대한영상의학회지 (Journal of the Korean Society of Radiology)

  • 제82권2호
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  • Pages.315-334
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  • 2021
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  • 1738-2637(pISSN)
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  • 2288-2928(eISSN)
대한영상의학회 (The Korean Society of Radiology)
권호 표지
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췌장 선암의 절제 가능성 평가

Radiologic Evaluation for Resectability of Pancreatic Adenocarcinoma

  • 황신혜 (국민건강보험 일산병원 영상의학과) ;
  • 박미숙 (연세대학교 의과대학 세브란스병원 영상의학과)
  • Shin Hye Hwang (Department of Radiology, National Health Insurance Service Ilsan Hospital) ;
  • Mi-Suk Park (Department of Radiology, Severance Hospital, Yonsei University College of Medicine)
  • 투고 : 2021.01.29
  • 심사 : 2021.03.17
  • 발행 : 2021.03.01
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⟨ 이전 논문 다음 논문 ⟩

초록

췌장 선암의 발견, 진단, 절제 가능성 평가, 병기 설정 및 치료 방침 결정에 영상 검사는 중요한 역할을 담당하고 있다. 최근에는 진단 당시 경계절제성 혹은 국소 진행성 췌장암을 진단 받은 경우 선행 보조 치료 또는 완화 치료 후 가능하면 근치적 절제술을 고려할 것이 권고된다. 이 종설에서는 췌장 선암의 절제 가능성 평가, 원격 전이의 진단 및 선행 보조 치료 또는 완화 치료 후 절제 가능성을 재평가할 때 영상 검사의 해석, 판독 기준 및 고려할 사항에 대하여 설명하고자 한다.

Imaging studies play an important role in the detection, diagnosis, assessment of resectability, staging, and determination of patient-tailored treatment options for pancreatic adenocarcinoma. Recently, for patients diagnosed with borderline resectable or locally advanced pancreatic cancers, it is recommended to consider curative-intent surgery following neoadjuvant or palliative therapy, if possible. This review covers how to interpret imaging tests and what to consider when assessing resectability, diagnosing distant metastasis, and re-assessing the resectability of pancreatic cancer after neoadjuvant or palliative therapy.

