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1 Institute for Biomaterials and Biomedical Engineering, 2 Departments of Obstetrics and Gynecology and 3 Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario M5S 1A8; 4 School of Biomedical Engineering, Dalhousie University, Halifax, Nova Scotia B3H 4H7; and 5 Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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We previously reported changes in mechanical properties and collagen cross-linking of the ovine thoracic aorta during perinatal development and postnatal maturation, and we now report changes in biochemical composition (elastin, collagen, and DNA contents per mg wet wt) over the same developmental intervals. A comparison of results from the present and previous studies has yielded novel and important observations concerning the relationship between aortic mechanics and composition during maturation. Developmental changes in aortic incremental elastic modulus at low tensile stress (Elow) closely followed changes in relative elastin content (i.e., per mg wet wt). An 89% increase in Elow during the perinatal period was associated with a 69% increase in relative elastin content, whereas neither variable changed during postnatal life. Incremental elastic modulus at high tensile stress (Ehigh) did not change during the perinatal period but increased 88% during postnatal life. This pattern closely paralleled changes in collagen cross-linking index, which did not change perinatally but almost doubled postnatally. In contrast, relative collagen content (per mg wet wt) increased only slightly from fetal to adult life, a trend that was unrelated to aortic mechanics. Substantial, progressive decreases in measures of wall viscosity (pressure wave attenuation coefficient and viscoelastic phase angle) from fetal to adult life followed the pattern observed for relative DNA (smooth muscle cell) content (per mg wet wt). Our findings suggest that accumulation of elastin per milligram wet weight contributes most to developmental changes in Elow, change in collagen cross-linking is the primary determinant of developmental changes in Ehigh, and cell accumulation contributes most to developmental changes in wall viscosity.
elasticity; viscoelasticity; development; elastin; collagen
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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THE VISCOELASTIC PROPERTIES of mature arteries are determined largely by the relative proportions of the main components of this composite tissue: elastin, collagen, and vascular smooth muscle cells. Elastin is thought to contribute most to the elastic properties at low and moderate blood pressures, with collagen making increasing contributions at higher pressures (33, 44). In contrast, smooth muscle cells are thought to be the principal source of viscosity in this tissue (29).
Although relative composition appears to explain mechanics in mature arteries, it is less clear that developmental changes in arterial viscoelasticity can be attributed entirely to differential accumulation of wall constituents. For example, developmental changes in arterial extracellular matrix include substantial remodeling and maturation of matrix proteins: fenestrae form and enlarge in elastic lamellae (45), and collagen undergoes extensive cross-linking (41). Furthermore, smooth muscle cells display developmental changes in phenotype that may influence their mechanical properties, e.g., through alterations in extent and organization of the cellular contractile apparatus (12, 17).
A particularly important phase of arterial remodeling occurs during the perinatal period. During this time, there are large changes in cardiovascular function, including closure of the foramen ovale and ductus arteriosus, loss of the placenta, redistribution of systemic blood flows, and substantial changes in central arterial pressure and cardiac output (20, 46), and large changes in arterial dimensions and wall constituents accompany these changes in function (7, 8, 23). Consequently, we initiated a series of studies on the ovine thoracic aorta during perinatal development and postnatal maturation. Sheep were chosen because of their suitable size and because perinatal cardiovascular function has been extensively studied in this species (1, 22, 35, 36, 46). In a previous study we observed dramatic changes in aortic mechanical properties that were specific to particular developmental intervals (42). Thus incremental elastic modulus (stiffness) of the aortic wall at low tensile stress (Elow) increased by 89% during perinatal development from the fetus to the lamb but was unchanged during postnatal maturation from the lamb to the adult. In contrast, incremental elastic modulus at high stress (Ehigh) was unchanged during perinatal development but increased by 88% during postnatal development. Aortic wall viscosity progressively decreased with age from fetal to adult life. A subsequent study showed that aortic collagen cross-linking changed little in the perinatal period but increased dramatically during postnatal life (41).
