THE
JOEL
RUPTURE
COHEN,
M.S.,
FORCE
S. BERT
LITWIK,
ASI) TENSILE AORTIC TISSUE M.D.,
ARNOLI)
HOMOGRAFT AORTIC MATERIM is luring used successfully in the reconstruction of a&tic or hypoplastic segments of the cardiovascular system. Informnt,ion on the durability of grafted tissue is important. Results of testing aortic t’issue strength have been reported [6, 16, 251. Most record only rupture force (maximal force necessary to rul&ure t&sue) rather than tensile strength (maximum force for rupture per unit crosssectional arca of tissue). Since aortic UXll t,hickness varies, tensile strength, rather than rupture force is a more meaningful tissue ljroperty for comparison of various samples. The purpose of this study is to examine t#hese propertics of untreated canine aortic tissue. This will serve as a baseline for comparison with aortic tissue which has been trtated hy sterilization and/or preservation. NETHODS
,4Nn
M.S.,
4XD
SAMUEL
FIXE,
M.D.
Preparation of Samples Prior to Tensiometer Testing
MATERIALS
Intact aortas, from the coronary vessels to the bifurcation of the abdominal aorta, were From the Department of CardiovascularSurger?:, Children’sHospital Medical Center and Harvard Medical School;Departmentof BiomedicalEngineerThe
ing, Nort,heastern University; Department of Dermatology, Massachusetts General Hospit,al, Boston, Massnchusetts. We wish to thank Dr. Charles Goolsby for his valuable suggestions. Supported by: Grant 260, Children’s Bureau, Maternal and Child Health Service, Department of Health. Education and Welfare; a Grant from the John ,4. Hartford Foundation; Contract No. D-4-49193-MD-2436, Surgical Research Branch, Medical Research and Development Command, U.S. Army, and NASA Grant NGR 22-011-007. Submitted for publication July 22, 1972. 321 0 1973 by Academic Prm, Inc. All rights of reproduction in any form reserved.
AARON,
OF CANIXI!:
obtained from 39 mongrel dogs. Thirty-two dogs weighed lo-15 kg. For comparison, two aortas were obtained from 3-kg puppies and five aortas from 18-26-kg mongrels. Specimens were removed within 4 hr postmortem and stored a maximum of 4 hr in normal saline.
Tissue tysed for Samples
Cop.wight
STRENGTH
Each aorta was divided into three segment’s: (1) ascending thoracic aorta and arch, (2) descending thoracic aorta and, (31 abdominal aorta (Fig. IA). A longitudinal incision was made along the inner radius of t,he ascending aorta and arch and between the origins of the intercostal arteries of the descending thoracic segment (Fig. 1B). Abdominal segments were cut longitudinally such that large-branch vessel orifices were located peripherally on the oltrned section (Fig. 1B). The experimental stress concentration caused by naturally occurring perforations (i.e., branch vessel orifices) was, therefore, minimized. From these sections of 31 aortas, transvcrsc specimens (Fig. lB, Table 1) were cut in a simicircular grooved, fixed shape using a specially designed cutter (Fig. 2). In adult dogs the ascending aorta provided one transverse specimen, t.he descending thoracic segment usually made seven, while the abdominal portion yielded five specimens. Xo samples were t&cd from the transverse aortic arch because of the curvature in that section and the resulting inaccuracies in stress-strain patterns. Aortas from 3-kg puppies yielded a total of nine test samples. sl)ccimens were cut in a longitudinal direc-
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orifices
-
from
transverse LONGITUDINAL
ILIAC
ART ki (81
(A)
Fig. 1. (a) The intact canine aorta was divided into three segments as shown. Designations Al-AV indicate fixed locations along the aorta and are reference for anatomical position. (AI, ascending aorta; AH-AIII, descending thoracic; AIV-AV, abdominal aort,a. Specimen 1, ascending thoracic; Specimens 2-8, descending thoracic; and Specimens 9-13, abdominal aorta). (b) The three segments are shown after t,he thoracic strips were cut longit,udinally and the abdominal segment was cut transversely into five equal sections. A specimen was made from each section. Table 1. Comparative Transverse Specimens Medium Specimen
Type
Specimen Direction
Control Longitudinal (a) High strain rate (b) Heavy dogs (c) Light dogs (d) * Significant b Significant c Stochastically d Stochastically e Descending
Statistical Studies of fhe Rupture Force and Tensile Strength of (a) Longitudinal at Low Strain Rates, (b) High Strain Rates with Low Strain Rates, (c) Heavy Dogs Weight Dogs, (d) Light Weight Dogs (Puppies) with Medium Weight Dogs
Transverse Longitudinal Transverse Transverse Transverse
at 5% level. at 1% level. bigger than controls. smaller than controls. thoracic aorta only.
