Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

The Role of Imaging in Current Treatment Strategies for Pancreatic Adenocarcinoma

  • Hyungjin Rhee (Department of Radiology, Severance Hospital, Yonsei University College of Medicine) ;
  • Mi-Suk Park (Department of Radiology, Severance Hospital, Yonsei University College of Medicine)
  • Received : 2019.11.17
  • Accepted : 2020.05.18
  • Published : 2021.01.01
Download PDF
⟨ Previous Next ⟩

Abstract

In pancreatic cancer, imaging plays an essential role in surveillance, diagnosis, resectability evaluation, and treatment response evaluation. Pancreatic cancer surveillance in high-risk individuals has been attempted using endoscopic ultrasound (EUS) or magnetic resonance imaging (MRI). Imaging diagnosis and resectability evaluation are the most important factors influencing treatment decisions, where computed tomography (CT) is the preferred modality. EUS, MRI, and positron emission tomography play a complementary role to CT. Treatment response evaluation is of increasing clinical importance, especially in patients undergoing neoadjuvant therapy. This review aimed to comprehensively review the role of imaging in relation to the current treatment strategy for pancreatic cancer, including surveillance, diagnosis, evaluation of resectability and treatment response, and prediction of prognosis.

Keywords

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin 2018;68:7-30 https://doi.org/10.3322/caac.21442
  2. Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C, et al. European cancer mortality predictions for the year 2019 with focus on breast cancer. Ann Oncol 2019;30:781-787 https://doi.org/10.1093/annonc/mdz051
  3. Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, et al. Cancer incidence and mortality patterns in Eeurope: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer 2018;103:356-387 https://doi.org/10.1016/j.ejca.2018.07.005
  4. Jung KW, Won YJ, Kong HJ, Lee ES. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2016. Cancer Res Treat 2019;51:417-430 https://doi.org/10.4143/crt.2019.138
  5. Ducreux M, Cuhna AS, Caramella C, Hollebecque A, Burtin P, Goere D, et al. Cancer of the pancreas: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2015;26 Suppl 5:v56-v68 https://doi.org/10.1093/annonc/mdv295
  6. Callery MP, Chang KJ, Fishman EK, Talamonti MS, William Traverso L, Linehan DC. Pretreatment assessment of resectable and borderline resectable pancreatic cancer: expert consensus statement. Ann Surg Oncol 2009;16:1727-1733 https://doi.org/10.1245/s10434-009-0408-6
  7. Tempero MA, Malafa MP, Al-Hawary M, Asbun H, Bain A, Behrman SW, et al. Pancreatic adenocarcinoma, version 2.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2017;15:1028-1061 https://doi.org/10.6004/jnccn.2017.0131
  8. Gilbert JW, Wolpin B, Clancy T, Wang J, Mamon H, Shinagare AB, et al. Borderline resectable pancreatic cancer: conceptual evolution and current approach to image-based classification. Ann Oncol 2017;28:2067-2076 https://doi.org/10.1093/annonc/mdx180
  9. Konstantinidis IT, Warshaw AL, Allen JN, Blaszkowsky LS, Castillo CF, Deshpande V, et al. Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? What is a "true" R0 resection? Ann Surg 2013;257:731-736 https://doi.org/10.1097/SLA.0b013e318263da2f
  10. Bockhorn M, Uzunoglu FG, Adham M, Imrie C, Milicevic M, Sandberg AA, et al. Borderline resectable pancreatic cancer: a consensus statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2014;155:977-988 https://doi.org/10.1016/j.surg.2014.02.001
  11. Bilimoria KY, Talamonti MS, Sener SF, Bilimoria MM, Stewart AK, Winchester DP, et al. Effect of hospital volume on margin status after pancreaticoduodenectomy for cancer. J Am Coll Surgs 2008;207:510-519 https://doi.org/10.1016/j.jamcollsurg.2008.04.033