These age-specific changes in aortic properties provide an important opportunity to relate developmental changes in wall mechanics to changes in wall constituents. The objectives of this study were 1) to measure the developmental changes in the biochemical composition of the ovine thoracic aorta from fetal to adult life and 2) to determine the relationship between these compositional changes and changes in collagen cross-linking (41) to the developmental changes in the mechanical properties of this vessel (42). By integrating the findings from our present and our previous studies, we have been able to relate changes in wall constituents to major features of wall mechanics. As predicted from studies of adult arterial systems, changes in arterial viscosity closely followed changes in relative smooth muscle cell content (as measured by DNA content per mg wet wt), and changes in incremental elastic modulus (stiffness) at low tensile stress paralleled changes in relative elastin content. In contrast to findings with mature arterial tissues, developmental changes in incremental modulus at high tensile stress did not correlate with relative collagen contents, which changed little during development; instead, they closely followed the extent of collagen cross-linking.
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EXPERIMENTAL PROCEDURES |
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TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Aortic biochemical composition. All animal procedures were approved by the Animal Care Committee of Mount Sinai Hospital and were conducted in accordance with guidelines approved by the Canadian Council of Animal Care.
Aortic tissue was collected from 119-day-gestation fetuses (full term
145 days), lambs at 21 days of age, and nonpregnant adult ewes.
Animals were heparinized (1 ml; 10,000 USP U/ml) and killed with an
overdose of anesthetic (pentobarbital sodium, Euthanyl, MTC
Pharmaceuticals, Cambridge, ON, Canada). Two aortic segments (each ~2
cm long) were obtained per animal for biochemical assessment of
relative collagen, elastin, and DNA (smooth muscle cell) content. Throughout this study, "relative" contents refer to contents per milligram of wet weight of tissue. One segment was excised from the
proximal descending thoracic aorta just below the aortic arch, and one
segment was taken from the distal descending thoracic aorta just
proximal to the diaphragm. Rectangular strips of tissue were cut from
the segments and were dipped into saline solution, removed, and spread
onto a clean surface. Both surfaces of the samples were lightly dabbed
twice with gauze, and the samples were rapidly placed into tared
plastic vials to obtain the wet weights. Samples were then lyophilized
for 48 h (to produce a constant dehydrated, dry weight) and reweighed
to determine the dry weights. Aortic wall water content was determined
from the wet and dry weights of the tissue.
Tissue samples were digested with cyanogen bromide (CNBr), a reagent
that cleaves proteins at methionine residues. Elastin lacks methionine
and is thus resistant to CNBr digestion, whereas collagen and other
methionine-containing proteins are solubilized. Samples were weighed
wet and, after lyophilization, were placed into 50-ml glass test tubes.
CNBr was directly measured into a tube previously flushed with
N2. An appropriate amount of 70% formic acid was added to make a 50 mg/ml CNBr solution. The tubes containing the tissue samples were flushed with
N2 for ~2 min, and the
CNBr-formic acid solution was added (~10 ml solution/g tissue). The
tubes were quickly flushed with
N2, capped, and lightly agitated
for 4 days in a fume hood. Digestion was terminated by addition of 30 ml of water. The tubes were left uncapped in a fume hood for 48 h.
The insoluble residue was removed from the CNBr extract, lyophilized,
and reconstituted in 6 N HCl at 110°C for 24 h. To determine the
elastin content, a ninhydrin assay (39) was performed on the hydrolyzed
residue after it was dried and redissolved in distilled water. Amino
acid analyses performed by the Hospital for Sick Children Biotechnology
Service Centre (Banting Institute, Toronto, ON, Canada) confirmed that
the amino acid content of the residue matched that of pure elastin. To
obtain the collagen content, the CNBr extract was frozen, lyophilized,
and hydrolyzed in 6 N HCl at 110°C for 24 h. The hydrolysate was
assayed for hydroxyproline by use of a colorimetric assay (43). The
collagen content was calculated from the hydroxyproline content with
the assumption that collagen contains 12.77% 4-hydroxyproline by weight.
