Imaging response evaluation of non-surgical therapy for pancreatic cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Yun ¹ , CAO Dan ² ,  SONG Bin ¹

1. Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Department of Abdominal Cancer, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

SONG Bin, Email: songlab_radiology@163.com

Keywords：

pancreatic cancer; chemotherapy; radiotherapy; neoadjuvant therapy; computed tomography; magnetic resonance imaging

DOI：

10.7507/1007-9424.202011011

Video：

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Objective To summarize the value of imaging in the evaluation of non-surgical therapy for pancreatic cancer.Method The relevant literatures about imaging evaluation of non-surgical therapy for pancreatic cancer were collected to make an review.Results At present, most of the imaging evaluation of non-surgical therapy for pancreatic cancer were based on the assessment of morphological characteristics of tumors, such as contrast-enhanced CT and MRI. However, only morphological changes of tumors could not accurately evaluate the response of pancreatic cancer after non-surgical treatment. A few studies had explored the value of functional imaging and artificial intelligence.Conclusions Non-surgical therapy provides new treatment opportunities for unresectable pancreatic cancer, especially the proposed of neoadjuvant therapy, which provides the possibility of operation for patients with advanced pancreatic cancer. More imaging indicators with stronger objectivity, higher accuracy, and wider universality need to be improved and developed in the future.

Citation： ZHANG Yun, CAO Dan, SONG Bin. Imaging response evaluation of non-surgical therapy for pancreatic cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(12): 1579-1583. doi: 10.7507/1007-9424.202011011 Copy

