Korean J Radiol.  2018 Oct;19(5):916-922. 10.3348/kjr.2018.19.5.916.

Histogram Analysis of Diffusion Kurtosis Magnetic Resonance Imaging for Diagnosis of Hepatic Fibrosis

Affiliations
  • 1Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai 200032, China. mengsuzeng@163.com
  • 2Department of Pathology, Zhongshan Hospital, Fudan University, Shanghai 200032, China.
  • 3MR Collaboration NEA, Siemens Ltd. China, Shanghai 201318, China.

Abstract


OBJECTIVE
To investigate the diagnostic value of diffusion kurtosis imaging (DKI) histogram analysis in hepatic fibrosis staging.
MATERIALS AND METHODS
Thirty-six rats were divided into carbon tetrachloride-induced fibrosis groups (6 rats per group for 2, 4, 6, and 8 weeks) and a control group (n = 12). MRI was performed using a 3T scanner. Histograms of DKI were obtained for corrected apparent diffusion (D), kurtosis (K) and apparent diffusion coefficient (ADC). Mean, median, skewness, kurtosis and 25th and 75th percentiles were generated and compared according to the fibrosis stage and inflammatory activity.
RESULTS
A total of 35 rats were included, and 12, 5, 5, 6, and 7 rats were diagnosed as F0-F4. The mean, median, 25th and 75th percentiles, kurtosis of D map, median, 25th percentile, skewness of K map, and 75th percentile of ADC map demonstrated significant correlation with fibrosis stage (r = −0.767 to 0.339, p < 0.001 to p = 0.039). The fibrosis score was the independent variable associated with histogram parameters compared with inflammatory activity grade (p < 0.001 to p = 0.041), except the median of K map (p = 0.185). Areas under the receiver operating characteristic curve of D were larger than K and ADC maps in fibrosis staging, although no significant differences existed in pairwise comparisons (p = 0.0512 to p = 0.847).
CONCLUSION
Corrected apparent diffusion of DKI histogram analysis provides added value and better diagnostic performance to detect various liver fibrosis stages compared with ADC.

Keyword

Liver; Fibrosis; Histogram analysis; Diffusion kurtosis imaging; Magnetic resonance imaging

MeSH Terms

Animals
Carbon
Diagnosis*
Diffusion*
Fibrosis*
Liver
Liver Cirrhosis
Magnetic Resonance Imaging*
Rats
ROC Curve
Carbon

Figure

  • Fig. 1 Example of DKI histogram analysis in rat graded A3F4.(A) Placement of region of interest on parametric map of K map. (B) Semi-logarithmic plot of hepatic diffusion-related signal decay with respect to increasing b-values demonstrates improved fit of measured data with diffusional kurtosis model compared with monoexponential ADC model. Corresponding histograms were generated for (C) D map, (D) K map, and (E) ADC map. Different distributions of parameters, as relatively low percentile D values with left-skewed broad distribution, high percentile K values with right-skewed broad distribution, and medium percentile ADC values are shown. (F) Microscopy shows liver with cirrhosis (F4) and severe inflammatory activity (A3) (hematoxylin-eosin stain, × 40). ADC = apparent diffusion coefficient, D = corrected apparent diffusion, DKI = diffusion kurtosis imaging, K = kurtosis

  • Fig. 2 ROC curves for identification of fibrosis grade (A) F1 or higher, (B) F2 or higher, and (C) F4 using histogram analyses for D, K, and ADC.Highest areas under ROC curve of all significant parameters for each magnetic resonance parameter are used. ROC analysis showed no significance in ADC for prediction of F4, and pairwise comparison was only conducted between D and K. ROC = receiver operating characteristics


