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Published in: Annals of Surgical Oncology 4/2018

01-04-2018 | Pancreatic Tumors

Survival Prediction in Pancreatic Ductal Adenocarcinoma by Quantitative Computed Tomography Image Analysis

Authors: Marc A. Attiyeh, MD, Jayasree Chakraborty, PhD, Alexandre Doussot, MD, PhD, Liana Langdon-Embry, BA, Shiana Mainarich, Mithat Gönen, PhD, Vinod P. Balachandran, MD, Michael I. D’Angelica, MD, Ronald P. DeMatteo, MD, William R. Jarnagin, MD, T. Peter Kingham, MD, Peter J. Allen, MD, Amber L. Simpson, PhD, Richard K. Do, MD, PhD

Published in: Annals of Surgical Oncology | Issue 4/2018

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Abstract

Background

Pancreatic cancer is a highly lethal cancer with no established a priori markers of survival. Existing nomograms rely mainly on post-resection data and are of limited utility in directing surgical management. This study investigated the use of quantitative computed tomography (CT) features to preoperatively assess survival for pancreatic ductal adenocarcinoma (PDAC) patients.

Methods

A prospectively maintained database identified consecutive chemotherapy-naive patients with CT angiography and resected PDAC between 2009 and 2012. Variation in CT enhancement patterns was extracted from the tumor region using texture analysis, a quantitative image analysis tool previously described in the literature. Two continuous survival models were constructed, with 70% of the data (training set) using Cox regression, first based only on preoperative serum cancer antigen (CA) 19-9 levels and image features (model A), and then on CA19-9, image features, and the Brennan score (composite pathology score; model B). The remaining 30% of the data (test set) were reserved for independent validation.

Results

A total of 161 patients were included in the analysis. Training and test sets contained 113 and 48 patients, respectively. Quantitative image features combined with CA19-9 achieved a c-index of 0.69 [integrated Brier score (IBS) 0.224] on the test data, while combining CA19-9, imaging, and the Brennan score achieved a c-index of 0.74 (IBS 0.200) on the test data.

