Current in vivo abdominal aortic aneurysm (AAA) imaging approaches tend to focus on maximum diameter but do not measure three-dimensional (3D) vascular deformation or strain. Complex vessel geometries, heterogeneous wall compositions, and surrounding structures can all influence aortic strain. Improved understanding of complex aortic kinematics has the potential to increase our ability to predict aneurysm expansion and eventual rupture. Here, we describe a method that combines four-dimensional (4D) ultrasound and direct deformation estimation to compute in vivo 3D Green-Lagrange strain in murine angiotensin II-induced suprarenal dissecting aortic aneurysms, a commonly used small animal model. We compared heterogeneous patterns of the maximum, first-component 3D Green-Lagrange strain with vessel composition from mice with varying AAA morphologies. Intramural thrombus and focal breakage in the medial elastin significantly reduced aortic strain. Interestingly, a dissection that was not detected with high-frequency ultrasound also experienced reduced strain, suggesting medial elastin breakage that was later confirmed via histology. These results suggest that in vivo measurements of 3D strain can provide improved insight into aneurysm disease progression. While further work is needed with both preclinical animal models and human imaging studies, this initial murine study indicates that vessel strain should be considered when developing an improved metric for predicting aneurysm growth and rupture.

References

1.
Wilson
,
J. S.
,
Virag
,
L.
,
Di Achille
,
P.
,
Karšaj
,
I.
, and
Humphrey
,
J. D.
,
2013
, “
Biochemomechanics of Intraluminal Thrombus in Abdominal Aortic Aneurysms
,”
ASME J. Biomech. Eng.
,
135
(
2
), p.
021011
.
2.
Satriano
,
A.
,
Rivolo
,
S.
,
Martufi
,
G.
,
Finol
,
E. A.
, and
Di Martino
,
E. S.
,
2015
, “
In Vivo Strain Assessment of the Abdominal Aortic Aneurysm
,”
J. Biomech.
,
48
(
2
), pp.
354
360
.
3.
Kurvers
,
H.
,
Veith
,
F.
,
Lipsitz
,
E.
,
Ohki
,
T.
,
Gargiulo
,
N.
,
Cayne
,
N.
,
Suggs
,
W.
,
Timaran
,
C.
,
Kwon
,
G.
, and
Rhee
,
S.
,
2004
, “
Discontinuous, Staccato Growth of Abdominal Aortic Aneurysms
,”
J. Am. Coll. Surg.
,
199
(
5
), pp.
709
715
.
4.
Glimaker
,
H.
,
Holmberg
,
L.
, and
Eriksson
,
I.
,
1991
, “
Natural History of Patients With Abdominal Aortic Aneurysm
,”
Eur. J. Vasc. Endovasc. Sci.
,
5
(
2
), pp.
125
130
.
5.
Lederle
,
F. A.
,
Noorbaloochi
,
S.
,
Nugent
,
S.
,
Taylor
,
B. C.
,
Grill
,
J. P.
,
Kohler
,
T. R.
, and
Cole
,
L.
,
2015
, “
Multicentre Study of Abdominal Aortic Aneurysm Measurement and Enlargement
,”
Br. J. Surg.
,
102
(
12
), pp.
1480
1487
.
6.
Heller
,
J. A.
,
Weinberg
,
A.
,
Arons
,
R.
,
Krishnasastry
,
K. V.
,
Lyon
,
R. T.
,
Deitch
,
J. S.
,
Schulick
,
A. H.
,
Bush
,
H. L.
, Jr.
, and
Kent
,
K. C.
,
2000
, “
Two Decades of Abdominal Aortic Aneurysm Repair: Have we Made Any Progress?
,”
J. Vasc. Surg.
,
32
(
6
), pp.
1091
1100
.
7.
Blankensteijn
,
J. D.
,
de Jong
,
S. E. C. A.
,
Prinssen
,
M.
,
van der Ham
,
A. C.
,
Buth
,
J.
