Abstract
Purpose
To investigate the value of texture analysis on unenhanced computed tomography (CT) to potentially differentiate mass-forming pancreatitis (MFP) from pancreatic ductal adenocarcinoma (PDAC).
Methods
A retrospective study consisting of 109 patients (30 MFP patients vs 79 PDAC patients) who underwent preoperative unenhanced CT between January 2012 and December 2017 was performed. Synthetic minority oversampling technique (SMOTE) algorithm was adopted to reconstruct and balance MFP and PDAC samples. A total of 396 radiomic features were extracted from unenhanced CT images. Mann–Whitney U test and minimum redundancy maximum relevance (MRMR) methods were used for the purpose of dimension reduction. Predictive models were constructed using random forest (RF) method, and were validated using leave group out cross-validation (LGOCV) method. Diagnostic performance of the predictive model, including sensitivity, specificity, accuracy, positive predicting value (PPV), and negative predicting value (NPV), was recorded.
Results
We applied 200% of SMOTE to MFP and PDAC patients, resulting in 90 MFP patients compared with 120 PDAC patients. Dimension reduction steps yielded 30 radiomic features using Mann–Whitney U test and MRMR methods. Ten radiomic features were retained using RF method. Four most predictive parameters, including GreyLevelNonuniformity_angle90_offset1, VoxelValueSum, HaraVariance, and ClusterProminence_AllDirection_offset1_SD, were used to generate the predictive model with preferable 92.2% sensitivity, 94.2% specificity, 93.3% accuracy, 92.2% PPV, and 94.2% NPV. Finally, in LGOCV analysis, a high pooled mean sensitivity, specificity, and accuracy (82.6%, 80.8%, and 82.1%, respectively) indicate a relatively reliable and stable predictive model.
Conclusions
Unenhanced CT texture analysis can be a promising noninvasive method in discriminating MFP from PDAC.
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References
Pourshams A, Sepanlou SG, Ikuta KS, Bisignano C, Safiri S, Roshandel G, Sharif M, Khatibian M, Fitzmaurice C, Nixon MR, Abbasi N, Afarideh M, Ahmadian E, Akinyemiju T, Alahdab F, Alam T, Alipour V, Allen CA, Anber NH, Ansari-Moghaddam A, Arabloo J, Badawi A, Bagherzadeh M, Belayneh YM, Biadgo B, Bijani A, Biondi A, Bjørge T, Borzì AM, Bosetti C, Briko AN, Briko NI, Carreras G, Carvalho F, Choi JYJ, Chu DT, Dang AK, Daryani A, Davitoiu DV, Demoz GT, Desai R, Dey S, Do HT, Do HP, Eftekhari A, Esteghamati A, Farzadfar F, Fernandes E, Filip I, Fischer F, Foroutan M, Gad MM, Gallus S, Geta B, Gorini G, Hafezi-Nejad N, Harvey JD, Hasankhani M, Hasanzadeh A, Hassanipour S, Hay SI, Hidru HD, Hoang CL, Hostiuc S, Househ M, Ilesanmi OS, Ilic MD, Irvani SSN, Jafari Balalami N, James SL, Joukar F, Kasaeian A, Kassa TD, Kengne AP, Khalilov R, Khan EA, Khater A, Khosravi Shadmani F, Kocarnik JM, Komaki H, Koyanagi A, Kumar V, La Vecchia C, Lopukhov PD, Manafi F, Manafi N, Manda AL, Mansour-Ghanaei F, Mehta D, Mehta V, Meier T, Meles HG, Mengistu G, Miazgowski T, Mohamadnejad M, Mohammadian-Hafshejani A, Mohammadoo-Khorasani M, Mohammed S, Mohebi F, Mokdad AH, Monasta L, Moossavi