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Dissection Properties of the

Gerhard Sommer
Institute for Biomechanics,
Human Aortic Media: An
Graz University of Technology,
8010 Graz, Austria Experimental Study
T. Christian Gasser Aortic dissection occurs frequently and is clinically challenging; the underlying mechan-
Department of Solid Mechanics,
ics remain unclear. The present study investigates the dissection properties of the media
Royal Institute of Technology (KTH),
of 15 human abdominal aortas (AAs) by means of direct tension tests 共n = 8兲 and peeling
100 44 Stockholm, Sweden
tests 共n = 12兲. The direct tension test demonstrates the strength of the media in the radial
Peter Regitnig direction, while the peeling test allows a steady-state investigation of the dissection
Institute of Pathology, propagation. To explore the development of irreversible microscopic changes during
Medical University Graz, medial dissection, histological images 共n = 8兲 from four AAs at different peeling stages
8036 Graz, Austria are prepared and analyzed. Direct tension tests of coin-shaped medial specimens result in
a radial failure stress of 140.1⫾ 15.9 kPa (mean⫾ SD, n = 8). Peeling tests of
Martin Auer rectangular-shaped medial strips along the circumferential and axial directions provide
Institute for Biomechanics, peeling force/width ratios of 22.9⫾ 2.9 mN/ mm 共n = 5兲 and 34.8⫾ 15.5 mN/ mm 共n
Graz University of Technology, = 7兲; the related dissection energies per reference area are 5.1⫾ 0.6 mJ/ cm2 and
8010 Graz, Austria 7.6⫾ 2.7 mJ/ cm2, respectively. Although student’s t-tests indicate that force/width values
of both experimental tests are not significantly different (␣ = 0.05, p = 0.125), the strikingly
Gerhard A. Holzapfel1 higher resisting force/width obtained for the axial peeling tests is perhaps indicative of
Institute for Biomechanics, anisotropic dissection properties of the human aortic media. Peeling in the axial direc-
Centre for Biomedical Engineering, tion of the aorta generates a remarkably “rougher” dissection surface with respect to the
Graz University of Technology, surface generated by peeling in the circumferential direction. Histological analysis of the
8010 Graz, Austria; stressed specimens reveals that tissue damage spreads over approximately six to seven
Department of Solid Mechanics, elastic laminae, which is about 15–18% of the thickness of the abdominal aortic media,
Royal Institute of Technology (KTH), which forms a pronounced cohesive zone at the dissection front.
100 44 Stockholm, Sweden 关DOI: 10.1115/1.2898733兴
e-mail: holzapfel@tugraz.at
Keywords: aortic dissection, dissection energy, failure stress, media, human abdominal
aorta

1 Introduction the adventitia, often with a lethal outcome 关2兴. For example, in the
absence of intervention, acute aortic dissections have a 90%
Arterial dissections may occur spontaneously or nonspontane-
chance of mortality, and the majority of these deaths occur within
ously as a result of traumatic and have been observed in several
arterial branches including the aorta. Aortic dissections frequently 48 h 关7兴.
result from an intimal tear 共see Ref. 关1兴 and references therein兲 or The incidence of spontaneous aortic dissection is 5–30 cases
from a perforation of the intima as, for example, caused by intra- per million people per year, and it strongly depends on the pres-
mural hemorrhage and hematoma formation 关2兴. Moreover, me- ence of risk factors. Among many others, chronic systemic hyper-
chanical traumatization of the intima due to the cannulation for tension, atherosclerosis, Marfan’s and Ehlers-Danlos syndromes,
catheter-based diagnostic and/or therapeutic interventions have aortic dilatation 共aneurysm兲, and coarctation of the aorta are well-
been identified as initiating aortic dissections 关3兴. These intimal established predisposing factors for aortic dissection 关2,8兴.
defects can cause concentrations of mechanical stress of the pres- Chronic systematic hypertension is the most common predispos-
surized aorta and may be the trigger for the propagation of the ing factor and has been present in 62–78% of patients with aortic
medial dissection. In addition, blunt traumatic aortic rupture fol- dissection 关2兴.
lowing motor vehicle accidents carries a high mortality and occurs A common cause of media dissection is balloon angioplasty, an
in 21% of car occupant deaths in the UK 关4兴. Traumatic aortic established and effective therapeutical intervention to reduce the
dissection is one consequence for blunt thoracic trauma patients severity of atherosclerotic stenosis 关9兴. Balloon angioplasty in-
关5兴. In a population-based long-term study, 86 cases of aortic dis- volves denudation of endothelium, disruption of the intima and
section were found in 84 patients 共mean age of 65.7 yr兲, 66 pa- the atherosclerotic plaque with frequent separation from or dissec-
tients were hospitalized and 18 nonhospitalized 关6兴. A total of tion of the media, and overstretching of nondiseased portions of
22.7% of the hospitalized patients died within the first 6 h, 33.3% the arterial wall, see, for example, Ref. 关10兴 and references
within 12 h, 50% within 24 h, and 68% in total died within the therein. In particular, dissection is a characteristic form of arterial
first two days after admission. Untreated, a dissection may propa- trauma involving laceration and/or cleavage of the arterial wall.
gate until it runs either back into the lumen, resulting in the redu- Plaque fracture and/or dissections are major contributors to the
plication of the aortic lumen 共false lumen兲, or it ruptures through gain in lumen following balloon angioplasty 关9兴. Moreover, dis-
section has been implicated as a contributing factor to both acute
procedural complications 共abrupt reclosure, ischemia, myocardial
1
Corresponding author. infarction, emergency surgery, and coronary microembolization
Contributed by the Bioengineering Division of ASME for publication in the JOUR-
NAL OF BIOMECHANICAL ENGINEERING. Manuscript received July 21, 2006; final manu-
关11–15兴兲 and chronic restenosis of the treatment site 关16兴. Luminal
script received October 11, 2007; published online March 28, 2008. Review con- gain, tissue injury, and the risk of wall fracture are quantities for
ducted by Yoram Lanir. consideration with this interventional procedure. Dissection sec-