Reference

1. Polasek M, Fuchs BC, Uppal R, Schühle DT, Alford JK, Loving GS, et al. Molecular MR imaging of liver fibrosis: a feasibility study using rat and mouse models. J Hepatol. 2012; 57:549–555. PMID: 22634342.
Article
2. Faria SC, Ganesan K, Mwangi I, Shiehmorteza M, Viamonte B, Mazhar S, et al. MR imaging of liver fibrosis: current state of the art. Radiographics. 2009; 29:1615–1635. PMID: 19959511.
Article
3. Trautwein C, Friedman SL, Schuppan D, Pinzani M. Hepatic fibrosis: concept to treatment. J Hepatol. 2015; 62(1 Suppl):S15–S24. PMID: 25920084.
Article
4. Yoon JH, Lee JM, Baek JH, Shin CI, Kiefer B, Han JK, et al. Evaluation of hepatic fibrosis using intravoxel incoherent motion in diffusion-weighted liver MRI. J Comput Assist Tomogr. 2014; 38:110–116. PMID: 24378888.
Article
5. Ahn SJ, Lee JM, Chang W, Lee SM, Kang HJ, Yang H, et al. Prospective validation of intra- and interobserver reproducibility of a new point shear wave elastographic technique for assessing liver stiffness in patients with chronic liver disease. Korean J Radiol. 2017; 18:926–935. PMID: 29089825.
Article
6. Lee GM, Kim YR, Ryu JH, Kim TH, Cho EY, Lee YH, et al. Quantitative measurement of hepatic fibrosis with gadoxetic acid-enhanced magnetic resonance imaging in patients with chronic hepatitis B infection: a comparative study on aspartate aminotransferase to platelet ratio index and fibrosis-4 index. Korean J Radiol. 2017; 18:444–451. PMID: 28458596.
Article
7. Xie S, Li Q, Cheng Y, Zhang Y, Zhuo Z, Zhao G, et al. Impact of liver fibrosis and fatty liver on T1rho measurements: a prospective study. Korean J Radiol. 2017; 18:898–905. PMID: 29089822.
Article
8. Jensen JH, Helpern JA, Ramani A, Lu HZ, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005; 53:1432–1440. PMID: 15906300.
Article
9. Rosenkrantz AB, Sigmund EE, Winnick A, Niver BE, Spieler B, Morgan GR, et al. Assessment of hepatocellular carcinoma using apparent diffusion coefficient and diffusion kurtosis indices: preliminary experience in fresh liver explants. Magn Reson Imaging. 2012; 30:1534–1540. PMID: 22819175.
Article
10. Sheng RF, Wang HQ, Yang L, Jin KP, Xie YH, Chen CZ, et al. Diffusion kurtosis imaging and diffusion-weighted imaging in assessment of liver fibrosis stage and necroinflammatory activity. Abdom Radiol (NY). 2017; 42:1176–1182. PMID: 27866239.
Article
11. Hu XX, Yang ZX, Liang HY, Ding Y, Grimm R, Fu CX, et al. Whole-tumor MRI histogram analyses of hepatocellular carcinoma: correlations with Ki-67 labeling index. J Magn Reson Imaging. 2017; 46:383–392. PMID: 27862582.
Article
12. Huang YQ, Liang HY, Yang ZX, Ding Y, Zeng MS, Rao SX. Value of MR histogram analyses for prediction of microvascular invasion of hepatocellular carcinoma. Medicine (Baltimore). 2016; 95:e4034. PMID: 27368028.
Article
13. Fujimoto K, Tonan T, Azuma S, Kage M, Nakashima O, Johkoh T, et al. Evaluation of the mean and entropy of apparent diffusion coefficient values in chronic hepatitis C: correlation with pathologic fibrosis stage and inflammatory activity grade. Radiology. 2011; 258:739–748. PMID: 21248235.
Article
14. Choi JY, Kim H, Sun M, Sirlin CB. Histogram analysis of hepatobiliary phase MR imaging as a quantitative value for liver cirrhosis: preliminary observations. Yonsei Med J. 2014; 55:651–659. PMID: 24719131.
Article
15. Kim H, Park SH, Kim EK, Kim MJ, Park YN, Park HJ, et al. Histogram analysis of gadoxetic acid-enhanced MRI for quantitative hepatic fibrosis measurement. PLoS One. 2014; 9:e114224. PMID: 25460180.
Article
16. Lagadec M, Doblas S, Giraudeau C, Ronot M, Lambert SA, Fasseu M, et al. Advanced fibrosis: correlation between pharmacokinetic parameters at dynamic gadoxetate-enhanced MR imaging and hepatocyte organic anion transporter expression in rat liver. Radiology. 2015; 274:379–386. PMID: 25289480.
Article
17. Dong D, Yin L, Qi Y, Xu L, Peng J. Protective effect of the total saponins from Rosa laevigata michx fruit against carbon tetrachloride-induced liver fibrosis in rats. Nutrients. 2015; 7:4829–4850. PMID: 26083117.
Article
18. Tamada T, Prabhu V, Li J, Babb JS, Taneja SS, Rosenkrantz AB. Prostate cancer: diffusion-weighted MR imaging for detection and assessment of aggressiveness-comparison between conventional and kurtosis models. Radiology. 2017; 284:100–108. PMID: 28394755.
19. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. Hepatology. 1996; 24:289–293. PMID: 8690394.
Article
20. Karlik SJ. Exploring and summarizing radiologic data. AJR Am J Roentgenol. 2003; 180:47–54. PMID: 12490475.
Article
21. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988; 44:837–845. PMID: 3203132.
Article
22. Liang HY, Huang YQ, Yang ZX, Ying D, Zeng MS, Rao SX. Potential of MR histogram analyses for prediction of response to chemotherapy in patients with colorectal hepatic metastases. Eur Radiol. 2016; 26:2009–2018. PMID: 26494642.
Article
23. Taouli B, Chouli M, Martin AJ, Qayyum A, Coakley FV, Vilgrain V. Chronic hepatitis: role of diffusion-weighted imaging and diffusion-tensor imaging for the diagnosis of liver fibrosis and inflammation. J Magn Reson Imaging. 2008; 28:89–95. PMID: 18581382.
24. Lambregts DM, Martens MH, Quah RC, Nikiforaki K, Heijnen LA, Dejong CH, et al. Whole-liver diffusion-weighted MRI histogram analysis: effect of the presence of colorectal hepatic metastases on the remaining liver parenchyma. Eur J Gastroenterol Hepatol. 2015; 27:399–404. PMID: 25874512.
25. Anderson SW, Barry B, Soto J, Ozonoff A, O'Brien M, Jara H. Characterizing non-gaussian, high b-value diffusion in liver fibrosis: stretched exponential and diffusional kurtosis modeling. J Magn Reson Imaging. 2014; 39:827–834. PMID: 24259401.
Article
26. Drevelegas K, Nikiforaki K, Constantinides M, Papanikolaou N, Papalavrentios L, Stoikou I, et al. Apparent diffusion coefficient quantification in determining the histological diagnosis of malignant liver lesions. J Cancer. 2016; 7:730–735. PMID: 27076855.
Article
27. Asayama Y, Nishie A, Ishigami K, Ushijima Y, Takayama Y, Okamoto D, et al. Histogram analysis of noncancerous liver parenchyma on gadoxetic acid-enhanced MRI: predictive value for liver function and pathology. Abdom Radiol (NY). 2016; 41:1751–1757. PMID: 27138437.
Article
28. Lambregts DM, Beets GL, Maas M, Curvo-Semedo L, Kessels AG, Thywissen T, et al. Tumour ADC measurements in rectal cancer: effect of ROI methods on ADC values and interobserver variability. Eur Radiol. 2011; 21:2567–2574. PMID: 21822946.
Article
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