Differences in mechanical properties of the common carotid artery and abdominal aorta in healthy males

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1 Differences in mechanical properties of the common carotid artery and abdominal aorta in healthy males Toste L~ne, MD, PhD, Flemming Hansen, MD, Peter Mangell, MD, and Bj6rn Sonesson, MD, Malmt, Sweden Purpose: Vascular disease is differentiated throughout the vascular regions, with central arteries more prone to dilation and with peripheral arteries more prone to occlusive disease. n this study we investigated the diameter and compliance in the common carotid artery and abdominal aorta in healthy males at varying ages to assess potential differences in the aging process. Methods: An ultrasound phase-locked echo-tracking system was used to determine differences in diameter and pulsatile diameter changes of the common carotid artery and abdominal aorta in 56 healthy Caucasian males ages 1 to 74 years. Pressure strain elastic modulus (p) and stiffness (f~) were calculated from diameter, pulsatile diameter change, and blood pressure obtained by the auscultatory method. Compliance was defined as the inverse of p and stiffness. Results: The diameter of both common carotid artery and abdominal aorta increases not only when a person is a child, but also when they are between 25 and 7 years old. The dilation in adults seems to be more accentuated in the abdominal aorta (27%) than in the conunon carotid artery (17%). p and stiffness (f~) are higher in the common carotid artery when a person is 1 years of age (p <.1 and.5). However, during aging, p and stiffness (f~) increase to a higher extent in the aorta than in the common carotid artery, with a significantly higher p and stiffness (f~) in the aorta when a person is 45 years and older (45 years:p <.5 andp = NS; 6 years:p <.1 andp <.1; 7 years:p <.1 andp <.1). Conclusions: This investigation demonstrates regional differences in diameter change and compliance in the common carotid artery and abdominal aorta and implies that the abdominal aorta is more prone to degenerative changes than the common carotid artery. This may be one etiologic factor for the regional differences in vascular disease. (J VAse SURG 1994;2: ) The mechanical properties of major arteries are of interest from both a physiologic and a pathophysiologic point of view because they have importance for cardiac work, blood pressure regulation, and possibly the development of vascular diseases. Thus the mechanical properties of arteries have been studied extensively in vitro~; there are also some invasive 2,3 and noninvasive 4 studies in animals and in From the Departments of Surgery and Clinical Physiology (Dr. Hansen), Lund University, Maim6 General Hospital, Maim6. Supported by the Faculty of Medicine, Lund University, Lund, Sweden. Reprint requests: Toste Liinne, MD, PhD, Department of Surgery, Lund University, Malta6 General Hospital, S Maim6, Sweden. Copyright 1994 by The Society for Vascular Surgery and nternational Society for Cardiovascular Surgery, North American Chapter /94/$ /1/ man. Of the methods used in vivo, however, local vascular changes cannot be assessed by means of pulse-wave velocity, 5 and the use of the diastolic pressure decline is limited because reflected pressure waves induce significant errors. 6 Angiography is invasive, z and surgically exposed vessels differ in compliance compared with unexposed ones. 4,8 Magnetic resonance imaging 9 and ultrasonography with either M mode 1 or echo-tracking techniques can, however, provide acceptable noninvasive means of measurements. Of these methods, the echo-tracking technique has the best resolution with reproducible results. H The echo-tracking principle was first described by Arndt et al. 12 in 1968 and later modified by Hokanson et al. ~3 to be independent of echo amplitude. The smallest vessel movement detectable with our echo-tracking system (Diamove; Teltec AB, Lurid, Sweden) is 8 ~m, 14 which by far exceeds the

