Ann Thorac Surg 2003;76:58-64
© 2003 The Society of Thoracic Surgeons
Original article: cardiovascular
Mechanical properties of porcine and human arteries: implications for coronary anastomotic connectors
Carolien J. van Andel, MSc, PhD,a,b,
Peter V. Pistecky, MScb,
Cornelius Borst, MD, PhDa*
a Experimental Cardiology Laboratory, Heart Lung Center Utrecht, University Medical Center Utrecht, Utrecht, Netherlands
b Department of Design, Engineering and Production, Delft University of Technology, Delft, The Netherlands
Accepted for publication February 4, 2003.
* Address reprint requests to Dr Borst, Experimental Cardiology, University Medical Center Utrecht, Room G02.523, Heart Lung Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands.
e-mail: c.borst{at}hli.azu.nl
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Abstract
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BACKGROUND: To determine whether the pig is an appropriate experimental animal for studies on distal anastomotic connectors in coronary artery bypass surgery, the mechanical properties of young porcine and old human coronary and internal mammary arteries were compared within and beyond the physiologic range of strains.
METHODS: Coronary arteries from 6 humans and 8 pigs were studied as well as internal mammary arteries of 3 humans and 6 pigs (human, aged 61 to 85 years; pig, 78.7 ± 5.8 kg [mean ± SD]). Pressure-diameter, pressure-axial force, circumferential and axial stress-strain relations, and dimensions were measured.
RESULTS: The dimensions of the porcine and human coronary and internal mammary artery were generally similar but wall thickness was smaller in the porcine internal mammary artery (0.35 ± 0.07 mm versus 0.71 ± 0.06 mm, respectively, p = 0.002). The porcine internal mammary artery wall was less elastic than the coronary artery wall, whereas in humans both arteries displayed similar elasticity. Overall the porcine arteries were far more elastic in both circumferential and axial direction compared with the human arteries. Consequently the porcine arteries could be safely stretched by 60% to 70% compared with about 20% for the human arteries before reaching their maximum circumferential strain.
CONCLUSIONS: The three times greater elasticity of porcine compared with human coronary and internal mammary artery walls may result in underestimation of wall stress and the risk of wall injury when coronary connectors that involve overstretching of the wall are evaluated in the pig.
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Introduction
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Closed-chest coronary surgery on the beating heart requires new techniques for construction of the anastomosis because of limited working space and other limitations inherent to thoracoscopic coronary surgery [1–3]. Novel coronary intervention and bypass techniques are usually tested on the porcine heart because of its good anatomic resemblance to the human heart [4, 5]. Many patents on anastomotic connectors show the use of anvils and other microstructures that may cause extreme local deformations in the arterial wall of both donor and recipient vessel [3]. Extreme deformations however may result in excessive wall injury.
Carmines and associates [6] reported some mechanical properties of porcine and human coronary arteries, although the use of frozen human specimens may have affected their results [7–9] and age categories were not specified. Others [10, 11] reported only incremental elastic moduli in the circumferential direction although arteries are known to have highly nonlinear stress-strain relations and to be anisotropic [12, 13].
It remains to be established whether the mechanical properties of porcine arteries sufficiently correspond to those of human arteries to allow predictions on connector induced stresses in the arterial wall. The objective of this investigation was to quantify in and beyond the physiologic range of wall stretch the nonlinear mechanical behavior of the coronary artery (CA) and the primary bypass conduit, the internal mammary artery (IMA) [14], and to compare the results in the pig with the findings in the human.
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Material and methods
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Porcine arteries
Fourteen Landrace pigs (weight 78.7 ± 5.8 kg) were used that were sacrificed in the course of other experiments that did not involve drug administration. Animals were treated according to the Guide for the Care and Use of Laboratory Animals (National Institutes of Health publication No. 85-23, revised 1985) and the studies were approved by the ethical committee on animal experiments, medical faculty, Utrecht University. From 8 pigs a cylindrical segment of the left anterior descending (LAD) or right coronary artery (RCA) was excised and from 6 pigs a segment of the left (LIMA) or right internal mammary artery (RIMA) was harvested. The segments were stored in saline at 4°C and measurements were performed within 24 hours after termination.
