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Non-Invasive Assessment of Mesenteric Hemodynamics with 4D flow MRI
Grant S Roberts1, Alejandro Roldan-Alzate2, Christopher J Francois2, and Oliver Wieben1,2

1Medical Physics, University of Wisconsin - Madison, Madison, WI, United States, 2Radiology, University of Wisconsin - Madison, Madison, WI, United States

Synopsis

Chronic mesenteric ischemia (CMI) is caused by inadequate blood flow to the intestines. This study investigates the use of 4D flow MRI to non-invasively assess the hemodynamics of the mesenteric circulation in patients with CMI and controls. Flow was measured in 9 vessels before and after meal challenges for 19 subjects suspected of CMI and 6 controls. Post-prandial flow increased significantly in the supraceliac aorta, superior mesenteric artery, superior mesenteric vein, and portal vein. The flow increase was drastically stunted in patients with CMI. This demonstrates the potential for 4D flow MRI in assisting the challenging diagnosis of CMI.

Introduction

Chronic mesenteric ischemia (CMI) is caused by a blood flow reduction to the intestines. Around 90% of cases are the result of atherosclerosis, however, conditions such as median arcuate ligament syndrome (MALS) may also result in CMI1. Patients with CMI typically present with postprandial abdominal pain, occurring 15-60 minutes after a meal. Recurrent symptoms may result in noticeable weight-loss and fear of food. If left unrecognized, CMI has the potential to progress into life-threatening acute ischemia with bowel infarction1. Thus, an importance is placed on the accurate diagnosis of CMI. This has traditionally been accomplished by invasive interventional angiography and duplex ultrasonography, but evaluation and visualization of mesenteric vasculature can be difficult. 2D phase contrast MRI has previously been proposed to functionally evaluate mesenteric vasculature2,3 and a recent 4D flow pilot study demonstrated a wide range of flow responses to a meal challenge in CMI patients4. This abstract further expands on the use of 4D flow MRI in assessing CMI through quantifying hemodynamics in the major vessels of the upper abdomen in patients and controls before and after a meal challenge.

Methods

In this IRB-approved and patient-compliant study, 19 subjects (age range 21-86y, mean = 49y, females = 13) presenting with symptoms of mesenteric ischemia and 6 healthy subjects (age range 31-46y, mean = 39y, females = 2) were imaged on clinical 1.5T and 3.0T scanners (GE Healthcare). One patient was brought for a second scan after surgical intervention. For all subjects, 4D flow data were acquired before and after a meal challenge using a radially undersampled trajectory (5-point PC-VIPR5,6) with full volumetric coverage of the upper abdomen: imaging volume: 32x32x24cm spherical; 1.25mm isotropic resolution; TR/TE = 6.4-8.4ms/2.2-2.5ms; VENC = 100-120 cm/s; intravascular contrast agent (0.03mmol/kg of gadofosveset trisodium (Lantheus, N. Billerica, MA)); with retrospective ECG and respiratory gating. Pre-prandial imaging was performed after 5 hours of fasting. After the first scan, subjects orally ingested 574 mL EnSure Plus® (Abbot Laboratories, Columbus, OH) and scanning was resumed 20 minutes after ingestion. 3D vessel segmentation from the PC data was performed semi-automatically using Mimics (Materialize, Leuven, Belgium). Flow visualization and flow analysis plane placement was accomplished in Ensight (CEI, Apex, NC) (Figures 1-2). Flow analysis was conducted in 6 arterial and 3 portal vessel segments. Arterial vessels: supraceliac aorta (SCAo), infrarenal aorta (IRAo), celiac artery (CA), superior mesenteric artery (SMA), right renal artery (RRA), and left renal artery (LRA). Portal vessels: splenic vein (SV), superior mesenteric vein (SMV), and portal vein (PV). Magnitude and velocity vector data from these 9 analysis planes were exported to a customized software package7 that allowed for manual vessel segmentation and hemodynamic analysis throughout the cardiac cycle. Statistical analysis was performed using paired t-tests (between pre- and post-prandial states) as well as a two-sample t-test (between groups) with a P<0.05 for establishing statistical significance.

Results

4D flow data were successfully obtained for all 52 flow scans. Figures 1-2 show representative streamline visualizations. The flow changes between pre and post meal measurements for patients and controls are shown in Figures 3-4. Notable observations with statistical significance include: flow increases in both groups in the SCAo (controls: 23.9%; patients: 10.4%), SMA(c:129.1%, p:35.6%), SMV(c:151.1%, p:81.7%), and PV(c:89.4%, p:46.7%) and a decrease in RRA flow (-14.5%) in patients. Cross comparing the flow difference between both groups showed a statistically significant difference in meal challenge responses, specifically, the ischemia group showed less change in flow after a meal in the SCAo, SMA, SMV, and PV (also Figure 3). The other vessels measured (IRAo, LRA, RRA, CA, and SV) did not show statistically significant meal response differences. Figure 5 shows results from a patient diagnosed with MALS, who was imaged before and after surgical intervention, showing dramatic changes in flow volumes after therapy.