Journal of Biomechanical Engineering Copyright © 2008 by ASME APRIL 2008, Vol. 130 / 021007-1

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Table 1 Failure properties of arterial tissue according to tensile, inflation, tearing, splitting, and peeling tests. Mean values are
presented with standard deviations.

Tensile test
Circ. strength Axial strength Radial strength
Tissue 共MPa兲 共MPa兲 共MPa兲 Reference

Human descending midthoracic aorta 1.72⫾ 0.89 1.47⫾ 0.91 — 关23兴


Human abdominal aorta — 1.21⫾ 0.33 — 关24兴
Human descending thoracic aorta 1.76⫾ 0.22 1.95⫾ 0.60 — 关25兴
Porcine thoracic aorta — — 0.061⫾ 0.004 关26兴
Human ascending thoracic aorta 1.80⫾ 0.24 1.71⫾ 0.14 — 关27兴
Human abdominal aorta — — 0.140⫾ 0.016 Present study

Inflation test
Tissue Ultimate stress 共MPa兲 Reference

Human descending midthoracic aorta 0.114⫾ 0.032 关28兴


Human descending thoracic aorta 2.7⫾ 1.5 关29兴

Tearing test
Tissue Circ. breaking stress 共MPa兲 Axial breaking stress 共MPa兲 Reference

Porcine upper descending thoracic aorta 2.19⫾ 0.57 0.18⫾ 0.44 关30兴
Porcine lower descending thoracic aorta 3.64⫾ 0.53 0.87⫾ 0.34 关30兴

Media splitting test


Tissue Max. pressure 共MPa兲 Splitting energy 共mJ/ cm2兲 Reference

Porcine descending thoracic aorta 0.077⫾ 0.002 15.9⫾ 0.9 关31兴


Human thoracic and abdominal aorta 0.079⫾ 0.029 0.17 关32兴
Porcine upper thoracic aorta 0.106⫾ 0.022 2.84⫾ 1.19 关33兴
Porcine lower thoracic aorta 0.109⫾ 0.019 2.90⫾ 1.21 关33兴
Porcine upper abdominal aorta 0.095⫾ 0.037 1.88⫾ 0.89 关33兴
Porcine lower abdominal aorta 0.085⫾ 0.027 11.34⫾ 4.05 关33兴
Porcine thoracic aorta 0.071 — 关20兴
Porcine descending thoracic aorta 0.073 — 关34兴

Peeling test
Tissue Circ. dissection energy 共mJ/ cm2兲 Axial dissection energy 共mJ/ cm2兲 Reference

Human abdominal aorta 5.1⫾ 0.6 7.6⫾ 2.7 Present study

ondary to tear propagation is a particular form of balloon tion strength across the lamellae of the media in the radial direc-
angioplasty-induced arterial trauma, and serves as an important tion, while the peeling experiment explores the fracture energy
predictor of clinical outcome after balloon angioplasty interven- required to propagate a dissection. Under certain assumptions, the
tion 关17兴. performed experiments allow an estimation of the constitutive
The rubberlike protein elastin, the stiff fibrous protein collagen, properties of medial dissection within the abdominal aorta. The
and smooth muscle cells influence the mechanical properties of gathered data have served as a basic input for the finite element
arterial walls. In the media of elastic arteries 共like the aorta兲, these modeling of the experiments, presented in the companion paper
three components are found to be organized in medial lamellar 关22兴. From the combined experimental and numerical investiga-
units 关18兴, each of which is about 10 ␮m thick 关19兴. These lami- tion, an accurate prediction of the dissection properties is feasible.
nated structures may be prone to separation creating a cleavage To this end, the material parameters in the finite element model,
plane parallel to the elastic lamellae 关20兴, and hence provide the which affects the dissection process, are varied until the numerical
mechanism to propagate a dissection in parallel to the lumen 关21兴. prediction matches the experimental data. In addition, the me-
Spontaneous aortic dissections typically show steady-state-like chanical study is enhanced by histology at different stages of the
failure propagation, which might indicate a kind of fatigue mecha- peeling test to explore the development of irreversible changes on
nism caused by the pulsatile loading of the aorta. By contrast, the microscale level during medial dissection.
balloon angioplasty causes extraordinarily high mechanical load-
ing to the 共stenotic兲 tissue during one or more episodes of treat- 1.1 Fracture Properties of the Aorta. To our knowledge, the
ment, and hence 共quasi兲static failure mechanisms seem to apply. approach in this study is new. However, a variety of methods have
Although arterial dissection is a frequently occurring phenomenon been developed and implemented with the goal to explore the
and a challenging clinical entity, the underlying biomechanical failure properties of aortic tissue. A summary of related experi-
properties remain largely unclear. mental data is given in Table 1 with respect to tensile, inflation,
The present study was carried out with the goal to investigate tearing, splitting, and peeling tests performed on human, porcine,
the dissection properties of the aortic media. Direct tension and and canine aortic tissues.
peeling experiments of the media of human abdominal aortas The following tests have been performed to determine the ten-
were performed. The direct tension test demonstrates the dissec- sile strength of aortic tissue: Uniaxial tensile tests in radial direc-

