Contrast-enhanced CT radiomics for predicting lymph node metastasis in pancreatic ductal adenocarcinoma: a pilot study

Ke Li1, Qiandong Yao2, Jingjing Xiao3, Meng Li3, Jiali Yang4, Wenjing Hou1, Mingshan Du1, Kang Chen1, Yuan Qu1, Lian Li1, Jing Li1, Xianqi Wang1, Haoran Luo1, Jia Yang4, Zhuoli Zhang5, Wei Chen1
1Department of Radiology, Southwest Hospital, Army Medical University, Chongqing, 400038, China
2Department of Radiology, Sichuan Science City Hospital, Mianyang, Sichuan, China
3Department of Medical Engineering, Xinqiao Hospital, Army Medical University, Chongqing, China
4Hepatopancreatobiliary Surgery, Southwest Hospital, Army Medical University, Chongqing, China
5Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

Tóm tắt

Abstract Background

We developed a computational model integrating clinical data and imaging features extracted from contrast-enhanced computed tomography (CECT) images, to predict lymph node (LN) metastasis in patients with pancreatic ductal adenocarcinoma (PDAC).

Methods

This retrospective study included 159 patients with PDAC (118 in the primary cohort and 41 in the validation cohort) who underwent preoperative contrast-enhanced computed tomography examination between 2012 and 2015. All patients underwent surgery and lymph node status was determined. A total of 2041 radiomics features were extracted from venous phase images in the primary cohort, and optimal features were extracted to construct a radiomics signature. A combined prediction model was built by incorporating the radiomics signature and clinical characteristics selected by using multivariable logistic regression. Clinical prediction models were generated and used to evaluate both cohorts.

Results

Fifteen features were selected for constructing the radiomics signature based on the primary cohort. The combined prediction model for identifying preoperative lymph node metastasis reached a better discrimination power than the clinical prediction model, with an area under the curve of 0.944 vs. 0.666 in the primary cohort, and 0.912 vs. 0.713 in the validation cohort.

Conclusions

This pilot study demonstrated that a noninvasive radiomics signature extracted from contrast-enhanced computed tomography imaging can be conveniently used for preoperative prediction of lymph node metastasis in patients with PDAC.

Từ khóa


Tài liệu tham khảo

Siegel RL, Miller KD, Dvm AJ. Cancer statistics, 2018. Ca A Cancer J Clin. 2018;68:11.

Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74:2913–21.

Hidalgo M. Pancreatic cancer. N Engl J Med. 2010;362:1605–17.

Zhang Q, Zeng L, Chen Y, Lian G, Qian C, Chen S, Li J, Huang K. Pancreatic Cancer epidemiology, detection, and management. Gastroenterol Res Pract. 2016;2016:8962321.

Dimastromatteo J, Houghton JL, Lewis JS, Kelly KA. Challenges of pancreatic Cancer. Cancer J. 2015;21:188–93.

Conroy T, Bachet JB, Ayav A, Huguet F, Lambert A, Caramella C, Marechal R, Van Laethem JL, Ducreux M. Current standards and new innovative approaches for treatment of pancreatic cancer. Eur J Cancer. 2016;57:10–22.

Basturk O, Saka B, Balci S, Postlewait LM, Knight J, Goodman M, Kooby D, Sarmiento JM, El-Rayes B, Choi H, et al. Substaging of lymph node status in resected pancreatic ductal adenocarcinoma has strong prognostic correlations: proposal for a revised N classification for TNM staging. Ann Surg Oncol. 2015;22(Suppl 3):S1187–95.

Paiella S, Sandini M, Gianotti L, Butturini G, Salvia R, Bassi C. The prognostic impact of Para-aortic lymph node metastasis in pancreatic cancer: a systematic review and meta-analysis. Eur J Surg Oncol. 2016;42:616–24.

Tol JA, Gouma DJ, Bassi C, Dervenis C, Montorsi M, Adham M, Andren-Sandberg A, Asbun HJ, Bockhorn M, Buchler MW, et al. Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the international study group on pancreatic surgery (ISGPS). Surgery. 2014;156:591–600.

Tran Cao HS, Zhang Q, Sada YH, Silberfein EJ, Hsu C, Van Buren G 2nd, Chai C, MHG K, Fisher WE, Massarweh NN. Value of lymph node positivity in treatment planning for early stage pancreatic cancer. Surgery. 2017;162:557–67.