DNA content was used as a measure of aortic smooth muscle cell number,
since vascular smooth muscle cells are the predominant cell type in
large arteries, and most of these cells in the large arteries of
healthy animals are diploid (31). DNA content was measured using a
fluorometric assay (21) on homogenized tissue extracts. This technique
utilizes the enhancement by DNA of the fluorescence of the dye
bisbenzimidazole (Hoescht-33258).
Biochemical results for each animal were expressed per milligram of wet
weight and were taken as a mean of values obtained from one sample from
the proximal and one from the distal aorta.
Aortic collagen cross-linking. Aortic collagen cross-linking and aortic mechanical properties were presented in our previous studies (41, 42). Primary features of these analyses are included here, since they are important to the comparisons that we make with biochemical composition.
Ovine aortic collagen cross-linking was assessed using hydrothermal isometric tension (HIT) tests in the age groups described above (41). In these tests, tissue samples are held under isometric tension in a bath of distilled water at 90°C. Under these conditions the isometric tension is largely supported by the denatured collagen network within the sample. The load decays because of hydrolysis of peptide bonds along the polymeric network of denatured collagen with slippage of chain fragments. The rate of relaxation can be related to the concentration of thermally stable collagen cross-links: if more cross-linking is present, the slippage of adjacent chain fragments will be inhibited, and the observed load relaxation will be slower. The load relaxation half-time (HIT t1/2) thus provides an index of collagen cross-linking. An index of total collagen cross-linking was obtained as the HIT t1/2 after immature cross-links were stabilized (reduced) to a heat-stable form with NaBH4 (2, 24-26, 30).Aortic mechanical properties.
Using in vivo and in vitro techniques, we characterized aortic
mechanical properties of the ovine aorta in the age groups described
above. These techniques have been described in detail previously (42).
Briefly, the true wave propagation coefficient (
) was used to
characterize aortic wall properties through in vivo studies. defines the propagation of a pressure wave in terms of a wave velocity
(c), which is largely determined by
aortic elasticity, and a wave attenuation coefficient
(a), which is determined largely by
aortic wall viscosity. Thus, in the absence of wave reflections from
downstream sites
|
(1) |
is the angular frequency
(s
1),
a is the wave attenuation coefficient
(cm1), and
c is the velocity (cm/s) of wave
propagation. In our studies, for each harmonic of the pressure wave
was determined using the three-pressure method of Gessner and Bergel
(18, 29), a technique that mathematically removes the effects of wave
reflections. Accordingly
|
(2) |
x is the pressure
sensor separation.
In vitro experiments were performed in a whole vessel mechanical
testing apparatus. The vessels were held at their in vivo longitudinal
strain and internally pressurized with static and pulsatile pressures
while intraluminal pressure was measured using a pressure transducer.
External vessel diameter was measured using a video dimension analyzer
(for static diameters) or sonomicrometry (for pulsatile diameters). The
complex viscoelastic modulus and phase angle (
) were determined from
simultaneous recordings of dynamic intraluminal pressure and vessel
diameter obtained at the same location. is the phase shift between
pulsatile pressure and diameter and provides a direct indicator of
arterial wall viscosity.
Aortic circumferential stress-strain relationships were derived from
incremental pressure-diameter measurements. Circumferential wall stress
(
circ) was computed using the
equation for a thick-walled vessel (28, 29)
|
(3) |
h, where
h is the wall thickness computed at
each pressure level.
Circumferential strain (
circ)
was calculated from the external diameter (D10)
at 10 mmHg, the lowest pressure at which the vessel was not collapsed)
and from the measured change in external diameter
(De D10)
|
(4) |
circ-circ
curve (Fig. 1).
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Statistics. For all compositional and mechanical parameters, statistical comparisons between age groups were made using a one-way ANOVA followed by a Student-Newman-Keuls test for multiple comparisons (SigmaStat 1.0, Jandel). A significant difference was concluded when P < 0.05. Values are means ± SE; n is the number of animals. Correlations were not performed between compositional and mechanical parameters, because paired data were not available.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Relative elastin content increased by 69% between fetal and postnatal
life, then showed no significant change in later development (Fig.