M, Moradzadeh R, Naik G, Negoi I, Nguyen CT, Nguyen LH, Nguyen TH, Olagunju AT, Olagunju TO, Pennini A, Rabiee M, Rabiee N, Radfar A, Rahimi M, Rath GK, Rawaf DL, Rawaf S, Reiner RC, Rezaei N, Rezapour A, Saad AM, Saadatagah S, Sahebkar A, Salimzadeh H, Samy AM, Sanabria J, Sarveazad A, Sawhney M, Sekerija M, Shabalkin P, Shaikh MA, Sharma R, Sheikhbahaei S, Shirkoohi R, Siddappa Malleshappa SK, Sisay M, Soreide K, Soshnikov S, Sotoudehmanesh R, Starodubov VI, Subart ML, Tabarés-Seisdedos R, Tadesse DBB, Traini E, Tran BX, Tran KB, Ullah I, Vacante M, Vahedian-Azimi A, Varavikova E, Westerman R, Wondafrash DDZ, Xu R, Yonemoto N, Zadnik V, Zhang ZJ, Malekzadeh R, Naghavi M (2019) The global, regional, and national burden of pancreatic cancer and its attributable risk factors in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol 4: 934–947. https://doi.org/10.1016/S2468-1253(19)30347-4
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68: 394-424. https://doi.org/10.1002/ijc.31937
Kleeff J, Korc M, Apte M, La Vecchia C, Johnson CD, Biankin AV, Neale RE, Tempero M, Tuveson DA, Hruban RH (2016) Pancreatic Cancer. Nat Rev Dis Primers 2: 16022. https://doi.org/10.1038/nrdp.2016.22
Zou X,Wei J,Huang Z,Zhou X,Lu Z,Zhu W,Miao Y (2019) Identification of a six-miRNA panel in serum benefiting pancreatic cancer diagnosis. Cancer Med 8: 2810-2822. https://doi.org/10.1002/cam4.2145
Yadav AK, Sharma R, Kandasamy D, Pradhan RK, Garg PK, Bhalla AS, Gamanagatti S, Srivastava DN, Sahni P, Upadhyay AD (2016) Perfusion CT – Can it resolve the pancreatic carcinoma versus mass forming chronic pancreatitis conundrum? Pancreatology 16: 979–987. https://doi.org/10.1016/j.pan.2016.08.011
Muhi A, Ichikawa T, Motosugi U, Sou H, Sano K, Tsukamoto T, Fatima Z, Araki T (2012) Mass-forming autoimmune pancreatitis and pancreatic carcinoma: differential diagnosis on the basis of computed tomography and magnetic resonance cholangiopancreatography, and diffusion-weighted imaging findings. J Magn Reson Imaging 35: 827–836. https://doi.org/10.1002/jmri.22881
Aslan S, Nural MS, Camlidag I, Danaci M (2019) Efficacy of perfusion CT in differentiating of pancreatic ductal adenocarcinoma from mass-forming chronic pancreatitis and characterization of isoattenuating pancreatic lesions. Abdom Radiol (NY) 44: 593–603. https://doi.org/10.1007/s00261-018-1776-9
Yin Q, Zou X, Zai X, Wu Z, Wu Q, Jiang X, Chen H, Miao F (2015) Pancreatic ductal adenocarcinoma and chronic mass-forming pancreatitis: Differentiation with dual-energy MDCT in spectral imaging mode. Eur J Radiol 84: 2470–2476. https://doi.org/10.1016/j.ejrad.2015.09.023
Ruan Z, Jiao J, Min D, Qu J, Li J, Chen J, Li Q, Wang C (2018) Multi-modality imaging features distinguish pancreatic carcinoma from mass-forming chronic pancreatitis of the pancreatic head. Oncol Lett 15: 9735–9744. https://doi.org/10.3892/ol.2018.8545
Wolske KM, Ponnatapura J, Kolokythas O, Burke LMB, Tappouni R, Lalwani N (2019) Chronic Pancreatitis or Pancreatic Tumor? A Problem-solving Approach. Radiographics 39: 1965–1982. https://doi.org/10.1148/rg.2019190011