Strain Rate (cm/min/cm) Thoracic
Abdominal
1.0 1.0 10.0 1.0 1.0
1.5 1.5 10.0 1.5 1.5
Weight of dog 0%)
Number of dogs
Mann-Whitney
18 8 6 5 2
Z Values
Rupture Ascending and Descending Thoracic
10-15 10-15 10-15 B-26 3
wifh with
2
8b,C&
319”*. 2.1”BC 3.l’J.d
Force Abdom. inal
Tensile Ascending and Descending Thoracic
Strength Abdominal
8.8”~”
3.‘ib,c.e
2.1a,o 3.4”,” 2.7”sd
4.l”*c 0.8
8.3b’C 1.1 0.9
1.0
1.6
COHEN
ET
AL.:
TENSILE
STRENGTH
OF
CSNINE
AORTIC
323
TISSUE
W:Smm h:6mm r : 1.5mm
SEMI-CIRCULAR SPECIMEN
Fig. 2. The specimen tached to a movable
GROOVED SHAPE
and its dimensions shaft,. The sortie
are shown on t,he left. On the right is the specimen cutter which was atsect,ion was placed on a Plexiglas plate and a specimen was stamped out.
tion from eight other aortas (lo-15 kg dogs) (Fig. 1, Table 1). Thickness measurements were made at the central grooved region of each specimen w&h a thickness gauge.* Tensile Strength Testing Specimens were placed between the pneumatic jaws of an electrically driven tensiomet’ert for testing. Samples from 33 aortas were elongated at a constant rate of 1 cm/min until rupture, with a strain rate of 1.0 cm/mm/cm of original specimen for thoracic specimens and 1.5 cm/min/cm of original specimen for abdominal specimens (Table 1). A~luminun~ foil and t&on specimens, cut to a similar shape, were also tcstcd at 1.0 cm/ min/cm. Six aortas were clongatcd at 10 cm/ nun with a strain rate of 10 cm/min/cm for bot,h thoracic and abdominal specimens, to test t#hc effect of strain rate. Slippage and t’earing of specimens at the jaw region was minimized by using one serrated jaw opposite a smooth jaw lined with adhesive tape. Force-elongation curves were recorded by a constant speed recorder and the ma,ximum force for rupture was measured. Tensile st8rcngth was calculated as the maximum force (rupture force) per original cross sectional area (spccimcn t’hickness multiplied by the * Fowlcr dial thickness Fowler Instruments, Boston, t Instron Tcnsiometer, Company, Canton, MA.
gauge, MA. Model
Model
#G1113,
TM-M,
Instron
minimum region).
width
at the semicircular
Statistical
Testing
grooved
A standard nonparametric statistical test, the Mann-Whitney Test [9], was used to determine whether dog size or strain rate had an effect upon the rupture force or the tensile strength of aortas. Computations for this aspect of the study were carried out on a digital computerf using the IBM program TJtest [2]. RESULTS T*nriations
in Aortic
Wall
Thickness
In a typical aorta, the thickness of specimens decreased as the distance from the origin of the aorta increased (Fig. 3). Saline soaking caused a 5-10s increase in the measured thickness. Since the tensile strength was calculated as the rupture force per original crosssectional area after saline soaking, the value obtained may bc in error to this extent. Normal variat,ions in thickness are included in tensile strength calculations. Therefore, statistical results for tensile strength may be diffcrent from that for rupture force which does not include thickness measurements. Tecrring of Tissue Samples Specimens were stretched until rupture. This usually began at the semicircular grooves and $ Control
Data
Corporation,
Model
3300.