2B).
This pattern very closely followed that displayed by Elow, which increased by 89%
perinatally and then showed no further change (Fig.
2A) and was very distinct from
developmental changes in collagen cross-linking and collagen and DNA
contents (Figs. 3 and
4).
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Despite the close relationship between relative collagen content and Ehigh in adult arteries (33), developmental changes in these two parameters were poorly correlated in our study. Relative collagen content increased gradually and by only 20% from fetal to adult life (Fig. 3C). In contrast, Ehigh did not change perinatally but increased dramatically (by 88%) during postnatal life (Fig. 3A). These developmental changes in Ehigh closely resembled those observed for the index of collagen cross-linking, which also did not change perinatally but increased by 82% during postnatal life (Fig. 3B). This pattern was not observed for any other structural component.
A progressive and substantial developmental decrease in relative aortic
DNA content, a measure of vessel cellularity (31), was observed.
Relative DNA content fell by 26% between fetus and lamb and a further
32% between lamb and adult (Fig.
4C). Similar decreases were observed
for both measures of arterial viscosity: a decreased by 46% from fetus to lamb
and a further 43% from lamb to adult sheep (Fig.
4A), and decreased by 12 and
25% over these corresponding phases of development (Fig.
4B). No structural component apart
from relative DNA content declined substantially during development.
Aortic wall water content fell only 6% during perinatal development,
with no change postnatally. (Water content for the fetal, lamb, and
adult aorta was 83.0 ± 0.6, 78.2 ± 0.14, and 77.8 ± 0.6%,
respectively.)
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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This study is the first to demonstrate the temporal association between changes in elastic and viscous mechanical properties and changes in structural components of the thoracic aorta during perinatal development and postnatal maturation. We present strong evidence that the conventional concept that relative elastin content determines arterial wall properties at low strain applies during development from fetal to adult life. Likewise, our data indicate that changes in wall viscosity may be attributable to changes in vessel cellularity, as indicated by relative DNA content. Interestingly, changes in aortic relative collagen content did not explain changes in Ehigh. Instead, changes in collagen cross-linking were associated with Ehigh. It was also noteworthy that changes in aortic structural components and mechanical properties occurred over different developmental intervals. Increased Elow and rapid accumulation of aortic elastin occurred perinatally, increased Ehigh and increased intermolecular collagen cross-linking occurred primarily after birth, and decreased viscosity and cellularity occurred during both intervals.
Each of the main arterial wall components (elastin, collagen, and smooth muscle cells) contributes uniquely to the overall mechanical properties of the tissue. The contribution of elastin and collagen to arterial elastic properties was elucidated in a classic and widely cited study by Roach and Burton (33). They compared arterial elastic properties (tension-circumference measurements) before and after differential digestion of collagen or elastin. They found that the initial slope of the curve was determined by elastin, whereas the final, higher slope of the curve was determined by collagen, which has a modulus ~2,000 times that of elastin (16). The transfer of stress from elastin to collagen with increasing strain (stress) has been attributed to the progressive engagement of collagen fibers that are crimped at low strains (3, 33, 44). Thus low-modulus elastin dominates arterial wall mechanics at low stress, whereas high-modulus collagen dominates at high stress. Although arterial elastic properties are determined by elastin and collagen, arterial wall viscosity is thought to be mainly a result of the presence of smooth muscle cells. This hypothesis has been supported by observations that arterial wall viscosity is correlated with smooth muscle cell content in vessels from different anatomic locations (5, 10) and with smooth muscle cell activation (3, 5, 11, 47). The viscous elements in the cellular structure of the smooth muscle cells have not been defined. Observations that arterial wall viscosity increases with smooth muscle cell activation (3, 5, 11, 47) suggest that the cellular contractile apparatus may behave as a viscous element. In addition, rheological studies of other cell types (37, 38) raise the possibility that the smooth muscle cell cytoplasm itself is highly viscoelastic.