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Fig. 1 Arterial layers prepared from an aortic patch „adventitia, media, intima—from left to
right…—donor: male, 63 yr. The arrangement of the test specimens with respect to the medial
patch is shown schematically on the central photograph. Cylindrical „coin-shaped… specimens
were prepared for the direct tension test, and circumferential and axial oriented strip speci-
mens for the peeling tests. The circumferential and axial directions of the artery are indicated
by ␪ and z, respectively. The photographed centimeter scale provides a dimensional reference.

tions 关26兴, circumferential and axial directions 关23,27兴, inflation the peeling test is fundamentally different from the “Tearing test”
tests on circular specimens incorporating bubble inflation tech- and the “Media splitting test,” which was noted by the introduc-
niques 关28兴, inflation tests of intact arteries 关29兴, and tearing tests tion of a separate category in the table.
of arterial strips 关30兴 were performed to determine the tensile
strength of aortic tissue. Besides that, in the literature, only a few
techniques have been presented to investigate the dissection prop- 2 Material and Methods
erties of the aortic media. A commonly used approach has been to 2.1 Material. In the present study, 19 human abdominal aor-
create a bleb by infusing a fluid into the media, as it was presented tas 共AAs兲 共age range 36– 75 yr, ten males and nine females兲 were
for human aortas decades ago 关35,36兴. This idea has been adopted harvested during autopsy within 24 h from death. We have taken
by Roach and co-workers to investigate dissection properties of segments from the infrarenal portion of the AA. It was a require-
the canine thoracic aortas 关21兴, the porcine aorta 关31,33兴, and the ment that pathological changes, such as severe atherosclerosis,
human aorta 关32兴. Moreover, they applied this method to isolated were not present in the specimens. In order to satisfy this require-
and pressurized porcine aortas in order to explore the mechanisms ment, the condition and texture of the intima were closely in-
of dissection propagation under more physiological circumstances spected by a trained pathologist. After harvesting, the specimens
关20,34兴. were stored in a calcium-free and glucose-free 0.9% physiological
The experimental data from tensile tests on aortas indicate that saline solution at 4 ° C until use. Use of autopsy material from
they are dependent on the anatomical site of the vessel and that human subjects was approved by the Ethics Committee, Medical
the tensile failure behavior is perhaps anisotropic 共see Table 1兲. University Graz, Austria. All tests were performed within 48 h
The aortic strength in the axial direction seems to be slightly from death.
lower than in the circumferential direction; however, the large
standard deviation makes this finding inconclusive. The failure 2.2 Specimen Preparation. We conducted two different me-
properties obtained from tensile tests suggest that the tensile chanical failure tests of the media of the AA specimens—denoted
strength of the human aorta is decreasing with increasing distance by 共i兲 direct tension tests and 共ii兲 peeling tests. The peripherally
from the heart. attached adipose and loose connective tissues were carefully re-
Tensile or inflation tests of soft biological tissue are poorly moved from the adventitia of the aortic patch. The AAs were then
suited to quantify the fracture energy of the tissue, since these cut along the axial direction to obtain flat rectangular tissue
testing methods cause unstable 共dynamic兲 failure, i.e., its propa- sheets. For the anatomical separation of the three layers, we tested
gation cannot be controlled. In contrast, tearing experiments, as various locations at which the layer separation process can easily
conducted in Ref. 关30兴, lead to controlled failure propagations of be initiated. The arterial layers were separated with careful dissec-
tissues and allow a quantification of the fracture energy. That pa- tion techniques and with the aid of a surgical scalpel. Reflected
per 关30兴 documents that the circumferential “breaking stress” light microscopy was used to inspect the layer preparation pro-
共evaluated through axial tearing experiments兲 exceeds the axial cess. The structured media could easily be distinguished from the
breaking stress 共evaluated through circumferential tearing experi- intimal and the adventitial tissues. In addition, for all specimens
ments兲, which is in accordance with findings from tensile tests. considered in the study, related histological images were prepared
Media splitting showed that the maximum splitting pressure is and investigated in order to confirm that specimens consisted only
fairly constant; however, the splitting energy decreases with distal of medial tissue. This technique has been successfully applied in
position along the aorta. For comparative purposes, the results the past 共see Refs. 关37,38兴兲. Particular attention has been paid to
from the direct tension and the peeling tests of the present study minimize the mechanical damage of the media including tissue
are included in Table 1. Note that the experimental approach of immersion in a 0.9% physiological saline solution throughout the