키워드

참고문헌

  1. Papavasiliou P, Arrangoiz R, Zhu F, Chun YS, Edwards K, Hoffman JP. The anatomic course of the first jejunal branch of the superior mesenteric vein in relation to the superior mesenteric artery. Int J Surg Oncol 2012;2012:538769
  2. De Angelis R, Sant M, Coleman MP, Francisci S, Baili P, Pierannunzio D, et al. Cancer survival in Europe 1999-2007 by country and age: results of EUROCARE--5-a population-based study. Lancet Oncol 2014;15:23-34
  3. National Cancer Center. Korea Cancer Registration Statistics, 2018. Korea Central Cancer Registry, Ministry of Health and Welfare. Available at. https://ncc.re.kr/cancerStatsList.ncc?searchKey=total&searchValue=&pageNum=1. Published 2020. Accessed Jan 10, 2021
  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
  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
  6. National Comprehensive Cancer Network. NCCN Clinical Practive Guideline in Oncology (NCCN Guidelines®): pancreatic adenocarcinoma, version 1.2021. Available at. https://www.nccn.org/store/login/login.aspx?ReturnURL=https://www.nccn.org/professionals/physician_gls/pdf/pancreatic.pdf. Published 2020. Accessed Jan 10, 2021
  7. 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
  8. Marion-Audibert AM, Vullierme MP, Ronot M, Mabrut JY, Sauvanet A, Zins M, et al. Routine MRI with DWI sequences to detect liver metastases in patients with potentially resectable pancreatic ductal carcinoma and normal liver CT: a prospective multicenter study. AJR Am J Roentgenol 2018;211:W217-W225
  9. Gonzalo-Marin J, Vila JJ, Perez-Miranda M. Role of endoscopic ultrasound in the diagnosis of pancreatic cancer. World J Gastrointest Oncol 2014;6:360-368
  10. 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
  11. Yamaguchi K, Okusaka T, Shimizu K, Furuse J, Ito Y, Hanada K, et al. Clinical practice guidelines for pancreatic cancer 2016 from the Japan Pancreas Society: a synopsis. Pancreas 2017;46:595-604
  12. Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, et al. AJCC cancer staging manual. 8th ed. Chicago: Springer International Publishing 2017
  13. 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
  14. 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
  15. 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
  16. Khorana AA, Mangu PB, Berlin J, Engebretson A, Hong TS, Maitra A, et al. Potentially curable pancreatic cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 2016;34:2541-2556
  17. Delpero JR, Sauvanet A. Vascular resection for pancreatic cancer: 2019 French recommendations based on a literature review from 2008 to 6-2019. Front Oncol 2020;10:40
  18. Malczak P, Sierze˛ga M, Stefura T, Kacprzyk A, Dros J, Skomarovska O, et al. Arterial resections in pancreatic cancer - Systematic review and meta-analysis. HPB (Oxford) 2020;22:961-968
  19. Mollberg N, Rahbari NN, Koch M, Hartwig W, Hoeger Y, Buchler MW, et al. Arterial resection during pancreatectomy for pancreatic cancer: a systematic review and meta-analysis. Ann Surg 2011;254:882-893
  20. Jegatheeswaran S, Baltatzis M, Jamdar S, Siriwardena AK. Superior mesenteric artery (SMA) resection during pancreatectomy for malignant disease of the pancreas: a systematic review. HPB (Oxford) 2017;19:483-490
  21. Gong H, Ma R, Gong J, Cai C, Song Z, Xu B. Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic cancer: a systematic review and meta-analysis. Medicine (Baltimore) 2016;95:e3061
  22. Yamamoto Y, Sakamoto Y, Ban D, Shimada K, Esaki M, Nara S, et al. Is celiac axis resection justified for T4 pancreatic body cancer? Surgery 2012;151:61-69
  23. Wu X, Tao R, Lei R, Han B, Cheng D, Shen B, et al. Distal pancreatectomy combined with celiac axis resection in treatment of carcinoma of the body/tail of the pancreas: a single-center experience. Ann Surg Oncol 2010;17:1359-1366
  24. Yamamoto T, Satoi S, Kawai M, Motoi F, Sho M, Uemura KI, et al. Is distal pancreatectomy with en-bloc celiac axis resection effective for patients with locally advanced pancreatic ductal adenocarcinoma?-Multicenter surgical group study. Pancreatology 2018;18:106-113
  25. Miura T, Hirano S, Nakamura T, Tanaka E, Shichinohe T, Tsuchikawa T, et al. A new preoperative prognostic scoring system to predict prognosis in patients with locally advanced pancreatic body cancer who undergo distal pancreatectomy with en bloc celiac axis resection: a retrospective cohort study. Surgery 2014;155:457-467
  26. Zaky AM, Wolfgang CL, Weiss MJ, Javed AA, Fishman EK, Zaheer A. Tumor-vessel relationships in pancreatic ductal adenocarcinoma at multidetector CT: different classification systems and their influence on treatment planning. Radiographics 2017;37:93-112
  27. Giovinazzo F, Turri G, Katz MH, Heaton N, Ahmed I. Meta-analysis of benefits of portal-superior mesenteric vein resection in pancreatic resection for ductal adenocarcinoma. Br J Surg 2016;103:179-191
  28. Peng C, Zhou D, Meng L, Cao Y, Zhang H, Pan Z, et al. The value of combined vein resection in pancreaticoduodenectomy for pancreatic head carcinoma: a meta-analysis. BMC Surg 2019;19:84