1.	van Veldhuisen E, van den Oord C, Brada LJ, et al. locally advanced pancreatic cancer: work-up, staging, and local intervention strategies. Cancers (Basel), 2019, 11(7): 976.
2.	Ducreux M, Cuhna AS, Caramella C, et al. Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2015, 26(Suppl 5): v56-v68.
3.	Tempero MA, Malafa MP, Al-Hawary M, et al. Pancreatic Adenocarcinoma, Version 2.2017, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw, 2017, 15(8): 1028-1061.
4.	Gilbert JW, Wolpin B, Clancy T, et al. Borderline resectable pancreatic cancer: conceptual evolution and current approach to image-based classification. Ann Oncol, 2017, 28(9): 2067-2076.
5.	Konstantinidis IT, Warshaw AL, Allen JN, 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(4): 731-736.
6.	Bilimoria KY, Talamonti MS, Sener SF, et al. Effect of hospital volume on margin status after pancreaticoduodenectomy for cancer. J Am Coll Surg, 2008, 207(4): 510-519.
7.	Rhee H, Park MS. the role of imaging in current treatment strategies for pancreatic adenocarcinoma. Korean J Radiol, 2020, [Online ahead of print].
8.	Neoptolemos JP, Palmer DH, Ghaneh P, 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(10073): 1011-1024.
9.	Conroy T, Hammel P, Hebbar M, et al. FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med, 2018, 379(25): 2395-2406.
10.	Wolfe AR, Robb R, Hegazi A, et al. Altered gemcitabine and nab-paclitaxel scheduling improves therapeutic efficacy compared to standard concurrent treatment in pre-clinical models of pancreatic cancer. Clin Cancer Res, 2020, [Online ahead of print].
11.	Kouzy R, Abi Jaoude J, Lin D, et al. patient-reported outcome measures in pancreatic cancer receiving radiotherapy. Cancers (Basel), 2020, 12(9): 2487.
12.	Chuong MD, Springett GM, Freilich JM, et al. Stereotactic body radiation therapy for locally advanced and borderline resectable pancreatic cancer is effective and well tolerated. Int J Radiat Oncol Biol Phys, 2013, 86(3): 516-522.
13.	Abi Jaoude J, Kouzy R, Nguyen ND, et al. Radiation therapy for patients with locally advanced pancreatic cancer: evolving techniques and treatment strategies. Curr Probl Cancer, 2020: 100607.
14.	中华医学会外科学分会胰腺外科学组, 中国研究型医院学会胰腺疾病专业委员会. 中国胰腺癌新辅助治疗指南 (2020版). 中华外科杂志, 2020, 58(9): 657-667.
15.	Iacobuzio-Donahue CA, Fu B, Yachida S, et al. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J Clin Oncol, 2009, 27(11): 1806-1813.
16.	Flak RV, Stender MT, Jensen TM, et al. Treatment of locally advanced pancreatic cancer with irreversible electroporation - a Danish single center study of safety and feasibility. Scand J Gastroenterol, 2019, 54(2): 252-258.
17.	Bear AS, Vonderheide RH, O’Hara MH. Challenges and opportunities for pancreatic cancer immunotherapy. Cancer Cell, 2020, [Online ahead of print].
18.	Chiorean EG, Von Hoff DD, Reni M, et al. CA19-9 decrease at8 weeks as a predictor of overall survival in a randomized phase Ⅲ trial (MPACT) of weekly nab-paclitaxel plus gemcitabine versus gemcitabine alone in patients with metastatic pancreatic cancer. Ann Oncol, 2016, 27(4): 654-660.
19.	Noda Y, Goshima S, Miyoshi T, et al. Assessing chemotherapeutic response in pancreatic ductal adenocarcinoma: histogram analysis of iodine concentration and CT number in single-source dual-energy CT. AJR Am J Roentgenol, 2018, 211(6): 1221-1226.
20.	Kawamoto S, Fuld MK, Laheru D, et al. Assessment of iodine uptake by pancreatic cancer following chemotherapy using dual-energy CT. Abdom Radiol (NY), 2018, 43(2): 445-456.
21.	Nishiofuku H, Tanaka T, Marugami N, et al. Increased tumour ADC value during chemotherapy predicts improved survival in unresectable pancreatic cancer. Eur Radiol, 2016, 26(6): 1835-1842.
