiration of pancreatic endocrine tumors: correlation with clinical behavior. Cancer. 2009;117:40–5.PubMed Alexiev BA, Darwin PE, Goloubeva O, et al. Proliferative rate in endoscopic ultrasound fine-needle aspiration of pancreatic endocrine tumors: correlation with clinical behavior. Cancer. 2009;117:40–5.PubMed
47.
go back to reference Jarufe NP, Coldham C, Orug T, et al. Neuroendocrine tumours of the pancreas: predictors of survival after surgical treatment. Dig Surg. 2005;22:157–62.PubMedCrossRef Jarufe NP, Coldham C, Orug T, et al. Neuroendocrine tumours of the pancreas: predictors of survival after surgical treatment. Dig Surg. 2005;22:157–62.PubMedCrossRef
48.
go back to reference Kazanjian KK, Reber HA, Hines OJ. Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg. 2006;141:765–9.PubMedCrossRef Kazanjian KK, Reber HA, Hines OJ. Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg. 2006;141:765–9.PubMedCrossRef
49.
go back to reference Sarmiento JM, Farnell MB, Que FG, et al. Pancreaticoduodenectomy for islet cell tumors of the head of the pancreas: long-term survival analysis. World J Surg. 2002;26:1267–71.PubMedCrossRef Sarmiento JM, Farnell MB, Que FG, et al. Pancreaticoduodenectomy for islet cell tumors of the head of the pancreas: long-term survival analysis. World J Surg. 2002;26:1267–71.PubMedCrossRef
50.
go back to reference Vagefi PA, Razo O, Deshpande V, et al. Evolving patterns in the detection and outcomes of pancreatic neuroendocrine neoplasms: the Massachusetts General Hospital experience from 1977 to 2005. Arch Surg. 2007;142:347–54.PubMedCrossRef Vagefi PA, Razo O, Deshpande V, et al. Evolving patterns in the detection and outcomes of pancreatic neuroendocrine neoplasms: the Massachusetts General Hospital experience from 1977 to 2005. Arch Surg. 2007;142:347–54.PubMedCrossRef
51.
go back to reference Chu QD, Hill HC, Douglass HO, et al. Predictive factors associated with long-term survival in patients with neuroendocrine tumors of the pancreas. Ann Surg Oncol. 2002;9:855–62.PubMedCrossRef Chu QD, Hill HC, Douglass HO, et al. Predictive factors associated with long-term survival in patients with neuroendocrine tumors of the pancreas. Ann Surg Oncol. 2002;9:855–62.PubMedCrossRef
52.
go back to reference Panzuto F, Nasoni S, Falconi M, et al. Prognostic factors and survival in endocrine tumor patients: comparison between gastrointestinal and pancreatic localization. Endocr Relat Cancer. 2005;12:1083–92.PubMedCrossRef Panzuto F, Nasoni S, Falconi M, et al. Prognostic factors and survival in endocrine tumor patients: comparison between gastrointestinal and pancreatic localization. Endocr Relat Cancer. 2005;12:1083–92.PubMedCrossRef
53.
go back to reference Solorzano CC, Lee JE, Pisters PW, et al. Nonfunctioning islet cell carcinoma of the pancreas: survival results in a contemporary series of 163 patients. Surgery. 2001;130:1078–85.PubMedCrossRef Solorzano CC, Lee JE, Pisters PW, et al. Nonfunctioning islet cell carcinoma of the pancreas: survival results in a contemporary series of 163 patients. Surgery. 2001;130:1078–85.PubMedCrossRef
54.
go back to reference Edge SB, Byrd DR, Compton CC, Fritz AG, Green FL, Trotti A. American Joint Committee on Cancer (AJCC) staging manual. 7th ed. New York: Springer-Verlag, 2010. Edge SB, Byrd DR, Compton CC, Fritz AG, Green FL, Trotti A. American Joint Committee on Cancer (AJCC) staging manual. 7th ed. New York: Springer-Verlag, 2010.
55.
go back to reference Bosman F, Carneiro F, Hruban R, et al. WHO classification of tumours of the digestive system. Lyon, France: IARC Press, 2010. Bosman F, Carneiro F, Hruban R, et al. WHO classification of tumours of the digestive system. Lyon, France: IARC Press, 2010.