Discussion

The patient group showed consistently lower flow rates than the controls, possibly due to overall compromised cardiovascular health. These differences were significantly amplified in their stunted flow responses to a meal challenge, particularly in the SMA, SMV, and PV. This is most likely due to intrinsic pathology that is preventing the vessels from fulfilling the demand for increased blood flow to the abdomen.

Conclusion

This study demonstrates the feasibility of using 4D flow MRI to non-invasively and comprehensively assess the functional response to a meal challenge in patients suspicious of possible mesenteric ischemia. Additionally, the comprehensive anatomical coverage of all mesenteric vessels can identify collateral pathways and further aid in diagnosis. In summary, this is a promising approach to quantitatively and qualitatively aid in the difficult diagnosis of mesenteric ischemia and studies with larger patient cohorts are warranted.

Acknowledgements

We gratefully acknowledge research support from GE Healthcare.

References

1. Wilkins LR, Stone JR. Chronic mesenteric ischemia. Tech Vasc Interv Radiol. 2015;18(1):31-37.

2. KC Li, Hopkins KL, Dalman RL CS. Simultaneous measurement of flow in the superior mesenteric vein and artery with cine phase-contrast MR imaging: value in diagnosis of chronic mesenteric ischemia—work in progress. Radiology. 1995;194(2):327-330.

3. Roldan-Alzate A, Frydrychowicz A, Said A, et al. Impaired regulation of portal venous flow in response to a meal challenge as quantified by 4D flow MRI. J Magn Reson Imaging. 2015;42(4):1009-1017.

4. Wieben O, Roldan-Alzate A, Reeder SB, et al. 4D Flow MRI for non-invasive assessment of Mesenteric Ischemia. ISMRM. 2013;(10):63.

5. Gu T, Korosec FR, Block WF, et al. PC VIPR: A high-speed 3D phase-contrast method for flow quantification and high-resolution angiography. Am J Neuroradiol. 2005;26(4):743-749.

6. Johnson KM, Lum DP, Turski PA, et al. Improved 3D Phase Contrast MRI with Off-resonance Corrected Dual Echo VIPR. Magn Reson Med. 2008;60(6):1329-1336.

7. Stalder AF, Russe MF, Frydrychowicz A, Bock J et al. Quantitative 2D and 3D phase contrast MRI: Optimized analysis of blood flow and vessel wall parameters. MRM. 2008;60(5):1218-1231.

Figures

Figure 1: 4D Flow MRI streamline images for a control subject (figures a and b) and an ischemia subject (figures c and d) both before (figures a and c) and after a meal challenge (figures b and d). The color scale for velocity and the number of streamline emitters are identical for all 4 images. Overall, this ischemia subject showed a reduced flow response after a meal.

Figure 2: 4D Flow MRI data shows streamline visualization of the venous system for a control subject (figures a and b) and an ischemia subject (figures c and d) both before (figures a and c) and after a meal challenge (figures b and d). The color scale for velocity and the number of streamlines emitters are identical for all images above. There is a reduced flow response to the meal challenge in the ischemic cohort.

Figure 3: The bar graph above shows average blood flow for the ischemic group. Standard deviation is provided for each vessel. Statistical significance is denoted by brackets and stars. A flow difference still exists between pre- and post-meal in the SCAo, SMA, SMV, and PV for the ischemia group but, when comparing this data to the control group, the change in flow in these vessels is far less drastic.

Figure 4: A two-sample t-test was performed on the change in pre- and post-meal flow values between both groups. Yellow indicates statistical significance. The control group showed an average blood flow increase in the SCAo, SMA, SMV, and PV. The ischemic group showed an average flow increase in the SMA, SMV, and PV as well as a decrease in flow in the RRA. There is less of an increase in flow in the SCAo, SMA, SMV, and PV for the ischemic subjects.

Figure 5: Patient diagnosed with median arcuate ligament syndrome (MALS). Images are shown before a) and after b) median arcuate ligament release surgery. Image a) clearly shows disturbed flow, due to the pinching of the CA caused by the median arcuate ligament. Image b) shows post-surgery flow. Flow in the CA increased by 156% after surgery.

Proc. Intl. Soc. Mag. Reson. Med. 26 (2018)
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