2 JOURNAL OF VASCULAR SURGRY Volume 2, Number 2 LCinne et al. 219 resolution capacity for the real-time scanner for static objects. t has previously been shown in postmortem specimens that arterial distensibility decreases with age. is This has been confirmed in vivo in our laboratory with an exponential decrease in compliance in the abdominal aorta (AO) in males. 16 Sex differences also seem to be obvious, with higher compliance in females than in males. 17 One reason that compliance decreases with age could be the relative increase of collagen as compared with elastin. However, the relative amount of elastin as compared with collagen is quite different in varying parts of the vasculature, with, in general, relatively more elastin in the central arteries than in the peripheral arteries, where there is a predominance of collagen? 8 Thus different regions of the arterial tree ought to show differences in mechanical properties. The purpose of this study was to examine in detail the differences in diameter and compliance in the common carotid artery (CCA) and AO in Caucasian males and examine their changes in relation to age. The CCA and the AO were chosen because development of atherosclerosis is common in both locations and aneurysm formation is common in the latter. MATRAL AND MTHODS The examinations were performed on 56 healthy nonsmoking Caucasian male volunteers, 1 to 74 years old. None had a history of cardiopulmonary disease or medication, and none had diabetes. The ratio between ankle-brachial artery pressure was greater than 1 in all subjects, indicating absence of obliterative atherosclerotic lesions in the arteries to the lower Limbs. ach subject, including the parents of the 1-year-old volunteers, gave informed consent to the examinations, which were approved by the thics Committee, Lund University, Sweden. For noninvasive monitoring of pulsatile diameter changes in the distal AO and the CCA, an electronic echo-tracking instrument (Diamove; Teltec AB) was used. This instrument is interphased with a real-time ultrasound scanner (UV 24 Hitachi, Tokyo, Japan) and fitted with a 3.5 MHz (AO) or 5 MHz (CCA) linear array scanner) 9 All examinations were performed with the subjects in the supine position and after at least 15 minutes at rest. The AO was insonated from the epigastrium. Measurements in the young were performed between the renal arteries and the aortic bifurcation, and in the adults measurements were performed about 3 cm proximal to the aortic bifurcation. The CCA was insonated from the neck behind the sternocleidomas- toid muscle, and measurements were performed 1 to 2 cm proximal to the bifurcation. The arteries were visualized in a longitudinal section on the real-time image. Two electronic markers, each representing one tracking gate, were aligned with and locked on the echoes from the posterior interphase of the anterior wall and the anterior interphase of the posterior wall, respectively. The echo-tracker measures the distance between the vessel walls perpendicular to the longitudinal axis of the vessel. A data acquisition system containing a personal computer type 386 (xpress, Tokyo, Japan) and a 12-bit analogue-to-digital converter (Analog Devices, nc., Norwood, Mass.) were included for the simultaneous monitoring of an electrocardiogram, and the vessel diameter. The smallest detectable movement is 8 xm, and the repetition frequency of the echo tracking loops is 87 Hz, that is, the time resolution is about 1.2 milliseconds. The added quantifying error from the data acquisition system to the electrocardiographic signal is 25 ~V. Arterial blood pressure was measured with auscultation with a sphygmomanometer on the left arm immediately after measurement of the pulsatile diameter. The arterial strain, or the fractional diameter change was defined as D systolic - D diastolic strain = D diastolic (1) Pressure strain elastic modulus (p) 2 was defined as P systolic - P diastolic p = x (D systolic - D diastolic)/d diastolic (2) P systolic and P diastolic are the maximum systolic and diastolic blood pressure levels in mm Hg. D systolic and D diastolic are the corresponding diam.- eters in millimeters. The p is measured in N/m 2. The constant in equation 2 accounts for the conversion from mm Hg to N/m 2. From the equation above it is obvious that the p is pressure-dependent because of the nonlinear pressure/diameter behavior of the arterial wall? 1 This somewhat limits its use. Hayashi et al.22 established a relation for calculation of compliance in vitro that is less dependent on pressure and based on the observed linear relation between the logarithm of relative pressure and distention ratio. The slope of this exponential function was called [3 or stiffness. This index characterizes the entire deformation behavior of the arterial wall without pressure dependence in the physiologic range. 22 This stiffness index was later modified and used in vivo by Kawasaki et al.23 t was defined as

