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Meakins-Christie Laboratories, Royal Victoria Hospital, McGill University, Montreal, Quebec, Canada H2X 2P2
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The lung extracellular matrix changes rapidly
with maturation. To further our understanding of the mechanisms
underlying lung tissue mechanics, we studied age-related changes in
mechanical properties in lung parenchymal strips from baby (10-15
days old), young (~3 wk old), and adult (~8 wk old) rats.
Subpleural strips were cut and suspended in a fluid-filled organ bath.
One end of the strip was attached to a force transducer and the other
to a servo-controlled lever arm. Measurements of force (F) and length (L) were recorded during sinusoidal
oscillations of various amplitudes and frequencies. Resistance modulus
(R) and elastance modulus (E) were estimated by fitting the equation of
motion to changes in stress (T) and stretch ratio (
). Hysteresivity
(
) was calculated as follows: = (R/E)2
f, where
f is frequency. Slow-cycling T- curves were measured by applying a constant slow length change. Finally, quasi-static T- curves were measured as stress was
increased from 0 to 6 kPa and back to 0 kPa in stepwise increments. Our results showed that lung tissue from immature rats was stiffer and less
hysteretic than tissue from more mature animals. In addition, tissue
from baby animals behaved in a manner compatible with an increased
vulnerability to plastic change.
tissue resistance; tissue elastance; stress relaxation; hysteresivity
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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IT HAS BEEN REPORTED that dynamic elastance and tissue resistance of the lungs decrease with age in humans and animals (6, 24). Dreshaj et al. (6) reported in piglets that tissue resistance, dynamic elastance, and the response to contractile stimulation change with maturation. Nardell and Brody (22) studied saline-filled excised lungs from rats aged 4 to 40 days and found that static lung compliance measured over the linear portion of the pressure-volume curve increased with age. They also studied lung volume-corrected compliance, which decreased from day 4 to day 20 and increased thereafter.
The lung parenchymal tissues play a key role in determining the resistive or viscoelastic behavior of the overall lung. This has been demonstrated under normal conditions and after induced constriction (6, 19). Parenchymal connective tissues (the collagen-elastin-proteoglycan matrix), the surface film, and contractile elements are responsible for this behavior (9).
The extracellular matrix alters rapidly during the postnatal stage. The amount of collagen and elastic fibers increases markedly during the first several weeks of life (22). The process of alveolarization occurs, which is characterized by an increase in the number and size of the alveolar walls and a decrease in alveolar thickness (5). In addition, the "ground substance" of the extracellular matrix, i.e., proteoglycans and glycoproteins, changes. For example, the concentration of hyaluronic acid and the amount of chondroitin sulfate proteoglycans have been shown to be substantially higher in neonatal rats than in more mature animals (16, 27). Hence, the maturing lung represents a naturally occurring model of altered extracellular matrix and a singular opportunity to study how changes in the extracellular matrix affect lung tissue mechanics.
In the present study we examined the viscoelastic behavior of isolated parenchymal strips from rat lungs of different ages. In this system, tissue resistance and hysteresis are most likely due to contact phenomena between stress-bearing elements and their surrounding matrix (20, 21, 29), inasmuch as the effects of the surface film, airway closure, and heterogeneous airway constriction (32) are excluded. In addition, we could characterize the specific material properties of the parenchyma without considering lung size per se. The pressure-volume curve of the lung and the length-tension curve of the parenchymal tissue are known to be highly nonlinear, and compliance increases proportionally to lung volume (14, 20, 23). Therefore, meaningful comparison of mechanical properties of lungs of different sizes or ages under a given condition, i.e., at the same pressure or at the same volume, becomes difficult. Measurements in isolated parenchymal strips allowed us to minimize this problem.
Specifically, we examined maturational differences in oscillatory
behavior of isolated strips and their dependence on oscillatory frequency and amplitude of length change. Oscillatory measurements were
performed at the same mean operating stress
(Tm). Because elastance and
resistance of soft tissues increase with stretch (18, 20, 23), we
reasoned that the length-tension relationship at a wide range of length
change would need to be characterized to compare groups with different
mechanical behavior. Therefore, we also measured slow-cycling and
quasi-static tension (T)-to-stretch ratio () curves. Finally, we
measured changes in tension during stress relaxation and the tendency
of the tissue to rupture during stretch.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Parenchymal strip preparation.
