Skip to main content
SpringerLink
Log in

WHO/ISUP grade and pathological T stage of clear cell renal cell carcinoma: value of ZOOMit diffusion kurtosis imaging and chemical exchange saturation transfer imaging

  • Oncology
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To evaluate the value of ZOOMit diffusion kurtosis imaging (DKI) and chemical exchange saturation transfer (CEST) imaging in predicting WHO/ISUP grade and pathological T stage in clear cell renal cell carcinoma (ccRCC).

Methods

Forty-six patients with ccRCC were included in this retrospective study. All participants underwent MRI including ZOOMit DKI and CEST. The non-Gaussian mean kurtosis (MK), mean diffusivity (MD), magnetization transfer ratio asymmetry (MTRasym (3.5 ppm)), and Ssat (3.5 ppm)/S0 were analyzed based on different WHO/ISUP grades and pT stages. Binary logistic regression was used to identify the best combination of the parameters. Pearson’s correlation coefficients were calculated between CEST and diffusion-related parameters.

Results

The ADC, MD, and Ssat (3.5 ppm)/S0 values were significantly lower for higher WHO/ISUP grade tumors, whereas the MK and MTRasym (3.5 ppm) were higher in higher WHO/ISUP grade and higher pT stage tumors. MTRasym (3.5 ppm) combined with MD (AUC, 0.930; 95% CI, 0.858–1.000) showed the best diagnostic efficacy in evaluating the WHO/ISUP grade. MTRasym (3.5 ppm) and MK were mildly positively correlated (r = 0.324, p = 0.028). Ssat (3.5 ppm)/S0 was moderately positively correlated with ADC (r = 0.580, p < 0.001), mildly positively correlated with MD (r = 0.412, p = 0.005), and moderately negatively correlated with MK (r = −0.575, p < .001).

Conclusion

The microstructural and biochemical assessment of ZOOMit DKI and CEST allowed for the characterization of different WHO/ISUP grades and pT stages in ccRCC. MTRasym (3.5 ppm) combined with MD showed the best diagnostic performance for WHO/ISUP grading.

Key Points

• Both diffusion kurtosis imaging (DKI) and chemical exchange saturation transfer (CEST) can be used to predict the WHO/ISUP grade and pathological T stage.

• MTRasym (3.5 ppm) combined with MD showed the highest AUC (0.930; 95% CI, 0.858–1.000) in WHO/ISUP grading.

• MTRasym at 3.5 ppm showed a positive correlation with mean kurtosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

APT:

Amide proton transfer

CEST:

Chemical exchange saturation transfer

DKI:

Diffusion kurtosis imaging

DWI:

Diffusion-weighted imaging

ICC:

Intraclass correlation coefficient

MTRasym (3.5 ppm):

Asymmetric magnetization transfer ratio at 3.5 ppm

ROC:

Receiver operating characteristic

ROI:

Region-of-interest

References

  1. Sung H, Ferlay J, Siegel RL et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    Article  PubMed  Google Scholar 

  2. Escudier B, Porta C, Schmidinger M et al (2019) Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up†. Ann Oncol 30:706–720

    Article  CAS  PubMed  Google Scholar 

  3. Zhao Y, Wu C, Li W et al (2021) 2-[(18)F]FDG PET/CT parameters associated with WHO/ISUP grade in clear cell renal cell carcinoma. Eur J Nucl Med Mol Imaging 48:570–579

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  5. Zhou H, Mao H, Dong D et al (2020) Development and external validation of radiomics approach for nuclear grading in clear cell renal cell carcinoma. Ann Surg Oncol 27:4057–4065

    Article  PubMed  Google Scholar 

  6. Demirjian NL, Varghese BA, Cen SY et al (2022) CT-based radiomics stratification of tumor grade and TNM stage of clear cell renal cell carcinoma. Eur Radiol 32:2552–2563

    Article  PubMed  Google Scholar 

  7. Woo S, Suh CH, Kim SY, Cho JY, Kim SH (2017) Diagnostic performance of DWI for differentiating high- from low-grade clear cell renal cell carcinoma: a systematic review and meta-analysis. AJR Am J Roentgenol 209:W374–w381

