Hsin-Jung yang1, Ilkay Oksuz2, Michael Klein3, Olivia Sobczyk3, Damini Dey1, Jane Sykes4, John Butler4, Xiaoming Bi5, Behzad Sharif1, Ivan Cokic1, Debiao Li1, Piotr Slomka1, Frank S Prato4, Joseph Fisher3, Sotirios Tsaftaris2, and Rohan Dharmakumar1
1Cedars Sinai Medical Center, Los Angeles, CA, United States, 2IMT School for Advanced Studies Lucca, 3University of Toronto, 4Lawson Health Research Institute, 5Siemens Healthcare
Synopsis
Although cardiac BOLD MRI can detect ischemic heart disease without ionizing radiation and contrast agents, its reliability remains poor due to the low sensitivity and specificity. We propose a novel strategy to overcome these barriers through: (i) an improved MRI strategy with free gas-exchange capability; (ii) repeat stimulation of heart using a validated prospective arterial CO2 targeting technique; and (iii) a statistical framework to increase the confidence measure of BOLD signal changes. Our results show that the proposed approach can be used to significantly increase the confidence in detecting myocardial BOLD response in conditions of health and disease.
Introduction
Cardiac BOLD MRI has evolved into a promising method for detecting
ischemic heart disease without ionizing radiation or contrast agents.
Nonetheless, in spite the technical advancements over the past 20 years that have
overcome major obstacles, its reliability remains poor. This limitation is
fundamentally a consequence of low sensitivity and specificity of weak myocardial
BOLD image contrast. In this study, we propose a novel strategy to overcome
these barriers through: (i) a confounder-corrected 3D T2 mapping at 3T (1) that is
performed at high-resolution with whole-heart coverage, rapid data collection, and
free-breathing acquisitions permitting free gas-exchange capability; (ii) repeat
stimulation of heart using a validated prospective arterial CO2 (PaCO2)
targeting technique (2); and (iii) a statistical framework to increase the
confidence measure of BOLD signal changes. We demonstrate herein that the
proposed approach enables a unique opportunity to reliably capture the BOLD
signal changes across multiple measurements during CO2-mediated
coronary vasodilation through unprecedented amplification in sensitivity and
specificity in health and disease. Methods
Fast, confounder-corrected, 3D BOLD MRI with
precisely targeted PaCO2:
Canines with
(n=5) and without (n=5) surgically controlled LAD stenosis were studied in a
3T clinical PET/MR system. A
fast, confounder-corrected, free-breathing 3D T2 mapping sequence (as
previously described) was prescribed during rest, under adenosine and under repeat arterial CO2 level (PaCO2)
modulations (baseline/normocapnic PaCO2 [PaCO2(-): 40mmHg];
hypercapnic PaCO2 [PaCO2(+): 60mmHg]. T2 mapping employed
SR-preparation with FLASH readout: TR/TE=3.2/1.6ms, flip angle=15°, spatial
resolution=2x2x5mm3 (14 partitions), adiabatic T2-prep
pulses and SR recovery time=350ms. Dynamic 13N-ammonia PET scans were
acquired for validation at rest and under adenosine. The repeat PaCO2 modulation and
acquisition protocol are illustrated in Figs. 1 (A and B). 3D T2 maps were
acquired during 4 blocks of repeat PaCO2
modulation (each block consisted 4 minutes normocapnia and 4 minutes of
hypercapnia).
Image
processing and statistical framework:
To
utilize the multiple measurements from repeated PaCO2 modulations,
all 3D T2 maps were registered to the initial PaCO2(-) T2
map using an image processing package (ANTs, stnava) to avoid inter-acquisition
motion. The registered images were segmented according to the AHA for analysis.
Segmental myocardial T2 values acquired
under repeat PaCO2(-) and PaCO2(+) were compared using
t-statistic to test the null hypothesis:
H0 [Null:
BOLD response present]:
T2 during PaCO2(-) = T2 during PaCO2(+)
H1 [Alternate:
BOLD response absent]:
T2 during PaCO2(-) ≠ T2 during PaCO2(+)
Segmental
t-scores and confidence of responses (CoR) were derived from integrated myocardial
T2 values from repeat PaCO2 modulations (Fig. 1C). t-score was
defined as: [meanT2[PaCO2(+)]-meanT2[PaCO2(-)]/standard
error[PaCO2(+), PaCO2(-)]); and CoRs were derived using
the t-score and the degree of freedom of the measurements. Null hypotheses were
rejected if CoR>0.95.
Results
Figure 2 shows representative findings in a healthy animal and an animal
with coronary stenosis. Healthy
Subjects: Panel A shows representative t-scores and CoR maps derived from
T2 maps acquired using 1 block and 4 blocks of PaCO2 stimulation. Note
that with increasing number of PaCO2 blocks both the t-scores and
CoRs are increased; and that with 4 blocks of PaCO2 modulation, all
segments reach CoRs >0.95. Panel B shows that PET myocardial perfusion
reserve (MPR) is substantially greater than 2 from the same animal. Panels C
and D show quantitative comparisons of t-scores and CoRs. These findings were
consistent across all animals. Coronary
Stenosis: Panels E, F, G, and H
show representative results from an animal with LAD stenosis. Note that while a
similar trend to the healthy subjects are evident in the remote segments, the
affected segments show no increase in t-scores or CoRs with increased blocks.
Panel E shows significantly lower t-scores and CoRs in the LAD territories from
maps with 4 blocks while no obvious spatial BOLD response is observable in maps
acquired with 1 block. Corresponding PET MPR (panel F) shows obvious perfusion
deficit in the affected territories as identified by maps acquired with 4 blocks.
Panels G and H show vastly improved capability to differentiate between remote
and affected segments with increasing number of blocks. These findings were
also consistent across all animals.Conclusions
Our findings here demonstrate that repeat coronary stimulations with
precisely targeted changes arterial CO2 can be used to significantly
increase the confidence in detecting myocardial BOLD response under conditions
of health and coronary stenosis. We expect our early findings to pave the way
for reliable the detection and quantification of ischemic myocardial volume without
contrast agents or ionizing radiation on the basis of BOLD MRI, and thereby
enabling accurate assessment of ischemic heart disease especially in patients with
advanced renal dysfunction. Acknowledgements
No acknowledgement found.References
1. Yang HJ, Sharif B, Pang J, Kali A, Bi X, Cokic I, Li D, Dharmakumar R. Free-Breathing, Motion-Corrected, Highly-Efficient Whole-Heart T2 Mapping at 3T with Hybrid Radial-Cartesian Trajectory. Magn Reson Med. 2015 Mar 6. doi: 10.1002/mrm.25576.
2.
Yang
HJ, Yumul R, Tang R, Cokic I, Klein
M, Kali A, Sobczyk O, Sharif B, Tang J, Bi X, Tsaftaris SA, Li D, Conte AH,
Fisher JA, Dharmakumar R. Assessment of Myocardial Reactivity to Controlled
Hypercapnia with Free-breathing T2-prepared Cardiac
Blood-Oxygen-Level-Dependent MR Imaging. Radiology. 2014 Apr 17:132549.