56.
go back to reference Keiser HR, Beaven MA, Doppman J, et al. Sipple’s syndrome: medullary thyroid carcinoma, pheochromocytoma, and parathyroid disease. Studies in a large family. NIH conference. Ann Intern Med. 1973;78:561–79.PubMed Keiser HR, Beaven MA, Doppman J, et al. Sipple’s syndrome: medullary thyroid carcinoma, pheochromocytoma, and parathyroid disease. Studies in a large family. NIH conference. Ann Intern Med. 1973;78:561–79.PubMed
57.
go back to reference Lee S, Shin JH, Han BK, et al. Medullary thyroid carcinoma: comparison with papillary thyroid carcinoma and application of current sonographic criteria. Am J Roentgenol. 2010;194:1090–4.CrossRef Lee S, Shin JH, Han BK, et al. Medullary thyroid carcinoma: comparison with papillary thyroid carcinoma and application of current sonographic criteria. Am J Roentgenol. 2010;194:1090–4.CrossRef
58.
go back to reference Buckley JA, Fishman EK. CT evaluation of small bowel neoplasms: spectrum of disease. Radiographics. 1998;18:379–92.PubMed Buckley JA, Fishman EK. CT evaluation of small bowel neoplasms: spectrum of disease. Radiographics. 1998;18:379–92.PubMed
59.
go back to reference Pantongrag-Brown L, Buetow PC, Carr NJ, et al. Calcification and fibrosis in mesenteric carcinoid tumor: CT findings and pathologic correlation. AJR Am J Roentgenol. 1995;164:387–91.PubMed Pantongrag-Brown L, Buetow PC, Carr NJ, et al. Calcification and fibrosis in mesenteric carcinoid tumor: CT findings and pathologic correlation. AJR Am J Roentgenol. 1995;164:387–91.PubMed
60.
go back to reference Magid D, Siegelman SS, Eggleston JC, et al. Pulmonary carcinoid tumors: CT assessment. J Comput Assist Tomogr. 1989;13:244–7.PubMedCrossRef Magid D, Siegelman SS, Eggleston JC, et al. Pulmonary carcinoid tumors: CT assessment. J Comput Assist Tomogr. 1989;13:244–7.PubMedCrossRef
61.
go back to reference Grewal RG, Austin JH. CT demonstration of calcification in carcinoma of the lung. J Comput Assist Tomogr. 1994;18:867–71.PubMedCrossRef Grewal RG, Austin JH. CT demonstration of calcification in carcinoma of the lung. J Comput Assist Tomogr. 1994;18:867–71.PubMedCrossRef
62.
go back to reference Chong S, Lee KS, Chung MJ, et al. Neuroendocrine tumors of the lung: clinical, pathologic, and imaging findings. Radiographics. 2006;26:41–57.PubMedCrossRef Chong S, Lee KS, Chung MJ, et al. Neuroendocrine tumors of the lung: clinical, pathologic, and imaging findings. Radiographics. 2006;26:41–57.PubMedCrossRef
63.
go back to reference Akata S, Okada S, Maeda J, et al. Computed tomographic findings of large cell neuroendocrine carcinoma of the lung. Clin Imaging. 2007;31:379–84.PubMedCrossRef Akata S, Okada S, Maeda J, et al. Computed tomographic findings of large cell neuroendocrine carcinoma of the lung. Clin Imaging. 2007;31:379–84.PubMedCrossRef
Metadata
Title
Pancreatic Neuroendocrine Tumors: Radiographic Calcifications Correlate with Grade and Metastasis
Authors
George A. Poultsides, MD, MSc
Lyen C. Huang, MD, MPH
Yijun Chen, MD
Brendan C. Visser, MD
Reetesh K. Pai, MD
R. Brooke Jeffrey, MD
Walter G. Park, MD, MSc
Ann M. Chen, MD
Pamela L. Kunz, MD
George A. Fisher, MD, PhD
Jeffrey A. Norton, MD
Publication date
01-07-2012
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 7/2012
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-012-2305-7

Other articles of this Issue 7/2012

Annals of Surgical Oncology 7/2012 Go to the issue