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Prepared incision Sandpaper

Sandpaper
F F

Lumen side Adventitia side


10 mm

Fig. 2 Macroscopic view of a representative specimen ready for a peeling test,


and sketch showing the 3D nature of the figure

whole separation process. Figure 1 shows the photographs of the perimental setup shown in Fig. 3兲. The specimens were investi-
separated intimal, medial, and adventitial layers 共from left to gated in a perspex container filled with 0.9% physiological saline
right兲, where it can be seen that even perforating vessels have not solution maintained at 37.0⫾ 1.0° C by a heater-circulation unit
caused any difficulties during the separation process. 共type Ecoline E 200; LAUDA, Lauda-Königshofen, Germany兲
While intimal and adventitial tissues were not further consid- and the tensile force were measured with a 10 N Class 1 strain
ered, the medial patches were used to prepare the specimens for gauge-load cell 共type TCA 10 N, code CTCA1K5; AEP transduc-
the conducted mechanical testing and for subsequent histological ers, Modena, Italy兲. The upper and the lower fixing clamps of the
investigations. A cylindrical blanking tool was used to punch out testing machine are moving in opposite directions, which keeps
eight coin-shaped specimens for the direct tension test 共6.0 mm the center of the specimen fixed in space. A position control res-
diameter, and 1.16⫾ 0.15 mm 共mean⫾ SD兲, thickness兲, subse- olution of 0.04 ␮m of the upper and the lower crosshead of the
quently denoted as D I–D VIII. These eight radial tension test tensile testing machine 共see Fig. 3兲 and a combined error of 0.03%
specimens were obtained from three different AAs. Several speci- of the 10 N load cell are specified by the manufacturer. For our
mens were obtained from the same aorta, as indicated in Fig. 1, case, this means that a combined error of 0.6 mN may occur at a
but note that only about one out of five direct tension tests was maximum occurring force of 2 N.
successful. A total of 12 rectangular-shaped strip specimens were While the specimens for the peeling test could directly be
cut out with a surgical scalpel for the peeling tests, whereas each mounted on the testing machine, an especially developed speci-
peeling sample was from a different AA. From Fig. 1, it can be
seen that the rectangular strips are either oriented in the circum-
ferential direction ␪ or in the axial direction z. Five specimens
Table 2 Thickness of the specimens D I–D VIII for the direct
were cut out along the circumferential direction of the aorta, sub-
tension test
sequently denoted as PC I–PC V, and seven specimens were cut
out along the axial direction of the aorta, subsequently denoted as Thickness
PA I–PA VII. Specimen 共mm兲
In order to get the specimens ready for testing, some final
preparations were required. After mounting the specimens for the DI 1.34
direct tension test on the testing machine, an incision of about D II 1.20
1.0 mm depth around the circumference of the circular specimen D III 0.97
D IV 1.04
was cut with an especially adapted surgical knife. This undercut
DV 1.27
provided the site for the initiation of failure 共and reduced the D VI 1.07
tissue diameter from 6.0 mm to 4.0 mm兲. The specimens devoted D VII 1.34
to the peeling test were split at one end to get two “tongues” D VIII 1.01
共8 – 10 mm in length兲 of about equal thickness for mounting them
on the testing machine. We used a superadhesive gel to glue rect- mean⫾ SD 1.16⫾ 0.15
angular pieces of sandpaper 共Grit: 320兲 at both sides of the
tongues to avoid slipping of the specimen in the clamps of the
testing machine during loading. A representative specimen, ready Table 3 Length Lpc, width, and thickness of the circumferen-
tial peeling test specimens PC I–PC V
for a peeling test, is shown in Fig. 2. The individual dimensions of
the aortic test specimens are summarized in Tables 2–4. Note that Length Lpc Width Thickness
the dimensions refer to the prepared medial patches, and that the Specimen 共mm兲 共mm兲 共mm兲
effective lengths of the peeling test specimens in the circumferen-
tial and axial directions are denoted as Lpc and Lpa, respectively. PC I 30.1 6.5 0.96
PC II 31.5 8.3 1.58
2.3 Mechanical Testing PC III 27.4 8.3 0.93
PC IV 27.1 9.3 1.15
2.3.1 Device. Mechanical tests were performed on a PC V 31.0 8.1 1.20
computer-controlled, screw-driven high-precision tensile testing
machine 共Messphysik, ␮-Strain Instrument ME 30-1, Fürstenfeld, mean⫾ SD 29.4⫾ 2.0 8.1⫾ 1.0 1.16⫾ 0.26
Austria兲, which was adapted for small biological specimens 共ex-