Human arteries
From six postmortem hearts (aged 61 to 85 years) a total of 10 segments of coronary arteries with different degrees of arteriosclerosis were used in this study. Only segments without visible or tactile calcified plaque were used. From three corpses the IMAs were harvested. The segments were stored in saline at 4°C and measurements took place within 72 hours postmortem.
Artery segment location and length
The proximal end of the excised porcine and human coronary artery segments was located approximately 20 mm distal from the origin of the artery. The segment length varied between 20 and 40 mm. For the external diameter versus transmural pressure measurements it was necessary to have a leak-free wall. The more distal parts of the coronary arteries however had too many side branches that required clipping. Too many clips would have negatively affected the precision of the intended measurements. Porcine and human IMA segments of 20 to 40 mm in length were excised proximal to the bifurcation.
Mechanical testing
Loose adventitial tissue was removed from the arterial segments. Side branches were carefully clipped. Both ends of the arterial segment were connected with sutures to vertical metallic cannulas. The cannulas were connected to a tensile testing machine ([MTS] Ivry sur Seine, France; accuracy displacement ± 0.05 mm and force ± 0.01 N) with which the axial lengthening of the segment could be controlled and the axial force was measured. In general an artery shortens after removal from its surrounding tissue. To restore its original in situ length the artery was prestretched in the axial direction. The upper cannula was closed and the lower cannula was connected to a reservoir with Tyrode solution (in mM: NaCl 140, KCl 4.9, MgSO4 1.2, NaH2PO4 1.8, and Hepes 5).
The cannulated segment was placed in a small rectangular chamber with four glass windows that was filled with the same Tyrode solution at a constant temperature of 37°C. A dual beam laser-micrometer (Beta LaserMike, Buckinghamshire, UK; accuracy on smooth steel rod ± 1 µm) was placed around the glass chamber with two beams pointing at the middle section of the arterial segment at an angle of 90 degrees. The laser device measured the external diameter of the artery during Tyrode inflation (0 to 300 mm Hg) with both beams simultaneously and calculated the average diameter, correcting for oval shaped segments. For the porcine arteries the pressure was elevated from 0 to 100 mm Hg with incremental steps of 10 mm Hg and from 100 to 300 mm Hg with incremental steps of 20 mm Hg. To establish a more constant mechanical response the arteries were preconditioned before the experiment by elevating the pressure to 200 mm Hg five times [12]. For the human arteries however the maximum pressure was set at 200 mm Hg and preconditioning to a maximum of 100 mm Hg because these arteries were more vulnerable to tearing.
Before the experiment the unloaded vessel length L (Fig 1)
was measured with a caliper. During the tests, the external diameter d and axial force f were measured as a function of rising transmural pressure p at several axial lengths l. After the tests a ring segment of approximately 5 mm in length was taken out of each artery at the spot where the diameter was measured by the laser. By taking digital pictures from microscopic images of these rings, the unloaded dimensions of external diameter D, midwall radius R, and wall thickness H could be determined with a computer. Assuming arterial wall incompressibility during transmural pressure increase in the arterial segment, the midwall radius r and the wall thickness h could be computed. The collected data were used to calculate the relative strains (e
, ez) and the true or Cauchy stresses (
, z) in the circumferential () and axial (z) directions [12, 15]. The relative strains for the middle surface of the vessel wall are given by Equation 1:
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The midwall stresses are given by Equation 2:
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Fig 1. Schematic representation of the arterial dimensions in the undeformed artery (left) and deformed artery (right) configuration. (D, d = external diameter; H, h = wall thickness; L, l = length; R, r = radius; = circumferential direction; z = axial direction.)
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Statistical Analysis
All statistical calculations were performed using SPSS software (version 10.0; SPSS, Chicago, IL). Data are presented as mean ± SD. An analysis of variance (ANOVA) with posthoc Tukey test was used to assess differences in external diameter and wall thickness among species and artery types. A p value less than 0.05 was considered statistically significant.