  12. Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg 2006;10:1199-1211 https://doi.org/10.1016/j.gassur.2006.08.018
  13. Neoptolemos JP, Stocken DD, Dunn JA, Almond J, Beger HG, Pederzoli P, et al. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg 2001;234:758-768 https://doi.org/10.1097/00000658-200112000-00007
  14. Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, et al. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann Surg Oncol 2006;13:1035-1046 https://doi.org/10.1245/ASO.2006.08.011
  15. Neoptolemos JP, Palmer DH, Ghaneh P, Psarelli EE, Valle JW, Halloran CM, et al. Comparison of adjuvant gemcitabine and capecitabine with gemcitabine monotherapy in patients with resected pancreatic cancer (ESPAC-4): a multicentre, open-label, randomised, phase 3 trial. Lancet 2017;389:1011-1024 https://doi.org/10.1016/S0140-6736(16)32409-6
  16. Conroy T, Hammel P, Hebbar M, Ben Abdelghani M, Wei AC, Raoul JL, et al. Folfirinox or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med 2018;379:2395-2406 https://doi.org/10.1056/NEJMoa1809775
  17. Tempero MA. NCCN guidelines updates: pancreatic cancer. J Natl Compr Canc Netw 2019;17:603-605
  18. Khorana AA, McKernin SE, Berlin J, Hong TS, Maitra A, Moravek C, et al. Potentially curable pancreatic adenocarcinoma: ASCO clinical practice guideline update. J Clin Oncol 2019;37:2082-2088 https://doi.org/10.1200/JCO.19.00946
  19. Mornex F, Girard N, Delpero JR, Partensky C. Radiochemotherapy in the management of pancreatic cancer-Part I: neoadjuvant treatment. Semin Radiat Oncol 2005;15:226-234 https://doi.org/10.1016/j.semradonc.2005.04.008
  20. Gillen S, Schuster T, Meyer Zum Buschenfelde C, Friess H, Kleeff J. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med 2010;7:e1000267
  21. Assifi MM, Lu X, Eibl G, Reber HA, Li G, Hines OJ. Neoadjuvant therapy in pancreatic adenocarcinoma: a meta-analysis of phase II trials. Surgery 2011;150:466-473 https://doi.org/10.1016/j.surg.2011.07.006
  22. Laurence JM, Tran PD, Morarji K, Eslick GD, Lam VW, Sandroussi C. A systematic review and meta-analysis of survival and surgical outcomes following neoadjuvant chemoradiotherapy for pancreatic cancer. J Gastrointest Surg 2011;15:2059-2069 https://doi.org/10.1007/s11605-011-1659-7
  23. US Preventive Services Task Force; Owens DK, Davidson KW, Krist AH, Barry MJ, Cabana M, Caughey AB, et al. Screening for pancreatic cancer: US preventive services task force reaffirmation recommendation statement. JAMA 2019;322:438-444 https://doi.org/10.1001/jama.2019.10232
  24. Harinck F, Konings IC, Kluijt I, Poley JW, van Hooft JE, van Dullemen HM, et al. A multicentre comparative prospective blinded analysis of EUS and MRI for screening of pancreatic cancer in high-risk individuals. Gut 2016;65:1505-1513 https://doi.org/10.1136/gutjnl-2014-308008
  25. Canto MI, Hruban RH, Fishman EK, Kamel IR, Schulick R, Zhang Z, et al. Frequent detection of pancreatic lesions in asymptomatic high-risk individuals. Gastroenterology 2012;142:796-804 https://doi.org/10.1053/j.gastro.2012.01.005
  26. Capurso G, Signoretti M, Valente R, Arnelo U, Lohr M, Poley JW, et al. Methods and outcomes of screening for pancreatic adenocarcinoma in high-risk individuals. World J Gastrointest Endosc 2015;7:833-842 https://doi.org/10.4253/wjge.v7.i9.833
  27. Karlson BM, Ekbom A, Lindgren PG, Kallskog V, Rastad J. Abdominal US for diagnosis of pancreatic tumor: prospective cohort analysis. Radiology 1999;213:107-111 https://doi.org/10.1148/radiology.213.1.r99oc25107
  28. Maringhini A, Ciambra M, Raimondo M, Baccelliere P, Grasso R, Dardanoni G, et al. Clinical presentation and ultrasonography in the diagnosis of pancreatic cancer. Pancreas 1993;8:146-150 https://doi.org/10.1097/00006676-199303000-00002
  29. Xu MM, Sethi A. Imaging of the pancreas. Gastroenterol Clin North Am 2016;45:101-116 https://doi.org/10.1016/j.gtc.2015.10.010