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Table 4 Length Lpa, width, and thickness of the axial peeling mounted on the testing machine and the circular test specimen
test specimens PA I–PA VII was placed in the cylindrical recess. The upper rod of the speci-
men holder was mounted on the testing machine, and a compres-
Length Lpa Width Thickness sion force of 1.0 N was applied to the specimen for about 5 min
Specimen 共mm兲 共mm兲 共mm兲
to allow the adhesive to react. Before testing, the specimen was
PA I 15.0 8.3 2.43 moistened with 0.9% physiological saline solution. Throughout
PA II 18.0 7.8 1.74 the whole test, the extension rate of 1.0 mm/ min was controlled
PA III 30.0 8.2 1.53 and the resisting force recorded. Moreover, the whole test was
PA IV 35.0 8.9 1.43 recorded by a charge coupled device 共CCD兲-camera and saved in
PA V 33.5 8.6 1.57 Super Video-Home-System 共SVHS兲 format. After the specimen
PA VI 25.0 8.2 1.39 was completely separated, the zero load level was defined and the
PA VII 15.0 7.4 1.82
failure surface has been visually inspected. Frequently, it hap-
mean⫾ SD 24.7⫾ 8.0 8.2⫾ 0.5 1.70⫾ 0.36
pened that failure occurred at the region where the specimen was
glued to the specimen holder and not at the location where the
incision was placed. If that was the case, the test was rejected. A
representative photograph of the end stage of a successful direct
men holder was used for the direct tension test. A small tension test is shown in Fig. 5.
cylindrical-shaped recess 共deepening兲 in each plastic rod, with Peeling test. Both tongues of the specimen were mounted on
fixed sandpaper 共Grit: 320兲 therein, leads to a strong specimen-rod the testing machine. Similar to the direct tension test, the exten-
connection. The coin-shaped specimens were then glued with cy- sion rate of 1.0 mm/ min was controlled, and the measured force
anoacrylate glue onto the fixed sandpapers on the two plastic rods recorded. The whole test was recorded, saved in SVHS format,
for mounting on the testing machine 共Fig. 4兲. and the zero load level was defined after complete separation of
the specimen. In order to account for effects of buoyancy, the
2.3.2 Protocol. Direct Tension Test. Cyanoacrylate glue was testing machine’s “buoyancy-force-displacement” curve was sub-
placed on the sandpaper into the cylindrical recess of the upper tracted from the achieved results. This curve was recorded for a
and lower rods of the specimen holder. The lower rod was then particular level of fluid in the perspex container but without a test

Load Cell

Load

Upper Crosshead
Fixing clamps

Specimen

Temperature- PC
controlled CPU 586
Tissue Bath CCD-Camera Video Processing
Length

Width

Lower Crosshead

16 Mhz Position PC
External Digital Control CPU 586
Motor
Controller Data Processing

PC-Control
Load
Position

Fig. 3 Schematic experimental setup

0.6 0.3
Specimen Sand paper
6
15

201.5

Fig. 4 Schematic direct tension fixing tool with a detailed drawing of the specimen-rod con-
nection. Dimensions are given in millimeters.

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20 mm
1 cm
Fig. 7 Photograph of a mechanically fixed specimen in the
Fig. 5 Representative photograph of the end stage of a suc- specimen holder
cessful direct tension test

it was fixed in 7% neutral-buffered formaldehyde solution 共pH


7.4兲, embedded in paraffin using standard techniques and prepared
specimen. A representative image of the medium stage of a cir- for histological investigations.
cumferentially oriented strip specimen during a peeling test is The media, which were partly dissected, were then sectioned at
shown in Fig. 6. 4 ␮m and stained with Elastica van Gieson. The applied tech-
Measurement of specimen dimensions. The geometrical dimen- nique allowed us to investigate, histologically, the gradual devel-
sions 共length, width, thickness兲 of the test specimens were mea- opment of the damage state in the media subjected to supraphysi-
sured optically before the individual tests by using a PC-based ological loading, and to trace and study the irreversible effects in
videoextensometer utilizing a full-image CCD camera. For the the medial tissue due to the mechanical loading.
length and width measurements, the strip samples were positioned
in air on a black plate in front of the CCD camera. After calibra- 3 Results and Interpretation
tion of the videoextensometer, its automatic edge recognition ca-
pability was used to quantify the dimensions. For the thickness 3.1 Direct Tension Test. Figure 8 presents the measured
measurement, the strip sample was positioned in air on a black force-displacement response of all eight coin-shaped media speci-
colored object plate of known thickness 共1 mm兲. One lateral side mens during the direct tension test. The thick 共solid兲 curve char-
acterizes the mean response of the individual tissue tests, which
of the gauge region of the strip sample was in plane with the
are denoted by thin curves. Note that after a radial extension of
lateral side of the object plate and oriented toward and perpen-
dicular to the CCD camera. Then the thickness of the contour approximately 4.5 mm, some curves drop down to zero so that
共sample plus object plate兲 was measured by the videoextensom- less than eight specimens are included in the averaging process
eter within the gauge region. The resulting thickness value of the above 4.5 mm. The mean curve represents the arithmetic mean
sample was determined then as the average of the contour thick- calculated with the data analysis software ORIGINPRO 7.5 共Origin-
ness along the gauge region minus the thickness of the object Lab Corporation兲.
plate. During the increasing displacement, the force-displacement re-
sponse shows a characteristic sequence, which we subsequently
2.4 Histology. In order to investigate irreversible changes of denote by the three regions: S1 for elastic, S2 for damage, and S3
the tissue’s microstructure due to the dissection, eight additional for failure 共see Fig. 8兲. Region S1, i.e., the initial phase of the
rectangular-shaped strips 共four circumferentially and four axially force-extension curve, is assumed to represent the tissue’s elastic
oriented兲 were prepared from four AAs. In contrast to the afore- response and is characterized by a steep slope in the force-
mentioned peeling tests, these strips were not dissected through- displacement curve. It is governed by the geometry of the test
out their whole length. We stopped the peeling approximately in specimen 共diameter, thickness, and incision depth兲 and the mate-
the middle of the strip length. For that reason, we designed a rial properties of the media of the human AA. At about 1.25 N,
specimen holder in order to “freeze” the loading state of the tissue the “elastic limit” is reached. Damage softening 共decreasing stiff-
sample 共Fig. 7兲. After mounting the tissue in the specimen holder, ness with increasing damage of the tissue 关39兴兲 and generation of