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Results
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Dimensions
The external diameter and wall thickness of the CA and IMA are listed in Table 1
(pig) and Table 2 (human). In pig and human the external diameter of the CA was similar, 3.44 ± 0.39 mm versus 3.54 ± 0.51 mm, respectively (p = 0.96). Wall thickness was also similar, 0.74 ± 0.17 mm versus 0.89 ± 0.21 mm, respectively (p = 0.20). In pig and human the IMA had a similar external diameter, 3.39 ± 0.46 mm versus 3.28 ± 0.07 mm (p = 0.96) but its wall thickness was smaller in the pig, 0.35 ± 0.07 mm versus 0.71 ± 0.06 mm (p = 0.002).
Pressure-diameter and Pressure-Axial force relations
Because of biological diversity and dimension variation, it proved to be difficult to determine an average pressure-diameter or pressure-force relation from all the samples. For the sake of clarity, one CA and one IMA was chosen from each group to show representative relations for the whole group.
Figure 2
shows the comparisons of the pressure-external diameter and pressure-axial force relation of a porcine and human CA subjected to three levels of axial prestretch. The initial, smallest axial prestretch approximated the in situ length of the artery. We applied larger axial prestretches in porcine arteries because they showed greater shortening than human arteries when excised from the surrounding tissue. In the range from 0 to 100 mm Hg the porcine CA expanded much more than the human CA.
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Fig 2. Measured pressure-diameter (upper panels) and pressure-axial force relation (lower panels) of one porcine coronary artery ([CA] Table 1, pig 5, left anterior descending artery [LAD]; solid box ez = 30%; solid triangle ez = 40%; solid circle ez = 50%) and one human CA (Table 2, human B, LAD; open box ez = 10%; open triangle ez = 20%; open circle ez = 25%) at three different values of axial prestretch ez. The markers indicate the data points.
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Similar to the difference in behavior of the porcine versus human CA (Fig 2), the porcine IMA showed a large increase in external diameter with pressure compared with the human IMA (Fig 3).
The S-shaped pressure-diameter curve of the porcine IMA, which is typical for an elastic artery, hardly changed with increasing axial prestretch. In the human IMA the S shape in the curve could hardly be identified. In the porcine IMA, the axial force tended to decrease with increasing pressure at all levels of axial prestretch whereas in the human IMA the axial force only increased (Fig 3).
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Fig 3. Measured pressure-diameter (upper panels) and pressure-axial force relation (lower panels) of one porcine internal mammary artery ([IMA] Table 1, pig 11, left internal mammary artery [LIMA]; solid box ez = 30%; solid triangle ez = 35%; solid circle ez = 45%; solid diamond ez = 55%) and one human IMA (Table 2, human B, LIMA 2; open box ez = 20%; open triangle ez = 30%; open circle ez = 40%) at three or four different values of axial prestretch ez. The markers indicate the data points.
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Calculated Stress-Strain relationships
Considerable variation in stress-strain relations was found. Consequently, the stress-strain relations in all tested specimens are presented through envelopes, within which all individual stress-strain relations are situated for one specific value of axial prestretch.
In Figure 4,
the circumferential (A) and axial stress-strain relation (B) of the porcine CA and IMA is shown for a 30% axial prestretch, the approximate in situ length of the segments. In the IMA the stresses were higher than in the CA, especially in the circumferential direction (Fig 4A). In the lower strain region the tangent of the stress-strain curves, namely the incremental elastic modulus, was higher for the IMA. The nonlinearity of the stress-strain relations is obvious for both types of arteries. Furthermore the difference in circumferential and longitudinal properties indicates that both arteries showed anisotropic behavior.
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Fig 4. (A) Circumferential stress and (B) axial stress versus circumferential strain relations for porcine coronary artery (solid circles; n = 8) and internal mammary artery (solid boxes; n = 6) at in situ axial prestretch ez = 30%. The envelopes include all individual stress-strain relations and the solid line is the mean stress-strain relation with the standard deviation presented through horizontal lines.