  29. Yu XZ, Li J, Fu DL, Di Y, Yang F, Hao SJ, et al. Benefit from synchronous portal-superior mesenteric vein resection during pancreaticoduodenectomy for cancer: a meta-analysis. Eur J Surg Oncol 2014;40:371-378
  30. 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
  31. 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
  32. 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
  33. Isaji S, Mizuno S, Windsor JA, Bassi C, Fernandez-Del Castillo C, Hackert T, et al. International consensus on definition and criteria of borderline resectable pancreatic ductal adenocarcinoma 2017. Pancreatology 2018;18:2-11
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. Kamisawa T, Isawa T, Koike M, Tsuruta K, Okamoto A. Hematogenous metastases of pancreatic ductal carcinoma. Pancreas 1995;11:345-349
  41. Wang W, He Y, Wu L, Ye L, Yao L, Tang Z. Efficacy of extended versus standard lymphadenectomy in pancreatoduodenectomy for pancreatic head adenocarcinoma. An update meta-analysis. Pancreatology 2019;19:1074-1080
  42. 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
  43. Muller MF, Meyenberger C, Bertschinger P, Schaer R, Marincek B. Pancreatic tumors: evaluation with endoscopic US, CT, and MR imaging. Radiology 1994;190:745-751
  44. Kim HR, Seo M, Nah YW, Park HW, Park SH. Clinical impact of fluorine-18-fluorodeoxyglucose positron emission tomography/computed tomography in patients with resectable pancreatic cancer: diagnosing lymph node metastasis and predicting survival. Nucl Med Commun 2018;39:691-698
  45. Santhosh S, Mittal BR, Bhasin DK, Rana SS, Gupta R, Das A, et al. Fluorodeoxyglucose-positron emission tomography/computed tomography performs better than contrast-enhanced computed tomography for metastasis evaluation in the initial staging of pancreatic adenocarcinoma. Ann Nucl Med 2017;31:575-581
  46. 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
  47. Kim HW, Lee JC, Paik KH, Kang J, Kim YH, Yoon YS, et al. Adjunctive role of preoperative liver magnetic resonance imaging for potentially resectable pancreatic cancer. Surgery 2017;161:1579-1587
  48. Hong SB, Choi SH, Kim KW, Kim SY, Kim JH, Kim S, et al. Meta-analysis of MRI for the diagnosis of liver metastasis in patients with pancreatic adenocarcinoma. J Magn Reson Imaging 2020;51:1737-1744
  49. Laghi A, Bellini D, Rengo M, Accarpio F, Caruso D, Biacchi D, et al. Diagnostic performance of computed tomography and magnetic resonance imaging for detecting peritoneal metastases: systematic review and meta-analysis. Radiol Med 2017;122:1-15
  50. 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
  51. Kim SJ, Lee SW. Diagnostic accuracy of 18F-FDG PET/CT for detection of peritoneal carcinomatosis; a systematic review and meta-analysis. Br J Radiol 2018;91:20170519
  52. O'Reilly D, Fou L, Hasler E, Hawkins J, O'Connell S, Pelone F, et al. Diagnosis and management of pancreatic cancer in adults: a summary of guidelines from the UK National Institute for Health and Care Excellence. Pancreatology 2018;18:962-970
  53. Neuzillet C, Gaujoux S, Williet N, Bachet JB, Bauguion L, Colson Durand L, et al. Pancreatic cancer: French clinical practice guidelines for diagnosis, treatment and follow-up (SNFGE, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO, ACHBT, AFC). Dig Liver Dis 2018;50:1257-1271
  54. Balaban EP, Mangu PB, Khorana AA, Shah MA, Mukherjee S, Crane CH, et al. Locally advanced, unresectable pancreatic cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 2016;34:2654-2668
  55. Mehtsun WT, Chipidza FE, Fernandez-Del Castillo C, Hemingway K, Fong ZV, Chang DC, et al. Are staging computed tomography (CT) scans of the chest necessary in pancreatic adenocarcinoma? Ann Surg Oncol 2018;25:3936-3942
  56. Pappas SG, Christians KK, Tolat PP, Mautz AP, Lal A, McElroy L, et al. Staging chest computed tomography and positron emission tomography in patients with pancreatic adenocarcinoma: utility or futility? HPB (Oxford) 2014;16:70-74
  57. Chang ST, Nguyen DC, Raptis C, Menias CO, Zhou G, Wang-Gillam A, et al. Natural history of preoperative subcentimeter pulmonary nodules in patients with resectable pancreatic adenocarcinoma: a retrospective cohort study. Ann Surg 2015;261:970-975
  58. Poruk KE, Kim Y, Cameron JL, He J, Eckhauser FE, Rezaee N, et al. What is the significance of indeterminate pulmonary nodules in patients undergoing resection for pancreatic adenocarcinoma? J Gastrointest Surg 2015;19:841-847
  59. Tzeng CW, Tran Cao HS, Lee JE, Pisters PW, Varadhachary GR, Wolff RA, et al. Treatment sequencing for resectable pancreatic cancer: influence of early metastases and surgical complications on multimodality therapy completion and survival. J Gastrointest Surg 2014;18:16-24; discussion 24-25
  60. Esposito I, Kleeff J, Bergmann F, Reiser C, Herpel E, Friess H, et al. Most pancreatic cancer resections are R1 resections. Ann Surg Oncol 2008;15:1651-1660
