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CT texture analysis in the differentiation of major renal cell carcinoma subtypes and correlation with Fuhrman grade

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Abstract

Objective

CT texture analysis (CTTA) using filtration-histogram–based parameters has been associated with tumor biologic correlates such as glucose metabolism, hypoxia, and tumor angiogenesis. We investigated the utility of these parameters for differentiation of clear cell from papillary renal cancers and prediction of Fuhrman grade.

Methods

A retrospective study was performed by applying CTTA to pretreatment contrast-enhanced CT scans in 290 patients with 298 histopathologically confirmed renal cell cancers of clear cell and papillary types. The largest cross section of the tumor on portal venous phase axial CT was chosen to draw a region of interest. CTTA comprised of an initial filtration step to extract features of different sizes (fine, medium, coarse spatial scales) followed by texture quantification using histogram analysis.

Results

A significant increase in entropy with fine and medium spatial filters was demonstrated in clear cell RCC (p = 0.047 and 0.033, respectively). Area under the ROC curve of entropy at fine and medium spatial filters was 0.804 and 0.841, respectively. An increased entropy value at coarse filter correlated with high Fuhrman grade tumors (p = 0.01). The other texture parameters were not found to be useful.

Conclusion

Entropy, which is a quantitative measure of heterogeneity, is increased in clear cell renal cancers. High entropy is also associated with high-grade renal cancers. This parameter may be considered as a supplementary marker when determining aggressiveness of therapy.

Key points

• CT texture analysis is easy to perform on contrast-enhanced CT.

• CT texture analysis may help to separate different types of renal cancers.

• CT texture analysis may enhance individualized treatment of renal cancers.

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Abbreviations

ccRCC:

Clear cell renal cell carcinoma

CTTA:

Computerized tomography (CT) texture analysis

pRCC:

Papillary renal cell carcinoma

RCC:

Renal cell carcinoma

ROC curve:

Receiver operating characteristic curve

SSF:

Spatial scaling factor associated with CTTA

References

  1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108

    Article  PubMed  Google Scholar 

  2. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Dicker D et al (2015) The global burden of cancer 2013. JAMA Oncol 1:505–527

  3. Moch H, Cubilla AL, Humphrey PA, Reuter VE, Ulbright TM (2016) The 2016 WHO classification of tumours of the urinary system and male genital organs-part a: renal, penile, and testicular tumours. Eur Urol 70:93–105

    Article  PubMed  Google Scholar 

  4. Hsieh JJ, Purdue MP, Signoretti S et al (2017) Renal cell carcinoma. Nat Rev Dis Primers 3:17009

    Article  PubMed  PubMed Central  Google Scholar 

  5. Fuhrman SA, Lasky LC, Limas C (1982) Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6:655–663

    Article  CAS  PubMed  Google Scholar 

  6. Young JR, Coy H, Kim HJ et al (2017) Performance of relative enhancement on multiphasic MRI for the differentiation of clear cell renal cell carcinoma (RCC) from papillary and chromophobe RCC subtypes and oncocytoma. AJR Am J Roentgenol 208:812–819

    Article  PubMed  Google Scholar 

  7. Mytsyk Y, Dutka I, Borys Y et al (2017) Renal cell carcinoma: applicability of the apparent coefficient of the diffusion-weighted estimated by MRI for improving their differential diagnosis, histologic subtyping, and differentiation grade. Int Urol Nephrol 49:215–224

    Article  CAS  PubMed  Google Scholar 

  8. Kasoji SK, Chang EH, Mullin LB, Chong WK, Rathmell WK, Dayton PA (2017) A pilot clinical study in characterization of malignant renal-cell carcinoma subtype with contrast-enhanced ultrasound. Ultrason Imaging 39:126–136

    Article  PubMed  Google Scholar 

  9. Young JR, Margolis D, Sauk S, Pantuck AJ, Sayre J, Raman SS (2013) Clear cell renal cell carcinoma: discrimination from other renal cell carcinoma subtypes and oncocytoma at multiphasic multidetector CT. Radiology 267:444–453