Moriya T, Kimura W, Hirai I, Takasu N, Mizutani M. Expression of MUC1 and MUC2 in ampullary cancer. Int J Surg Pathol. 2011;19:441–7.

Wang SC, Parekh JR, Porembka MR, Nathan H, D'Angelica MI, DeMatteo RP, Fong Y, Kingham TP, Jarnagin WR, Allen PJ. A pilot study evaluating serum MMP7 as a preoperative prognostic marker for pancreatic ductal adenocarcinoma patients. J Gastrointest Surg. 2016;20:899–904.

Tao L, Zhang L, Peng Y, Tao M, Li G, Xiu D, Yuan C, Ma C, Jiang B. Preoperative neutrophil-to-lymphocyte ratio and tumor-related factors to predict lymph node metastasis in patients with pancreatic ductal adenocarcinoma (PDAC). Oncotarget. 2016;7:74314–24.

Roche CJ, Hughes ML, Garvey CJ, Campbell F, White DA, Jones L, Neoptolemos JP. CT and pathologic assessment of prospective nodal staging in patients with ductal adenocarcinoma of the head of the pancreas. AJR Am J Roentgenol. 2003;180:475–80.

Brizi MG, Natale L, Manfredi R, Barbaro B, Vecchioli A, Marano P. Staging of pancreatic ductal adenocarcinoma with spiral CT and MRI. Rays. 2001;26:151–9.

Tseng DS, van Santvoort HC, Fegrachi S, Besselink MG, Zuithoff NP, Borel Rinkes IH, van Leeuwen MS, Molenaar IQ. Diagnostic accuracy of CT in assessing extra-regional lymphadenopathy in pancreatic and peri-ampullary cancer: a systematic review and meta-analysis. Surg Oncol. 2014;23:229–35.

Fong ZV, Tan WP, Lavu H, Kennedy EP, Mitchell DG, Koniaris LG, Sauter PK, Rosato EL, Yeo CJ, Winter JM. Preoperative imaging for resectable periampullary cancer: clinicopathologic implications of reported radiographic findings. J Gastrointest Surg. 2013;17:1098–106.

Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, Bussink J, Monshouwer R, Haibe-Kains B, Rietveld D, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.

Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, They Are Data. Radiology. 2016;278:563–77.

Huang Y, Liu Z, He L, Chen X, Pan D, Ma Z, Liang C, Tian J, Liang C. Radiomics signature: a potential biomarker for the prediction of disease-free survival in early-stage (I or II) non-small cell lung Cancer. Radiology. 2016;281:947–57.

Yip SS, Aerts HJ. Applications and limitations of radiomics. Phys Med Biol. 2016;61:R150–66.

Permuth JB, Choi J, Balarunathan Y, Kim J, Chen DT, Chen L, Orcutt S, Doepker MP, Gage K, Zhang G, et al. Combining radiomic features with a miRNA classifier may improve prediction of malignant pathology for pancreatic intraductal papillary mucinous neoplasms. Oncotarget. 2016;7:85785–97.

Hanania AN, Bantis LE, Feng Z, Wang H, Tamm EP, Katz MH, Maitra A, Koay EJ. Quantitative imaging to evaluate malignant potential of IPMNs. Oncotarget. 2016;7:85776–84.

Li ZS, Li Q. The latest 2010 WHO classification of tumors of digestive system. Zhonghua Bing Li Xue Za Zhi. 2011;40:351–4.

Chun YS, Pawlik TM, Vauthey JN. 8th edition of the AJCC Cancer staging manual: pancreas and Hepatobiliary cancers. Ann Surg Oncol. 2018;25:845–7.

Fargnoli R, Fusi I. Computerized tomography of pancreatic tumors. Tumori. 1999;85:S3–5.

de Savornin Lohman EAJ, de Bitter TJJ, van Laarhoven C, Hermans JJ, de Haas RJ, de Reuver PR. The diagnostic accuracy of CT and MRI for the detection of lymph node metastases in gallbladder cancer: a systematic review and meta-analysis. Eur J Radiol. 2019;110:156–62.

Sauerbrei W, Royston P, Binder H. Selection of important variables and determination of functional form for continuous predictors in multivariable model building. Stat Med. 2007;26:5512–28.

Kramer AA, Zimmerman JE. Assessing the calibration of mortality benchmarks in critical care: the Hosmer-Lemeshow test revisited. Crit Care Med. 2007;35:2052–6.