Conclusion

We present two continuous survival prediction models for resected PDAC patients. Quantitative analysis of CT texture features is associated with overall survival. Further work includes applying the model to an external dataset to increase the sample size for training and to determine its applicability.
Appendix
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Literature
1.
2.
go back to reference Alexakis N, Halloran C, Raraty M, Ghaneh P, Sutton R, Neoptolemos JP. Current standards of surgery for pancreatic cancer. Br J Surg. 2004;91(11):1410–1427.CrossRefPubMed Alexakis N, Halloran C, Raraty M, Ghaneh P, Sutton R, Neoptolemos JP. Current standards of surgery for pancreatic cancer. Br J Surg. 2004;91(11):1410–1427.CrossRefPubMed
3.
go back to reference Kneuertz PJ, Pitt HA, Bilimoria KY, et al. Risk of morbidity and mortality following hepato-pancreato-biliary surgery. J Gastrointest Surg. 2012;16(9):1727–1735.CrossRefPubMed Kneuertz PJ, Pitt HA, Bilimoria KY, et al. Risk of morbidity and mortality following hepato-pancreato-biliary surgery. J Gastrointest Surg. 2012;16(9):1727–1735.CrossRefPubMed
4.
go back to reference Ferrone CR, Brennan MF, Gonen M, et al. Pancreatic adenocarcinoma: the actual 5-year survivors. J Gastrointest Surg. 2008;12(4):701–706.CrossRefPubMed Ferrone CR, Brennan MF, Gonen M, et al. Pancreatic adenocarcinoma: the actual 5-year survivors. J Gastrointest Surg. 2008;12(4):701–706.CrossRefPubMed
5.
go back to reference Birkmeyer JD, Siewers AE, Finlayson E V, et al. Hospital volume and surgical mortality in the United States. N Engl J Med. 2002;346(15):1128–1137.CrossRefPubMed Birkmeyer JD, Siewers AE, Finlayson E V, et al. Hospital volume and surgical mortality in the United States. N Engl J Med. 2002;346(15):1128–1137.CrossRefPubMed
6.
go back to reference Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg. 1997;226(3):248–260.CrossRefPubMedPubMedCentral Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg. 1997;226(3):248–260.CrossRefPubMedPubMedCentral
7.
go back to reference Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic nomogram for patients undergoing resection for adenocarcinoma of the pancreas. Ann Surg. 2004;240(2):293–298.CrossRefPubMedPubMedCentral Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic nomogram for patients undergoing resection for adenocarcinoma of the pancreas. Ann Surg. 2004;240(2):293–298.CrossRefPubMedPubMedCentral
8.
9.
go back to reference Ji F, Fu SJ, Guo ZY, et al. Prognostic value of combined preoperative lactate dehydrogenase and alkaline phosphatase levels in patients with resectable pancreatic ductal adenocarcinoma. Med. 2016;95(27):e4065.CrossRefPubMedPubMedCentral Ji F, Fu SJ, Guo ZY, et al. Prognostic value of combined preoperative lactate dehydrogenase and alkaline phosphatase levels in patients with resectable pancreatic ductal adenocarcinoma. Med. 2016;95(27):e4065.CrossRefPubMedPubMedCentral
10.
go back to reference Distler M, Pilarsky E, Kersting S, Grutzmann R. Preoperative CEA and CA 19-9 are prognostic markers for survival after curative resection for ductal adenocarcinoma of the pancreas: a retrospective tumor marker prognostic study. Int J Surg. 2013;11(10):1067–1072.CrossRefPubMed Distler M, Pilarsky E, Kersting S, Grutzmann R. Preoperative CEA and CA 19-9 are prognostic markers for survival after curative resection for ductal adenocarcinoma of the pancreas: a retrospective tumor marker prognostic study. Int J Surg. 2013;11(10):1067–1072.CrossRefPubMed
11.
go back to reference Salmiheimo A, Mustonen H, Stenman UH, et al. Systemic inflammatory response and elevated tumour markers predict worse survival in resectable pancreatic ductal adenocarcinoma. PLoS ONE. 2016;11(9):e0163064.CrossRefPubMedPubMedCentral Salmiheimo A, Mustonen H, Stenman UH, et al. Systemic inflammatory response and elevated tumour markers predict worse survival in resectable pancreatic ductal adenocarcinoma. PLoS ONE. 2016;11(9):e0163064.CrossRefPubMedPubMedCentral
12.
go back to reference Poruk KE, Blackford AL, Weiss MJ, et al. Circulating tumor cells expressing markers of tumor initiating cells predict poor survival and cancer recurrence in patients with pancreatic ductal adenocarcinoma. Clin Cancer Res. 2017;23(11):2681–2690.CrossRefPubMed Poruk KE, Blackford AL, Weiss MJ, et al. Circulating tumor cells expressing markers of tumor initiating cells predict poor survival and cancer recurrence in patients with pancreatic ductal adenocarcinoma. Clin Cancer Res. 2017;23(11):2681–2690.CrossRefPubMed
13.
go back to reference Haider S, Wang J, Nagano A, et al. A multi-gene signature predicts outcome in patients with pancreatic ductal adenocarcinoma. Genome Med. 2014;6(12):105.CrossRefPubMedPubMedCentral Haider S, Wang J, Nagano A, et al. A multi-gene signature predicts outcome in patients with pancreatic ductal adenocarcinoma. Genome Med. 2014;6(12):105.CrossRefPubMedPubMedCentral