3 22 L#nne et al. JOURNAL OF VASCULAR SURGRY August Common carotid artery Abdominal aorta ~ 6.5 o A,J Male 17 years sap 11 dap 7 stiffness 3.5 A lz-.~ s < ~.o i J " B Male 17 years.2 s sap 11 dap 7 stiffness 3. A 8-9- L- O O " " L_ C //~ Male 67 years sap ' / ~ dap 8 +. j / \ stiffness 1.3 2a~.2 s < D Male 67 years //~ sap 145 / / [ ~'~ stiffness 25.9 Fig. 1. Representative tracings of diameter curves from CCA and AO in one 17-year-old (A and B) and one 67-year-old (C and D) healthy male during heart cycle. SAP, Systolic arterial pressure (mm Hg), DAP, diastolic arterial pressure (ram Hg). Loge (P systolic/p diastolic) [5 = (D systolic - lj diastolic)/d diastolic (3) Compliance as a general term was defined as the inverse relation of both p and stiffness ([3), because the two indexes show parallel changes. The compliance includes both structural and functional variables, that is, the intrinsic elastic property of the vessel wall and the mean arterial pressure (MAP). This is necessary in noninvasive in vivo measurements of compliance because it is not possible to correct it to common MAP. The brachial arterial blood pressure obtained by the auscultatory method was approximated as the systemic blood pressure in the AO and the CCA. t is well known that the arterial pressure waves undergo transformation, with peaks more prominent as the waves travel further from the heart. However, these differences in central and peripheral pressures are reduced and disappear at older ages. 24 When intraarterial pressure measured in the AO is compared with brachial blood pressure as measured by the auscultatory method, it is found that the pulse pressure is approximately 1% less intraarterially than by the auscultatory method. 2s Recalculation of these data shows a slight systematic underestimation of the p and stiffness (J3) when the auscultatory method is used. The interobserver and intraobserver variability of the measured pulsatile diameter changes with the system used was 1% to 15%, and, compiled with blood pressure measurements in calculating p and stiffness (13), the variability slightly increased to 15% to 2%. 11 Three consecutive measurements were performed on the CCA and the AO in each individual with calculations of p and stiffness (13) from the corresponding diameter, pulsatile diameter changes, and

4 JOURNAL OF VASCULAR SURGRY Volume 2, Number 2 L~inne et al. 221 blood pressure obtained by the auscultatory method. The averages of the values from each individual were then compiled into the corresponding age group. MAP was taken as the diastolic pressure plus one third of the pulse pressure. The heart rate was monitored by electrocardiography. The results are expressed as mean -+ SD. The Student's t test was used for statistical analyses, andp <.5 was chosen as the level of significance. Linear regression with calculation of correlation coefficients (r) was used to relate age with increase in diameter (percentage) in the CCA and AO. To evaluate the influence of age, blood pressure, aortic, and CCA diameter on the arterial stiffness, a multiplicative multiple stepwise linear regression model was used. A m.m "O m RSULTS Fig. 1 shows representative tracings of diameter curves from the AO and the CCA in a 17-yearold male and a 67-year-old man, respectively. ach curve is based on nine consecutive cardiac cycles. The mean diameter of the CCA in the 17-year-old male (Fig. 1, A) was 6.8 mm, and the diameter increase during systole was.9 ram, that is, 13.2% of the mean diameter. n the 67-year-old man (Fig. 1, C) the mean diameter was 8.7 mm, and the diameter increase during systole was.5 mm; that is, 5.8% of the mean diameter. Calculated stiffness ([3) was 3.5 and 1.3, respectively. The mean diameter of the AO in the 17-year-old male (Fig. 1, B) was 16.1 mm, and the diameter increase during systole was 2.3 mm; that is, 14.3% of the mean diameter. The corresponding values in the 67-year-old man (Fig. 1, D) were 22.9 mm,.5 mm and 2.2%, respectively. Calculated stiffness ([3) was 3. and 25.9, respectively. n Fig. 2 the