Rasha Elmghirbi1,2, Nagaraja N. Tavarekere3, Stephen L. Brown4, Swayamprava Panda1, Kelly A. Keenan3, Glauber Cabral1, Hassan Bagher-Ebadian2,4, and James R. Ewing1,2
1Neurology, Henry Ford Hospital, Detroit, MI, United States, 2Physics, Oakland University, Rochester Hills, MI, United States, 3Neurosurgery, Henry Ford Hospital, Detroit, MI, United States, 4Radiation Oncology, Henry Ford Hospital, Detroit, MI, United States
Synopsis
An elevated tumor interstitial fluid pressure (TIFP) is a critical element for
assessing therapeutic response. This study demonstrates the use of DCE-MRI to estimate TIFP, and validates
that estimate by an invasive method in a rat glioblastoma model, with
and without treatment interventions.
Significant positive correlations between MRI-derived TIFP estimates and
invasive measures of TIFP were found in all groups (e.g., for untreated group, R2=0.76,
p<0.0001). These findings validate an MRI-estimated TIFP as a noninvasive
measure of TIFP in embedded cerebral
tumors, and suggest that it may be a useful tool in assessing tumor
response to therapy.
Purpose:
To use dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) to
estimate tumor Interstitial fluid pressure (TIFP) and hydraulic conductivity in
a rat model of embedded cerebral tumor; to validate that estimate with a direct
invasive measure of TIFP. TIFP, elevated in most solid tumors, limits central
perfusion in a tumor and thus limits the efficacy of common therapies. An
elevated TIFP is considered a mark of aggressiveness, and a decreased TIFP is a
predictor of response to therapy1. TIFP has been measured by such
invasive methods as the wick-in-needle (WIN) technique, but this direct measure
is impractical in many tumor types, and in repeated
studies.Methods:
A
model for estimating TIFP was developed, based on the mean flux of the contrast
agent Magnevist at the tumor periphery; this flux is driven by the IFP gradient
at the tumor surface (see Fig.1), and by such characteristics of the
interstitium as porosity and interstitial hydraulic conductivity.
Twenty-two athymic rats were inoculated intracerebrally with U251 glioblastoma tumor cells. DCE-MRI
was conducted in control, bevacizumab-treated,
and cilengitide+RT-treated rats, followed by a needle-based WIN measurement of
TIFP for each animal. By using model selection to define the edge of the
tumor, and the application of Patlak and Logan plots to DCE-MRI data,
extracellular volume fraction, VD (i.e., porosity) in the tumor2,
and velocity of exudate fluid at the tumor surface were derived3. Hydraulic
conductivity was estimated for each animal by using the Kozeny–Carman equation4, which
depends mainly on VD, and TIFP was estimated via Darcy’s law4, which relates the IFP gradient and the
velocity of exudate fluid at the tumor surface through hydraulic conductivity. TIFP
estimates were compared to WIN measures performed immediately after the DCE-MRI
study.Results:
The mean of the
estimated hydraulic conductivity (MRI-K) in the control group was (2.3 ± 3.1) x 10-5 [mm2/mmHg-s],
which is in agreement with other reports. See
Fig. 2, showing significant positive correlations between WIN-TIFP and MRI-TIFP in all
groups. In the control group, MRI-TIFP was a strong predictor of WIN-TIFP (R2
= 0.76, p<0.0001). Similarly, in the treated Bevacizumab and Cilengitide+RT groups, MRI-TIFP remarkably
predicted WIN-TIFP ( R2 = 0.84, p= 0.009), and (R2
= 0.80, p = 0.005), respectively. Discussion:
These results demonstrate that, if hydraulic conductivity can be
estimated from the measured porosity of the tissue, then TIFP can be
noninvasively estimated. Neglecting the individual tumor’s differences in
hydraulic conductivity in determining TIFP may lead to substantial systematic
errors in estimation of TIFP. A poor correlation between the MRI-TIFP and WIN-TIFP
(R2=0.13, p= 0.23) occurred when a fixed value of hydraulic
conductivity was applied in our model instead of the MRI-K for the control group.
A multivariate analysis of WIN-TIFP and MRI tumor vascular parameters confirmed
these results, showing that VD in the tumor (i.e., tumor porosity),
the main factor in estimating MRI-K, was found to be the
most tumor parameter to describe TIFP with p= 0.0002.Conclusion
These findings demonstrate that TIFP can be estimated noninvasively
using DCE-MRI in embedded cerebral
tumors. Since the methods are noninvasive, they might be a useful tool
in both pre-clinical and clinical
studies for assessing tumor response to therapy. Acknowledgements
The authors thank Ms.
Jun Xu for her superb technical assistance.References
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Interstitial fluid pressure in tumors: therapeutic barrier and biomarker of
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Peritumoral tissue compression is predictive of exudate flux in a rat model of
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Phenomena in Biological Systems: Pearson Prentice Hall; 2010.