    Article  PubMed  Google Scholar 

  8. Li Q, Cao B, Tan Q, Liu K, Jiang S, Zhou J (2021) Prediction of muscle invasion of bladder cancer: a comparison between DKI and conventional DWI. Eur J Radiol 136:109522

    Article  PubMed  Google Scholar 

  9. Gao A, Zhang H, Yan X et al (2022) Whole-tumor histogram analysis of multiple diffusion metrics for glioma genotyping. Radiology 302:652–661

    Article  PubMed  Google Scholar 

  10. Zhang Q, Yu X, Ouyang H et al (2021) Whole-tumor texture model based on diffusion kurtosis imaging for assessing cervical cancer: a preliminary study. Eur Radiol 31:5576–5585

    Article  PubMed  Google Scholar 

  11. Wang K, Cheng J, Wang Y, Wu G (2019) Renal cell carcinoma: preoperative evaluate the grade of histological malignancy using volumetric histogram analysis derived from magnetic resonance diffusion kurtosis imaging. Quant Imaging Med Surg 9:671–680

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sim KC, Park BJ, Han NY, Sung DJ, Kim MJ, Han YE (2020) Efficacy of ZOOMit coronal diffusion-weighted imaging and MR texture analysis for differentiating between benign and malignant distal bile duct strictures. Abdom Radiol (NY) 45:2418–2429

    Article  PubMed  Google Scholar 

  13. Yıldırım İO, Sağlık S, Çelik H (2017) Conventional and ZOOMit DWI for evaluation of testis in patients with ipsilateral varicocele. AJR Am J Roentgenol 208:1045–1050

    Article  PubMed  Google Scholar 

  14. Chen M, Feng C, Wang Q et al (2021) Comparison of reduced field-of-view diffusion-weighted imaging (DWI) and conventional DWI techniques in the assessment of cervical carcinoma at 3.0T: image quality and FIGO staging. Eur J Radiol 137:109557

    Article  PubMed  Google Scholar 

  15. Li L, Wang L, Deng M et al (2015) Feasibility study of 3-T DWI of the prostate: readout-segmented versus single-shot echo-planar imaging. AJR Am J Roentgenol 205:70–76

    Article  PubMed  Google Scholar 

  16. Ohno Y, Yui M, Koyama H et al (2016) Chemical exchange saturation transfer MR imaging: preliminary results for differentiation of malignant and benign thoracic lesions. Radiology 279:578–589

    Article  PubMed  Google Scholar 

  17. Zhou J, Zaiss M, Knutsson L et al (2022) Review and consensus recommendations on clinical APT-weighted imaging approaches at 3T: application to brain tumors. Magn Reson Med 88:546–574

    Article  PubMed  PubMed Central  Google Scholar 

  18. Takayama Y, Nishie A, Togao O et al (2018) Amide proton transfer MR imaging of endometrioid endometrial adenocarcinoma: association with histologic grade. Radiology 286:909–917

    Article  PubMed  Google Scholar 

  19. Joo B, Han K, Ahn SS et al (2019) Amide proton transfer imaging might predict survival and IDH mutation status in high-grade glioma. Eur Radiol 29:6643–6652

    Article  PubMed  PubMed Central  Google Scholar 

  20. Loi L, Zimmermann F, Goerke S et al (2020) Relaxation-compensated CEST (chemical exchange saturation transfer) imaging in breast cancer diagnostics at 7T. Eur J Radiol 129:109068

    Article  PubMed  Google Scholar 

  21. Liu R, Zhang H, Niu W et al (2019) Improved chemical exchange saturation transfer imaging with real-time frequency drift correction. Magn Reson Med 81:2915–2923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu R, Zhang H, Qian Y et al (2021) Frequency-stabilized chemical exchange saturation transfer imaging with real-time free-induction-decay readout. Magn Reson Med 85:1322–1334

    Article  CAS  PubMed  Google Scholar 

  23. Zhang Y, Heo HY, Lee DH et al (2016) Selecting the reference image for registration of CEST series. J Magn Reson Imaging 43:756–761

