Measurements on the Elasticity and Damping of Isolated Aortic Strips of the Dog By RICHARD W. LAWTON, M.D. The ex|3erimentiil data obtained on the viscoelastic behavior of isolated aortic strips of the dog consist of: (]) the resonant or natural frequency of forced or free longitudinal vibration; (2) the logarithmic decrement. From these data, static and dynamic moduli and the time constants for the specimens are computed. Variations of these values with frequency, temperature and elongation are presented. The experimental observations are not adequately explained by a simple mechanical analogue. An alternative explanation is offered based on studies of dynamic elasticity in high polymers. Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 B ECAUSE T H E AORTA functions in a dynamic fashion, the experimental evaluation of its mechanical properties by dynamic methods is highly pertinent. However, the normal distending force for the aorta is complex. The characteristic shape of the pulse wave results from a large number of sinusoidal harmonically related waves of varying amplitudes and frequencies. The rapid pressure fluctuations in early systole are represented by high frequency components; in late diastole low frequencies prevail so that the distension of the segment is nearly static. In addition, the static volume-pressure curve for the aorta is nonlinear so that variations in the mean pressure within it may be expected to change its mechanical properties as a whole. Thus, the elastic and viscous behavior of the aorta during life may vary in a complex fashion throughout the cardiac cycle and from cycle to cycle. The experimental data and the analysis that follows is an attempt to simplify the complex problem of the mechanical behavior of the aorta under dynamic conditions. The measurements consist of: (1) the resonant or natural frequency obtained during forced or free vibration of isolated aortic strips of the dog, (2) the logarithmic decrement of the freely vibrat- ing specimen, (3) the static elongation for a given load and, (4) the temperature. The amplitude of vibration was usually held to less than 5 per cent of the specimen length. At these amplitudes the length-tension relation for aortic strips is assumed to be linear. METHODS The apparatus for the study of free and forced longitudinal vibrations in isolated aortic strips is shown diagrammatically in figure 1. Data on 30 strips from 15 animals were studied. The strips were cut in the long axis from the opened aorta and measured approximately 1 X 5 cms. Specimens were sometimes used fresh but often were stored overnight or longer in Ringers solution in the icebox. The thickness was measured with a stage micrometer. The strip was suspended between spring clamps; the upper clamp was held in the chuck of a phonograph cutter head which was set in vibration by a low frequency oscillator-amplifier combination. The amplitude of vibration of the lower end of the specimen was detected by means of a light-shielded photovoltaic cell (Photovolt #S90) and a dc light source. The low frequency spectrum (0-25 c.p.s.) was explored, and the resonant frequency, that is, the frequency for maximum amplitude, determined for each applied weight by observation of the signal on an oscilloscope. Measurements of the logarithmic decrement were carried out by photographing the slow-sweep oscilloscope trace of the decline in amplitude during free vibration. Arrangement was made to modulate the trace with a 60-cycle timing signal in order to improve the accuracy of the measurement of frequency during free vibration. In general, the amplitude of vibration of the low end of the strip was held to below five per cent of the specimen length. At these levels, little or no frequency variation occurred during free vibration. From the Aviation Medical Acceleration Laboratory, U. S. Naval Development Center, Johnsville and Department of Physiology, University of Pennsylvania School of Medicine, Philadelphia, Pa. This investigation was supported in part by a research grant from the National Heart Institute, U. S. Public Health Service. Received for publication February 28, 1955. Experiments were performed in moist air; the specimen was suspended within a tubular lucite 403 Circulation Rrtearck, Volume III, Juli IMS 404 ELASTICITY AND DAMPING OF AORTIC STRIPS Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 temperature-controlled moist chamber, fitted on one side with an optically flat window through which length measurements of the specimen were made by means of a precision cathetometer. The distance between two ink dots placed in the middle section of the strip was determined. This procedure reduced end effects on the measurements. Suitably stable air temperatures and high humidity were obtained by bubbling air through a reflux condenser containing water of known temperature which opened into one side of the chamber. At high humidity, fogging was prevented by thermal radiation from a thermostatically controlled soldering iron directed at the area through which length measurements were made. At equilibrium, temperatures were stable to within approximately ±0.5 C. Both air temperature and specimen temperature were measured by copper-constantan thermocouples. When a wide range of temperatures was required (0-60 C), experiments were performed in a large walk-in chamber (KoldHold) where a high humidity could be maintained. The experimental procedure was as follows: before beginning any stress-strain experiment, the