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measured (I = fl
at t,he grooved region standard deviation).
progressed transversely across the center of each specimen. The intima and media usually ruptured first, followed by the adventitia; rupture of all three aortic layers was rarely simultaneous. This pattern of tearing was seen with both transverse and longitudinal specimcns. Force-E
6,
DECEMBER
1972
AY
AIP
of transverse
specimens
from
12 aortas
2 ; .5 Y e 0 0 I.Oy
longa tion Curves
Representative force-elongation curves arc shown in Fig. 4. In a typical transverse specimen from the thoracic aorta, there was one distinct peak (or maximum force) in the forceelongation curve which usually corresponded to the rupture of the intima and media together (Fig. 4A). This was usually followed by elongation of the adventitia at a much lower tensile force. By contrast, in a typical transverse specimen from t,he abdominal aorta, there were two distinct peaks in the force-elongation curve (Fig. 43%).The first corresponded to rupture of the intima and media. The second elevation in force occurred due to the relatively intact adventitia or in some cases,the adventitia with an attached medial layer. This second peak was usually lower than the initial peak. In the 16% of cases in which the second peak was higher, it exceeded the first by less than 10%.
NO.
Alll POSITION
An.
Fig. 3. The average thickness function of anatomical position
13,
shown
as a
ELONGATION OF ADVENTITIA
(81 50
100
ELONGATION
(%I 200
250 I
AND MEDIA PEAK ASSOCIATED WITH ADVENTITIAL ELONGATION
2 8 .5E
0
I 100
ZOO ELONGATIONW
400
Fiq. 4. Typical force-elongation curves of transverse specimens from (a) thoracic aorta and from (b) abdominal aorta. The second peak force for abdominal specimens was due to the relatively intact adventitia or the adventitia with an attached medial strip.
The initial peak on the above curves was called the rupture force. In longitudinal specimens, only a single peak occurred in the force-elongation curves for both the thoracic and abdominal regions. Rupture-Force at Various Positions Rupture force varied with anatomical positions along the aorta for both t’ransverse and
COHEN
ET
SL.:
TENSILE
STRENGTH
longitudinally cut specimens (Fig. 5). With transverse samples, a maximum force to rupt,ure was observed in the ascending aorta, and a minimum was found in the proximal regions of the descending thoracic aorta (Table 2). The rupture force then increased progressively in ann~l~les from more distal parts of the thorncic aorta. It dccrcased again in samples from the abtioniinal aorta. \\7itll longitudinally cut samples, a minimum rupture force was found in the region of the ascending aorta. Rupture force then increased in specimens from aortas in the direction of blood flow reaching a maximum in the midabdominal region. In the ascending aorta specimens the rupture force of longitudinal samples was IA that of transrersc samples. For both the descending thoracic and abdominal regions, the rupture force of longitudinal spccimcns was significantly greater than transverse specimens (Table I! Fig. 5).
OF
CAXINE
I
3000
Transverse specimens (%I ltupture force” Tensile strength’ Longitrtdinal specimens c’;b) Rupture force0 Tensile strength”
I
I AII ANATOMICAL
AlIl AFZ POSITION
AY
Fig. 6. The average rupture force shown as a function of anatomical position for transverse specimens from 18 aortas and longitudinal specimens from eight aortas. 31-;ZV indicate fixed locations along the aorta and are rcfcrence p0int.s for anatomical position. Statistical comparisons are summarized in Table 1 (I = 2 1 standard deviation).
3%
from from from
of Minimum
Proximal Half of Descending Thoracic Aorta
Distal Half of Descending Thoracic Aorta
Abdominal Aorta
0.0
84.2
10.5
5.3
11.8
82.3
5.9
0.0
50.0
50.0
0.0
0.0
0.0
0.0
0.0
100 18 aortas. 12 aortas. eight aortas.
Tensile Strength
I ONGIT”DIN*L~
AI
Location
Ascend ing I Aorta
__._. _-.. ..-
5000
TISSUE
Table 2. Summary of the Locaiion of the JfiGmcrrn Rupture Force and Tensile Strength for Transverse and Longitudinally Taken Specimens of Aorta
a Data b Data c Data
‘Oooot’
AORTIC
Measurements
The tensile strength varied with anatomical position for both transverse and longitudinally sampled aortas (Fig. 6). Wit’h transverse samples the minimum tensile strength occurred at the aortic isthmus and increased lnogressively in samples taken from more distal portions of the thoracic aorta, reaching a maximum in the aorta near the diaphragm or distally. The tcnsilt strength of longitudinal specimens was minimal in ascending aortic samples and increased as the distance from the heart increased,, reaching a peak in the midabdominal region. In ascending and descending thoracic aortas the tensile strength varied from 3 to 18 kg/cm” for transverse specimens and from 3 to 43 kg/ ~111~for longitudinal specimens. In the abdominal aort’a the tensile strength ranged from 9 to 25 kg/cm2 for transverse and from 33 to 80 kgj’cmz for longitudinal specimens. Tensile strength values of longitudinally sampled abdominal and distal descending thorncic aortas were much larger than values ob-
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tained from samples taken in a transverse direction in similar regions (Table 3). The values of tensile strength in the proximal descending thoracic region did not change as much with specimen direction (longitudinal vs t)ransverse) .