    Article  PubMed  Google Scholar 

  24. Yu X, Lin M, Ouyang H, Zhou C, Zhang H (2012) Application of ADC measurement in characterization of renal cell carcinomas with different pathological types and grades by 3.0T diffusion-weighted MRI. Eur J Radiol 81:3061–3066

    Article  PubMed  Google Scholar 

  25. Parada Villavicencio C, Mc Carthy RJ, Miller FH (2017) Can diffusion-weighted magnetic resonance imaging of clear cell renal carcinoma predict low from high nuclear grade tumors. Abdom Radiol (NY) 42:1241–1249

    Article  PubMed  Google Scholar 

  26. Tang L, Zhou XJ (2019) Diffusion MRI of cancer: from low to high b-values. J Magn Reson Imaging 49:23–40

    Article  PubMed  Google Scholar 

  27. Cao J, Luo X, Zhou Z et al (2020) Comparison of diffusion-weighted imaging mono-exponential mode with diffusion kurtosis imaging for predicting pathological grades of clear cell renal cell carcinoma. Eur J Radiol 130:109195

    Article  PubMed  Google Scholar 

  28. Zhu J, Luo X, Gao J, Li S, Li C, Chen M (2021) Application of diffusion kurtosis tensor MR imaging in characterization of renal cell carcinomas with different pathological types and grades. Cancer Imaging 21:30

    Article  PubMed  PubMed Central  Google Scholar 

  29. Khor LY, Dhakal HP, Jia X et al (2016) Tumor necrosis adds prognostically significant information to grade in clear cell renal cell carcinoma: a study of 842 consecutive cases from a single institution. Am J Surg Pathol 40:1224–1231

    Article  PubMed  Google Scholar 

  30. Jones KM, Pollard AC, Pagel MD (2018) Clinical applications of chemical exchange saturation transfer (CEST) MRI. J Magn Reson Imaging 47:11–27

    Article  PubMed  Google Scholar 

  31. Togao O, Yoshiura T, Keupp J et al (2014) Amide proton transfer imaging of adult diffuse gliomas: correlation with histopathological grades. Neuro Oncol 16:441–448

    Article  CAS  PubMed  Google Scholar 

  32. Adams LC, Ralla B, Jurmeister P et al (2019) Native T1 mapping as an in vivo biomarker for the identification of higher-grade renal cell carcinoma: correlation with histopathological findings. Invest Radiol 54:118–128

    Article  PubMed  Google Scholar 

  33. Khlebnikov V, Polders D, Hendrikse J et al (2017) Amide proton transfer (APT) imaging of brain tumors at 7 T: the role of tissue water T(1) -Relaxation properties. Magn Reson Med 77:1525–1532

    Article  CAS  PubMed  Google Scholar 

  34. Li A, Xu C, Liang P et al (2020) Role of chemical exchange saturation transfer and magnetization transfer MRI in detecting metabolic and structural changes of renal fibrosis in an animal model at 3T. Korean J Radiol 21:588–597

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This retrospective study was approved by the Ethics Committee of Tongji Hospital of Huazhong University of Science and Technology. Requirement for informed consent was waived.

Funding

This study has received funding by the National Natural Science Foundation of China (No. 82071889 and 81971605).

Author information

Author notes

  1. Yi Zhang and Zhen Li contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China

    Shichao Li, Kangwen He, Guanjie Yuan, Xiaoyan Meng, Cui Feng & Zhen Li

  2. Key Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, Hangzhou, Zhejiang, China

    Xingwang Yong & Yi Zhang

  3. Russell H. Morgan Department of Radiology and Radiological Science, the Johns Hopkins Medical Institutions, Baltimore, Maryland, USA

    Ihab R. Kamel

Authors
  1. Shichao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kangwen He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guanjie Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingwang Yong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaoyan Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cui Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ihab R. Kamel
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yi Zhang or Zhen Li.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Zhen Li (Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology).

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• observational

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, S., He, K., Yuan, G. et al. WHO/ISUP grade and pathological T stage of clear cell renal cell carcinoma: value of ZOOMit diffusion kurtosis imaging and chemical exchange saturation transfer imaging. Eur Radiol 33, 4429–4439 (2023). https://doi.org/10.1007/s00330-022-09312-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-022-09312-2

Keywords

Search

Navigation