  30. Walters DM, Lapar DJ, de Lange EE, Sarti M, Stokes JB, Adams RB, et al. Pancreas-protocol imaging at a high-volume center leads to improved preoperative staging of pancreatic ductal adenocarcinoma. Ann Surg Oncol 2011;18:2764-2771 https://doi.org/10.1245/s10434-011-1693-4
  31. Raman SP, Reddy S, Weiss MJ, Manos LL, Cameron JL, Zheng L, et al. Impact of the time interval between MDCT imaging and surgery on the accuracy of identifying metastatic disease in patients with pancreatic cancer. AJR Am J Roentgenol 2015;204:W37-W42 https://doi.org/10.2214/AJR.13.12439
  32. Bipat S, Phoa SS, van Delden OM, Bossuyt PM, Gouma DJ, Lameris JS, et al. Ultrasonography, computed tomography and magnetic resonance imaging for diagnosis and determining resectability of pancreatic adenocarcinoma: a meta-analysis. J Comput Assist Tomogr 2005;29:438-445 https://doi.org/10.1097/01.rct.0000164513.23407.b3
  33. Treadwell JR, Zafar HM, Mitchell MD, Tipton K, Teitelbaum U, Jue J. Imaging tests for the diagnosis and staging of pancreatic adenocarcinoma: a meta-analysis. Pancreas 2016;45:789-795 https://doi.org/10.1097/MPA.0000000000000524
  34. Toft J, Hadden WJ, Laurence JM, Lam V, Yuen L, Janssen A, et al. Imaging modalities in the diagnosis of pancreatic adenocarcinoma: a systematic review and meta-analysis of sensitivity, specificity and diagnostic accuracy. Eur J Radiol 2017;92:17-23 https://doi.org/10.1016/j.ejrad.2017.04.009
  35. Prokesch RW, Chow LC, Beaulieu CF, Bammer R, Jeffrey RB Jr. Isoattenuating pancreatic adenocarcinoma at multi-detector row CT: secondary signs. Radiology 2002;224:764-768 https://doi.org/10.1148/radiol.2243011284
  36. Kim JH, Park SH, Yu ES, Kim MH, Kim J, Byun JH, et al. Visually isoattenuating pancreatic adenocarcinoma at dynamic-enhanced CT: frequency, clinical and pathologic characteristics, and diagnosis at imaging examinations. Radiology 2010;257:87-96 https://doi.org/10.1148/radiol.10100015
  37. Motosugi U, Ichikawa T, Morisaka H, Sou H, Muhi A, Kimura K, et al. Detection of pancreatic carcinoma and liver metastases with gadoxetic acid-enhanced MR imaging: comparison with contrast-enhanced multi-detector row CT. Radiology 2011;260:446-453 https://doi.org/10.1148/radiol.11103548
  38. Roche CJ, Hughes ML, Garvey CJ, Campbell F, White DA, Jones L, et al. CT and pathologic assessment of prospective nodal staging in patients with ductal adenocarcinoma of the head of the pancreas. AJR Am J Roentgenol 2003;180:475-480 https://doi.org/10.2214/ajr.180.2.1800475
  39. Dirisamer A, Schima W, Heinisch M, Weber M, Lehner HP, Haller J, et al. Detection of histologically proven peritoneal carcinomatosis with fused 18F-FDG-PET/MDCT. Eur J Radiol 2009;69:536-541 https://doi.org/10.1016/j.ejrad.2007.11.032
  40. Chen FM, Ni JM, Zhang ZY, Zhang L, Li B, Jiang CJ. Presurgical evaluation of pancreatic cancer: a comprehensive imaging comparison of CT versus MRI. AJR Am J Roentgenol 2016;206:526-535 https://doi.org/10.2214/AJR.15.15236
  41. Jeon SK, Lee JM, Joo I, Lee DH, Ahn SJ, Woo H, et al. Magnetic resonance with diffusion-weighted imaging improves assessment of focal liver lesions in patients with potentially resectable pancreatic cancer on CT. Eur Radiol 2018;28:3484-3493 https://doi.org/10.1007/s00330-017-5258-1
  42. Choi SY, Kim YK, Min JH, Cha DI, Jeong WK, Lee WJ. The value of gadoxetic acid-enhanced MRI for differentiation between hepatic microabscesses and metastases in patients with periampullary cancer. Eur Radiol 2017;27:4383-4393 https://doi.org/10.1007/s00330-017-4782-3
  43. Kim HJ, Park MS, Lee JY, Han K, Chung YE, Choi JY, et al. Incremental role of pancreatic magnetic resonance imaging after staging computed tomography to evaluate patients with pancreatic ductal adenocarcinoma. Cancer Res Treat 2019;51:24-33 https://doi.org/10.4143/crt.2017.404