Leung TK, Lee CM, Wang FC, Chen HC, Wang HJ (2005) Difficulty with diagnosis of malignant pancreatic neoplasms coexisting with chronic pancreatitis. World J Gastroenterol 11: 5075–5078. https://doi.org/10.3748/wjg.v11.i32.5075
Tajima Y, Kuroki T, Tsutsumi R, Isomoto I, Uetani M, Kanematsu T (2007) Pancreatic carcinoma coexisting with chronic pancreatitis versus tumor-forming pancreatitis: Diagnostic utility of the time-signal intensity curve from dynamic contrast-enhanced MR imaging. World J Gastroenterol 13: 858–865. https://doi.org/10.3748/wjg.v13.i6.858
Fritscher-Ravens A, Brand L, Knöfel WT, Bobrowski C, Topalidis T, Thonke F, de Werth A, Soehendra N (2002) Comparison of endoscopic ultrasound-guided fine needle aspiration for focal pancreatic lesions in patients with normal parenchyma and chronic pancreatitis. Am J Gastroentero 97: 2768–2775. https://doi.org/10.1111/j.1572-0241.2002.07020.x
Chu LC, Goggins MG, Fishman EK (2017) Diagnosis and Detection of Pancreatic Cancer. Cancer J 23: 333-342. https://doi.org/10.1097/PPO.0000000000000290
Gonoi W, Hayashi TY, Okuma H, Akahane M, Nakai Y, Mizuno S, Tateishi R, Isayama H, Koike K, Ohtomo K (2017) Development of pancreatic cancer is predictable well in advance using contrast-enhanced CT: a case–cohort study. Eur Radiol 27: 4941–4950. https://doi.org/10.1007/s00330-017-4895-8
Lubner MG, Smith AD, Sandrasegaran K, Sahani DV, Pickhardt PJ (2017) CT Texture Analysis : Definitions, Applications, Biologic Correlates, and Challenges. Radiographics 37: 1483-1503. https://doi.org/10.1148/rg.2017170056
Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: Images Are More than Pictures, They Are Data. Radiology 278: 563-577. https://doi.org/10.1148/radiol.2015151169
De Robertis R, Cardobi N, Ortolani S, Tinazzi Martini P, Stemmer A, Grimm R, Gobbo S, Butturini G, D’Onofrio M (2019) Intravoxel incoherent motion diffusion-weighted MR imaging of solid pancreatic masses: reliability and usefulness for characterization. Abdom Radiol (NY) 44:131-139. https://doi.org/10.1007/s00261-018-1684-z
Choi MH, Lee YJ, Yoon SB, Choi JI, Jung SE, Rha SE (2019) MRI of pancreatic ductal adenocarcinoma: texture analysis of T2-weighted images for predicting long-term outcome. Abdom Radiol (NY) 44:122-130. https://doi.org/10.1007/s00261-018-1681-2
De Robertis R, Maris B, Cardobi N, Tinazzi Martini P, Gobbo S, Capelli P, Ortolani S, Cingarlini S, Paiella S (2018) Can histogram analysis of MR images predict aggressiveness in pancreatic neuroendocrine tumors? Eur Radiol 28:2582-2591. https://doi.org/10.1007/s00330-017-5236-7
D’Onofrio M, Ciaravino V, Cardobi N, De Robertis R, Cingarlini S, Landoni L, Capelli P, Bassi C, Scarpa A (2019) CT Enhancement and 3D Texture Analysis of Pancreatic Neuroendocrine Neoplasms. Sci Rep 9:2176. https://doi.org/10.1038/s41598-018-38459-6
Kocak B, Durmaz ES, Ates E, Kaya OK, Kilickesmez O (2019) Unenhanced CT Texture Analysis of Clear Cell Renal Cell Carcinomas: A Machine Learning–Based Study for Predicting Histopathologic Nuclear Grade. AJR Am J Roentgenol. [Epub ahead of print] https://doi.org/10.2214/AJR.18.20742