Sandpaper
F F

Lumen side Adventitia side

Fig. 6 Representative image of a circumferentially oriented strip specimen


during a peeling test acquired from the videoextensometer, and sketch show-
ing the 3D nature of the image

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S1 S2 S3

S3a S3b F
u

Primary Secondary
mode mode

Force F (N)
S1 ... Elastic
S2 ... Damage
S3 ... Failure

Displacement u (mm)

Fig. 8 Force-displacement behavior for all 8 coin-shaped specimens during


the direct tension test. The thick „solid… curve characterizes the arithmetic
mean response.

microdefects characterize Region S2, which is a region that still gest that the primary dissection S3a is followed by a peelinglike
has increasing resistance to extension. As illustrated in MacLean failure mechanism S3b, which determines a plateau in the force-
et al. 关26兴 共Fig. 4 therein兲, there may be ruptured elastin layers on displacement curve until it drops to zero 共see Fig. 8兲.
a microscale that lead to cavities and to the characteristic pattern
for microdefects in the media. The state of damage evolves further 3.2 Peeling Test. The applied peeling test caused a slow and
until a displacement of about u = 0.85 mm, with the limit force of controlled dissection propagation, where the force-displacement
Fmax = 1.76⫾ 0.20 N 共mean⫾ SD, n = 8兲, is reached, and microde- curve is characterized by a jagged plateau region. In the follow-
fects coalesced. Consequently, the media dissects, which is indi- ing, the results of the peeling of human AA media in circumfer-
cated by the decreasing force in Region S3. Our experiments sug- ential and axial directions are presented separately. Figures 9 and
Force/Width F/w (mN/mm)

F 2l F

Path l (mm)

Fig. 9 Force/width versus dissection path for all five circumferential strip
specimens during the peeling test. The thick „solid… curve characterizes the
arithmetic mean response.

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2l
F F

Force/Width F/w (mN/mm)

Path l (mm)

Fig. 10 Force/width versus dissection path for all seven axial strip specimens
during the peeling test. The thick „solid… curve characterizes the arithmetic
mean response.

10 illustrate the measured force/width with respect to the dissec- the arithmetic means of the experimental data of the five circum-
tion path during the peeling test, where the thick 共solid兲 curves ferentially and seven axially oriented test specimens, i.e., the thick
denote the arithmetic means of the individual tests 共five in circum- 共solid兲 curves in Figs. 9 and 10, were fitted to the horizontal lines
ferential and seven in axial direction兲, which themselves are illus- in the force/width-dissection graph. These defined the average
trated by thin curves. peeling force/width of Fpc = 22.9⫾ 2.9 mN/ mm 共mean⫾ SD, n
We fitted the experimental data of the individual experiments to = 5兲 and of Fpa = 34.8⫾ 15.5 mN/ mm 共mean⫾ SD, n = 7兲 共see
horizontal lines in the force/width-dissection graph, i.e., to con- Table 5兲 of human abdominal medias along the circumferential
stant peeling forces per width, which is motivated by assuming and axial directions, respectively. The student’s t-test 共significance
共ideal兲 rectangular geometries and homogeneous mechanical
level of ␣ = 0.05兲 gives a p value of 0.125, which indicates that the
properties of each specimen. The calculated average resisting
force/width values of both tests are not significantly different.
forces with their related standard deviations of the individual test
However, the strikingly higher resisting force/width obtained for
specimens in circumferential 共PC I–PC V兲 and axial 共PAI–PA VII兲
the axial peeling tests with respect to the circumferential peeling
directions are summarized in Table 5. As can be seen from these
data, and, as already illustrated in Figs. 9 and 10, there is a smaller tests is perhaps indicative of anisotropic dissection properties of
scatter of the circumferential test specimens when compared to the human aortic media.
the axial test specimens, which indicates anisotropic properties of 3.3 Histological Investigation. As mentioned in Sec. 2.4,
the human aortic media in that respect. eight additional rectangular-shaped strips were prepared and dis-
In addition to the investigation of the individual peeling tests, sected up to about the middle of their lengths, and, consequently,
the stress state was “frozen” in a specifically designed device.
Related histological images were prepared. Figure 11共a兲 shows
Table 5 Peeling force/width defining the circumferential and the media in a kind of “frozen stress state,” which straightens the
axial peeling properties of human AA medias: PC I–PC V and
PA I–PA VII refer to the individual specimens for the circumfer- elastic laminae, and the intermingled collagen fibers and smooth
ential and axial peeling tests, respectively. The values Fpc and muscle cells might straighten as well. Figure 11共b兲 shows the
Fpa denote the arithmetic means of the peeling force/width of media embedded under stress-free conditions. The parallel sheets
the five circumferentially and the seven axially oriented test of elastic laminae are attached to each other by fine elastin, col-
specimens, respectively. lagen fibers, and smooth muscle cells, as indicated in the histo-
logical images presented in Fig. 11. For a detailed explanation of
Circumferential peeling Axial peeling the transmural organization of the arterial media, see the electro-
microscopical study 关40兴. We found an average of 40⫾ 4
Specimen Force/Width 共mN/mm兲 Specimen Force/Width 共mN/mm兲 共mean⫾ SD, n = 8兲, lamellar units in the human abdominal aortic
media of the investigated specimens. Note that collagen fiber
PC I 25.2⫾ 2.2 PA I 37.9⫾ 8.2 bundles and smooth muscle cells are barely seen in these images
PC II 22.6⫾ 1.8 PA II 38.0⫾ 5.6 because of the choice of stain, which accentuates elastin fibers.
PC III 21.0⫾ 1.6 PA III 47.6⫾ 9.0 The microscopical damage to the media during the peeling in
PC IV 26.2⫾ 2.9 PA IV 17.0⫾ 3.0
circumferential and axial directions is nicely illustrated in Figs.
PC V 19.3⫾ 2.9 PA V 22.8⫾ 4.3
— — PA VI 20.8⫾ 5.3
12共a兲 and 12共b兲, as can be seen by the area at the dissection front.
— — PA VII 59.3⫾ 10.9 In this area, a pronounced cohesive zone has developed, within
which fiber bridging might play a dominant role. The elastic lami-
— Fpc = 22.9⫾ 2.9 — Fpa = 34.8⫾ 15.5 nae are torn apart and the formation of cavities in between them is
observed 共see Figs. 12共c兲 and 12共d兲 for a zoom into the dissection