LONGITUDINAL
Eflect of Animal Weight on Rupture Force and Tensile Stren.gth. Rupture force of thoracic and abdominal aorta specimens from puppies was significantly smaller than for lo-15-kg dogs (Fig. 7, Table 1). Likewise, rupture force was significantly larger in samples from 18-26-kg dogs. Tensile strength from both puppies and large dogs was not significantly different from that of lo-15-kg mongrels (Fig. 8, Table 1). Strain Rate I AI
AII
AIB AIX POSITION
ANATOMICAL
For thoracic specimens the tensiometer jaw separation was s/R in. prior to testing. For abdominal samples this separation was 1% in. because of limitation of sample size. The strain rate was, therefore, 1 cm/min/cm for thoracic specimens and 1.5 cm/min/cm for abdominal
AP
Fig. G. The average tensile strength shown as a function of anatomical position for transverse specimens from 12 aortas and longitudinal specimens from eight aortas. Statistical comparisons are summarized in Table 1. Table
d. The Average Tensile Strength of Transverse and Longitudinul of the 13 Locations Tested. Aortic Position Designations i-13 the Aodic Origin
Aortic Increase
Aortic
Positiona
-
1 ______i Tensile Strength (kg/cm2) Transverseb Longitudinal0 Batio of Transverse to Longitudinal Tensile Strengths Collagen (%) Apter et al. Harkness et al. Elastin (%) Apter et al. Harkness et al.
7.40 3.29 2.2
15.2 2 4.0 4 2
2
5.18 7.75 0.67
18.2 20.6
Y-
4
3
6 ____
_-
!
G.7( 5 6.5: 0.4 1 10.2; 1.1 0.6:
15.4 -
Specimens and Their Ratio at Each with Increasing Distance from
7
I-
s
9
12.51 42.61 0.25
12.60 49.89 0.25
10.00 17.41 0.57
12.1: 19.94 0.61
14.9: 29.u 0.5.
-
10
11
13.65 59.88 0.23
12 __ 14.32 55.38 0.26
13.7 -
14.4 22.4
14.1” -
15.4 25.4
22.8 34.0
-
-
27.8
33.3
39.4
42.0 -
42.0 32.6
11.0d -
37.6 29.0
32.1 22.5
29.2 16.3
12.3
-
10.8
13 _ 15.00 53.95 0.28
25.0 19.7 -
B 1, Ascending thoracic; 2-8, descending thoracic; the aorta, the collagen and elastin concentrations b Average from 12 aortas. c Average from eight aortas. d Average of two data points.
9-11, abdominal aorta. For the corresponding position along from Apter et al. [3] and Harkness et al. [13] are also given.
COHEN
ET
AL.:
TEhWLE
STRENGTH
,HIGH STRAIN RATE (IOcm/cm/MINlJTE)
OF
CANINE
AORTIC
TISSUE
3’7
(0)
900 z 2 000 5 Y 700 0: e g 600 iz a’ 500
400
300 I00
1 ~1
I
I AlI ANATOMICAL
AlU POSITION
AIX
AP
Fig. 7. Comparison of average aortic rupture force as a function of anatomical position for: five heavy weight dogs (X-25 kg), two light weight dogs (3 kg) with 18 controls (lo-15 kg); high strain rate (six aortas) compared with controls at low strain rates (18 aortas). The curves are drawn freehand. Statistical comparisons are summarized in Table 1.
epccimens. Initial tcst’ing of six abdominal aortas showed no significant variation of eitdlcr rupture force or tensile st(rcngth due to t’liis strain rate difference. Increasing the strain rate to 10 cm/min/cm significantly increased both rupture force and tensile strength in the thoracic region but only rupture force in the abdominal region (Table 1, Figs. 7, 8). An increase in tensile strength and rupture force values wit,11 an increase in strain rate conforms with the expected behavior of plastic materials [15]. We cannot explain the lack of significant alteration in tensile strength with difference in strain rate in the abdominal region. Stntistical Xignificance Results of the Mann-Whitney Test computations are summarized in Table 1.