strip was stretched rapidly by hand to 50-75 per cent of its initial length and then released. Several cycles of such stretching and recoil enhanced the reversibility of subsequent stress-strain measurements, as has been noted by other investigators.1 • ! Initially, the largest weight to be used was hung on the specimen which was allowed to elongate to constant length or until the rate of elongation became insignificant. The specimen was then progressively unloaded. Before measuring the length for a given load, the resonant frequency was determined and the logarithmic decline during free vibration photographed. The specimen then was allowed one to two minutes to reach equilibrium length and temperature. After all the weights were removed, the specimen was progressively loaded again and the resonant frequency and the logarithmic decrement determined as before. Finally, the specimen was completely unloaded and the unstretched length determined. EQUATIONS FOR ANALYSIS OF THE DATA The experimental data may be expressed in terms, of a simple model composed of a parallel elastic and viscous component. For a mass of m grams hanging from an elastic element of constant G dynes/cm, and a parallel viscous element of damping constant b dynes sec./cm., the frequency of simple harmonic; motion is given by Page3 as G/m - (6/2m)J (1) where co» = 2TT times /, the natural frequency in c.p.s. The logarithmic decrement is 5 (2) "» 1T&/W1O). For the case of forced vibration the resonant frequency cor is wr! = G/m - (b/m)5 (3) Ordinarily when the damping is small the last term of equations 1 and 3 may be neglected so that Wa1 = a)r* = G/m. In the calculation of G for aortic strips the damping term has been omitted. Thisleads to an error in G of only one per cent or less. While G and b are characteristic of the model of the particular specimen under test, the modulusof elasticity E, and the coefficient of internal viscosity 7, representative of the tissue as a whole, are, according to Ballou and Smith,-4 E = (L/A)G dynes/cm.1, (4> 7 = (L/A)b dynes sec./cm.2 (5) and, where L = the stretched sample length in cm., and A •» the stretched cross-sectional area, in cm.1" The relaxation time or time constant r is T ™ y/E — b/G sec. (6) The relaxation time T is the time required for the stress to relax to 1/e of its initial value. For small damping 5 = TTGOT and the phase angle <f> between the displacement and the force according to Nolle' is given approximately by Tan <f> — 5/v = FIG. 1. Diagram of apparatus. Specimen suspended from cutter head (C.H.) supporting weight (WT.) within moist chamber. OS, low frequency oscillator; AM, amplifier; SC, oscilloscope; PRE-AM., oscilloscope preamplifier; PC, photovoltaic cell; D.C.L.T., dc light source; T, thermocouple; CATH., cathetometer. GOT (7) For these experiments on aortic strips <f> was usually less than 5 degrees. RESULTS Effects of Temperature. In figure 2, at a constant load of 37.5 grams, the values for the resonant frequency GO, the logarithmic decre- 405 RICHARD W. LAWTON Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 25 35 40 TEMP 45 CO 55 Fici. 2. Effects of temperature on resonant frequency (u), logarithmic decrement (&), resting length (Lo), stretched length (/>), and ratio L/La(a). Ordinates for L and Lo = dot separation in mms. The resonant frequency u «• 2rf where / = frequency in c.p.s. ment 5, the resting length Lo, and the extended length L for a typical isolated dog aortic strip are shown as a function of temperature. The relative change in length, L/Lo or a, also is computed. Variations in resonant frequency are observed between 20 and 40 C where there is a general trend towards a lower frequency with higher ternperatures. In other experiments, at temperatures below 15 and above 45 C, a sharp rise in frequency occurred. Although the logarithmic decrement seems to parallel the resonant frequency between 26 and 38 C in figure 2, the relationship is not •exact. The calculated spring constant, G, has fallen about 13 per cent over this temperature interval. Although the magnitude of the viscous term in equation (3) is reduced by 47 per cent over this same temperature range, its contribution to the calculated value of the spring constant at 38 C is only 0.10 per cent while at 2G C it is 0.26 per cent. This substantial change in the viscous term thus exerts a negligible effect on the value of the spring constant as measured by resonant frequency determinations under these experimental conditions and another explanation for the frequency change must be sought. At temperatures below 15 C and above 45 C the logarithmic decrement rises markedly. Changes in the stretched and unstretched length of the specimen with temperature always occur. As a general rule, however, the ratio L/Lo is relatively independent of temperature in the physiological range as shown in the diagram so that it has been used to present the data in the subsequent sections. Dijnaviic and Static Moduli. In figure 3, values for the elastic moduli for a typical isolated aortic strip are shown under static (E.) and dynamic conditions (Ed) at constant temperature. Because both E. and EH are characteristic of the specimen only at a given elongation the stretched length (L) and the stretched cross-sectional area (A) must be used in the calculations. Previous investigations8 have established that elongation of isolated aortic strips is isovolumetric. Accordingly, the unstretched length Lo and unstretched cross-sectional area Ao are converted to their stretched counterparts by the relations L = LQCX, and A = A0/a. The equations for the static and dynamic moduli for figure 3 are then given by: AAL L A dynes/cm.2; (a. - \)Ao GLo dynes/cm.4 (8) (9) RELATIVE LENGTH (L/Lo) FIG. 3. Comparison of static (E.) and dynamic (Ed) moduli at various elongations for typical aortic strip of the dog. 406 ELASTICITY AND DAMPING OF AORTIC STRIPS TABLE 1.