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(a) (b)

25µm 25µm

Fig. 11 Representative histological images of the microstructure of „a… stretched and „b… unstretched human aortic media.
Elastica van Gieson „EVG… staining, 4 ␮m thick sections. Original magnification 800Ã.

tips兲. Consequently, under radial 共tensile兲 loading of the medial evident in the photomicrographs. The observed damage spreads
tissue, interconnected fine elastin fibers, and interlaminar muscle over approximately six to seven elastic laminae, which is about
cells are torn loose from their attachments to each other and to 15–18% of the thickness of the abdominal aortic media. Note that
adjacent elastin 共similar to the study 关26兴兲; ruptured fine fibers are we could not observe circular-shaped nuclei of the smooth muscle

Fig. 12 Histological images of a representative aortic media during peeling in „a… circumferential and „b… axial directions.
Original magnification 20Ã. Histological images „c… and „d… represent magnifications of the dissection tips and highlight the
irreversible mechanism of separation at the micrographic level. Original magnification 400Ã. EVG staining, 4 ␮m thick
sections.

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(a) 100µm (b) 100µm

r r
dissected surface dissected surface

z
θ

Fig. 13 Representative histological images illustrating the “roughness” of the generated dis-
section surface during peeling in the „a… circumferential and „b… axial directions. EVG staining,
4 ␮m thick sections. Original magnification 100Ã.