DISCUSSION Stress Characteristics of Specimen Shape Due to t’he limited amount of aortic canine tissue available for transverse specimens, it was not possible to use a standard tensile test shape [4] over the whole length of the a0rt.a. Rectangular shaped strips when tested tended to tear at the jaw region in an unpredictable way. The semicircular grooved specimen shape used was such that rupture usually occurred in t#he midportion of each specimen. A small number which did not initially tear at the central grooved region were excluded from the rupture test data presented, in conformity with mat’crials test procedures. Stress concentration occurs in the grooved region because of specimen geometry. The ratio of maximum stress in this minimum sec-
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_ (IOcm/cm/MINUTE)
CONTROLS
(0)
4
3
i
I AI
AP ANATOMICAL
Am AH POSITION
AY
Fig. 8. Comparison of average tensile strength as a function of anatomical position for five heavy weight dogs (18-26 kg), two light weight dogs (3 kg) with 12 controls (IO-15 kg) ; high strain rate (six aortas) compared with controls at low strain rates (12 aortas). The curves are drawn freehand. Statistical comparisons are summarized in Table 1.
tion to its average is called the stress concentration factor, Kt [18]. For the semicircular shaped specimen with the initial dimensions mentioned previously (Fig. 2), K, has been determined as 1.9 for homogeneous, isotropic material [8, 18, 231. Thus, the maximum stress in the grooved region should be 1.9 times that of the average stress. However, as the specimens were elongated, the radius of curvature at the grooved region increased relative to the minimum width. Measurements of aortic samples taken from photographs just prior to rupture, indicate that the stress concentration factor, Kt , would be 1.1-1.2 if the specimen were homogeneous, isotropic and elastic. The aorta, however, is viscoelastic and is neither homogeneous nor isotropic. Therefore, for the purpose
of the present study, iXt has been assumed to equal 1.0 with a probable error of 10-20s. In rupture tests with semicircular grooved specimens of Teflon, significant elongation with an increased radius of curvature occurred at the grooved region. Due to this geometric change, as discussed above for aortic specimens, we would expect the stress concentration factor at rupture to be reduced for the specimens. The calculated value of our Teflon specimens, with Kt assumed equal to 1.0 was 2.9 kpsi. This is within the reported range of 1.5-3.3 kpsi [20]. Thus, it appears that stress concentration is negligible for this Teflon specimen shape. In rupture tests with similar specimens of aluminum foil, significant elongation with in-
COHEN
ET
AL.:
TENSILE
STRENGTH
creased radius of curvature did not occur at the grooved region. Thus, we would expect a stress concentrat’ion of about 1.9 as predicted from the initial geometric shape. The calculated value of tensile strength from our aluminum foil specimens was 8.9 kpsi which is about 1.5 times smaller than the 13 kpsi reported for the aluminum foil [l]. Thus, the estimated stress concentration factor for aluminum foil of the shape used is about 1.5. This differs from the 1.9 previously determined for our original geometrical shape by about 25%. Bared on these studies, we think that a K, of 1.0 is acceptable for the testing of semicircular grooved aortic specimens. In other words, the error due to the assumption of negligible stress concentration in our specimens at rupture is acceptable for these studies. Standard deviations of 5 and 6% were obtained for the tensile strengths of aluminum foil and Teflon specimens, respectively. These spccimcns were cut similarly to aortic specimens with the instrument shown in Fig. 2. Thus, our experimental technique appears to be reproducible to this extent. We think this experimental error is acceptable for the biological material tested for this report. Rupture Force Variation Hiertonn and Jordan [16] reported that the rupture force of transverse specimensof canine aortas was relatively similar (about 800 g) in the different aortic regions. They also concluded that the rupture force of longitudinal specimens was about the same (800 g) in the thoracir region but much higher (2600 g) in the abdominal aorta. Zehnder [25], testing transverse st’rips of human aorta, reported a range of 600-2600 g for rupture force with a gradual decrease from the ascending aort,a to the proximal descending thoracic aorta. Statistical analysis (F test: P < 0.01) of our data from canine aortas has shown significant variations in rupture force with anatomical position for both longitudinally and transversely taken specimens. These variations in rupture force with position are probably due to changeS both in tissue thickness, as shown by our data, and in composition [3, 12, 161.