    Article  PubMed  Google Scholar 

  10. Pierorazio PM, Hyams ES, Tsai S et al (2013) Multiphasic enhancement patterns of small renal masses (</=4 cm) on preoperative computed tomography: utility for distinguishing subtypes of renal cell carcinoma, angiomyolipoma, and oncocytoma. Urology 81:1265–1271

    Article  PubMed  Google Scholar 

  11. Cheville JC, Lohse CM, Zincke H, Weaver AL, Blute ML (2003) Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. Am J Surg Pathol 27:612–624

    Article  PubMed  Google Scholar 

  12. Kim JK, Kim TK, Ahn HJ, Kim CS, Kim KR, Cho KS (2002) Differentiation of subtypes of renal cell carcinoma on helical CT scans. AJR Am J Roentgenol 178:1499–1506

    Article  PubMed  Google Scholar 

  13. Miles KA, Ganeshan B, Hayball MP (2013) CT texture analysis using the filtration-histogram method: what do the measurements mean? Cancer Imaging 13:400–406

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA (2013) Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology 266:326–336

    Article  PubMed  Google Scholar 

  15. Goh V, Ganeshan B, Nathan P, Juttla JK, Vinayan A, Miles KA (2011) Assessment of response to tyrosine kinase inhibitors in metastatic renal cell cancer: CT texture as a predictive biomarker. Radiology 261:165–171

    Article  PubMed  Google Scholar 

  16. Yu H, Scalera J, Khalid M et al (2017) Texture analysis as a radiomic marker for differentiating renal tumors. Abdom Radiol (NY). https://doi.org/10.1007/s00261-017-1144-1

    Article  PubMed  Google Scholar 

  17. Raman SP, Chen Y, Schroeder JL, Huang P, Fishman EK (2014) CT texture analysis of renal masses: pilot study using random forest classification for prediction of pathology. Acad Radiol 21:1587–1596

    Article  PubMed  PubMed Central  Google Scholar 

  18. Lubner MG, Stabo N, Abel EJ, Del Rio AM, Pickhardt PJ (2016) CT textural analysis of large primary renal cell carcinomas: pretreatment tumor heterogeneity correlates with histologic findings and clinical outcomes. AJR Am J Roentgenol 207:96–105

    Article  PubMed  Google Scholar 

  19. Chen F, Huhdanpaa H, Desai B et al (2015) Whole lesion quantitative CT evaluation of renal cell carcinoma: differentiation of clear cell from papillary renal cell carcinoma. Springerplus 4:66

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bektas CT, Kocak B, Yardimci AH et al (2018) Clear cell renal cell carcinoma: machine learning-based quantitative computed tomography texture analysis for prediction of Fuhrman nuclear grade. Eur Radiol. https://doi.org/10.1007/s00330-018-5698-2

    Article  PubMed  Google Scholar 

  21. Ng F, Ganeshan B, Kozarski R, Miles KA, Goh V (2013) Assessment of primary colorectal cancer heterogeneity by using whole-tumor texture analysis: contrast-enhanced CT texture as a biomarker of 5-year survival. Radiology 266:177–184

    Article  PubMed  Google Scholar 

  22. Ganeshan B, Miles KA (2013) Quantifying tumour heterogeneity with CT. Cancer Imaging 13:140–149

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ganeshan B, Abaleke S, Young RC, Chatwin CR, Miles KA (2010) Texture analysis of non-small cell lung cancer on unenhanced computed tomography: initial evidence for a relationship with tumour glucose metabolism and stage. Cancer Imaging 10:137–143

    Article  PubMed  PubMed Central  Google Scholar 

  24. Yip C, Landau D, Kozarski R et al (2014) Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology 270:141–148

    Article  PubMed  Google Scholar 

  25. Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K (2012) Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol 67:157–164

    Article  CAS  PubMed  Google Scholar 

  26. Sasaguri K, Takahashi N, Gomez-Cardona D et al (2015) Small (< 4 cm) renal mass: differentiation of oncocytoma from renal cell carcinoma on biphasic contrast-enhanced CT. AJR Am J Roentgenol 205:999–1007

