Jiahui Li1, Alina Allen2, Yi Sui1, Dan Rettmann 3, Ann Shimakawa4, Glenn Slavin5, Kevin J. Glaser1, Sudhakar K. Venkatesh1, Taofic Mounajjed6, Vijay Shah7, Richard L. Ehman1, and Meng Yin1
1Radiology, Mayo Clinic, Rochester, MN, United States, 2Gastroenterology, Mayo Clinic, Rochester, MN, United States, 3GE Healthcare, Waukesha, WI, United States, 4GE Healthcare, Menlo Park, CA, United States, 5GE Healthcare, Silver Spring, MD, United States, 6Anatomic Pathology, Mayo Clinic, Rochester, MN, United States, 7Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, United States
Synopsis
In 27 clinical patients, we performed multi-parametric
hepatic MRI, including proton density fat fraction with R2* correction, MR
Elastography (MRE), and T1 mapping to characterize nonalcoholic steatohepatitis
(NASH). Fat fraction and multiple MRE-assessed mechanical
parameters successfully diagnosed NASH (p<0.05 for all). Diagnostic
abilities of all parameters were evaluated based on steatosis, inflammation and
ballooning scores respectively. Spearman correlations were used to analyze the correlations
between imaging parameters. We found that T1 relaxation time had a significantly positive correlation (ρ=0.72, p=0.0005) with fat fraction. In summary, multi-parametric MRI is a potential imaging surrogate
for diagnosing NASH.
Introduction
Nonalcoholic
steatohepatitis (NASH) is defined as an accumulation of liver fat associated
with inflammation and subsequent hepatocellular ballooning, the diagnosis of
which usually relies on histology findings. Either MR Spectroscopy or chemical
shift based fat fraction methods have been well-established for quantifying
liver fat content1. Some studies have shown that T1 mapping with T2*
correction has promise in diagnosing nonalcoholic fatty liver disease (NAFLD), and
a high accuracy for distinguishing NASH and ballooning from simple steatosis2.
Investigators have also found that MRE-assessed shear stiffness and damping
ratio have great potential in predicting nonalcoholic fatty liver disease
activity score (NAS) in both preclinical and clinical subjects3. Also,
shear attenuation has an equivalent accuracy as liver stiffness for detecting
hepatic fibrosis and inflammation4. So the purpose of our study is
to evaluate the capability of all the aforementioned multiple MRI/MRE
parameters, including fat fraction, R2*, MR Elastography (MRE), and T1
mapping, in characterizing disease severity in clinical patients with
biopsy-proven NAFLD/NASH.Methods
All
activities related to human subjects were reviewed and approved by our
institutional review board. Multi-parametric MRI, including fat fraction, R2*,
multi-frequency 3D MRE (30, 40, 60Hz), and T1 mapping,
were acquired on 24 NAFLD/NASH patients and 3 patients with healthy livers. 20
of the patients had liver biopsy results available, while biopsy results on 7 patients
are pending. All the examinations
were carried out on 1.5T whole-body GE imager as described in our previous
study [cite 2017 ISMRM abstract on NASH patients]. We derived
hepatic shear stiffness, attenuation, and damping ratio from MRE at multiple
frequencies. Fat fraction and R2* were obtained with the IDEAL-IQ sequence. In
order to avoid the opposing effect of iron on T1 mapping, we measured R2* values
(40.38±9.43s-1). Pairwise comparisons (nonparametric Dunn method for
joint ranking) were performed for the mean values of fat fraction, shear
stiffness, attenuation, damping ratio, and T1 value among different groups of NASH
diagnosis and histologic findings (steatosis, lobular inflammation, and ballooning).
Spearman’s correlations were used to analyze the relationships between imaging parameters.
For all statistical analysis a significance level of less than 0.05 was used
and a correlation coefficient (ρ) greater than 0.7 was
considered good.Results
Figure
1 demonstrates an example of multi-parametric MR images obtained from a patient
with NASH. Fat fraction and shear
stiffness was significantly higher in NASH patients (15.68±7.70% vs.
9.04±6.96%, 3.48±1.61kPa vs. 2.24±0.31kPa, p=0.0276, p=0.0182, respectively),
while attenuation and damping ratio was significantly lower (7.60±3.41m-1
vs. 12.37±3.27m-1, 0.06±0.04 vs. 0.12±0.05, p=0.0011, p=0.0029,
respectively). However, T1 value didn’t show significant changes (Figure 2). We
found that both the fat fraction and T1 value correlate well with steatosis (p=0.0010,
p=0.0041, respectively), moreover, the fat fraction can differentiate varying steatosis
score (p=0.0459). T1 mapping had a good correlation with fat fraction (ρ=0.72,
p=0.0005), while the other parameters didn’t (Figure 3). Figure 4 demonstrates
that both shear stiffness and attenuation can distinguish inflammation at early
stage (p=0.0277, p=0.0165, respectively), while fat fraction and T1 mapping had
no significant changes. Figure 5 illustrates that fat fraction, attenuation,
and T1 mapping were sensitive to hepatocellular ballooning (p<0.0001,
p=0.0173, p=0.0084, respectively), while shear stiffness and damping ratio were
not.Discussion
As expected,
in the natural history of NAFLD progression fat fraction had excellent
agreements with the steatosis changes and hepatocellular ballooning. We
observed that shear stiffness and attenuation had significant changes when there
was lobular inflammation, which were consistent with previous findings4.
Our results showed that attenuation was also sensitive to ballooning (p=0.0173).
MRE provides independent biomarkers for detecting inflammation and fibrosis
respectively, even with coexisting steatosis (no correlations between MRE and
PDFF). It echoes our previous findings well. On the contrary, T1 value had a good
correlation with fat fraction (ρ=0.72, p=0.0005), when distinguishing steatosis
and ballooning, so they may not be independent parameters. A limitation of this
study cohort was that the histologic readings were clustered in either the very
early or end stages of liver diseases. We will enroll more patients to obtain
better distribution of NASH severity. Our future work will include: 1) a
longitudinal study to evaluate the capability of multi-parametric MRI/MRE in
monitoring disease regression in response to interventional therapies; 2) further
validation of multi-parametric MRI diagnostic ability in patients with
different etiologies, such as alcoholic hepatitis (AH) or viral hepatitis (HCV,
HBV) or combinations of both.Conclusion
Multi-parametric
MRI is very promising for diagnosing NASH with quantified hepatic steatosis, lobular
inflammation, and hepatocellular ballooning. As an ongoing study, we will include more clinical
data to form a sophisticated statistical prediction model for NASH diagnosis.Acknowledgements
This research was funded by NIBIB grants EB017197 (M.Y) and EB001981 (R.L.E)References
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