  44. Tamm EP, Bhosale PR, Vikram R, de Almeida Marcal LP, Balachandran A. Imaging of pancreatic ductal adenocarcinoma: state of the art. World J Radiol 2013;5:98-105 https://doi.org/10.4329/wjr.v5.i3.98
  45. Ichikawa T, Erturk SM, Motosugi U, Sou H, Iino H, Araki T, et al. High-b value diffusion-weighted MRI for detecting pancreatic adenocarcinoma: preliminary results. AJR Am J Roentgenol 2007;188:409-414 https://doi.org/10.2214/AJR.05.1918
  46. Matsuki M, Inada Y, Nakai G, Tatsugami F, Tanikake M, Narabayashi I, et al. Diffusion-weighed MR imaging of pancreatic carcinoma. Abdom Imaging 2007;32:481-483 https://doi.org/10.1007/s00261-007-9192-6
  47. Fukukura Y, Takumi K, Kamimura K, Shindo T, Kumagae Y, Tateyama A, et al. Pancreatic adenocarcinoma: variability of diffusion-weighted MR imaging findings. Radiology 2012;263:732-740 https://doi.org/10.1148/radiol.12111222
  48. Kato K, Nihashi T, Ikeda M, Abe S, Iwano S, Itoh S, et al. Limited efficacy of 18F-FDG PET/CT for differentiation between metastasis-free pancreatic cancer and mass-forming pancreatitis. Clin Nucl Med 2013;38:417-421 https://doi.org/10.1097/RLU.0b013e3182817d9d
  49. Rijkers AP, Valkema R, Duivenvoorden HJ, van Eijck CH. Usefulness of F-18-fluorodeoxyglucose positron emission tomography to confirm suspected pancreatic cancer: a meta-analysis. Eur J Surg Oncol 2014;40:794-804 https://doi.org/10.1016/j.ejso.2014.03.016
  50. Matsumoto I, Shirakawa S, Shinzeki M, Asari S, Goto T, Ajiki T, et al. 18-fluorodeoxyglucose positron emission tomography does not aid in diagnosis of pancreatic ductal adenocarcinoma. Clinl Gastroenterol Hepatol 2013;11:712-718 https://doi.org/10.1016/j.cgh.2012.12.033
  51. Ghaneh P, Hanson R, Titman A, Lancaster G, Plumpton C, Lloyd-Williams H, et al. PET-PANC: multicentre prospective diagnostic accuracy and health economic analysis study of the impact of combined modality 18fluorine-2-fluoro-2-deoxy-d-glucose positron emission tomography with computed tomography scanning in the diagnosis and management of pancreatic cancer. Health Technol Assess 2018;22:1-114 https://doi.org/10.3310/hta22070
  52. Farma JM, Santillan AA, Melis M, Walters J, Belinc D, Chen DT, et al. PET/CT fusion scan enhances CT staging in patients with pancreatic neoplasms. Ann Surg Oncol 2008;15:2465-2471 https://doi.org/10.1245/s10434-008-9992-0
  53. Agarwal B, Abu-Hamda E, Molke KL, Correa AM, Ho L. Endoscopic ultrasound-guided fine needle aspiration and multidetector spiral CT in the diagnosis of pancreatic cancer. Am J Gastroenterol 2004;99:844-850 https://doi.org/10.1111/j.1572-0241.2004.04177.x
  54. Nawaz H, Fan CY, Kloke J, Khalid A, McGrath K, Landsittel D, et al. Performance characteristics of endoscopic ultrasound in the staging of pancreatic cancer: a meta-analysis. JOP 2013;14:484-497
  55. Sa˘ftoiu A, Vilmann P. Role of endoscopic ultrasound in the diagnosis and staging of pancreatic cancer. J Clin Ultrasound 2009;37:1-17 https://doi.org/10.1002/jcu.20534
  56. Banafea O, Mghanga FP, Zhao J, Zhao R, Zhu L. Endoscopic ultrasonography with fine-needle aspiration for histological diagnosis of solid pancreatic masses: a meta-analysis of diagnostic accuracy studies. BMC Gastroenterol 2016;16:108
  57. Okasha HH, Naga MI, Esmat S, Naguib M, Hassanein M, Hassani M, et al. Endoscopic ultrasound-guided fine needle aspiration versus percutaneous ultrasound-guided fine needle aspiration in diagnosis of focal pancreatic masses. Endosc Ultrasound 2013;2:190-193 https://doi.org/10.4103/2303-9027.121239
  58. Micames C, Jowell PS, White R, Paulson E, Nelson R, Morse M, et al. Lower frequency of peritoneal carcinomatosis in patients with pancreatic cancer diagnosed by EUS-guided FNA vs. percutaneous FNA. Gastrointest Endosc 2003;58:690-695 https://doi.org/10.1016/S0016-5107(03)02009-1