Vickers AJ, Cronin AM, Elkin EB, Gonen M. Extensions to decision curve analysis, a novel method for evaluating diagnostic tests, prediction models and molecular markers. Bmc Med Inform Decis Mak. 2008;8:53.

Shin D W, Lee J, Kim J, et al. Validation of the American Joint Committee on Cancer 8th edition staging system for the pancreatic ductal adenocarcinoma. Eur J Surg Oncol. 2019;45(11):2159–65.

Murakami Y, Uemura K, Sudo T, Hashimoto Y, Yuasa Y, Sueda T. Prognostic impact of Para-aortic lymph node metastasis in pancreatic ductal adenocarcinoma. World J Surg. 2010;34:1900–7.

Kim SH, Hwang HK, Lee WJ, Kang CM. Identification of an N staging system that predicts oncologic outcome in resected left-sided pancreatic cancer. Medicine (Baltimore). 2016;95:e4035.

Showalter TN, Winter KA, Berger AC, Regine WF, Abrams RA, Safran H, Hoffman JP, Benson AB, MacDonald JS, Willett CG. The influence of total nodes examined, number of positive nodes, and lymph node ratio on survival after surgical resection and adjuvant chemoradiation for pancreatic cancer: a secondary analysis of RTOG 9704. Int J Radiat Oncol Biol Phys. 2011;81:1328–35.

Roland CL, Yang AD, Katz MH, Chatterjee D, Wang H, Lin H, Vauthey JN, Pisters PW, Varadhachary GR, Wolff RA, et al. Neoadjuvant therapy is associated with a reduced lymph node ratio in patients with potentially resectable pancreatic cancer. Ann Surg Oncol. 2015;22:1168–75.

Delpero JR, Jeune F, Bachellier P, Regenet N, Le Treut YP, Paye F, Carrere N, Sauvanet A, Adham M, Autret A, et al. Prognostic value of resection margin involvement after Pancreaticoduodenectomy for ductal adenocarcinoma: updates from a French prospective multicenter study. Ann Surg. 2017;266:787–96.

Zhou G, Niu L, Chiu D, He L, Xu K. Changes in the expression of serum markers CA242, CA199, CA125, CEA, TNF-alpha and TSGF after cryosurgery in pancreatic cancer patients. Biotechnol Lett. 2012;34:1235–41.

Cui D, Peng Y, Zhang C, et al. Macrophage migration inhibitory factor mediates metabolic dysfunction induced by atypical antipsychotic therapy. J Clin Invest. 2018;128(11):4997–5007.

Kickingereder P, Gotz M, Muschelli J, Wick A, Neuberger U, Shinohara RT, Sill M, Nowosielski M, Schlemmer HP, Radbruch A, et al. Large-scale Radiomic profiling of recurrent Glioblastoma identifies an imaging predictor for stratifying anti-Angiogenic treatment response. Clin Cancer Res. 2016;22:5765–71.

Eilaghi A, Baig S, Zhang Y, Zhang J, Karanicolas P, Gallinger S, Khalvati F, Haider MA. CT texture features are associated with overall survival in pancreatic ductal adenocarcinoma - a quantitative analysis. BMC Med Imaging. 2017;17:38.

Cassinotto C, Chong J, Zogopoulos G, Reinhold C, Chiche L, Lafourcade JP, Cuggia A, Terrebonne E, Dohan A, Gallix B. Resectable pancreatic adenocarcinoma: role of CT quantitative imaging biomarkers for predicting pathology and patient outcomes. Eur J Radiol. 2017;90:152–8.

Attiyeh MA, Chakraborty J, Doussot A, Langdon-Embry L, Mainarich S, Gonen M, Balachandran VP, D'Angelica MI, DeMatteo RP, Jarnagin WR, et al. Survival prediction in pancreatic ductal adenocarcinoma by quantitative computed tomography image analysis. Ann Surg Oncol. 2018;25:1034–42.

Lynn MA, Tumes DJ, Choo JM, Sribnaia A, Blake SJ, Leong LEX, Young GP, Marshall HS, Wesselingh SL, Rogers GB, et al. Early-life antibiotic-driven Dysbiosis leads to Dysregulated vaccine immune responses in mice. Cell Host Microbe. 2018;23:653–60 e655.

Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a Radiomics Nomogram for preoperative prediction of lymph node metastasis in colorectal Cancer. J Clin Oncol. 2016;34:2157–64.