22.	Cuneo KC, Chenevert TL, Ben-Josef E, et al. A pilot study of diffusion-weighted MRI in patients undergoing neoadjuvant chemoradiation for pancreatic cancer. Transl Oncol, 2014, 7(5): 644-649.
23.	Wang ZJ, Behr S, Consunji MV, et al. Early response assessment in pancreatic ductal adenocarcinoma through integrated PET/MRI. AJR Am J Roentgenol, 2018, 211(5): 1010-1019.
24.	Glicksman RM, Chung H, Myrehaug S, et al. stereotactic radiotherapy for pancreatic cancer: a single-institution experience. Cureus, 2020, 12(9): e10618.
25.	Talbot A, Devos L, Dubus F, et al. Multimodal imaging in radiotherapy: focus on adaptive therapy and quality control. Cancer Radiother, 2020, 24(5): 411-417.
26.	Ziegler M, Nakamura M, Hirashima H, et al. Accumulation of the delivered treatment dose in volumetric modulated arc therapy with breath-hold for pancreatic cancer patients based on daily cone beam computed tomography images with limited field-of-view. Med Phys, 2019, 46(7): 2969-2977.
27.	Wagner M, Antunes C, Pietrasz D, et al. CT evaluation after neoadjuvant FOLFIRINOX chemotherapy for borderline and locally advanced pancreatic adenocarcinoma. Eur Radiol, 2017, 27(7): 3104-3116.
28.	Barreto SG, Loveday B, Windsor JA, et al. Detecting tumour response and predicting resectability after neoadjuvant therapy for borderline resectable and locally advanced pancreatic cancer. ANZ J Surg, 2019, 89(5): 481-487.
29.	Katz MH, Fleming JB, Bhosale P, et al. Response of borderline resectable pancreatic cancer to neoadjuvant therapy is not reflected by radiographic indicators. Cancer, 2012, 118(23): 5749-5756.
30.	Cassinotto C, Cortade J, Belleannée G, et al. An evaluation of the accuracy of CT when determining resectability of pancreatic head adenocarcinoma after neoadjuvant treatment. Eur J Radiol, 2013, 82(4): 589-593.
31.	Okada KI, Hirono S, Kawai M, 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(3): 161-168.
32.	Dalah E, Erickson B, Oshima K, et al. Correlation of ADC with pathological treatment response for radiation therapy of pancreatic cancer. Transl Oncol, 2018, 11(2): 391-398.
33.	Chang JS, Choi SH, Lee Y, et al. Clinical usefulness of ¹⁸F-fluorodeoxyglucose-positron emission tomography in patients with locally advanced pancreatic cancer planned to undergo concurrent chemoradiation therapy. Int J Radiat Oncol Biol Phys, 2014, 90(1): 126-133.
34.	Borhani AA, Dewan R, Furlan A, et al. Assessment of response to neoadjuvant therapy using CT texture analysis in patients with resectable and borderline resectable pancreatic ductal adenocarcinoma. AJR Am J Roentgenol, 2020, 214(2): 362-369.
35.	Ciaravino V, Cardobi N, DE Robertis R, et al. CT texture analysis of ductal adenocarcinoma downstaged after chemotherapy. Anticancer Res, 2018, 38(8): 4889-4895.
36.	Khalvati F, Zhang Y, Baig S, et al. prognostic value of CT radiomic features in resectable pancreatic ductal adenocarcinoma. Sci Rep, 2019, 9(1): 5449.
37.	Nasief H, Hall W, Zheng C, et al. Improving treatment response prediction for chemoradiation therapy of pancreatic cancer using a combination of delta-radiomics and the clinical biomarker CA19-9. Front Oncol, 2020, 9: 1464.
38.	Nasief H, Zheng C, Schott D, et al. A machine learning based delta-radiomics process for early prediction of treatment response of pancreatic cancer. NPJ Precis Oncol, 2019, 3: 25.
39.	Flak RV, Stender MT, Stenholt L, et al. Imaging response evaluation after local ablative treatments in locally advanced pancreatic cancer: an expedited systematic review. HPB (Oxford), 2020, 22(8): 1083-1091.

