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In Vivo Quantification of Aortic Stiffness in Abdominal Aortic Aneurysm Patients using MR Elastography: A Longitudinal Study
Huiming Dong1,2, Brian Raterman1, Xiaokui Mo3, Prateek Kalra1, Richard White1, and Arunark Kolipaka1

1Department of Radiology, The Ohio State University Wexner Medical Center, Columbus, OH, United States, 2Department of Biomedical Engineering, The Ohio State University, Columbus, OH, United States, 3Center for Biostatistics, The Ohio State University, Columbus, OH, United States

Synopsis

Abdominal aortic aneurysm (AAA) rupture causes death in 90% of AAA patients. Clinically, the rupture potential is evaluated using AAA diameter. Aortic stiffness can potentially provide more accurate rupture risk assessment. Therefore, the aim of this study is to use non-invasive MR elastography (MRE) to estimate aortic stiffness in AAA patients, and study the relationship between stiffness and AAA diameter. Results showed that aortic stiffness varied during the serial follow-up, demonstrating (1) no correlation between AAA stiffness and diameter, and (2) AAA diameter may not be an accurate indicator for rupture potential.

Introduction

Abdominal aortic aneurysm (AAA) is an abnormal vascular dilation of the abdominal aorta. Although the disease usually progresses without significant symptoms, AAA can eventually lead to aortic rupture, making it a leading cause of death in the United States [1]. Clinically, AAAs with diameter ≥5.0cm are considered high-risk, suggesting higher chances of rupture when compared to those with diameter <5.0cm. However, several studies have shown that small AAAs (<5.0cm) can also rupture, demonstrating that diameter is a poor indicator for rupture potential [2-4]. Aortic stiffness has been suggested as a better alternative for rupture risk assessment as it can provide critical information about the overall AAA mechanical integrity. MR elastography (MRE) is a phase-contrast MR technique for estimating the shear stiffness of soft tissues. It has been demonstrated that it is feasible to non-invasively evaluate aortic stiffness in healthy volunteers [5-6], AAA patients [7] and large animal models [8] using aortic MRE. Despite the effort in studying relationships between arterial stiffness and cardiovascular diseases, a longitudinal study has not been performed in which AAA stiffness and diameter variation are serially tracked during the course of AAA development using MRE. Moreover, the correlation between AAA stiffness and diameter remains unknown. Therefore, the aim of this work is to serially follow AAA patients every 6 months to obtain MRE-measured AAA stiffness for understanding the change in stiffness and diameter during the development of the disease.

Methods

In this study, 37 AAA patients were recruited. Each patient was serially scanned for every 6 months. Among all patients, 37, 13, 7, 4 and 1 patient visited the scanner 1-5 times in a span of three years, respectively.

MR imaging was performed in a 3T MR scanner (TimTrio, Siemens Healthcare, Erlangen, Germany) using a GRE MRE sequence [9]. Patients were scanned in head first-supine position as demonstrated in Figure 1. The imaging parameters included: TE/TR= 21/25ms. FOV=400x400mm2; reconstruction matrix size=256x256; slice thickness=6mm; no. of slices=3; mechanical frequency=60Hz; motion encoding gradient frequency=60Hz; three-directional motion encoding; 4 phase offsets.

Aortic MRE data was processed using MRElab (Mayo Clinic, Rochester, MN). The first harmonic displacement was filtered using eight 4th-order Butterworth band-pass directional filters with cutoffs of 1-40waves/FOV to eliminate longitudinal waves and wave reflections. Subsequently, a local-frequency estimation (LFE) inversion was performed on the 3D volumetric MRE dataset to obtain spatial frequencies from the filtered displacement data in each motion encoding direction [10]. The reported stiffness is then calculated by a weighted combination of first harmonic amplitudes in all three directions.

Results and Discussion

Figure 2 demonstrates the magnitude images in sagittal view, wave images and corresponding stiffness maps of the same patient during his 3 serial visits. The AAA diameters were 5.6cm, 5.8cm and 5.9cm for these 3 visits, respectively. The mean AAA stiffness measured by MRE was 6.10±2.53, 8.34±3.26 and 10.26±5.14kPa.

AAA with similar diameter had different stiffness. Figure 3 displays AAAs with various diameters and stiffness values from different patients. Small AAAs (i.e., AAAs<5.0cm) were not necessarily more compliant than large AAAs (i.e., AAAs>5.0cm) and vice versa, indicating that AAA diameter may not be adequate to determine the mechanical integrity of aneurysms.

The stiffness of AAA measured at patients’ first visit was significantly higher than that of remote AAA region (i.e., the normal portion of the abdominal aorta) (p<0.0001). Figure 4 demonstrates aortic stiffness and AAA diameter variation of all patients during different visits. The mean aortic stiffness was 4.94±1.69kPa (normal aorta at visit 1), and 7.85±2.51, 8.39±1.79, 7.29±1.44, 10.28±0.32 and 10.73kPa for AAA at visit 1 to visit 5, respectively.

There was no significant difference in AAA diameter among different visits. The mean AAA diameter was 4.68±1.36, 4.18±0.74, 4.24±0.93, 4.52±1.09 and 4.09cm for visit 1 to visit 5, respectively.

There was no significant correlation observed between MRE-derived aortic stiffness and AAA diameter with a Pearson correlation coefficient -0.048 (p=0.726). Moreover, the change in aortic stiffness did not correlate to the change in AAA diameter (R2=0.0966). The change in diameter and AAA stiffness was measured by comparing each follow-up visit to the first visit. Figure 5 displays the scatter plot of aortic stiffness and AAA diameter, demonstrating that the overall mechanical integrity of AAA was not correlated to its size.