OF
CANINE
AORTIC
TISSUE
329
Tensile Strength Variation Tensile strength is defined as the maximum tensile stress developed during the course of loading a material to rupture, where stress can be expressed in kg/cm”, lb/in.’ or in other suitable units. The literature contains few reports of the aortic tensile strength. In most of these the term has been misused. Several investigators have confused the force required to rupture the material (in grams, kilograms, or pounds) with the tensile strength and have referred to the rupture force as tensile strength. For specimensof fixed width the rupture force is a measure of relative strength only when the thickness of the specimen remains constant, and the stress concentrations are equal. Since thickness varies with position in aortas, the rupture force is not a measure of tensile strength. Significant variation wit’h position is present in the tensile strength of both longitudinal and transverse specimens (F test: P < 0.01). Traumatic rupture of the intact human aorta occurs with much higher frequency at the isthmus and in the ascending aort’a [lo, 221. Interestingly, minimal tensile strength occurred at these two locations in our studies. Rupture Force and Tensile Strength ilnisotropy One might expect the strength of aortic tissue in longitudinal and transverse planes to be proportional to in viva stresseson these tissues in these directions. The rupture force and, correspondingly, the tensile strength of longitudinal and transversely cut specimens from the same aortic regions are, in general, different (Figs. 5, 6). Therefore, there may be different in viva stresseson the aorta in longitudinal and transverse directions. Aortic Composition as a Factor in Wall Strength The endothelial cells and smooth muscle have been reported to contribute very little to the “elastic tension” of the aorta [5, 191. Therefore, the strength of the aorta can be attributed mostly to elastin and collagen. Elastin is a material of low tensile strength
330
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and large extensibility, while collagen has a high tensile strength and a very small extensibility [5, 21, 241. Hass [14] reported the tensile strength of human “arterial elastin” to be l-7 kg/cm2. Harkness [13] concluded from data on mammalian tendon that the tensile strength of collagen is in the range of 1500-3000 kg/cm2. For canine aortas, we found that, in general, the tensile strength increased as the distance from the aortic valve increased. Others [3, 121 have reported an overall increase in collagen and a decrease in elastin percentages as this distance increases. These elastin and collagen percentages when plotted against our tensile strength data for similar anatomical positions (Table 3) show a linear relationship between collagen concentration and tensile strength (Fig. 9). This agrees wit’h the observation of Levene [17], who proposed that the rupture strength of the aorta increased with collagen content. Likewise, tensile strength appears to decrease as the elastin increases (Fig. 10).
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Thus, as aortic composition changes to that of increased collagen and decreased elastin, tcnsile strength increases. Gustavson [II] states that “tensile strength measured on a strip of skin really gives the strength of the fiber weave.” Similarly, the fiber arrangement of the aortic tissue may affect its tensile strength as illustrated by tensile strength difference between longitudinal a,nd transverse specimens (Fig. 6). Furthermore, difference between the tensile strengths of longitudinal and transverse specimens when compared to either collagen or elastic concentraCons (Figs. 9, 10) may illustrate the importance of fiber weave as a factor in tensile strength determinations. In our st,udies we assume the interruption of fibers due to cutting specimens has not markedly affected tensile strength measurements. This may not be true, but we know of no way to test this. In the present study, the tensile strength of canine aortas, tested as semicircular grooved
LONGITUDINAL SPECIMENS VS DATA OF APTEA ET AL 9)
LONGITUDINAL SPECIMENS VS DATA OF HARKNESS
ETA1
TRANSVERSE SPECIMENS VS DATA OF APTER ET AL
DATA OF HARKNESS
00
IO
20 COLLAGEN
30
40
ET AL
50
60
1x1
Fig. 9. Average tensile strength of transverse and longitudinal specimens along the canine aorta plotted against the collagen concentration reported by Apter et al. [3] and Harkness et al. [E] for similar anatomical positions. Linear regression coefficients for the straight line plot were computed from the data in Table 3 by t,he method of least squares.
COHEN
ET
AL.:
TENSILE
STREKGTH
OF
VS DATA
CANINE
AORTIC
OF APTER
TISSUE
331
ET AL
- so“E \o 01 Y az 5 z kz I* w i m 2
40-
30LONGITUDINAL SPECIMENS
VS
A
-\
w
0 0
IO
Fig. IO. Average tensile strength of transverse the elastin concentration reported by Apter Linear regression coefficients for the straight of least squares.