  59. Ngamruengphong S, Swanson KM, Shah ND, Wallace MB. Preoperative endoscopic ultrasound-guided fine needle aspiration does not impair survival of patients with resected pancreatic cancer. Gut 2015;64:1105-1110 https://doi.org/10.1136/gutjnl-2014-307475
  60. Singhi AD, George B, Greenbowe JR, Chung J, Suh J, Maitra A, et al. Real-time targeted genome profile analysis of pancreatic ductal adenocarcinomas identifies genetic alterations that might be targeted with existing drugs or used as biomarkers. Gastroenterology 2019;156:2242-2253. e4 https://doi.org/10.1053/j.gastro.2019.02.037
  61. Lowery MA, Jordan EJ, Basturk O, Ptashkin RN, Zehir A, Berger MF, et al. Real-time genomic profiling of pancreatic ductal adenocarcinoma: potential actionability and correlation with clinical phenotype. Clin Cancer Res 2017;23:6094-6100 https://doi.org/10.1158/1078-0432.CCR-17-0899
  62. Amin MB, Edge SB, Greene FL, Byrd DR, Brookland RK, Washington MK, et al. AJCC cancer staging manual, 8th ed. Chicago: Springer, 2017
  63. Schlitter AM, Jesinghaus M, Jager C, Konukiewitz B, Muckenhuber A, Demir IE, et al. pT but not pN stage of the 8th TNM classification significantly improves prognostication in pancreatic ductal adenocarcinoma. Eur J Cancer 2017;84:121-129 https://doi.org/10.1016/j.ejca.2017.06.034
  64. van Roessel S, Kasumova GG, Verheij J, Najarian RM, Maggino L, de Pastena M, et al. International validation of the eighth edition of the American Joint Committee on Cancer (AJCC) TNM staging system in patients with resected pancreatic cancer. JAMA Surg 2018;153:e183617
  65. Allen PJ, Kuk D, Castillo CF, Basturk O, Wolfgang CL, Cameron JL, et al. Multi-institutional validation study of the American Joint Commission on Cancer (8th edition) changes for T and N staging in patients with pancreatic adenocarcinoma. Ann Surg 2017;265:185-191 https://doi.org/10.1097/SLA.0000000000001763
  66. Kamarajah SK, Burns WR, Frankel TL, Cho CS, Nathan H. Validation of the American Joint Commission on Cancer (AJCC) 8th edition staging system for patients with pancreatic adenocarcinoma: a surveillance, epidemiology and end results (SEER) analysis. Ann Surg Oncol 2017;24:2023-2030 https://doi.org/10.1245/s10434-017-5810-x
  67. Katz MH, Marsh R, Herman JM, Shi Q, Collison E, Venook AP, et al. Borderline resectable pancreatic cancer: need for standardization and methods for optimal clinical trial design. Ann Surg Oncol 2013;20:2787-2795 https://doi.org/10.1245/s10434-013-2886-9
  68. Al-Hawary MM, Francis IR, Chari ST, Fishman EK, Hough DM, Lu DS, et al. Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the society of abdominal radiology and the American Pancreatic Association. Radiology 2014;270:248-260 https://doi.org/10.1148/radiol.13131184
  69. Hong SB, Lee SS, Kim JH, Kim HJ, Byun JH, Hong SM, et al. Pancreatic cancer CT: prediction of resectability according to NCCN criteria. Radiology 2018;289:710-718 https://doi.org/10.1148/radiol.2018180628
  70. Soriano A, Castells A, Ayuso C, Ayuso JR, de Caralt MT, Gines MA, et al. Preoperative staging and tumor resectability assessment of pancreatic cancer: prospective study comparing endoscopic ultrasonography, helical computed tomography, magnetic resonance imaging, and angiography. Am J Gastroenterol 2004;99:492-501 https://doi.org/10.1111/j.1572-0241.2004.04087.x
  71. Loizou L, Duran CV, Axelsson E, Andersson M, Keussen I, Strinnholm J, et al. Radiological assessment of local resectability status in patients with pancreatic cancer: interreader agreement and reader performance in two different classification systems. Eur J Radiol 2018;106:69-76 https://doi.org/10.1016/j.ejrad.2018.06.014
  72. Joo I, Lee JM, Lee ES, Son JY, Lee DH, Ahn SJ, et al. Preoperative CT classification of the resectability of pancreatic cancer: interobserver agreement. Radiology 2019;293:343-349 https://doi.org/10.1148/radiol.2019190422