mean diameter in the CCA and AO in relation to age (1 to 74 years) for all the subjects is shown. The diameter of the CCA increased from 6.9 +_.8 mm to mm, whereas the increase in the aorta was more marked from 11.1 _+ 1.7 mm to mm. Note that the diameter increase in the AO as compared with CCA was most apparent in the growing period. However, a further increase in the aortic diameter as compared with CCA was evident also in the adults. n Fig. 3 the changes in percentage of the mean diameter in the CCA and AO are seen in adult men 25 to 74 years of age. A larger increase (linear regression [r =.99]) in aortic diameter (27%), as compared with CCA (17%) (r =.89), can be seen. Fig. 4 shows the decrease in arterial strain or the fractional diameter change in the CCA and AO in relation to age. When a person is 1 years of age, the i== Age (years) Fig. 2. Mean diameter increase in CCA (C) and in AO (A) with age in 56 healthy male volunteers. Note more marked diameter increase in aorta in young and in adults. CCA has lower strain ( ) than the AO ( ) p <.5, whereas when a person is 46 years and older, the reverse is the case; at 46 years the CCA is.8 +_.2 versus the AO of.4-+.2(p <.1); at 6 years the CCA is.6 +_.2 versus the AO of (p <.1); and at 74 years the CCA is.5 _+.2 versus the AO of.3 _+.1 (p <.1). Fig. 5 shows the stiffness ([3) in the CCA and AO in relation to age. Stiffness ([3) in the CCA increased from to 14.2 _ However, the increase was more pronounced in the aorta (from to ). The corresponding values for p are shown in Table, where p in the CCA increased from to Also regarding p, the increase was more pronounced in the aorta (from to 3.35 _+ 1.4). Note the significantly higher p and stiffness ([3) in CCA as compared with AO when a person is 1 years of age and the increase of p and stiffness ([3) in the AO,

5 222 LSnneetal. JOURNAL OF VASCULAR SURGRY August " P 2" F_,2 -o 1.= (/) L,., Age (Years) Fig. 3. Mean diameter increase (%) in CCA (C) and AO (A) in adult men, 25 to 74 years of age. Note more marked increase in aortic diameter as compared with carotid artery. which is much more pronounced than that of CCA when a person is increasingly older. This indicates an inverse relationship with significantly higher p and stiffness ([3) in the AO instead of CCA from 46 years of age onward. The variables correlated to the arterial stiffness ([3) (p and stiffness) were analyzed with multiplicative multiple stepwise linear regression. t was found that age (both p and stiffness [[3]) by far showed the strongest correlation and, to a lesser degree, the arterial diameter ( ~ 1%) in both the aorta (stiffness [[3]) and the CCA (stiffness [[3]). n p there was no correlation to diameter, but there was to blood pressure (~ 1.5%), whereas blood pressure showed no correlation to the increase in stiffness (13). The multiple regression for both p and stiffness ([3) showed in aorta r =.95 (p <.1), and in CCA r =.84 (p <.1). The background data on arterial pressure, diameter and p in the AO and in the CGA of the 56 male subjects arc compiled in Table. DSCUSSON n this study the age-related changes in diameter and compliance of the CCA and distal AO in healthy Caucasian males, 1 to 74 years old, were investigated with a noninvasive ultrasonic echo-tracking technique. The diameter increased in both the CCA and the AO, both in the growing period and in adults. However, the increase was more pronounced, Age (years) Fig. 4. Change in strain (fractional aortic diameter change) in CCA ((2) and AO (A) with age in 56 healthy male volunteers. Note lesser strain in CCA as compared with AO at young age, whereas reverse is the case from 46 years of age onwards. in the AO. p and stiffness ([3), (i.e., the inverse of compliance), in the CCA were initially higher than in the AO, but at increasing age p and stiffness ([3) increased much more in the AO than in the CCA. Thus at 46 years of age onward p and stiffness ([3) were significantl~(.higher in the AO than in the CCA. The ultrasomc echo-tracking technique offers several advantages compared with other methods because of its simplicity and noninvasive character. t is of crucial importance, however, that the method has good accuracy and resolution capacity. Direct comparison of pressure and diameter curves shows great similarities, 21 and the echo-tracking technique seems at present to be the method of choice for studying local vascular wall movements of major arteries in vivo. H The CCA and aortic diameter increased rapidly in early systole because of the rapid increase in arterial pressure (Fig. 1). The dicrotic wave, seen on the declining part of the diameter curve in diastole both in the CCA and AO in the young males, most likely indicates reflexions from vessel branch points, bifur-