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Variation in the individual stress-strain relations of the human arteries was too large to calculate an average relation. Consequently the circumferential and axial stress-strain relations of all human CAs and IMAs are presented in Figure 5
for 10% (CA) and 20% axial prestretch (IMA) next to the porcine stress-strain envelope at 30% axial prestretch so that all specimens can be compared at their approximate in situ length.
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Fig 5. Circumferential stress versus circumferential strain relations for (A) each individual human coronary artery (CA) and (B) internal mammary artery (IMA), and axial stress versus circumferential strain for (C) each individual human CA and (D) IMA, enclosed in an envelope. The human CA is displayed at an axial prestretch ez = 10% and the human IMA at ez = 20%. The envelopes of the porcine stress-strain relations are equal to those shown in Figure 4. They have been included to compare porcine with human arteries all at their in situ length. The arrowhead in (B) indicates that the envelope continues outside the scope of the figure until it reaches the size as shown in Fig 4(A).
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The most striking observation was that in the pig the circumferential strain was about three times larger than in the human arteries. In the porcine CA the circumferential and axial stress was lower at a given circumferential strain compared with the human CA. At a given strain the incremental elastic modulus was much lower for all porcine arteries. This indicates that the porcine arterial walls are far more elastic than the human ones.
Comment
The principal finding of the study was that the wall of both the IMA and the CA was far more elastic in the young, 78.7 ± 5.8 kg pig than in the human aged 61 to 85 years. The principal inference from this finding is that wall stress and wall injury in the human may be underestimated when coronary connectors that involve overstretching of the wall are evaluated in the pig.
Anatomy and Stress-Strain relation
The CA and the IMA are anatomically different blood vessels. The CA is a muscular artery, whereas the IMA is an elastic artery [16, 17]. As a result at similar external diameters their mechanical properties differ. Part of this difference may be attributed to the smaller wall thickness in the IMA that increases the stress. Although the IMA is classified as an elastic artery, the steeper stress-strain curves (Fig 4) show that in the pig it is actually less elastic than the CA for the major part of the strain range. The stress-strain envelopes of the human CA and IMA (Fig 5) were similar. The variable individual human stress-strain relations within the envelope reflect the variable degree of arteriosclerosis.
The mechanical properties of the CA and IMA are likely to be affected by the reactivity to vasoconstrictors, in particular at their most distal parts [18], but that aspect was outside the scope of the present study. The differences in arterial stress-strain relations between individuals were larger than the differences within one individual between the LAD, RCA, and circumflex artery, or between the LIMA and RIMA. This applied to both porcine and human arteries.
Stress-strain relation: pig versus human
The incremental elastic modulus at physiologic pressures is commonly used to represent the mechanical behavior of the vascular wall [10, 11]. One single value of this modulus however is basically inadequate in predicting the mechanical response to connector induced wall stretch because stress-strain relations of arteries are highly nonlinear, as illustrated in Figures 4 and 5. The only available complete stress-strain relations on porcine and human coronary arteries are from Carmines and coworkers [6] although they did not specify human age categories and the human arteries were frozen, which may have affected their results [7–9]. Furthermore they showed stress-strain results of only one porcine and one human coronary artery. As is clear from the present data (Fig 5), variation in human stress-strain relations was considerable.
Chamiot-Clerc and colleagues [19] found similar strains in the human IMA although the stresses were higher. They used the Laplace formula to calculate the stresses, which means they assumed that the wall thickness is negligible compared with the external diameter. According to Table 2 however the wall thickness/diameter ratio is approximately 20%. Therefore we chose to calculate the average midwall stresses. Neither human IMA axial mechanical properties nor porcine IMA mechanical properties are available in the literature.
