Intravoxel incoherent motion diffusion imaging of the liver: Optimal b-value subsampling and impact on parameter precision and reproducibility

doi:10.1016/j.ejrad.2014.09.003

European Journal of Radiology

Volume 83, Issue 12, December 2014, Pages 2109-2113

https://doi.org/10.1016/j.ejrad.2014.09.003 Get rights and content

Highlights

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We assess the precision and reproducibility of liver IVIM diffusion parameters.
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Liver IVIM DWI can be performed with 4 b-values with good parameter precision.
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Liver IVIM DWI can be performed with 4 b-values with good parameter reproducibility.

Abstract

Purpose

To increase diffusion sampling efficiency in intravoxel incoherent motion (IVIM) diffusion-weighted imaging (DWI) of the liver by reducing the number of diffusion weightings (b-values).

Materials and methods

In this IRB approved HIPAA compliant prospective study, 53 subjects (M/F 38/15, mean age 52 ± 13 y) underwent IVIM DWI at 1.5 T using 16 b-values (0–800 s/mm²), with 14 subjects having repeat exams to assess IVIM parameter reproducibility. A biexponential diffusion model was used to quantify IVIM hepatic parameters (PF: perfusion fraction, D: true diffusion and D*: pseudo diffusion). All possible subsets of the 16 b-values were probed, with number of b values ranging from 4 to 15, and corresponding parameters were quantified for each subset. For each b-value subset, global parameter estimation error was computed against the parameters obtained with all 16 b-values and the subsets providing the lowest error were selected. Interscan estimation error was also evaluated between repeat exams to assess reproducibility of the IVIM technique in the liver. The optimal b-values distribution was selected such that the number of b-values was minimal while keeping parameter estimation error below interscan reproducibility error.

Results

As the number of b-values decreased, the estimation error increased for all parameters, reflecting decreased precision of IVIM metrics. Using an optimal set of 4 b-values (0, 15, 150 and 800 s/mm²), the errors were 6.5, 22.8 and 66.1% for D, PF and D* respectively. These values lie within the range of test–retest reproducibility for the corresponding parameters, with errors of 12.0, 32.3 and 193.8% for D, PF and D* respectively.

Conclusion

A set of 4 optimized b-values can be used to estimate IVIM parameters in the liver with significantly shorter acquisition time (up to 75%), without substantial degradation of IVIM parameter precision and reproducibility compared to the 16 b-value acquisition used as the reference.

Introduction

Diffusion weighted imaging (DWI) has been extensively investigated in abdominal organs such as the liver, kidneys and pancreas, using molecular diffusion as a marker of tissue structure in healthy and pathologic tissue [1], [2], [3], [4], [5], [6], [7], [8], [9], [10]. Additionally, extracting tissue perfusion using intravoxel incoherent motion (IVIM) DWI has the potential to detect and characterize focal liver lesions and diffuse parenchymal disease [3], [11], [12], [13], [14], [15], [16]. In spite of an increasing number of applications of DWI without or with IVIM, there is no clear consensus regarding the optimal protocol to be used. One crucial question pertains to the diffusion-encoding strategy, which defines the ability to separate blood perfusion from true diffusion effects via a proper choice of the number and distribution of diffusion weightings, or b-values. Previous abdominal IVIM DWI studies have used ad hoc distributions of 5–16 b-values that sample both perfusion (≤100 s/mm²) and diffusion (>100 s/mm²) regimes [12], [13], [14], [15]. Because more b-value samples involve longer scan time, there is a need to use the smallest possible number of b-values. We hypothesize that the number of b-values could be reduced while still enabling correct IVIM parameter estimation, without affecting the reproducibility of the technique.

Two recent studies have proposed methods for optimizing b-value sampling for IVIM. Zhang et al. [17] used an error propagation model to determine the best set of b-values in the renal parenchyma and renal lesions. Lemke et al. [18] have proposed a series of b-values by sequentially adding b-values that minimize the fit errors for a range of IVIM parameters in the pancreas. Both studies used IVIM model decay curves with added Gaussian noise, with optimal b-values distributions chosen such that the errors in estimated D, PF and D* were minimized. Although these model-based approaches yield interesting results, they have limitations. First, the models assume a Gaussian noise figure. Physiologic signal fluctuations in a diffusion experiment could result in more complex noise properties that may be difficult to model. Another restriction is the consideration of fixed IVIM parameters in simulations, while a population with liver disease may present a wide range of parameters, thus making the proposed optimal b-value distributions less robust.

The purpose of this study is to present a data-driven descriptive analysis of liver IVIM parameter precision when a small set of b-values is used for parameter computation, and to determine the minimal number and optimal distribution of b-values necessary for reproducible IVIM parameter quantification in the liver.