15.
go back to reference Marchegiani G, Andrianello S, Malleo G, et al. Does size matter in pancreatic cancer?: Reappraisal of tumour dimension as a predictor of outcome beyond the TNM. Ann Surg. 2017;266(1):142–148.CrossRefPubMed Marchegiani G, Andrianello S, Malleo G, et al. Does size matter in pancreatic cancer?: Reappraisal of tumour dimension as a predictor of outcome beyond the TNM. Ann Surg. 2017;266(1):142–148.CrossRefPubMed
16.
go back to reference Zhang H, Graham CM, Elci O, et al. Locally advanced squamous cell carcinoma of the head and neck: CT texture and histogram analysis allow independent prediction of overall survival in patients treated with induction chemotherapy. Radiology. 2013;269(3):801-809.CrossRefPubMed Zhang H, Graham CM, Elci O, et al. Locally advanced squamous cell carcinoma of the head and neck: CT texture and histogram analysis allow independent prediction of overall survival in patients treated with induction chemotherapy. Radiology. 2013;269(3):801-809.CrossRefPubMed
17.
go back to reference Win T, Miles KA, Janes SM, et al. Tumor heterogeneity and permeability as measured on the CT component of PET/CT predict survival in patients with non-small cell lung cancer. Clin Cancer Res. 2013;19(13):3591–3599.CrossRefPubMed Win T, Miles KA, Janes SM, et al. Tumor heterogeneity and permeability as measured on the CT component of PET/CT predict survival in patients with non-small cell lung cancer. Clin Cancer Res. 2013;19(13):3591–3599.CrossRefPubMed
18.
go back to reference Simpson AL, Adams LB, Allen PJ, et al. Texture analysis of preoperative CT images for prediction of postoperative hepatic insufficiency: a preliminary study. J Am Coll Surg. 2015;220(3):339–346.CrossRefPubMed Simpson AL, Adams LB, Allen PJ, et al. Texture analysis of preoperative CT images for prediction of postoperative hepatic insufficiency: a preliminary study. J Am Coll Surg. 2015;220(3):339–346.CrossRefPubMed
19.
go back to reference Aerts HJ, Velazquez ER, Leijenaar RT, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMedPubMedCentral Aerts HJ, Velazquez ER, Leijenaar RT, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMedPubMedCentral
20.
go back to reference Al-Hawary MM, Francis IR, Chari ST, et al. Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the Society of Abdominal Radiology and the American Pancreatic Association. Radiology. 2014;270(1):248–260.CrossRefPubMed Al-Hawary MM, Francis IR, Chari ST, et al. Pancreatic ductal adenocarcinoma radiology reporting template: consensus statement of the Society of Abdominal Radiology and the American Pancreatic Association. Radiology. 2014;270(1):248–260.CrossRefPubMed
21.
go back to reference Haralick Shanmugam K, Dinstein IR. Textural Features for Image Classification. IEEE Trans Syst Man Cybern. 1973;SMC-3(6):610–621. Haralick Shanmugam K, Dinstein IR. Textural Features for Image Classification. IEEE Trans Syst Man Cybern. 1973;SMC-3(6):610–621.
22.
go back to reference Tang X. Texture information in run-length matrices. IEEE Trans Image Process. 1998;7(11):1602–1609.CrossRefPubMed Tang X. Texture information in run-length matrices. IEEE Trans Image Process. 1998;7(11):1602–1609.CrossRefPubMed
23.
go back to reference Ojala T, Pietikäinen M, Harwood D. A comparative study of texture measures with classification based on feature distributions. Pattern Recognit. 1996;29(1):51–59.CrossRef Ojala T, Pietikäinen M, Harwood D. A comparative study of texture measures with classification based on feature distributions. Pattern Recognit. 1996;29(1):51–59.CrossRef
24.
go back to reference Buczkowski S, Hildgen P, Cartilier L. Measurements of fractal dimension by box-counting: a critical analysis of data scatter. Physica A. 1998;252(1–2):23–34.CrossRef Buczkowski S, Hildgen P, Cartilier L. Measurements of fractal dimension by box-counting: a critical analysis of data scatter. Physica A. 1998;252(1–2):23–34.CrossRef
25.
go back to reference Chakraborty J, Rangayyan RM, Banik S, Mukhopadhyay S, Leo Desautels JE. Statistical measures of orientation of texture for the detection of architectural distortion in prior mammograms of interval-cancer. J Electron Imaging. 2012;21(3):33010–33013.CrossRef Chakraborty J, Rangayyan RM, Banik S, Mukhopadhyay S, Leo Desautels JE. Statistical measures of orientation of texture for the detection of architectural distortion in prior mammograms of interval-cancer. J Electron Imaging. 2012;21(3):33010–33013.CrossRef
27.