—Effect of Temperature on the Static (E,) ami Dynamic (Ed) Moduli, the Relative Length (a), the Product (or) and the Resilience (R) Temp F grama 26.7 37.7 50.2 50.2 Liu 1.280 1.287 E, x io« Ed x 10" 2.94 2.89 6.47 5.76 0.044 0.036 0.69 0.79 Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 Over the entire range of elongations the dynamic moduli are higher than the static values. A similar elevation is found in the case of many high polymers studied by dynamic methods.7 Both static and dynamic moduli may have minimum values at small elongations. The curvature and the dependence on elongation under dynamic conditions is much more pronounced than under static conditions. In table 1, 15 pairs of observations on 8 strips from 4 dogs are given illustrating the effects of temperature on the static and dynamic moduli. To obtain these data the procedure employed was as follows: Observations were first made at room temperature (average value 26.7 C). The temperature then was raised (average value 37.7 C) and, after equilibration for approximately one hour at the new temperature, the observations were repeated. Only two temperatures were used. Values given in the table are averages and include a range of loads from 12.5 to 107.5 Gm. Xote that despite a 10 C change in temperature, the average relative length a is nearly constant so that the average E, is also approximately constant. The dynamic modulus of elasticity Ed, however, decreases with a rise in temperature. Viscous Behavior. The relaxation time is independent of the specimen dimensions and is, therefore, experimentally a reliable measure of the viscous properties of the specimen (equation 6). A number of quantities may be derived which are primarily dependent on the relaxation time. For instance, the fraction of the vibration energy persisting in the second of two successive free oscillations, the so-called dynamic work recovery or resilience,-4 is given by R = e —2 r u T (10) Values for WT and R are given in table 1. The resilience is a measure of the magnitude of the hysteresis loop and is temperature dependent. For length-tension experiments its value is equal to the work area below the retraction curve (work recovery) divided by the work area below the elongation curve (work input). A general relation between w and r appears to exist in the case of aortic strips over the limited frequency range of our data. This suggests that cor might be treated as a characteristic constant for the tissue under these experimental conditions, as has been noted for some polymer systems by other investigators.4 In figure 4 data from two dogs are presented. At constant temperature (28 C) four static stress-strain cycles were performed on a single aortic strip from each dog. Values for a> and r were determined at various points along the curves. At the end of each stress-strain cycle approximately 1 cm. was cut from the end of the strip. This alteration in length produced a somewhat wider range of frequencies. The average value for ur is 0.077 for these experiments and the solid line in the diagram roughly approximates the experimental points. At this temperature the resilience is thus approxi- 0 004. 0003 0.00 20 30 40 50 60 70 8 0 9 0 FREOUENCY (CJ) FIG. 4. Plot of resonant frequency (u) vs. relaxation time (T). Solid line equals theproduutur = 0.077. For explanation see text. RICHARD W. LAWTON Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 12 13 14 15 16 17 RELATIVE LENGTH [ L / L o ) Fia. 5. Variations of the resonant frequency (u), tlie logarithmic decrement (S), the spring constant (0), and the "coefficients of hysteresis" UT and u6 with elongation. Note that the ordinate for UT has been expanded as compared to that for S, although I0 6/r II — UT. mutely 0.62. Given cor constant and because ub/G = cor, one might expect the quantity col) to follow quite closely the form of the curve for the spring constant, G. This appears to be only approximately the case for many high polymers7 and also for aortic strips as indicated in figure 5. The value of cor goes through a minimum. This elongation, where viscous loases are a minimum, represents the area of maximum energy transfer. In the intact dog maximum energy transfer in the aorta appears to take place in the range of normal mean aortic pressure according to the experiments of Peterson.8 "Whether identical elongations of the aorta are involved requires further study. Preliminary calculations indicate that this is the case. DISCUSSION A departure from physiological conditions has been made in this study and certain pre- •±07 cautions taken in order to simplify analysis of the viscoelastic behavior of the aorta. The preliminary stretching procedure brings about reversible static stress-strain behavior and, in addition, reduces the magnitude of the viscous losses so that the contribution to the calculated dynamic modulus by this factor is small (equations 1 and 3). This latter effect may be related in part to the disappearance of active smooth muscle participation in the elastic response of fresh specimens. Such losses as are present may be