The perinatal increase in Elow was likely caused by the rapid perinatal accumulation of aortic elastin. In our study we have demonstrated a strong relationship with development between Elow and the relative content of elastin during the perinatal period. This finding is consistent with previous observations of rapid accumulations of aortic elastin during the interval surrounding birth in rats (17), rabbits (27), sheep (8), and humans (9). This observation suggests that developmental increases in the proportion of aortic elastin increase its contribution to aortic mechanical properties, thus increasing wall stiffness at low stress levels.
The rapid perinatal accumulation of elastin in the aortic wall likely adapts this tissue to the large change in hemodynamic conditions it experiences after birth. For instance, total stroke volume increases by more than twofold between 1 and 5 wk postpartum in lambs (46). An increased stroke volume after birth would place an increased load on the thoracic aorta, especially in the proximal region, since this vessel acts as a buffering chamber or "windkessel," storing part of the ventricular stroke volume during systole (6). During diastole, elastic recoil of the aortic wall propels this volume to the periphery, thereby creating continuous peripheral blood flow. Windkessel function of the aorta relies heavily on the low stiffness and reversible extensibility of the vessel; thus a rapid perinatal increase in elastin may modulate the windkessel function of the aorta to accommodate the dramatic postpartum increase in stroke volume.
Although aortic Elow and elastin changed most during perinatal development, aortic Ehigh and collagen were altered during postnatal development. Because of the progressive engagement of stiff collagen fibers with increasing stress, the high-stress behavior of the arterial wall is dominated by the collagen meshwork (3, 33, 44). Our study suggests that the postnatal increase in aortic Ehigh is likely caused by the postnatal increase in intermolecular collagen cross-linking. The cross-linking index that we employed accounts for collagen cross-links in mature (nonreducible) and immature (reducible) forms, since both contribute to mechanical properties of collagenous tissues (13). Our observations are in agreement with previous studies that report age-related increases in collagen cross-linking in skin of several species (4, 14, 25, 34) and in ovine pericardium (30). The relationship we observed between collagen cross-linking index and Ehigh is consistent with previous studies that show correlations between collagen cross-linking and "ultimate" mechanical parameters (i.e., values at high stresses or strains) in other collagenous tissues (bone, tendon, skin) (15, 40). It is interesting to note that the relative content of collagen was only slightly increased with age, with no significant change during postnatal development. The latter observation has also been reported for the human aorta (9). Our observation that developmental changes in Ehigh were associated with intermolecular collagen cross-linking suggests that increased cross-linking may increase the stiffness of the collagen fiber network, as previously hypothesized for other tissues (15, 40).
The postnatal increase in collagen cross-linking likely serves an important mechanical role in adapting the tissue to the increased tensile stress it experiences postpartum. The primary role of collagen in connective tissues is to provide structural integrity under applied tensile stress. Collagen is suited to carry out this role because of the extraordinary tensile strength and stiffness of its fibrils, properties that are largely a result of strong axial and lateral bonding afforded by intermolecular and intramolecular cross-links. Intermolecular cross-links are particularly important as stabilizers of the fibrils, since they prevent slippage of adjacent molecules under applied tensile stress (19). By thus preventing plastic strain under applied stress, intermolecular cross-links greatly contribute to the yield stress and ultimate tensile stress (strength) of the collagen matrix. Indeed, correlations between intermolecular cross-linking and tensile strength have been demonstrated in skin, tendon, and bone (15, 40). Thus, by increasing the strength and stiffness of aortic collagen, a postnatal increase in intermolecular collagen cross-linking may serve to resist the concomitant 143% increase in aortic physiological wall stress (42).