20
30 ELASTIN
40
I 50
(%I
and longitudinal specimens along the canine aorta plotted against et al. [3] and Harkness et al. [12] for similar anatomical positions. line plot were computed from the data in Table 3 by the method
specimens, varied from 3 to 25 kg/cm2 for transverse specimens and from 3 to 80 kg/cm’ for longitudinal specimens. In the proximal descending thoracic aorta the tensile strength of transverse specimens obtained by us was about three times that reported by Hass [14] for arterial elastin in the same region. In determining tensile strength, Hass found the cross-sectional area of elastin alone to be about’ 37”; of original thickness of t’he aorta. If our aortas contained the same fraction of elastin and the tensile strength of these aortas were due solely to elastin, then our calculated aortic elastin tensile strength would be about nine times (3/0.37) that obtained by Hass. Therefore, we can conclude that the tensile strength of the aorta is not due to the elastin fibers per se: though the elnstin fibers probably play an important role. Coulson et al. [7] showed a8marked decrease in tensile strength following elastin digestion. They felt that elastin contributes to the mechanical properties of
the collagen by “binding its fibrils together,” in agreement with the concept of Wolinsky and Glagov [24]. It is possible that the elastin fibers contribute to the strength of the aorta in this manner. Where our tensile strengths were highest (60 kg/cm2) the collagen concentration was reported as approximately 30%. Where tensile strengths were lowest (3 kg/cm2), the collagen concentration was still greater than 10% (Table 3, Fig. 9). If one considers the collagen as being solely responsible for tensile strength of the intact aorta, then our maximum tensile st’rength for aortic collagen would be about 200 kg/cm2 (60 kg/cm2 + 0.30). Similar calculations of maximum tensile strength for collagen in the region where the collagen concentration is lowest (greater than 10%) give a value less than the above. Our value for aortic collagen tensile strength is, therefore, much lower than the tensile strength for mammalian tendon collagen (1500-3000 kg/cm’, [13]) but
332
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much nearer to the value of about 100 kg/cm2 calculated by Coulson et al. [7] from rings of thoracic aorta. Thus, the tensile strength of the aorta is related to collagen content, but does not appear to be dependent upon the strength of collagen fibers per se. It is possible that the “weave” of the aort’a is significant as regards the tensile strength. Separation rather than breakage of fibers may occur at rupture. Another possibility is that there is elastin to collagen binding which breaks on rupture. SUMMARY
AND
CONCLUSIONS
(1) A reproducible technique was developed for determining the rupture force and tensile strength of transverse and longitudinal specimens of canine aortic tissue. The effects of strain rate and animal size were examined. (2) The thickness of the canine aorta decreases with distance from the heart. (3) In stressed aortic specimens, the intima and media usually ruptured prior to the adventitia. (4) The force to rupture transverse specimens of canine aortic tissue is large in the ascending aorta, reaches a minimum in the proximal descending thoracic region and increases to a maximum at the diaphragm. The force to rupture longitudinal specimens of aortic tissue is minimal in the ascending aorta, and in general increases with distance from the aortic origin reaching a maximum in the midabdominal region. (5) In general, the tensile strength of transverse aortic specimens increases with distance from the aortic origin reaching a maximum at the diaphragm or distally in the abdominal aorta. The tensile strength of longitudinal specimens of aortic tissue is minimal in the ascending aorta, and in general, increases with dist(ance from t’he aortic origin reaching a maximum in the midabdominal region. For ascending and descending thoracic aorta, the tensile strength varied from 3 to 18 kg/cm2 for transverse specimens, and from 3 to 43 kg/cm” for longitudinal specimens. In abdominal aorta, the tensile strength varied from 9 to 25 kg/cm2 for transverse specimens and from 33 to 80 kg/cm2 for longitudinal specimens. (6) Rupture force and tensile strength ani-
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sotropies have been found. The anisotropy is negligible in the proximal descending thoracic aorta, moderate in the ascending and distal descending thoracic aorta, and large in the abdominal aorta. (7) It appears as though several factors may be involved in the strength of aortic tissue. Collagen and elastin concentration and fiber orientation and weave are import)ant. REFERENCES 1. Anonymous,
2.
3.
4.
0.
6.
7.
S.
9.
10.
11.
12.
13.