  61. Rau BM, Bochow J, Kutsch AL, Weinrich M, Alsfasser G, Klar E. Low completion rate of adjuvant chemotherapy in resected pancreatic cancer in clinical routine care. Pancreatology 2015;15:S107
  62. DePeralta DK, Ogami T, Zhou JM, Schell MJ, Powers BD, Hodul PJ, et al. Completion of adjuvant therapy in patients with resected pancreatic cancer. HPB (Oxford) 2020;22:241-248
  63. Chawla A, Molina G, Pak LM, Rosenthal M, Mancias JD, Clancy TE, et al. Neoadjuvant therapy is associated with improved survival in borderline-resectable pancreatic cancer. Ann Surg Oncol 2020;27:1191-1200
  64. Sutton JM, Abbott DE. Neoadjuvant therapy for pancreas cancer: past lessons and future therapies. World J Gastroenterol 2014;20:15564-15579
  65. Jang JY, Han Y, Lee H, Kim SW, Kwon W, Lee KH, et al. Oncological benefits of neoadjuvant chemoradiation with gemcitabine versus upfront surgery in patients with borderline resectable pancreatic cancer: a prospective, randomized, open-label, multicenter phase 2/3 trial. Ann Surg 2018;268:215-222
  66. Versteijne E, Suker M, Groothuis K, Akkermans-Vogelaar JM, Besselink MG, Bonsing BA, et al. Preoperative chemoradiotherapy versus immediate surgery for resectable and borderline resectable pancreatic cancer: results of the Dutch randomized phase III PREOPANC trial. J Clin Oncol 2020;38:1763-1773
  67. 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
  68. Miyasaka Y, Ohtsuka T, Kimura R, Matsuda R, Mori Y, Nakata K, et al. Neoadjuvant chemotherapy with gemcitabine plus nab-paclitaxel for borderline resectable pancreatic cancer potentially improves survival and facilitates surgery. Ann Surg Oncol 2019;26:1528-1534
  69. Masui T, Doi R, Kawaguchi Y, Sato A, Nakano K, Ito T, et al. Concurrent gemcitabine+S-1 neoadjuvant chemotherapy contributes to the improved survival of patients with small borderline-resectable pancreatic cancer tumors. Surg Today 2016;46:1282-1289
  70. Motoi F, Unno M. Neoadjuvant treatment for resectable pancreatic adenocarcinoma: what is the best protocol? Ann Gastroenterol Surg 2020;4:100-108
  71. Pai RK, Pai RK. Pathologic assessment of gastrointestinal tract and pancreatic carcinoma after neoadjuvant therapy. Mod Pathol 2018;31:4-23
  72. Kalimuthu SN, Serra S, Dhani N, Chetty R. The spectrum of histopathological changes encountered in pancreatectomy specimens after neoadjuvant chemoradiation, including subtle and less-well-recognised changes. J Clin Pathol 2016;69:463-471
  73. Xia BT, Fu B, Wang J, Kim Y, Ahmad SA, Dhar VK, et al. Does radiologic response correlate to pathologic response in patients undergoing neoadjuvant therapy for borderline resectable pancreatic malignancy? J Surg Oncol 2017;115:376-383
  74. Dudeja V, Greeno EW, Walker SP, Jensen EH. Neoadjuvant chemoradiotherapy for locally advanced pancreas cancer rarely leads to radiological evidence of tumour regression. HPB (Oxford) 2013;15:661-667
  75. 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
  76. 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
  77. 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
  78. 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
  79. Dhir M, Malhotra GK, Sohal DPS, Hein NA, Smith LM, O'Reilly EM, et al. Neoadjuvant treatment of pancreatic adenocarcinoma: a systematic review and meta-analysis of 5520 patients. World J Surg Oncol 2017;15:183
  80. Naumann P, Ottensmeier F, Farnia B, Ben-Josef E, Liermann J, Maier-Hein KH, et al. Radiographic response of vessel involvement and resectability after neoadjuvant chemoradiation in patients with locally advanced pancreatic cancer. Am J Clin Oncol 2020;43:776-783
  81. 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
  82. Joo I, Lee JM, Lee ES, Ahn SJ, Lee DH, Kim SW, et al. Preoperative MDCT assessment of resectability in borderline resectable pancreatic cancer: effect of neoadjuvant chemoradiation therapy. AJR Am J Roentgenol 2018;210:1059-1065
  83. Kim BR, Kim JH, Ahn SJ, Joo I, Choi SY, Park SJ, et al. CT prediction of resectability and prognosis in patients with pancreatic ductal adenocarcinoma after neoadjuvant treatment using image findings and texture analysis. Eur Radiol 2019;29:362-372
  84. Ahmed SA, Mourad AF, Hassan RA, Ibrahim MAE, Soliman A, Aboeleuon E, et al. Preoperative CT staging of borderline pancreatic cancer patients after neoadjuvant treatment: accuracy in the prediction of vascular invasion and resectability. Abdom Radiol (NY) 2021;46:280-289
  85. Morgan DE, Waggoner CN, Canon CL, Lockhart ME, Fineberg NS, Posey JA 3rd, et al. Resectability of pancreatic adenocarcinoma in patients with locally advanced disease downstaged by preoperative therapy: a challenge for MDCT. AJR Am J Roentgenol 2010;194:615-622
  86. Park S, Jang JK, Byun JH, Kim JH, Lee SS, Kim HJ, et al. CT in the prediction of margin-negative resection in pancreatic cancer following neoadjuvant treatment: a systematic review and meta-analysis. Eur Radiol 2020 Oct [Epub]. https://doi.org/10.1007/s00330-020-07433-0