Tameshwar Ganesh1,2, Marvin Estrada3, James Duffin4, and Hai-Ling Margaret Cheng1,2,5,6
1Leslie Dan Faculty of Pharmacy, University of Toronto, Toronto, ON, Canada, 2Physiology & Experimental Medicine, Hospital for Sick Children Research Institute, Toronto, ON, Canada, 3Lab Animal Services, Hospital for Sick Children, Toronto, ON, Canada, 4Anesthesia, University of Toronto, Toronto, ON, Canada, 5Institute of Biomaterials & Biomedical Engineering, University of Toronto, Toronto, ON, Canada, 6The Edward S. Rogers Sr. Department of Electrical & Computer Engineering, University of Toronto, Toronto, ON, Canada
Synopsis
Inspiring
gases with altered O2 and CO2 levels is an approach to assess the health of the
cerebral vasculature. However, application of this technique in the body is new
and less well understood compared to its application in the brain. In this
study, we adopt a comprehensive approach to investigate the MR signatures of
abdominal tissue response to a wide spectrum of gas challenges. Results in the
liver, kidney, and muscle of healthy rats confirmed T2* as a robust marker of
blood oxygen saturation but suggested that T1, other than its conventional association
to tissue oxygenation, may a marker of blood volume changes.TARGET AUDIENCE
Physiologists, radiologists, oncologists
PURPOSE
The
integration of MR imaging and a gas challenge stimulus (i.e. application of
inspired gases containing different levels of O2 and CO2)
is a method for non-invasively assessing cerebral vascular response in both
health and disease. The application of this approach to assess extra-cranial
tissue is an emerging research topic
1-3 but is much less thoroughly
characterized and understood, especially in the hypoxic regime. In this study, we
adopt a comprehensive approach to systematically study and characterize the MRI
responses of various extra-cranial tissues to graded levels of hyperoxia, hypercapnia,
and hypoxia, using a dedicated gas-mixing circuit for controlled delivery to healthy
rats.
METHODS
This
study was approved by our institutional animal care committee. A system
consisting of a computer-controlled gas mixer, an MR-compatible isoflurane
vaporizer, and an MR-compatible ventilator was built to control the delivery of
precise levels of gases to small animals. Twelve female adult Sprague Dawley
rats (Charles River Laboratories) weighing 250-300 g were anesthetized on 5%
isoflurane, intubated with a 14-gauge angiocatheter, and transferred to a water
blanket maintained at 38°C.
The endotracheal tube was connected to the gas delivery system, and sensors of
a mouse oximeter were clipped to the hindpaw to monitor heart rate and blood
oxygen saturation. The animal was maintained on 2% isoflurane for the rest of
the experiment, resting supine inside an 8-channel wrist coil and imaged on a
3-Tesla scanner (Achieva 3.0 T TX, Philips Medical Systems). Baseline coronal
3D T1-weighted spoiled-gradient echo images with fat
suppression were acquired: TR=3.73 ms, TE=1.85 ms, FA=20°, NSA=3, FOV=100mm, ten 3-mm slices, 0.7x0.7 mm in-plane. After 20 minutes of baseline
normoxia (21% O2), gas challenges of 10 minute duration were
applied, interleaved with 20 minutes of normoxia to return to baseline, during
which time ventilation was increased to 104 breaths per minute to wash out
residual CO2. Four different types of gas challenge were studied:
graded hyperoxia, hypercapnia, hypoxia, and hypercapnic hypoxia. Four animals
were used to study each level of gas stimulus. Toward the end of the gas
challenge, T1 mapping was performed using a variable flip angle approach
4:
FA=2, 10, 20°,
TR=5 ms, TE=1.85 ms, NSA=3. T2* mapping was performed using a gradient-echo
sequence: TR=50ms, TE=2ms, 32 echoes with 1.485ms spacing, FA=30°, NSA=2. MRI data was analyzed using in-house
software in Matlab (v.8.3). Regions of interest were outlined on the liver,
kidney cortex, and paraspinal muscle to obtain mean T1 and T2* values. Changes
in relaxation times from baseline were compared across animals using two-way
ANOVA and post-hoc Tukey-Kramer tests performed at the 95% confidence level.
RESULTS
Fig
1 shows anatomical images and T1 and T2* maps of the liver and kidney in an
animal subjected to hypercapnic hypoxia (other gas stimuli not shown). Figs 2 and 3 compare relative changes in T2* and T1 in different abdominal tissues
across all animals for all gas challenge levels. As seen in Fig 2, T2*
decreased consistently for all hypercapnic and
hypoxic challenges, consistent with measured decreases in blood oxygen
saturation levels (27% to 45%). T1 decreased on hyperoxia, consistent with
increased tissue oxygenation, but decreased also for hypercapnic and hypoxic
challenges. As expected, the heart rate lowered (6% to 16%) on hyperoxia and
increased (13% to 60%) on many of the hypercapnic and hypoxic challenges.
DISCUSSION
T2*
is a sensitive marker of blood oxygen saturation, to the extent that concurrent
physiological responses can be potentially masked. T1 is sensitive to tissue
oxygenation only under hyperoxia; for hypercapnic and hypoxic challenges, T1
changes are not consistent with changes in tissue oxygenation, suggesting the
role of T1 as a weak marker of blood volume.
CONCLUSION
T2*
and T1 have complementary roles in evaluating extra-cranial tissue response to
a broad range of gas challenges.
Acknowledgements
Funding from the Heart & Stroke Foundation of Canada and the Natural Sciences and Engineering Research Council of Canada.References
1. Winter JD et al. Normal tissue quantitative T1 and T2* MRI relaxation
time responses to hypercapnic and hyperoxic gases. Acad Radiol 2011; 18(9);1159-1167.
2. O’Connor JP et al. Organ-specific
effects of oxygen and carbogen gas inhalation on tissue longitudinal relaxation
times. Magn Reson Med 2007; 58(3):490-496.
3. Pohlmann A et al. Detailing the relation
between renal T2* and renal tissue pO2 using an integrated approach of
parametric magnetic resonance imaging and invasive physiological measurements.
Invest Radiol 2014;49(8):547-560.
4. Cheng HL and Wright GA. Rapid high-resolution T(1)
mapping by variable flip angles: accurate and precise measurements in the
presence of radiofrequency field inhomogeneity. Magn Reson Med 2006; 55(3):566-574.