go back to reference Yoon SH, Lee JM, Cho JY, et al. Small (≤ 20 mm) pancreatic adenocarcinomas: analysis of enhancement patterns and secondary signs with multiphasic multidetector CT. Radiology. 2011;259(2):442–452.CrossRefPubMed Yoon SH, Lee JM, Cho JY, et al. Small (≤ 20 mm) pancreatic adenocarcinomas: analysis of enhancement patterns and secondary signs with multiphasic multidetector CT. Radiology. 2011;259(2):442–452.CrossRefPubMed
28.
go back to reference Kim JH, Park SH, Yu ES, et al. Visually isoattenuating pancreatic adenocarcinoma at dynamic-enhanced CT: frequency, clinical and pathologic characteristics, and diagnosis at imaging examinations. Radiology. 2010;257(1):87–96.CrossRefPubMed Kim JH, Park SH, Yu ES, et al. Visually isoattenuating pancreatic adenocarcinoma at dynamic-enhanced CT: frequency, clinical and pathologic characteristics, and diagnosis at imaging examinations. Radiology. 2010;257(1):87–96.CrossRefPubMed
29.
go back to reference Ichikawa T. A comparative study of histopathological findings and CT images related to pancreatic carcinomas. An attempt at diagnosis in tissue characterization by CT [in Japanese]. Nihon Ika Daigaku Zasshi. 1992;59(3):23–29. Ichikawa T. A comparative study of histopathological findings and CT images related to pancreatic carcinomas. An attempt at diagnosis in tissue characterization by CT [in Japanese]. Nihon Ika Daigaku Zasshi. 1992;59(3):23–29.
30.
go back to reference Vyas SJ, Puri YS, John BJ, et al. Radiological tumor density and lymph node size correlate with survival in resectable adenocarcinoma of the pancreatic head: a retrospective cohort study. J Cancer Res Ther. 2016;12(1):417–421.CrossRefPubMed Vyas SJ, Puri YS, John BJ, et al. Radiological tumor density and lymph node size correlate with survival in resectable adenocarcinoma of the pancreatic head: a retrospective cohort study. J Cancer Res Ther. 2016;12(1):417–421.CrossRefPubMed
31.
go back to reference Yue Y, Osipov A, Fraass B, et al. Identifying prognostic intratumor heterogeneity using pre- and post-radiotherapy 18F-FDG PET images for pancreatic cancer patients. J Gastrointest Oncol. 2017;8(1):127–138.CrossRefPubMedPubMedCentral Yue Y, Osipov A, Fraass B, et al. Identifying prognostic intratumor heterogeneity using pre- and post-radiotherapy 18F-FDG PET images for pancreatic cancer patients. J Gastrointest Oncol. 2017;8(1):127–138.CrossRefPubMedPubMedCentral
32.
go back to reference Yamamoto T, Sugiura T, Mizuno T, et al. Preoperative FDG-PET predicts early recurrence and a poor prognosis after resection of pancreatic adenocarcinoma. Ann Surg Oncol. 2015;22(2):677–684.CrossRefPubMed Yamamoto T, Sugiura T, Mizuno T, et al. Preoperative FDG-PET predicts early recurrence and a poor prognosis after resection of pancreatic adenocarcinoma. Ann Surg Oncol. 2015;22(2):677–684.CrossRefPubMed
33.
go back to reference Hyun SH, Kim HS, Choi SH, et al. Intratumoral heterogeneity of 18F-FDG uptake predicts survival in patients with pancreatic ductal adenocarcinoma. Eur J Nucl Med Mol Imaging. 2016;43(8):1461–1468.CrossRefPubMed Hyun SH, Kim HS, Choi SH, et al. Intratumoral heterogeneity of 18F-FDG uptake predicts survival in patients with pancreatic ductal adenocarcinoma. Eur J Nucl Med Mol Imaging. 2016;43(8):1461–1468.CrossRefPubMed
34.
go back to reference Okada T, Linguraru MG, Hori M, Summers RM, Tomiyama N, Sato Y. Abdominal multi-organ segmentation from CT images using conditional shape-location and unsupervised intensity priors. Med Image Anal. 2015;26(1):1–18.CrossRefPubMedPubMedCentral Okada T, Linguraru MG, Hori M, Summers RM, Tomiyama N, Sato Y. Abdominal multi-organ segmentation from CT images using conditional shape-location and unsupervised intensity priors. Med Image Anal. 2015;26(1):1–18.CrossRefPubMedPubMedCentral
35.
go back to reference Cai J, Lu L, Zhang Z, Xing F, Yang L, Yin Q. Pancreas Segmentation in MRI using Graph-Based Decision Fusion on Convolutional Neural Networks. Med Image Comput Comput Assist Interv. 2016;9901:442-450.PubMedPubMedCentral Cai J, Lu L, Zhang Z, Xing F, Yang L, Yin Q. Pancreas Segmentation in MRI using Graph-Based Decision Fusion on Convolutional Neural Networks. Med Image Comput Comput Assist Interv. 2016;9901:442-450.PubMedPubMedCentral
Metadata
Title
Survival Prediction in Pancreatic Ductal Adenocarcinoma by Quantitative Computed Tomography Image Analysis
Authors
Marc A. Attiyeh, MD
Jayasree Chakraborty, PhD
Alexandre Doussot, MD, PhD
Liana Langdon-Embry, BA
Shiana Mainarich
Mithat Gönen, PhD
Vinod P. Balachandran, MD
Michael I. D’Angelica, MD
Ronald P. DeMatteo, MD
William R. Jarnagin, MD
T. Peter Kingham, MD
Peter J. Allen, MD
Amber L. Simpson, PhD
Richard K. Do, MD, PhD
Publication date
01-04-2018
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 4/2018
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-017-6323-3

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