The ends of the stress-strain curves in the Figures 4 and 5 represent the mechanical properties at 300 mm Hg for the porcine arteries and at 200 mm Hg for the human arteries. Beyond this point the stress-strain curves will be almost vertical, namely the stresses rise exponentially with minimum additional strain. Eventually this will cause the artery to tear, the so-called bursting pressure point. During the experiments we observed in three pilot experiments that pressures above 200 mm Hg caused the human arteries to tear whereas the porcine arteries could easily be pressurized until 300 mm Hg. Figure 5 illustrates that the porcine arteries could be safely stretched circumferentially until 60% to 70% (left side of the stress-strain envelope) whereas the human arteries could only be stretched until about 20%, which makes the porcine arteries approximately three times more elastic than the human arteries.
Wall stress and anastomotic intimal hyperplasia
Intimal thickening at the anastomotic suture line is greater in prosthetic grafts than in vein grafts [20], which suggests that suture line intimal thickening may be related to compliance mismatch in addition to prosthetic material properties. Increased graft stiffness leads to a substantial increase in the maximum anastomotic mean stress in the distal end-to-side anastomosis [21] and to more distal anastomotic intimal hyperplasia [22]. As an arterial graft, the IMA is to be preferred to an arterialized vein or prosthetic graft, which are less elastic [23]. In contrast to the human, in the pig the IMA wall appeared to be less elastic than the CA wall. This elasticity mismatch might augment intimal hyperplasia in distal anastomotic devices when overstretching of the arteries is necessary [3].
Clinical implications for coronary bypass connectors
The present study leads to a word of caution about relying too much on satisfactory experimental coronary connector results obtained in young animals. As the porcine arterial walls were about three times more elastic than human arterial walls in both longitudinal and circumferential direction, coronary connector induced wall strain will result in far less wall stress in the pig than in human arteries. As a result the pig model will underestimate the risk of wall tears and bleeding. According to Figure 5, a safety value of approximately 20% strain must be considered in the human CA and IMA. We have no experimental experience with clinically applied coronary connectors but from a recent patent literature study [3], an engineering guess can be made about the magnitude of the wall stretch imposed by various connectors.
The GraftConnector (Jomed International, Helsingborg, Sweden) [24] for example requires the IMA to be everted over a ring of 2 to 2.5 mm in diameter. The strain at the everted inner wall can be estimated according to Equation 3 (assuming unchanged wall thickness):
Applying this device to the human IMA with the average properties as listed in Table 2, results in wall strains of about 80% to 110% whereas in the porcine IMA this will be maximally 20%, mainly because of its smaller wall thickness.
Furthermore the reported [25] stretches of the CA due to the inserted GraftConnector stent are up to 92%, which may not influence the anastomosis directly because of the polytetrafluoroethylene covered stent but it may cause tearing of the CA at the end of the stent. Another example of an anastomosis connector, the St. Jude Medical stainless steel connector [26], creates a coronary arteriotomy by first inserting a needle in the arterial wall and then dilating it to a hole with a diameter of 2 mm. Even if the needle creates a hole of 1 mm in diameter, the strain is still 100%.
Anastomotic connectors that overstretch the anastomotic orifice will induce more wall injury and may elicit more anastomotic intimal hyperplasia than nonoverstretching devices because of higher wall stress at comparable strain. Owing to the greater elasticity of its arteries the pig model is less sensitive to these stretch effects than the human. Before its clinical introduction, it is therefore to be recommended to test an anastomotic connector additionally in the pig that has been fed an atherogenic diet and, preferably, in the fresh human cadaver. In conclusion when a coronary connector requires overstretching of the arterial wall, successful implantation and long-term patency in the pig may not provide full guarantee for absence of adverse effects in the human.
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Acknowledgments
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The authors would like to thank M. H. P. van Rijen, C. W. J. Verlaan, and R. Mansvelt Beck for their assistance with the experiments. Furthermore, S. Plomp and W. J. A. van Wolveren, Department of Functional Anatomy, University Medical Center Utrecht, are gratefully acknowledged for providing human arteries. We thank M. J. C. van Gemert, P. A. Wieringa, and J. S. Scheltes for comments on the manuscript. Carolien J. van Andel and this research was supported by the Technology Foundation STW (Grant UGN 66.4183), the applied science division of The Netherlands Organization for Scientific Research, NWO, and the technology program of the Ministry of Economic Affairs.
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Abstract
Introduction