,
van Sterkenburg
,
S. M. M.
,
Verhagen
,
H. J. M.
,
Buskens
,
E.
, and
Grobbee
,
D. E.
,
2005
, “
Two-Year Outcomes After Conventional or Endovascular Repair of Abdominal Aortic Aneurysms
,”
N. Engl. J. Med.
,
352
(
23
), pp.
2398
2405
.
8.
Hellenthal
,
F. A.
,
Pulinx
,
B.
,
Welten
,
R. J.
,
Teijink
,
J. A.
,
van Dieijen-Visser
,
M. P.
,
Wodzig
,
W. K.
, and
Schurink
,
G. W.
,
2012
, “
Circulating Biomarkers and Abdominal Aortic Aneurysm Size
,”
J. Surg. Res.
,
176
(
2
), pp.
672
678
.
9.
Choke
,
E.
,
Cockerill
,
G.
,
Wilson
,
W. R. W.
,
Sayed
,
S.
,
Dawson
,
J.
,
Loftus
,
I.
, and
Thompson
,
M. M.
,
2005
, “
A Review of Biological Factors Implicated in Abdominal Aortic Aneurysm Rupture
,”
Eur. J. Vasc. Endovasc. Surg.
,
30
(
3
), pp.
227
244
.
10.
Goergen
,
C. J.
,
Johnson
,
B. L.
,
Greve
,
J. M.
,
Taylor
,
C. A.
, and
Zarins
,
C. K.
,
2007
, “
Increased Anterior Abdominal Aortic Wall Motion
,”
J. Endovasc. Ther.
,
14
(
4
), pp.
574
584
.
11.
Goergen
,
C. J.
,
Azuma
,
J.
,
Barr
,
K. N.
,
Magdefessel
,
L.
,
Kallop
,
D. Y.
,
Gogineni
,
A.
,
Grewall
,
A.
,
Weimer
,
R. M.
,
Connolly
,
A. J.
,
Dalman
,
R. L.
,
Taylor
,
C. A.
,
Tsao
,
P. S.
, and
Greve
,
J. M.
,
2011
, “
Influences of Aortic Motion and Curvature on Vessel Expansion in Murine Experimental Aneurysms
,”
Arterioscler., Thromb., Vasc. Biol.
,
31
(
2
), pp.
270
279
.
12.
Goergen
,
C. J.
,
Barr
,
K. N.
,
Huynh
,
D. T.
,
Eastham-Anderson
,
J. R.
,
Choi
,
G.
,
Hedehus
,
M.
,
Dalman
,
R. L.
,
Connolly
,
A. J.
,
Taylor
,
C. A.
,
Tsao
,
P. S.
, and
Greve
,
J. M.
,
2010
, “
In Vivo Quantification of Murine Aortic Cyclic Strain, Motion, and Curvature: Implications for Abdominal Aortic Aneurysm Growth
,”
J. Magn. Reson. Imaging
,
32
(
4
), pp.
847
858
.
13.
Thubrikar
,
M. J.
,
Labrosse
,
M.
,
Robicsek
,
F.
,
Al-Soudi
,
J.
, and
Fowler
,
B.
,
2001
, “
Mechanical Properties of Abdominal Aortic Aneurysm Wall
,”
J. Med. Eng. Technol.
,
25
(
4
), pp.
133
142
.
14.
Barrett
,
H. E.
,
Cunnane
,
E. M.
,
Hidayat
,
H.
,
O'Brien
,
J. M.
,
Moloney
,
M. A.
,
Kavanagh
,
E. G.
, and
Walsh
,
M. T.
,
2018
, “
On the Influence of Wall Calcification and Intraluminal Thrombus on Prediction of Abdominal Aortic Aneurysm Rupture
,”
J. Vasc. Surg.
,
67
(
4
), pp.
1234
1246.
15.