    Article  PubMed  Google Scholar 

  27. Delahunt B, Eble JN, Egevad L, Samaratunga H (2019) Grading of renal cell carcinoma. Histopathology 74:4–17

    Article  PubMed  Google Scholar 

  28. Ding J, Xing Z, Jiang Z et al (2018) CT-based radiomic model predicts high grade of clear cell renal cell carcinoma. Eur J Radiol 103:51–56

    Article  PubMed  Google Scholar 

  29. Zhang X, Wang Y, Yang L et al (2018) Delayed enhancement of the peritumoural cortex in clear cell renal cell carcinoma: correlation with Fuhrman grade. Clin Radiol 73:982 e981-982 e987

    Article  PubMed  Google Scholar 

  30. Gu L, Li H, Wang Z et al (2018) A systematic review and meta-analysis of clinicopathologic factors linked to oncologic outcomes for renal cell carcinoma with tumor thrombus treated by radical nephrectomy with thrombectomy. Cancer Treat Rev 69:112–120

    Article  PubMed  Google Scholar 

  31. Aickin M, Gensler H (1996) Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. Am J Public Health 86:726–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lubner MG, Smith AD, Sandrasegaran K, Sahani DV, Pickhardt PJ (2017) CT texture analysis: definitions, applications, biologic correlates, and challenges. Radiographics 37:1483–1503

    Article  PubMed  Google Scholar 

  33. Sandrasegaran K, Lin Y, Asare-Sawiri M, Taiyini T, Tann M (2019) CT texture analysis of pancreatic cancer. Eur Radiol 29:1067–1073

    Article  PubMed  Google Scholar 

  34. Zhang GM, Sun H, Shi B, Jin ZY, Xue HD (2017) Quantitative CT texture analysis for evaluating histologic grade of urothelial carcinoma. Abdom Radiol (NY) 42:561–568

    Article  Google Scholar 

  35. Davnall F, Yip CS, Ljungqvist G et al (2012) Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice? Insights Imaging 3:573–589

    Article  PubMed  PubMed Central  Google Scholar 

  36. Veloso Gomes F, Matos AP, Palas J et al (2015) Renal cell carcinoma subtype differentiation using single-phase corticomedullary contrast-enhanced CT. Clin Imaging 39:273–277

    Article  PubMed  Google Scholar 

  37. Sheir KZ, El-Azab M, Mosbah A, El-Baz M, Shaaban AA (2005) Differentiation of renal cell carcinoma subtypes by multislice computerized tomography. J Urol 174:451–455 discussion 455

    Article  PubMed  Google Scholar 

  38. Shebel HM, Elsayes KM, Sheir KZ et al (2011) Quantitative enhancement washout analysis of solid cortical renal masses using multidetector computed tomography. J Comput Assist Tomogr 35:337–342

    Article  PubMed  Google Scholar 

  39. Ruppert-Kohlmayr AJ, Uggowitzer M, Meissnitzer T, Ruppert G (2004) Differentiation of renal clear cell carcinoma and renal papillary carcinoma using quantitative CT enhancement parameters. AJR Am J Roentgenol 183:1387–1391

    Article  PubMed  Google Scholar 

  40. Zhang J, Lefkowitz RA, Ishill NM et al (2007) Solid renal cortical tumors: differentiation with CT. Radiology 244:494–504

    Article  PubMed  Google Scholar 

  41. Leng S, Takahashi N, Gomez Cardona D et al (2017) Subjective and objective heterogeneity scores for differentiating small renal masses using contrast-enhanced CT. Abdom Radiol (NY) 42:1485–1492

    Article  Google Scholar 

  42. Yip C, Davnall F, Kozarski R et al (2015) Assessment of changes in tumor heterogeneity following neoadjuvant chemotherapy in primary esophageal cancer. Dis Esophagus 28:172–179

    Article  CAS  PubMed  Google Scholar 

  43. Skogen K GB, Good T, Critchley G, Miles KA (2011) Imaging heterogeneity in gliomas using texture analysis. Cancer Imaging 11 Spec No A:A113