6 JOURNAL OF VASCULAR SURGRY Volume 2, Number 2 Li~nne et al. 223 cations, and resistance vessels.26 This dicrotic wave no longer exists in the elderly, but instead a clear-cut accentuation of the diameter curve in late systole (Fig. 1). This depends in all probability on the fact that the reflected waves move faster in the less compliant older vessels with an earlier interaction in the pulse pressure curve with accentuation of late systole instead of diastole. 27 The pressure/diameter relationship of the arterial wall is curvilinear, as is evident from simultaneous recordings of arterial pressure and diameter, 2'21 and it appears biphasic with an inflection at approximately 9 to 11 mm Hg, that is, between the diastolic and systolic pressures. Above this pressure range, the vessel is stiffer (less compliant). 1,21 Available data indicate that both elastin and collagen contribute to the wall mechanics. lastin is preferentially load bearing during small distentions, whereas collagen is load bearing during large distentions. 28,29 Thus the rapid increase in diameter at arterial pressures below the inflection probably mainly reflects stretching of elastin, whereas both elastin and collagen contribute to the tension of the wall above the infection. n this study we have chosen to define the arterial compliance as the inverse of p and stiffness ([3). These indexes are to some extent dependent on blood pressure and represent mean values of nonlinear curves, which somewhat limits their application. However, stiffness (13) is less dependent on pressure than p 16'21 but equally sensitive to the change in compliance observed during aging (Fig. 5 and Table ). Stiffness (13) may therefore be a more useful index of arterial compliance. The differences in p and stiffness (13) between the CCA and AO could be the result of several factors. One is the blood pressure, which was obtained from the brachial artery and was assumed to be equal to the pressure in the CCA and AO. t is known that there are minor blood pressure differences between central and peripheral arteries, which could induce an error, although the CCA and AO are approximately at the same distance from the heart. However, at older ages no blood pressure differences in the arterial system are seen. Thus the differences in compliance between the CCA and AO are valid. Furthermore, the blood pressure curves in children are similar in central and peripheral arteries. 3 This, together with measurements of compliance in an animal model that show differences of the same magnitude as in the 1-year-old males (unpublished results, April 1994), indicates that the compliance values in the youngest are valid as well. n young adults, however, this could induce an error in the qa q..m 3 2 1,,/ i i i i Age (years) Fig. 5. Change in stiffness in CCA (C) and AO (A) with age in 56 healthy male volunteers. Note higher stiffness (13) in CCA as compared with AO at young age, whereas reverse is the case from 46 years of age onward. compliance calculations. Other factors are the wall thickness and the vessel wall content. The normal aging process of the vessel wall includes vessel wall thickening and a decrease in elastin concentration, a progressive fraying of elastic lamellae with architectural rearrangements and an increase in collagen content. Along with these degenerative changes the distensibility of the arteries decreases with age. However, the wall thickening with age in the CCA " - - and the AO seems to be of the same magmtuae. 15 Thus the compliance curves represented by p and stiffness ([3) (Fig. 5 and Table ) could imply that the degenerative changes are more marked in the AO as compared with the CCA. The relative amount of collagen and elastin in different arterial beds was examined in a study by Fisher and Llaurado, 18 who showed that elastin was predominating in the thoracic aorta, whereas outside the thorax the reverse was the case. Thus the relation between collagen and elastin was.49 in the thoracic aorta, 1.58 in the abdominal aorta, and 2.55 in the C