1. van Veldhuisen E, van den Oord C, Brada LJ, et al. locally advanced pancreatic cancer: work-up, staging, and local intervention strategies. Cancers (Basel), 2019, 11(7): 976.
2. Ducreux M, Cuhna AS, Caramella C, et al. Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2015, 26(Suppl 5): v56-v68.
3. Tempero MA, Malafa MP, Al-Hawary M, et al. Pancreatic Adenocarcinoma, Version 2.2017, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw, 2017, 15(8): 1028-1061.
4. Gilbert JW, Wolpin B, Clancy T, et al. Borderline resectable pancreatic cancer: conceptual evolution and current approach to image-based classification. Ann Oncol, 2017, 28(9): 2067-2076.
5. Konstantinidis IT, Warshaw AL, Allen JN, 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(4): 731-736.
6. Bilimoria KY, Talamonti MS, Sener SF, et al. Effect of hospital volume on margin status after pancreaticoduodenectomy for cancer. J Am Coll Surg, 2008, 207(4): 510-519.
7. Rhee H, Park MS. the role of imaging in current treatment strategies for pancreatic adenocarcinoma. Korean J Radiol, 2020, [Online ahead of print].
8. Neoptolemos JP, Palmer DH, Ghaneh P, 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(10073): 1011-1024.
9. Conroy T, Hammel P, Hebbar M, et al. FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med, 2018, 379(25): 2395-2406.
10. Wolfe AR, Robb R, Hegazi A, et al. Altered gemcitabine and nab-paclitaxel scheduling improves therapeutic efficacy compared to standard concurrent treatment in pre-clinical models of pancreatic cancer. Clin Cancer Res, 2020, [Online ahead of print].
11. Kouzy R, Abi Jaoude J, Lin D, et al. patient-reported outcome measures in pancreatic cancer receiving radiotherapy. Cancers (Basel), 2020, 12(9): 2487.
12. Chuong MD, Springett GM, Freilich JM, et al. Stereotactic body radiation therapy for locally advanced and borderline resectable pancreatic cancer is effective and well tolerated. Int J Radiat Oncol Biol Phys, 2013, 86(3): 516-522.
13. Abi Jaoude J, Kouzy R, Nguyen ND, et al. Radiation therapy for patients with locally advanced pancreatic cancer: evolving techniques and treatment strategies. Curr Probl Cancer, 2020: 100607.
14. 中华医学会外科学分会胰腺外科学组, 中国研究型医院学会胰腺疾病专业委员会. 中国胰腺癌新辅助治疗指南 (2020版). 中华外科杂志, 2020, 58(9): 657-667.
15. Iacobuzio-Donahue CA, Fu B, Yachida S, et al. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J Clin Oncol, 2009, 27(11): 1806-1813.
16. Flak RV, Stender MT, Jensen TM, et al. Treatment of locally advanced pancreatic cancer with irreversible electroporation - a Danish single center study of safety and feasibility. Scand J Gastroenterol, 2019, 54(2): 252-258.
17. Bear AS, Vonderheide RH, O’Hara MH. Challenges and opportunities for pancreatic cancer immunotherapy. Cancer Cell, 2020, [Online ahead of print].
18. Chiorean EG, Von Hoff DD, Reni M, et al. CA19-9 decrease at8 weeks as a predictor of overall survival in a randomized phase Ⅲ trial (MPACT) of weekly nab-paclitaxel plus gemcitabine versus gemcitabine alone in patients with metastatic pancreatic cancer. Ann Oncol, 2016, 27(4): 654-660.
19. Noda Y, Goshima S, Miyoshi T, et al. Assessing chemotherapeutic response in pancreatic ductal adenocarcinoma: histogram analysis of iodine concentration and CT number in single-source dual-energy CT. AJR Am J Roentgenol, 2018, 211(6): 1221-1226.
20. Kawamoto S, Fuld MK, Laheru D, et al. Assessment of iodine uptake by pancreatic cancer following chemotherapy using dual-energy CT. Abdom Radiol (NY), 2018, 43(2): 445-456.
21. Nishiofuku H, Tanaka T, Marugami N, et al. Increased tumour ADC value during chemotherapy predicts improved survival in unresectable pancreatic cancer. Eur Radiol, 2016, 26(6): 1835-1842.
22. Cuneo KC, Chenevert TL, Ben-Josef E, et al. A pilot study of diffusion-weighted MRI in patients undergoing neoadjuvant chemoradiation for pancreatic cancer. Transl Oncol, 2014, 7(5): 644-649.
23. Wang ZJ, Behr S, Consunji MV, et al. Early response assessment in pancreatic ductal adenocarcinoma through integrated PET/MRI. AJR Am J Roentgenol, 2018, 211(5): 1010-1019.
24. Glicksman RM, Chung H, Myrehaug S, et al. stereotactic radiotherapy for pancreatic cancer: a single-institution experience. Cureus, 2020, 12(9): e10618.
25. Talbot A, Devos L, Dubus F, et al. Multimodal imaging in radiotherapy: focus on adaptive therapy and quality control. Cancer Radiother, 2020, 24(5): 411-417.
26. Ziegler M, Nakamura M, Hirashima H, et al. Accumulation of the delivered treatment dose in volumetric modulated arc therapy with breath-hold for pancreatic cancer patients based on daily cone beam computed tomography images with limited field-of-view. Med Phys, 2019, 46(7): 2969-2977.
27. Wagner M, Antunes C, Pietrasz D, et al. CT evaluation after neoadjuvant FOLFIRINOX chemotherapy for borderline and locally advanced pancreatic adenocarcinoma. Eur Radiol, 2017, 27(7): 3104-3116.
28. Barreto SG, Loveday B, Windsor JA, et al. Detecting tumour response and predicting resectability after neoadjuvant therapy for borderline resectable and locally advanced pancreatic cancer. ANZ J Surg, 2019, 89(5): 481-487.
29. Katz MH, Fleming JB, Bhosale P, et al. Response of borderline resectable pancreatic cancer to neoadjuvant therapy is not reflected by radiographic indicators. Cancer, 2012, 118(23): 5749-5756.
30. Cassinotto C, Cortade J, Belleannée G, et al. An evaluation of the accuracy of CT when determining resectability of pancreatic head adenocarcinoma after neoadjuvant treatment. Eur J Radiol, 2013, 82(4): 589-593.
31. Okada KI, Hirono S, Kawai M, 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(3): 161-168.
32. Dalah E, Erickson B, Oshima K, et al. Correlation of ADC with pathological treatment response for radiation therapy of pancreatic cancer. Transl Oncol, 2018, 11(2): 391-398.
33. Chang JS, Choi SH, Lee Y, et al. Clinical usefulness of ¹⁸F-fluorodeoxyglucose-positron emission tomography in patients with locally advanced pancreatic cancer planned to undergo concurrent chemoradiation therapy. Int J Radiat Oncol Biol Phys, 2014, 90(1): 126-133.
34. Borhani AA, Dewan R, Furlan A, et al. Assessment of response to neoadjuvant therapy using CT texture analysis in patients with resectable and borderline resectable pancreatic ductal adenocarcinoma. AJR Am J Roentgenol, 2020, 214(2): 362-369.
35. Ciaravino V, Cardobi N, DE Robertis R, et al. CT texture analysis of ductal adenocarcinoma downstaged after chemotherapy. Anticancer Res, 2018, 38(8): 4889-4895.
36. Khalvati F, Zhang Y, Baig S, et al. prognostic value of CT radiomic features in resectable pancreatic ductal adenocarcinoma. Sci Rep, 2019, 9(1): 5449.
37. Nasief H, Hall W, Zheng C, et al. Improving treatment response prediction for chemoradiation therapy of pancreatic cancer using a combination of delta-radiomics and the clinical biomarker CA19-9. Front Oncol, 2020, 9: 1464.
38. Nasief H, Zheng C, Schott D, et al. A machine learning based delta-radiomics process for early prediction of treatment response of pancreatic cancer. NPJ Precis Oncol, 2019, 3: 25.
39. Flak RV, Stender MT, Stenholt L, et al. Imaging response evaluation after local ablative treatments in locally advanced pancreatic cancer: an expedited systematic review. HPB (Oxford), 2020, 22(8): 1083-1091.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Imaging response evaluation of non-surgical therapy for pancreatic cancer

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