  44. Castellano G, Bonilha L, Li LM, Cendes F (2004) Texture analysis of medical images. Clin Radiol 59:1061–1069

    Article  CAS  PubMed  Google Scholar 

  45. Yang Z, Tang LH, Klimstra DS (2011) Effect of tumor heterogeneity on the assessment of Ki67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol 35:853–860

    Article  PubMed  Google Scholar 

  46. Oh S, Sung DJ, Yang KS et al (2017) Correlation of CT imaging features and tumor size with Fuhrman grade of clear cell renal cell carcinoma. Acta Radiol 58:376–384

    Article  PubMed  Google Scholar 

  47. Beddy P, Genega EM, Ngo L et al (2014) Tumor necrosis on magnetic resonance imaging correlates with aggressive histology and disease progression in clear cell renal cell carcinoma. Clin Genitourin Cancer 12:55–62

    Article  PubMed  Google Scholar 

  48. 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 276:787–796

    Article  PubMed  Google Scholar 

  49. Thompson RH, Kurta JM, Kaag M et al (2009) Tumor size is associated with malignant potential in renal cell carcinoma cases. J Urol 181:2033–2036

    Article  PubMed  PubMed Central  Google Scholar 

  50. Turun S, Banghua L, Zheng S, Wei Q (2012) Is tumor size a reliable predictor of histopathological characteristics of renal cell carcinoma? Urol Ann 4:24–28

    Article  PubMed  PubMed Central  Google Scholar 

  51. Hayano K, Tian F, Kambadakone AR et al (2015) Texture analysis of non-contrast-enhanced computed tomography for assessing angiogenesis and survival of soft tissue sarcoma. J Comput Assist Tomogr 39:607–612

    Article  PubMed  PubMed Central  Google Scholar 

  52. Schieda N, Thornhill RE, Al-Subhi M et al (2015) Diagnosis of sarcomatoid renal cell carcinoma with CT: evaluation by qualitative imaging features and texture analysis. AJR Am J Roentgenol 204:1013–1023

    Article  PubMed  Google Scholar 

  53. Smith AD, Gray MR, del Campo SM et al (2015) Predicting overall survival in patients with metastatic melanoma on antiangiogenic therapy and RECIST stable disease on initial posttherapy images using CT texture analysis. AJR Am J Roentgenol 205:W283–W293

    Article  PubMed  Google Scholar 

  54. Takahashi N, Leng S, Kitajima K et al (2015) Small (< 4 cm) renal masses: differentiation of angiomyolipoma without visible fat from renal cell carcinoma using unenhanced and contrast-enhanced CT. AJR Am J Roentgenol 205:1194–1202

    Article  PubMed  Google Scholar 

  55. Ng F, Kozarski R, Ganeshan B, Goh V (2013) Assessment of tumor heterogeneity by CT texture analysis: can the largest cross-sectional area be used as an alternative to whole tumor analysis? Eur J Radiol 82:342–348

    Article  PubMed  Google Scholar 

  56. Cornejo KM, Dong F, Zhou AG et al (2015) Papillary renal cell carcinoma: correlation of tumor grade and histologic characteristics with clinical outcome. Hum Pathol 46:1411–1417

    Article  PubMed  Google Scholar 

  57. Sika-Paotonu D, Bethwaite PB, McCredie MR, William Jordan T, Delahunt B (2006) Nucleolar grade but not Fuhrman grade is applicable to papillary renal cell carcinoma. Am J Surg Pathol 30:1091–1096

    Article  PubMed  Google Scholar 

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Correspondence to Kumaresan Sandrasegaran.

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The scientific guarantor of this publication is Kumaresan Sandrasegaran, M.D.

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Deng, Y., Soule, E., Samuel, A. et al. CT texture analysis in the differentiation of major renal cell carcinoma subtypes and correlation with Fuhrman grade. Eur Radiol 29, 6922–6929 (2019). https://doi.org/10.1007/s00330-019-06260-2

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  • DOI: https://doi.org/10.1007/s00330-019-06260-2

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