Phillips
,
E. H.
,
Yrineo
,
A. A.
,
Schroeder
,
H. D.
,
Wilson
,
K. E.
,
Cheng
,
J.-X.
, and
Goergen
,
C. J.
,
2014
, “
Morphological and Biomechanical Differences in the Elastase and AngII ApoE−/− Rodent Models of Abdominal Aortic Aneurysms
,”
BioMed Res. Int.
,
2015
, p.
413189
.
16.
Derwich
,
W.
,
Wittek
,
A.
,
Pfister
,
K.
,
Nelson
,
K.
,
Bereiter-Hahn
,
J.
,
Fritzen
,
C. P.
,
Blase
,
C.
, and
Schmitz-Rixen
,
T.
,
2016
, “
High Resolution Strain Analysis Comparing Aorta and Abdominal Aortic Aneurysm With Real Time Three Dimensional Speckle Tracking Ultrasound
,”
Eur. J. Vasc. Endovasc. Surg.
,
51
(
2
), pp.
187
193
.
17.
Soepriatna
,
A. H.
,
Damen
,
F. W.
,
Vlachos
,
P. P.
, and
Goergen
,
C. J.
,
2017
, “
Cardiac and Respiratory-Gated Volumetric Murine Ultrasound
,”
Int. J. Cardiovasc. Imaging
,
34
(
5
), pp.
713
724
.
18.
Boyle
,
J. J.
,
Kume
,
M.
,
Wyczalkowski
,
M. A.
,
Taber
,
L. A.
,
Pless
,
R. B.
,
Xia
,
Y.
,
Genin
,
G. M.
, and
Thomopoulos
,
S.
,
2014
, “
Simple and Accurate Methods for Quantifying Deformation, Disruption, and Development in Biological Tissues
,”
J. R. Soc., Interface
,
11
(
100
), pp.
20140685
20140685
.
19.
Boyle
,
J. J.
,
Soepriatna
,
A. H.
,
Damen
,
F. W.
,
Rowe
,
R. A.
,
Pless
,
R. B.
,
Kovacs
,
A.
,
Goergen
,
C. J.
,
Thomopoulos
,
S.
, and
Genin
,
G. M.
,
2018
, “
Regularization-Free Strain Mapping in Three Dimensions, With Application to Cardiac Ultrasound
,”
ASME J. Biomech. Eng.
,
141
(
1
), p.
011010
.
20.
Daugherty
,
A.
,
Manning
,
M. W.
, and
Cassis
,
L. A.
,
2000
, “
Angiotensin II Promotes Atherosclerotic Lesions and Aneurysms in Apolipoprotein E–Deficient Mice
,”
J. Clin. Invest.
,
105
(
11
), pp.
1605
1612
.
21.
Trachet
,
B.
,
Aslanidou
,
L.
,
Piersigilli
,
A.
,
Fraga-Silva
,
R. A.
,
Sordet-Dessimoz
,
J.
,
Villanueva-Perez
,
P.
,
Stampanoni
,
M. F. M.
,
Stergiopulos
,
N.
, and
Segers
,
P.
,
2017
, “
Angiotensin II Infusion Into ApoE-/- Mice: A Model for Aortic Dissection Rather Than Abdominal Aortic Aneurysm?
,”
Cardiovasc. Res.
,
113
(
10
), pp.
1230
1242
.
22.
Damen
,
F. W.
,
Adelsperger
,
A. R.
,
Wilson
,
K. E.
, and
Goergen
,
C. J.
,
2016
, “
Comparison of Traditional and Integrated Digital Anesthetic Vaporizers
,”
J. Am. Assoc. Lab. Anim. Sci.
,
54
(
6
), pp.
756
762
.https://www.ncbi.nlm.nih.gov/pubmed/26632785
23.