Collewet G, Strzelecki M, Mariette F (2004) Influence of MRI acquisition protocols and image intensity normalization methods on texture classification. Magn Reson Imaging 22: 81–91. https://doi.org/10.1016/j.mri.2003.09.001
Shafiq-Ul-Hassan M, Zhang GG, Latifi K, Ullah G, Hunt DC, Balagurunathan Y, Abdalah MA, Schabath MB, Goldgof DG, Mackin D, Court LE, Gillies RJ, Moros EG (2017) Intrinsic dependencies of CT radiomic features on voxel size and number of gray levels. Med Phys 44: 1050–1062. https://doi.org/10.1002/mp.12123
Hodgdon T,McInnes MD,Schieda N,Flood TA,Lamb L,Thornhill RE (2015) Can Quantitative CT Texture Analysis be Used to Differentiate Fat-poor Renal Angiomyolipoma from Renal Cell Carcinoma on Unenhanced CT Images? Radiology 276:787-96. https://doi.org/10.1148/radiol.2015142215
Nakamura M, Kajiwara Y, Otsuka A, Kimura H (2013) LVQ-SMOTE - Learning Vector Quantization based Synthetic Minority Over-sampling Technique for biomedical data. BioData Min 6: 16. https://doi.org/10.1186/1756-0381-6-16
Gu D, Hu Y, Ding H, Wei J, Chen K, Liu H, Zeng M, Tian J (2019) CT radiomics may predict the grade of pancreatic neuroendocrine tumors: a multicenter study. Eur Radiol 29: 6880-6890. https://doi.org/10.1007/s00330-019-06176-x
Yang J, Guo X, Ou X, Zhang W, Ma X (2019) Discrimination of Pancreatic Serous Cystadenomas From Mucinous Cystadenomas With CT Textural Features : Based on Machine Learning. Front Oncol 9: 494. https://doi.org/10.3389/fonc.2019.00494
Ren S, Chen X, Wang Z, Zhao R, Wang J, Cui W, Wang Z (2019) Differentiation of hypovascular pancreatic neuroendocrine tumors from pancreatic ductal adenocarcinoma using contrast-enhanced computed tomography. PLoS One 14: e0211566. https://doi.org/10.1371/journal.pone.0211566
Takahashi N, Leng S, Kitajima K, Gomez-Cardona D, Thapa P, Carter RE, Leibovich BC, Sasiwimonphan K, Sasaguri K, Kawashima A (2015) Small (< 4 cm) renal masses: Differentiation of angiomyolipoma without visible fat from renal cell carcinoma using unenhanced and contrast-enhanced CT. Am J Roentgenol 205: 1194–1202. https://doi.org/10.2214/AJR.14.14183
Cannella R, Borhani AA, Minervini MI, Tsung A, Furlan A (2019) Evaluation of texture analysis for the differential diagnosis of focal nodular hyperplasia from hepatocellular adenoma on contrast-enhanced CT images. Abdom Radiol (NY) 44: 1323–1330. https://doi.org/10.1007/s00261-018-1788-5
Acknowledgements
We thank all authors for their continuous and excellent support with patient data collection, imaging analysis, statistical analysis, and valuable suggestions for the article.
Funding
This study was supported by Jiangsu provincial key research and development program (BE2017772), the National Natural Science Foundation of China (81771899), and Innovative Development Foundation of Department in Jiangsu Hospital of TCM (Y2019CX27).
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Ren, S., Zhao, R., Zhang, J. et al. Diagnostic accuracy of unenhanced CT texture analysis to differentiate mass-forming pancreatitis from pancreatic ductal adenocarcinoma. Abdom Radiol 45, 1524–1533 (2020). https://doi.org/10.1007/s00261-020-02506-6
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DOI: https://doi.org/10.1007/s00261-020-02506-6