  73. Witkowski ER, Smith JK, Ragulin-Coyne E, Ng SC, Shah SA, Tseng JF. Is it worth looking? Abdominal imaging after pancreatic cancer resection: a national study. J Gastrointest Surg 2012;16:121-128 https://doi.org/10.1007/s11605-011-1699-z
  74. Sheffield KM, Crowell KT, Lin YL, Djukom C, Goodwin JS, Riall TS. Surveillance of pancreatic cancer patients after surgical resection. Ann Surg Oncol 2012;19:1670-1677 https://doi.org/10.1245/s10434-011-2152-y
  75. Tzeng CW, Abbott DE, Cantor SB, Fleming JB, Lee JE, Pisters PW, et al. Frequency and intensity of postoperative surveillance after curative treatment of pancreatic cancer: a cost-effectiveness analysis. Ann Surg Oncol 2013;20:2197-2203 https://doi.org/10.1245/s10434-013-2889-6
  76. Daamen LA, Groot VP, Heerkens HD, Intven MPW, van Santvoort HC, Molenaar IQ. Systematic review on the role of serum tumor markers in the detection of recurrent pancreatic cancer. HPB (Oxford) 2018;20:297-304 https://doi.org/10.1016/j.hpb.2017.11.009
  77. White RR, Paulson EK, Freed KS, Keogan MT, Hurwitz HI, Lee C, et al. Staging of pancreatic cancer before and after neoadjuvant chemoradiation. J Gastrointest Surg 2001;5:626-633 https://doi.org/10.1016/S1091-255X(01)80105-0
  78. Sasson AR, Wetherington RW, Hoffman JP, Ross EA, Cooper H, Meropol NJ, et al. Neoadjuvant chemoradiotherapy for adenocarcinoma of the pancreas: analysis of histopathology and outcome. Int J Gastrointest Cancer 2003;34:121-128 https://doi.org/10.1385/IJGC:34:2-3:121
  79. Cassinotto C, Cortade J, Belleannee G, Lapuyade B, Terrebonne E, Vendrely V, et al. An evaluation of the accuracy of CT when determining resectability of pancreatic head adenocarcinoma after neoadjuvant treatment. Eur J Radiol 2013;82:589-593 https://doi.org/10.1016/j.ejrad.2012.12.002
  80. Michelakos T, Pergolini I, Castillo CF, Honselmann KC, Cai L, Deshpande V, et al. Predictors of resectability and survival in patients with borderline and locally advanced pancreatic cancer who underwent neoadjuvant treatment with FOLFIRINOX. Ann Surg 2019;269:733-740 https://doi.org/10.1097/SLA.0000000000002600
  81. Katz MH, Fleming JB, Bhosale P, Varadhachary G, Lee JE, Wolff R, et al. Response of borderline resectable pancreatic cancer to neoadjuvant therapy is not reflected by radiographic indicators. Cancer 2012;118:5749-5756 https://doi.org/10.1002/cncr.27636
  82. Ferrone CR, Marchegiani G, Hong TS, Ryan DP, Deshpande V, McDonnell EI, et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg 2015;261:12-17 https://doi.org/10.1097/SLA.0000000000000867
  83. Baliyan V, Kordbacheh H, Parakh A, Kambadakone A. Response assessment in pancreatic ductal adenocarcinoma: role of imaging. Abdom Radiol (NY) 2018;43:435-444 https://doi.org/10.1007/s00261-017-1434-7
  84. Cassinotto C, Sa-Cunha A, Trillaud H. Radiological evaluation of response to neoadjuvant treatment in pancreatic cancer. Diagn Interv Imaging 2016;97:1225-1232 https://doi.org/10.1016/j.diii.2016.07.011
  85. Gassner EM, Poskaite P. Imaging response evaluation after novel neoadjuvant treatments of pancreatic cancer. European Surgery 2019;51:146-152
  86. Cassinotto C, Mouries A, Lafourcade JP, Terrebonne E, Belleannee G, Blanc JF, et al. Locally advanced pancreatic adenocarcinoma: reassessment of response with CT after neoadjuvant chemotherapy and radiation therapy. Radiology 2014;273:108-116 https://doi.org/10.1148/radiol.14132914
  87. Kim YE, Park MS, Hong HS, Kang CM, Choi JY, Lim JS, et al. Effects of neoadjuvant combined chemotherapy and radiation therapy on the CT evaluation of resectability and staging in patients with pancreatic head cancer. Radiology 2009;250:758-765 https://doi.org/10.1148/radiol.2502080501
  88. Marchegiani G, Todaro V, Boninsegna E, Negrelli R, Sureka B, Bonamini D, et al. Surgery after FOLFIRINOX treatment for locally advanced and borderline resectable pancreatic cancer: increase in tumour attenuation on CT correlates with R0 resection. Eur Radiol 2018;28:4265-4273 https://doi.org/10.1007/s00330-018-5410-6