The Aluminum Data Book, p. 16-5-1, Reynolds Metals Co., 1962. Anonymous, Subroutine rtcst. In IBM Application Program. System/360 Scientific Subroutine Package (360A-CM-03X) Version II. Programmer’s Manual. p. 48, IBM Corp., White Plains, NY, 1966. Spter, J. T., Rabnowitz, M., and Cummings, D. H. Correlation of visco-elastic properties of large arteries with microscopic structure. II. Collagen, elastin and muscle determined chemically: histologically, and physiologically. Ciw. Res. 19:104121. 1966. ASTM Designation : D170859T. Tentative Method of Test for Tensile Properties of Plastics by Use of Microtensile Specimens. In 1964 Book of ASTM Standards, Part 27, Plastics-General Methods of Testing, pp. 577-581. The American Society for Testing Materials, Philadelphia. P.4. Burton, A. C. Relation of structure to function of the tissues of the wall of blood vessels. Physiol. Rev. 34:619-642, 1954. Couleon. W. F., and Carnes, W. H. Cardiovnscwlal studies on copper-deficient swine. II. Mechanical properties of the aorta. Lrrb. Invest. 11:1316-1321, 1962. Coulson. W. F., Weissman, N.. and Carncs, W. H. Cardiovascular studies on copper deficient swine. VII. Mechanical properties of aortic and dermal collagen. Lab. Invest. 14 :303-309, 1965. Faupel, J. H. Engineering Design. A Synthe.sis of Stress Analysis and Jfnterials Engineering. pp. 774-788. J. Wiley and Sons, Sew York. 196s. Fisz, M. Probability Theory and Muthemntical Statistics, 3rd edition, pp. 449-456, J. Wiley and Sons, New York, 1963. Greendvke, R. M. Traumatic rupture of the aorta: Special reference to automobile accidents. JAMA 195 :527-530, 1966. Gustavson, I(. H. The Chemistry and Reactivity of Collagen, pp. 140-147, Academic Press, New York, 1956. Harkness, M. I,. R., Harkness, R. D., and McDonald, D. 8. The collagen and elastin content of the arterial wall in the dog. Proc. Roy. SOC. [Biol.] 146:541-551. 1957. Harkness, R. D. Mechanical properties of collapenous tissues. In B. S. Gould. (Ed.), Treatise on
COHE?i
ET
AL.:
TENSILE
STRENGTH
Collngen, Vol. 2, Biology of Collagen, Part A, pp. 247-310. Academic Press, New York, 1968. 14. Hass, G. M. Elastic tissue II. A study of the elasticity and tensile strength of elastic tissue isolated from the human aorta. Arch. Path. (Chicngo) 34 :971-981, 1942. 15. Hayden. H. W., Moffat, W. G., and Wolff, J. The Strztctrrre and Properties of Materials, Vol. III, Mechanical Behavior, p. 130. J. Wiley and Sons, New York: 1965. 16. Hiertonn. T. E., and Jordon, P. The tensile strength of canine aortic segments. Angiology 7 :21-26, 1956. 17. Levenc. C. I. Collagen as a tensile component in the developing chick aorta. &it. J. Exp. Path. 42 :8’&94, 1961. 18. Lipaon. C., and Juvinall, R. C. Handbook of S1rev.s and Strength Design and Material Applicalions, pp. 27-38, 247. The Macmillan Co., New York, 1963.
OF
CAXINE
AORTIC
TISSUE
333
19. MacDonald, D. A. Blood Flow in Arteries, pp. 146176, The Williams and Wilkins Co., Baltimore, MD, 1960. 20. McClintock, I?. A., and Argon, A. S. Mechanical Behavior of Materials, pp. 258-259, AddisonWesley, Reading, MA, 1966. 21. McGill. I. G. Arterial elastin-A4 review. Guy Hosp. Rep. 115:91-104, 1966. 22.Strassman ,G. Traumatic rupture of the aorta. Amer. Heart .J. 33 :508-515, 1947. 23. Timoshenko, S. Strength of Materials, Part II, Advanced Theory and Problems, 2nd Edition, pp. 318-324, D. Van Nostrand Co., New York, 1941. 24. Wolinsky, H., and Galgov, S. Structural basis for the static mechanical properties of the aortic media. Circ. Res. 14:400413, 1964. 25. Zehnder, M. A. Serrei bfestigkeit und ealstizitat der aorta, beitrag zur traumatischen aortenruptur. Schweiz. Med. Wschr. 85 :203-208, 1955.