Conclusion

MRE demonstrated that aortic stiffness varied during the serial follow-up, indicating changes in AAA wall integrity. There was no correlation found between aortic stiffness and AAA diameter, suggesting that AAA diameter did not indicate the mechanical integrity of aneurysms. Therefore, aortic MRE is a potential tool for AAA diagnosis and may provide accurate rupture risk assessment.

Acknowledgements

No acknowledgement found.

References

[1] Kuivaniemi H, Platsoucas CD, Tilson 3rd MD. Aortic aneurysms: an immune disease with a strong genetic component. Circulation 2008;117(2):242-252.

[2] Brewster DC, Cronenwett JL, Hallett JW Jr, Johnston KW, Krupski WC, Matsumura JS. Guidelines for the treatment of abdominal aortic aneurysms. Report of a subcommittee of the Joint Council of the American Association for Vascular Surgery and Society for Vascular Surgery. J Vasc Surg 2003;37:1106-17.

[3] Nicholls SC, Gardner JB, Meissner MH, Johansen HK. Rupture in small abdominal aortic aneurysms. J Vasc Surg 1998;28:884-8.

[4] Lederle FA, Wilson SE, Johnson GR, Reinke DB, Littooy FN, Acher CW, et al. Immediate repair compared with surveillance of small abdominal aortic aneurysms. N Engl J Med 2002;346:1437-44.

[5] Damughatla AR, Raterman B, Sharkey-Toppen T, Jin N, Simonetti OP, White RD, Kolipaka A. Quantification of Aortic Stiffness Using MR Elastography and Its Comparison to MRI-Based Pulse Wave Velocity. J Magn Reson Imaging 2015;41(1):44-51.

[6] Kenyhercz WE, Raterman B, Illapani VS, Dowell J, Mo X, White RD, Kolipaka A. Quantification of aortic stiffness using magnetic resonance elastography: Measurement reproducibility, pulse wave velocity comparison, changes over cardiac cycle, and relationship with age. Magn Reson Med 2016;75(5):1920-1926.

[7] Kolipaka A, Illapani VS, Kenyhercz W, Dowell JD, Go MR, Starr JE, Vaccaro PS, White RD. Quantification of abdominal aortic aneurysm stiffness using magnetic resonance elastography and its comparison to aneurysm diameter. J Vasc Surg 2016;64(4):966-974.

[8] Dong H, Mazumder R, Illapani VS, Mo X, Simonetti OP, White RD, Kolipaka A. In Vivo Quantification of Aortic Stiffness Using MR Elastography in Hypertensive Porcine Model. Magn Reson Med 2017, DOI: 10.1002/mrm.26601.

[9] Chamarthi S, Raterman B, Mazumder R, Michaels A, Oza V, Hanje J, Bolster B, Jin N, White RD, Kolipaka A. Rapid Acquisition Technique for MR Elastography of the Liver. Magn Reson Imaging 2014;32(6):679-683.

[10] Knutsson H, Westin CF, Granlund G. Local multiscale frequency and bandwidth estimation. Image Processing, 1994,IEEE International Conference 1994;Vol. 1:36-40.

Figures

Figure 1. Experimental Set-Up for In Vivo Aortic MRE. Aortic MRE measurements were performed in AAA patients using head first-supine position. Mechanical waves were generated via an active pneumatic driver placed outside the scan room. A passive driver was placed in the abdomen region of patients and the driver was connected to the active driver through plastic tube. The mechanical wave frequency was 60Hz for achieving optimal tissue penetration and spatial resolution.

Figure 2. Aortic MRE Measurements in One Patient during 3 Serial Visits. Magnitude images in sagittal view of the same patient from his 3 serial visits (a-c) were displayed to demonstrate the disease progression. The AAA diameter increased from 5.6 to 5.8cm during his 3 visits. Snapshots of propagating waves along readout direction (i.e., the vertical direction) at four different time points in the abdominal aorta were shown (d-f). The mean aortic stiffness increased as the disease developed. The mean aortic stiffness measured by MRE (g-i) was 6.10±2.53, 8.34±3.26 and 10.26±5.14kPa for first to third visit, respectively.

Figure 3. Aortic Stiffness and AAA Diameters in Different Patients. Magnitude images in sagittal view and stiffness maps of AAAs with different diameters. Small AAAs (k) were not necessarily more compliant than large AAAs (b) and vice versa. Moreover, AAAs with similar diameters could have considerably different mean aortic stiffness (e.g., b vs. d), demonstrating that AAA diameter may not be an accurate indicator of the mechanical integrity of aneurysms.

Figure 4. Variation in Aortic Stiffness and AAA Diameter. Aortic stiffness varied during the serial follow-up, indicating changes in the mechanical integrity of AAA wall (a). The stiffness of AAA was significantly higher than that of remote AAA region (i.e., the normal portion of the abdominal aorta) during patients’ first visit, (p<0.0001). There was no significant difference in AAA diameter among different visits (b).

Figure 5. Correlation between Aortic Stiffness and AAA Diameter. (a) shows that there was no significant correlation observed between MRE-derived aortic stiffness and AAA diameter with Pearson correlation coefficient -0.048 (p=0.726). Additionally, (b) demonstrates that the change in aortic stiffness did not correlated to the change in AAA diameter (R2=0.0966), suggesting that AAA diameter was independent of the aortic stiffness and thus could not provide adequate insight of rupture potential.

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