Damen
,
F. W.
,
Berman
,
A. G.
,
Soepriatna
,
A. H.
,
Ellis
,
J. M.
,
Buttars
,
S. D.
,
Aasa
,
K. L.
, and
Goergen
,
C. J.
,
2017
, “
High-Frequency 4-Dimensional Ultrasound (4DUS): A Reliable Method for Assessing Murine Cardiac Function
,”
Tomography
,
3
(
4
), pp.
180
187
.
24.
Updegrove
,
A.
,
Wilson
,
N. M.
,
Merkow
,
J.
,
Lan
,
H.
,
Marsden
,
A. L.
, and
Shadden
,
S. C.
,
2017
, “
SimVascular: An Open Source Pipeline for Cardiovascular Simulation
,”
Ann. Biomed. Eng.
,
45
(
3
), pp.
525
541
.
25.
Ahrens
,
J.
,
Geveci
,
B.
, and
Law
,
C.
,
2005
,
ParaView: An End-User Tool for Large Data Visualization
,
Academic Press
, Los Alamos, NM.
26.
Vallabhaneni
,
S.
,
Gilling-Smith
,
G. L.
,
How
,
T. V.
,
Carter
,
S. D.
,
Brennan
,
J. A.
, and
Harris
,
P. L.
,
2004
, “
Heterogeneity of Tensile Strength and Matrix Metalloproteinase Activity in the Wall of Abdominal Aortic Aneurysms
,”
J. Endovasc. Ther.
,
11
(
4
), pp.
494
502
.
27.
Phillips
,
E. H.
,
Di Achille
,
P.
,
Bersi
,
M. R.
,
Humphrey
,
J. D.
, and
Goergen
,
C. J.
,
2017
, “
Multi-Modality Imaging Enables Detailed Hemodynamic Simulations in Dissecting Aneurysms in Mice
,”
IEEE Trans. Med. Imaging
,
36
(
6
), pp.
1297
1305
.
28.
Trachet
,
B.
,
Bols
,
J.
,
Degroote
,
J.
,
Verhegghe
,
B.
,
Stergiopulos
,
N.
,
Vierendeels
,
J.
, and
Segers
,
P.
,
2015
, “
An Animal-Specific FSI Model of the Abdominal Aorta in Anesthetized Mice
,”
Ann. Biomed. Eng.
,
43
(
6
), pp.
1298
1309
.
29.
Feintuch
,
A.
,
Ruengsakulrach
,
P.
,
Lin
,
A.
,
Zhang
,
J.
,
Zhou
,
Y.-Q.
,
Bishop
,
J.
,
Davidson
,
L.
,
Courtman
,
D.
,
Foster
,
F. S.
,
Steinman
,
D. A.
,
Henkelman
,
R. M.
, and
Ethier
,
C. R.
,
2007
, “
Hemodynamics in the Mouse Aortic Arch as Assessed by MRI, Ultrasound, and Numerical Modeling
,”
Am. J. Physiol. Heart Circ. Physiol.
,
292
(
2
), pp.
H884
H892
.
30.
Acuna
,
A.
,
Berman
,
A.
,
Damen
,
F.
,
Myers
,
B.
,
Adelsperger
,
A.
,
Bayer
,
K.
,
Brindise
,
M.
,
Bungart
,
B. L.
,
Kiel
,
A. M.
,
Morrison
,
R.
,
Muskat
,
J.
,
Wasilczuk
,
K.
,
Wen
,
Y.
,
Zhang
,
J.
,
Zito
,
P.
, and
Goergen
,
C.
,
2018
, “
Computational Fluid Dynamics of Vascular Disease in Animal Models
,”
ASME J. Biomech. Eng.
,
140
(
8
), p.
080801
.
31.
Ford
,
M. D.
,
Black
,
A. T.
,
Cao
,
R. Y.
,
Funk
,
C. D.
, and
Piomelli
,
U.
,
2011
, “
Hemodynamics of the Mouse Abdominal Aortic Aneurysm
,”
ASME J. Biomech. Eng.
,
133
(
12
), p.
121008
.
You do not currently have access to this content.