Our observations of a gradually decreasing aortic wall cellularity from fetal to adult life are supported by previous studies that report decreasing cellularity in human aorta from 12 wk of gestation to 3 mo postpartum (9) and in rat aorta from birth to 12 wk postpartum (17). The high cellularity of the young, developing aorta is not surprising, because concentrations of matrix proteins are low (17) and aortic smooth muscle cells are required for the rapid matrix synthesis and remodeling that occur during perinatal development (7, 8). In particular, aortic smooth muscle cells rapidly synthesize elastin (which increases 69% during the perinatal period), a protein that, once synthesized, exhibits very low turnover. Thus, with development, cellularity decreases as matrix protein (especially elastin) concentration increases.
The identical age-related changes we observed in aortic wall viscosity and relative smooth muscle cell content provide further evidence that smooth muscle cells are the main contributor to artery wall viscosity (3, 5, 10, 11, 47). Previous studies have provided two lines of evidence to support this hypothesis. First, smooth muscle cell content and wall viscosity in vessels from different anatomic locations are strongly correlated, e.g., muscular arteries have higher wall viscosities than elastic arteries (5, 10). Second, wall viscosity is increased with smooth muscle cell activation in a given vessel (3, 5, 11, 47). Our study has now shown a very strong temporal relationship between wall viscosity and relative smooth muscle cell content in the same vessel, an observation that provides compelling evidence that these cells are the primary source of arterial wall viscosity. Aortic wall water content decreased only 6% during the perinatal period and was unchanged during postnatal development. This observation is not surprising given that most tissues dehydrate to some extent after birth. Our observations confirm that developmental decreases in aortic wall viscosity are related to decreases in tissue cellularity, not hydration.
The mechanical properties of a composite tissue are determined by 1) the mechanical properties of its individual components, 2) their relative proportions (volume fractions), 3) their structural geometry and orientation, and 4) the coupling between them. As a first approximation to characterize the mechanics of this composite material, this study has described the changes in the relative proportions of the wall components and assessed the coupling between collagen fibers. We have not, however, assessed the developmental changes in the structural geometry and orientation of these components, which may also contribute to the age-related changes in the aortic mechanical properties. These changes may involve alterations in 1) the size and/or number of fenestrae in elastic lamellae, 2) collagen fibril diameter and/or crimp, and 3) the degree of coupling between these components. Furthermore, the intrinsic mechanical properties of the wall constituents, as well as their relative contents, may also change during development and maturation. For instance, the mechanical properties of elastin and collagen may change with age. Furthermore, phenotypic changes in smooth muscle cells that occur during development (12, 17, 32) may influence their mechanical properties through alterations in their contractile apparatus.
In summary, we have demonstrated similar age-related trends in important mechanical features of the thoracic aorta and specific changes in aortic wall structural composition during perinatal and postnatal development. Interestingly, these changes occur over different developmental intervals. As the aorta becomes progressively less cellular from fetal to adult life, wall viscosity is concurrently reduced. This observation provides further evidence that smooth muscle cells are the principal source of viscosity in the artery wall. Rapid perinatal remodeling increases the content of elastin and its contribution to wall mechanics at physiological pressure. This likely serves to enhance the windkessel function of the aorta, thereby accommodating the postnatal increase in ventricular stroke volume. By contrast, a postnatal increase in intermolecular collagen cross-linking increases the contribution of collagen to aortic wall mechanics, stiffening and strengthening the wall and thereby resisting the large postnatal increase in wall tensile stress.
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ACKNOWLEDGEMENTS |
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This work was supported by grants to S. L. Adamson and B. L. Langille from the Heart and Stroke Foundation of Ontario and to J. M. Lee from the Natural Sciences and Engineering Research Council of Canada. S. L. Adamson and B. L. Langille are Career Investigators of the Heart and Stroke Foundation of Ontario, and S. M. Wells is an awardee of a Medical Research Council of Canada Studentship.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: S. L. Adamson, Samuel Lunenfeld Research Institute, Rm. 138-P Mount Sinai Hospital, 600 University Ave., Toronto, ON, Canada M5G 1X5 (E-mail: adamson{at}mshri.on.ca).
Received 28 December 1998; accepted in final form 21 May 1999.
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TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
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