7 224 L~inne et al. JOURNAL O1: VASCULAR SURGRY August 1994 Table. Aortic and carotid artery compliance at different ages (mean SD) AP syst AP diast MAP D max D min p Age (yr.) Artery (mm Hg) (mm Hg) (ram Hg) (ram) (mm) (1 s x N x m -2) (n = 9) AO 11 _ _ C P < (n = 8) AO _ C _ NS 25 _+ 3 (n = 8) AO C 116 _ NS 46 _+ 4 (n = 7) AO _ _+.6 C _+.34 NS (n = 11) AO 132 _ _.49 C 132 _ P <.1 74 _+ 6 (n = 13) AO _ _+ 1.4 C 153 _ _+.84 P <.1 AP, Arterial pressure; MAP, mean arterial pressure; D max, maximum systolic diameter; D m/n, minimum diastolic diameter; p, pressure strain elastic modulus. carotid artery. (See also Nichols and O'Rourke24.) This could provide the basis of different mechanical behavior in different vascular beds, which clearly can be seen in the 1-year-old males investigated with a stiffer CCA as compared with the AO. The difference seems to diminish with increasing age, and at 15 to 25 years no difikrences in mechanical behavior between the two vascular regions are seen. This is probably the reason why other investigators have not found any differences in elasticity between the AO and CCA at younger ages. 23 This study shows that p and stiffness (13) in the AO increase rapidly at older ages to a significantly larger degree than in the CCA. This is in contrast to other investigators who have found approximately equal values of p and stiffness (13) at all ages in the CCA and the AO. 23'31 Because there seems to be large sex differences in the arterial compliance, 17 one reason for the divergent results could be the fact that these investigators included both women and men in their materials. Wolinsky and Glagov 32 found an avascular inner part of the media of the human abdominal aortic wall. This is in contrast to other mammals with corresponding size and thickness of the aortic wall, in whom the inner part of the wall was perfused by vasa vasorum. They also found a lesser number oflamellar elastic units in the wall than expected. Thus the estimated mean tension per lamellae in the human AO was much higher than that of any of the other mammalian vascularized aortic media examined. This could account for one factor responsible in accentuating the degeneration of the aortic wall with increased stiffness as a consequence. As the artery dilates (Fig. 2) the circumferential wall tension and stress increase according to Laplace's law and may further accentuate the degeneration. Difference in the degree of dilation with age, with the thoracic aorta diameter increasing to a greater degree than the AO, 33 may explain the apparent appearance of a new reflection site in the AO of adult human beings. 34 This may also explain the greater propensity for degeneration of the aortic wall as compared with CCA, on the basis of greater shear stress of the aortic wall at a region of relative narrowing. One interesting clinical reflexion is the predominance of aneurysm formation in the distal abdominal aorta as compared with the CCA. n an in vitro study Moritake et al.3s found high stiffness to be a probable etiologic factor in cerebral aneurysm formation. An increased stiffness is also found in abdominal aortic aneurysms as compared with normal aortas. 16 n conclusion, these results indicate a differential behavior of arterial wall mechanics in different vascular beds, as demonstrated in an increased stiflhess in the CCA compared with the AO at young age, n aging, however, there seems to be a more marked degeneration in the aortic wall, with a successively larger increase of stiffness in the AO as compared with the CCA and also a more marked dilation. This seems to be of relevance in discussing the pathophysiologic behavior of the CCA and the AO with differences in prevalence in atherosclerosis and aneurysm formation. We thank the staff of the Department of Clinical Physiology, Maim6 General Hospital, for skilled assistance. RFRNCS 1. Dobrin P. Vascular mechanics. n: Shepherd JT, Abboud FM, eds., Handbook of physiology: part, peripheral circulation and organ blood flow. Baltimore: Williams & Wilkins, eds. 1983;: Busse R, Bauer RD, Schabert A, Summa Y, Bumm P, Wetterer. The mechanical properties of exposed human

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