  89. Wagner M, Antunes C, Pietrasz D, Cassinotto C, Zappa M, Sa Cunha A, et al. CT evaluation after neoadjuvant FOLFIRINOX chemotherapy for borderline and locally advanced pancreatic adenocarcinoma. Eur Radiol 2017;27:3104-3116 https://doi.org/10.1007/s00330-016-4632-8
  90. Chen X, Oshima K, Schott D, Wu H, Hall W, Song Y, et al. Assessment of treatment response during chemoradiation therapy for pancreatic cancer based on quantitative radiomic analysis of daily CTs: an exploratory study. PLoS One 2017;12:e0178961
  91. Park MS, Klotz E, Kim MJ, Song SY, Park SW, Cha SW, et al. Perfusion CT: noninvasive surrogate marker for stratification of pancreatic cancer response to concurrent chemo- and radiation therapy. Radiology 2009;250:110-117 https://doi.org/10.1148/radiol.2493080226
  92. Akisik MF, Sandrasegaran K, Bu G, Lin C, Hutchins GD, Chiorean EG. Pancreatic cancer: utility of dynamic contrast-enhanced MR imaging in assessment of antiangiogenic therapy. Radiology 2010;256:441-449 https://doi.org/10.1148/radiol.10091733
  93. Okada KI, Hirono S, Kawai M, Miyazawa M, Shimizu A, Kitahata Y, et al. Value of apparent diffusion coefficient prior to neoadjuvant therapy is a predictor of histologic response in patients with borderline resectable pancreatic carcinoma. J Hepatobiliary Pancreat Sci 2017;24:161-168 https://doi.org/10.1002/jhbp.430
  94. Dalah E, Erickson B, Oshima K, Schott D, Hall WA, Paulson E, et al. Correlation of ADC with pathological treatment response for radiation therapy of pancreatic cancer. Transl Oncol 2018;11:391-398 https://doi.org/10.1016/j.tranon.2018.01.018
  95. Heinrich S, Schafer M, Weber A, Hany TF, Bhure U, Pestalozzi BC, et al. Neoadjuvant chemotherapy generates a significant tumor response in resectable pancreatic cancer without increasing morbidity: results of a prospective phase II trial. Ann Surg 2008;248:1014-1022 https://doi.org/10.1097/SLA.0b013e318190a6da
  96. Kittaka H, Takahashi H, Ohigashi H, Gotoh K, Yamada T, Tomita Y, et al. Role of 18F-fluorodeoxyglucose positron emission tomography/computed tomography in predicting the pathologic response to preoperative chemoradiation therapy in patients with resectable T3 pancreatic cancer. World J Surg 2013;37:169-178 https://doi.org/10.1007/s00268-012-1775-x
  97. Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 2013;369:1691-1703 https://doi.org/10.1056/NEJMoa1304369
  98. Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, et al.;The Groupe Tumeurs Digestives of Unicancer and the PRODIGE Intergroup. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 2011;364:1817-1825 https://doi.org/10.1056/NEJMoa1011923
  99. Philip PA, Mooney M, Jaffe D, Eckhardt G, Moore M, Meropol N, et al. Consensus report of the National Cancer Institute clinical trials planning meeting on pancreas cancer treatment. J Clin Oncol 2009;27:5660-5669 https://doi.org/10.1200/JCO.2009.21.9022
  100. Ramanathan RK, Goldstein D, Korn RL, Arena F, Moore M, Siena S, et al. Positron emission tomography response evaluation from a randomized phase III trial of weekly nab-paclitaxel plus gemcitabine versus gemcitabine alone for patients with metastatic adenocarcinoma of the pancreas. Ann Oncol 2016;27:648-653 https://doi.org/10.1093/annonc/mdw020
  101. Bradley A, Van Der Meer R. Upfront surgery versus neoadjuvant therapy for resectable pancreatic cancer: systematic review and bayesian network meta-analysis. Sci Rep 2019;9:4354
  102. Raufi AG, Manji GA, Chabot JA, Bates SE. Neoadjuvant treatment for pancreatic cancer. Semin Oncol 2019;46:19-27 https://doi.org/10.1053/j.seminoncol.2018.12.002
  103. Lee S, Kim SH, Park HK, Jang KT, Hwang JA, Kim S. Pancreatic ductal adenocarcinoma: rim enhancement at MR imaging predicts prognosis after curative resection. Radiology 2018;288:456-466 https://doi.org/10.1148/radiol.2018172331