related primarily to the fibrous structures in the specimen. When precautions concerning the nature of the vibration and the state of the vessel are taken, and the data are analyzed by a simple mechanical analogue, the so-called "elastic constant" of the system varies continuously with elongation under both static and dynamic conditions. The elastic behavior of isolated aortic strips, therefore, cannot be considered as linear except over a small range of elongation. The increase of the elastic moduli under dynamic conditions and the decrease in the dynamic moduli with a rise in temperature are not readily explained. The contribution of the viscous term to the value of the dynamic modulus in both cases is small and conventional concepts of damping (proportional to velocity) apparently cannot account for the experimental observations. A reasonable suggestion, however, has been made8 on the basis of studies of the dynamic behavior of polymeric systems in general. If the specimen is imagined as being composed of a randomly intermeshed network of molecular chains, the uncoiling process under dynamic conditions might be impeded by network entanglement. Because of these entanglement effects, portions of the molecular chains do not participate in the elastic response; the chain as a whole behaves as though it were shorter and, thus, of more limited extensibility. An elevated modulus results. As the frequency changes (at constant temperature), the percent of the network which responds, changes, and accordingly, the time constant for the system changes such that cor appears to be approximately a constant (fig. 4). As the temperature is increased, the thermal motions 408 ELASTICITY AND DAMPING OF AORTIC STRIPS Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 of the molecules increase, entanglement is reduced, uncoiling is enhanced and the dynamic modulus is reduced. The observed viscous behavior of the specimen may be interpreted, then, as related only to that portion of the network participating in the responses and to vary with the percent of the network involved. Even for relatively low frequencies of vibration this model suggests that the untangling of the molecular chains during extension of the specimen might be noticeably different from their behavior during recoil. Presumably these differences might account in part for the hysteresis loops observed in biological tissues such as the aorta. While the behavior of the specimen during extension might be quite variable, depending upon the manner of uncoiling the chains, the behavior during recoil might be more reproducible, as appears to be the case for aortic specimens.1'2 The dependence of the elastic modulus and the damping on the driving frequency has physiological meaning in terms of the frequency spectrum of the pressure pulse in the aorta during life. To the extent that these data are applicable to the living situation, it would appear that the high frequency components present during early systole should result in a larger modulus, a small displacement and small damping. In late diastole, where low frequencies predominate, a smaller modulus, a larger displacement and greater damping are to be expected. CONCLUSIONS Measurements of the static and dynamic moduli and the damping in isolated aortic strips of the dog indicate that changes in the dynamic modulus with temperature and the increase of the dynamic over the static moduli cannot be accounted for on the basis of conventional viscous behavior. A qualitative explanation of these changes based on variable entanglement of molecular chains in a polymer model is offered. ACKNOWLEDGEMENT It is with pleasure that the author acknowledges the skillful technical assistance of Mr. Herman Sharma and the helpful criticism of Professor Allen King of the Department of Physics, Dartmouth College. REFERENCES 1 REMINGTON, J. W., HAMILTON, W. F. AND DOW, P.: Some difficulties involved in the prediction of the stroke volume from the pulse wave velocity. Am. J. Physiol. 144: 536, 1945. 'KRAFKA, J., JR.: Comparative study of histophysics of aorta. Am. J. Physiol. 125: 1, 1939. PAGE, L.: Introduction to Theoretical Physics. 1 New York, Van Nostrand, 1935. BALLOU, J. W. AND SMITH, J. C : Dynamic meas* urements of polymer physical properties. J. Appl. Physics 20: 493, 1949. 6 NOLLE, A. W.: Dynamic mechanical proi>erties of rubber-like materials. J. Polymer Sc. 5: 1, 1950. 6 LAWTON, R. W.: The thermoelastic behavior of isolated aortic strips of the dog. Circulation Research 2: 344, 1954. T MOONEY, M. AND BLACK, S. A.: Elongation hysteresis of hevea and synthetic elastomers. Canadian J. Res. 28F: S3, 1950. 8 PETERSON, L. H.: The dynamics of pulsatile blood flow. Circulation Research 2: 127, 1954. 1 MEYER, K. H.: Natural and Synthetic High Polymers. Ed. 2, New York, Interscience, I960, p. 737. Measurements on the Elasticity and Damping of Isolated Aortic Strips of the Dog RICHARD W. LAWTON Downloaded from http://circres.ahajournals.org/ by guest on June 14, 2017 Circ Res. 1955;3:403-408 doi: 10.1161/01.RES.3.4.403 Circulation Research is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1955 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7330. Online ISSN: 1524-4571 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://circres.ahajournals.org/content/3/4/403 Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Circulation Research can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. 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