cells within the damage zone, as discovered in the study 关20兴, region below 10%, and it is most likely that this is too small to
which is most probably due to the low resolution of the histology. activate mechanisms responsible for stiffness increase at higher
Microscopical images of the generated dissection surface high- strains. The final peelinglike failure mechanism region, denoted as
light that peeling in the axial direction creates a remarkably S3b, determines a plateau in the force-displacement curve until it
“rougher” dissection surface compared to that generated by peel- drops to zero, see Fig. 8. It seems that the layered structure of the
ing in the circumferential direction 共two representative images are media favors the peeling mechanism along the lamellar layers. A
shown in Fig. 13兲. In particular, the dissection during the peeling dissection within one lamella throughout the whole dissection
in circumferential direction propagates mainly between adjacent path did not occur, but we observed outward and inward devia-
elastic laminae, while the one in the axial direction frequently tions from the lamellar layers. Consequently, the applied experi-
crosses elastic layers. Interestingly, it sometimes happened that mental approach, i.e., the direct tension test leads to multiple dis-
the dissection runs either toward the internal elastic membrane or sections between the different medial layers and a peelinglike
toward the external elastic membrane during the peeling in the failure mechanism, as it is illustrated in Fig. 5, determines the
axial direction, which, in a way, mimics the process of aortic force-displacement characteristics at larger displacements.
dissection, as observed in clinical practice, i.e., where the dissec- The following is now a brief discussion of the experimental
tion runs either back into the lumen or outward into the adventitia. findings of this work with respect to the existing literature, where
Consequently, it was not possible to dissect the whole specimen. the radial failure stress and the energy required to propagate a
This, however, never happened by peeling rectangular-shaped dissection is investigated in detail.
specimens along the circumferential direction. The histology of In order to better quantify the results of the direct tension test
the media might explain the observed anisotropic dissection prop- we assume, mainly for simplicity, a homogeneous stress state to
erty of the human AA, and the formation of a rougher dissection be present. For that case, the 共average兲 radial failure stress can be
surface due to the peeling in the axial direction, as illustrated in estimated as Fmax / 共d2␲ / 4兲 = 140.1⫾ 15.9 kPa 共mean⫾ SD, n = 8兲,
Fig. 13. The smooth muscle cells in the media are oriented fairly where Fmax = 1.76⫾ 0.20 N 共mean⫾ SD, n = 8兲, and d = 4.0 mm
circumferentially 关19兴 and may provide a more pronounced resis- denotes the effective diameter of the circular specimens. It needs
tance to the dissection in the axial direction 共for example, it is to be emphasized that the conducted direct tension tests have
easier to run parallel to the furrows of a ploughed field than across caused stress concentrations at the incision of the specimen, and
them兲. Consequently, the creation of the rougher dissection sur- due to its small size this “edge effect” cannot be neglected. Nev-
face during peeling of axially oriented test specimens might ex- ertheless, this approach gives an estimation of the upper limit of
plain the “higher” resisting force/width and “variance” compared the radial failure stress of the investigated human abdominal aor-
to the results from peeling in circumferential direction. tic media, and we may compare the failure stress with the one
provided in Ref. 关26兴. That study on porcine thoracic aortas 关26兴
4 Discussion reported a failure of 61.4⫾ 4.3 kPa 共mean⫾ SD, n = 7兲, which is a
The present study was conducted to explore medial dissection value approximately half that determined in our experiments on
of the human abdominal aorta. Therefore, direct tension and peel- human AAs. The disagreement may be explained by species dif-
ing tests are proposed, which render defined mechanical problems, ferences and high variances.
and hence allow the quantification of the tissue’s dissection prop- Regarding the peeling tests, there is an oscillation of the force
erties. The failure mechanisms related to the peeling investigation about some mean “plateau” level 共see Figs. 9 and 10兲, which is
in terms of localized intramedial dissection at the microscale level similar to the results obtained from tearing pig descending tho-
has been demonstrated by related histological investigations. racic aortas, as provided in Ref. 关30兴. The oscillation is due to an
According to the results from the direct tension test, the devel- instability inherent in this kind of experiment, which is called
opment of medial dissection may be characterized within the three “stick-slip tearing” in rubber mechanics, see, for example, Ref.
regions of the force-displacement graph, i.e., Region S1, which 关44兴. Based on the given results for the peeling test, we may now
we assumed to be elastic, damage accumulation S2, and localiza- estimate the energy required to propagate the medial dissection.
tion of damage 共failure兲 S3, see Fig. 8. It is noted that the recorded According to the performed experiments, the external work is
force-displacement curve within S1 remains about linear and does found to be Wext c = 2.0Fpclpc = 1.67⫾ 0.33 mJ/ mm 共mean⫾ SD, n
not show stiffness increase at higher strains, as typically known = 5兲 and Wext
a = 2.0F palpa = 2.02⫾ 1.41 mJ/ mm 共mean⫾ SD, n = 7兲,
from arterial tissue 共see Ref. 关41兴 or Refs. 关10,42,43兴 for over- for the circumferential and axial peeling tests, respectively 共Fpc,
views兲. Hence, the tissue might be seen as linear elastic in the Fpa are according to Table 5, and lpc, lpa are the current lengths of
radial direction, which is in clear contrast to the elastic properties the specimens in the circumferential and axial directions before
in circumferential and axial directions. Note that the direct tension separation兲. Next, we assume that the creation of a new surface
tests exhibit average strains in the loading direction within the S1 due to the dissection is the only dissipation present during the test,

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i.e., the separated medial tissue behaves fully 共hyper兲elastic. With Acknowledgment
this assumption, the dissection energy may then be determined by
The authors are indebted to the late C. A. J. Schulze-Bauer,
subtracting the elastic stored energy 共right before complete sepa-
MD, M.Sc. who helped to initiate the early part of this study. They
ration of the medial strip兲 from the external work. Moreover, we gratefully acknowledge the generous help of Professor Peter B.
assume simple tension of the dissected media to be the represen- Canham, The University of Western Ontario, Canada, who sug-
tative loading mode before complete separation, and hence we gested a number of valuable improvements to the substance of the
neglect inhomogeneities at the clamps and the dissection as well. text. Financial support for this research was provided by the Aus-
The average peeling forces and the referential dimensions of the trian Science Foundation under START-Award Y74-TEC, and by
specimens define the first Piola–Kirchhoff stresses Ppc the Fonds zur Fortsetzung Christian’s Forschung. This support is
= 4.90⫾ 2.34 kPa/ mm 共mean⫾ SD, n = 5兲 and Ppa gratefully acknowledged.
= 5.02⫾ 3.60 kPa/ mm 共mean⫾ SD, n = 7兲, for the circumferential
and axial peeling tests, respectively. These stresses are very low
so that it can be justified to assume a linear relationship between References
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Welastic
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way. The stored energy needs to be subtracted in order to estimate plasty and its Influence on Acute Complications,” Int. J. Cardiol., 31, pp.
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