  104. Zhu L, Shi X, Xue H, Wu H, Chen G, Sun H, et al. CT imaging biomarkers predict clinical outcomes after pancreatic cancer surgery. Medicine (Baltimore) 2016;95:e2664
  105. Fukukura Y, Takumi K, Higashi M, Shinchi H, Kamimura K, Yoneyama T, et al. Contrast-enhanced CT and diffusion-weighted MR imaging: performance as a prognostic factor in patients with pancreatic ductal adenocarcinoma. Eur J Radiol 2014;83:612-619 https://doi.org/10.1016/j.ejrad.2013.12.016
  106. Cassinotto C, Chong J, Zogopoulos G, Reinhold C, Chiche L, Lafourcade JP, et al. Resectable pancreatic adenocarcinoma: role of CT quantitative imaging biomarkers for predicting pathology and patient outcomes. Eur J Radiol 2017;90:152-158 https://doi.org/10.1016/j.ejrad.2017.02.033
  107. Yun G, Kim YH, Lee YJ, Kim B, Hwang JH, Choi DJ. Tumor heterogeneity of pancreas head cancer assessed by CT texture analysis: association with survival outcomes after curative resection. Sci Rep 2018;8:7226
  108. Hattori Y, Gabata T, Zen Y, Mochizuki K, Kitagawa H, Matsui O. Poorly enhanced areas of pancreatic adenocarcinomas on late-phase dynamic computed tomography: comparison with pathological findings. Pancreas 2010;39:1263-1270 https://doi.org/10.1097/MPA.0b013e3181dbc583
  109. Muraoka N, Uematsu H, Kimura H, Imamura Y, Fujiwara Y, Murakami M, et al. Apparent diffusion coefficient in pancreatic cancer: characterization and histopathological correlations. J Magn Reson Imaging 2008;27:1302-1308 https://doi.org/10.1002/jmri.21340
  110. Wang Y, Chen ZE, Nikolaidis P, McCarthy RJ, Merrick L, Sternick LA, et al. Diffusion-weighted magnetic resonance imaging of pancreatic adenocarcinomas: association with histopathology and tumor grade. J Magn Reson Imaging 2011;33:136-142 https://doi.org/10.1002/jmri.22414
  111. Hayano K, Miura F, Wada K, Suzuki K, Takeshita K, Amano H, et al. Diffusion-weighted MR imaging of pancreatic cancer and inflammation: prognostic significance of pancreatic inflammation in pancreatic cancer patients. Pancreatology 2016;16:121-126 https://doi.org/10.1016/j.pan.2015.10.004
  112. Chen BB, Tien YW, Chang MC, Cheng MF, Chang YT, Yang SH, et al. Multiparametric PET/MR imaging biomarkers are associated with overall survival in patients with pancreatic cancer. Eur J Nucl Med Mol Imaging 2018;45:1205-1217 https://doi.org/10.1007/s00259-018-3960-0
  113. Kurosawa J, Tawada K, Mikata R, Ishihara T, Tsuyuguchi T, Saito M, et al. Prognostic relevance of apparent diffusion coefficient obtained by diffusion-weighted MRI in pancreatic cancer. J Magn Reson Imaging 2015;42:1532-1537 https://doi.org/10.1002/jmri.24939
  114. Choi HJ, Kang CM, Lee WJ, Song SY, Cho A, Yun M, et al. Prognostic value of 18F-fluorodeoxyglucose positron emission tomography in patients with resectable pancreatic cancer. Yonsei Med J 2013;54:1377-1383 https://doi.org/10.3349/ymj.2013.54.6.1377
  115. Kitasato Y, Yasunaga M, Okuda K, Kinoshita H, Tanaka H, Okabe Y, et al. Maximum standardized uptake value on 18F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography and glucose transporter-1 expression correlates with survival in invasive ductal carcinoma of the pancreas. Pancreas 2014;43:1060-1065 https://doi.org/10.1097/MPA.0000000000000185
  116. Yamamoto T, Sugiura T, Mizuno T, Okamura Y, Aramaki T, Endo M, et al. Preoperative FDG-PET predicts early recurrence and a poor prognosis after resection of pancreatic adenocarcinoma. Ann Surg Oncoly 2015;22:677-684 https://doi.org/10.1245/s10434-014-4046-2
  117. Lee JW, Kang CM, Choi HJ, Lee WJ, Song SY, Lee JH, et al. Prognostic value of metabolic tumor volume and total lesion glycolysis on preoperative 18F-FDG PET/CT in patients with pancreatic cancer. J Nucl Med 2014;55:898-904 https://doi.org/10.2967/jnumed.113.131847