Section snippets

Subjects

This HIPAA compliant prospective study funded by NIDDK was approved by the local institution review board, and included a total of 53 subjects (M/F 38/15, mean age 52 ± 13 y) enrolled in a prospective liver fibrosis study at 1.5 T with written consent obtained prior to the exam. The data from 20 of these 53 subjects has been used in a previous study that assessed the test–retest reproducibility of IVIM measurement [19]. Seven subjects were healthy volunteers and 46 subjects had liver disease (43

Reference parameters computed using 16 b-values and reproducibility of the technique

Parameter values obtained with 16 b-values (used as the reference) and ranges are given in Table 2. Parameter convergence during the nonlinear least squares fitting was within parameter limits in all cases except in 5 subjects, where the upper limit was reached for D*. The average eSNR at b = 800 s/mm² was 51.6 ± 20.6. The test–retest reproducibility of parameter estimation (Table 2) was highest for D, intermediate for PF and lowest for D* with σ_repeat of 12.0%, 32.3% and 193.8% respectively.

Parameter evolution when decreasing the number of b-values

Table 3

Discussion

By evaluating both blood perfusion and molecular diffusion components in tissues, IVIM DWI has the potential to help characterize diffuse liver disease [13], [15], focal liver and pancreatic lesions [14], [23], [24] and renal function [25], [26]. However, the separation of diffusion and pseudo diffusion requires multiple b-values that, if coupled with signal averaging, multiple diffusion direction measurements and/or navigator gated acquisition, may result in prohibitively long scan times. We

Conflict of interest

Hadrien Dyvorne, Guido Jajamovich, Suguru Kakite have no conflict of interest to declare.

Bachir Taouli has no conflict of interest to declare related to this work. Not related to this work. B.T. is consultant for Bayer Healthcare.

Bernd Kuehn has no conflict of interest to declare related to this work. Not related to this work. B.K. is an employee of Siemens Healthcare.

Acknowledgement

This research was funded by NIDDK Grant 1R01DK087877.

References (27)

M.S. Park et al.
Hepatocellular carcinoma: detection with diffusion-weighted versus contrast-enhanced magnetic resonance imaging in pretransplant patients
Hepatology
(2012)
R.V. Mulkern et al.
Biexponential characterization of prostate tissue water diffusion decay curves over an extended b-factor range
Magn Reson Imaging
(2006)
A. Lemke et al.
Toward an optimal distribution of b values for intravoxel incoherent motion imaging
Magn Reson Imaging
(2011)
B. Taouli et al.
Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients
Radiology
(2003)
H.C. Thoeny et al.
Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience
Radiology
(2005)
D.M. Koh et al.
Colorectal hepatic metastases: quantitative measurements using single-shot echo-planar diffusion-weighted MR imaging
Eur Radiol
(2006)
A. Muhi et al.
High-b-value diffusion-weighted MR imaging of hepatocellular lesions: estimation of grade of malignancy of hepatocellular carcinoma
J Magn Reson Imaging
(2009)
M.F. Akisik et al.
Assessment of chronic pancreatitis: utility of diffusion-weighted MR imaging with secretin enhancement
Radiology
(2009)
B. Taouli et al.
Diffusion-weighted MR imaging of the liver
Radiology
(2010)
A.B. Rosenkrantz et al.
Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade
AJR Am J Roentgenol
(2010)

Y. Wang et al.

Diffusion-weighted MR imaging of solid and cystic lesions of the pancreas

Radiographics

(2011)

K. Sandrasegaran et al.

Usefulness of diffusion-weighted imaging in the evaluation of renal masses

AJR Am J Roentgenol

(2010)

I. Yamada et al.

Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging

Radiology

(1999)

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¹: Icahn School of Medicine at Mount Sinai, United States.

²: Division of Radiology, Tottori University, Japan.

View full text

Intravoxel incoherent motion diffusion imaging of the liver: Optimal b-value subsampling and impact on parameter precision and reproducibility

Highlights

Abstract

Purpose

Materials and methods

Results

Conclusion

Introduction

Section snippets

Subjects

Reference parameters computed using 16 b-values and reproducibility of the technique

Parameter evolution when decreasing the number of b-values

Discussion

Conflict of interest

Acknowledgement

Hepatology

Magn Reson Imaging

Magn Reson Imaging

Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients

Radiology

Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience

Radiology

Colorectal hepatic metastases: quantitative measurements using single-shot echo-planar diffusion-weighted MR imaging

Eur Radiol

High-b-value diffusion-weighted MR imaging of hepatocellular lesions: estimation of grade of malignancy of hepatocellular carcinoma

J Magn Reson Imaging

Assessment of chronic pancreatitis: utility of diffusion-weighted MR imaging with secretin enhancement

Radiology

Diffusion-weighted MR imaging of the liver

Radiology

Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade

AJR Am J Roentgenol

Diffusion-weighted MR imaging of solid and cystic lesions of the pancreas

Radiographics

Usefulness of diffusion-weighted imaging in the evaluation of renal masses

AJR Am J Roentgenol

Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging

Radiology