Three groups of Sprague-Dawley rats were obtained from Charles River
(St. Constant, PQ, Canada): adult (~8 wk old) male, young (~3 wk
old) male, and baby (10-15 days old) male and female rats. Three
separate groups of strips from different groups of rats were used for
each experiment (Table 1). Each animal was
anesthetized with pentobarbitone sodium (30 mg/kg ip). The thorax
was opened, and the animals were exsanguinated by severing
the inferior vena cava. The heart, lungs, and trachea were carefully
resected en bloc and rinsed in a modified Krebs solution [in mM:
118 NaCl, 4.5 KCl, 1.2 KH2PO4,
25.5 NaHCO3, 2.5 CaCl2, 1.2 MgSO4, and 10.0 D-(+)-glucose (Sigma Chemical,
St. Louis, MO)] with pH 7.4. Lung parenchymal strips were cut
from the subpleural edge of the lung, and the pleura was removed. The
resting (unloaded) length
(Lr) and wet
weight of each strip were measured.
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Experimental apparatus. Metal clips were glued to either end of the tissue strip with cyanoacrylate. Steel music wires (0.5 mm diameter) were attached to the clips, and the strip was suspended vertically in an organ bath filled with Krebs solution that was maintained at 37°C and continuously bubbled with 95% O2-5% CO2. A mercury bead was placed in the bottom of the organ bath, allowing the wire to pass through the bath but preventing the Krebs solution from leaking out. One end of the strip was attached to a force transducer (model 400A, Cambridge Technologies, Watertown, MA) that had an operating range of ±10 g, resolution of 200 µg, and compliance of 1 µm/g, and the other end was attached to a servo-controlled lever system (model 300B, Cambridge Technologies). The lever arm was capable of peak-to-peak length excursions of 8 mm and a length resolution of 1 µm. The lever system was connected to a function generator (model 3030, BK Precision, Chicago, IL), which controlled the frequency, amplitude, and waveform of the oscillation. The resting tension was set by means of a thumbscrew system that effected changes in the vertical displacement of the force transducer. Length and force output signals were digitized with an analog-to-digital converter (model DT2801-A, Data Translation, Marlborough, MA) and recorded on an AT-compatible computer with use of LABDAT data acquisition software (RHT-InfoDat, Montreal, PQ, Canada).
The linearity and hysteresis of the system were tested by measuring the stiffness of a steel spring of stiffness comparable to that of the tissue strip. The spring was suspended in the bath by music wire in the same manner as the strip. The frequency and amplitude dependence of the system were assessed over a range of frequencies (0.1-10 Hz). The spring stiffness did not show any dependence on oscillation frequency below 10 Hz. The hysteresivity () of the system was independent of
frequency and had a value of <0.01.
Measurement of oscillatory mechanics.
Parenchymal strips were preconditioned by slowly cycling the tissue
from zero stress to a maximum of 6 kPa Lagrangian stress over a cycling
period of 10 s. Lagrangian tensile stress (T) was calculated from the
following formula
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(1) |
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(2) |
is mass density of the tissue taken as 1.06 g/cm3; () was defined as
L/Lr,
where L is the operating length. After three cycles of preconditioning were performed, tension was adjusted to
a value ~10-20% larger than 3 kPa, and stress relaxation was allowed to occur for 45 min.
After stress adaptation, T was adjusted again to 3 kPa and left to
stabilize for 6 min, during which time we considered that a plateau
tension had been reached. Sinusoidal length oscillations with an
amplitude (
) of 1%
Lr at different
frequencies (0.3, 1, 3, and 10 Hz) were applied. Thirty-second
recordings of force and length were collected at each frequency. The
frequency was varied in random order. The oscillatory amplitude was
changed to 3% and then 10%
Lr, and
recordings at each frequency were repeated. During these measurements,
mean length was not changed.
Elastance modulus (E) and resistance modulus (R) were estimated by
fitting the equation of motion
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(3) |
,
a dimensionless variable coupling the dissipative and elastic behaviors
(9), was calculated with the following equation
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(4) |
Measurement of slow-cycling T- curve, stress
relaxation, and failure curve.
Four to five cycles of 0.02-Hz constant-rate length perturbations were
applied to each strip as preconditioning.
After the strip was held at
Lr for 6 min,
tension was adjusted to a value slightly larger than 3 kPa. During the
subsequent 45-min stress relaxation, force was recorded. We fit the
following two equations to the recorded data
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(5) |
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(6) |
1 and
2 are time constants.
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loops for a given strip were almost identical, with the exception of the first loop. The last unloading limbs were
used for analysis. We calculated elastance modulus (dT/d) as a
function of T. We also calculated at a stress of 3 kPa (Fig. 1).
Finally, each strip was stretched from
Lr at a rate of
~2%
Lr/s
until the strip ruptured or reached ~2.6 (failure test). From
this measurement, we constructed T- curves and defined the yielding
point as the maximum stress before an abrupt decrease in stress with
further stretch.
Measurement of quasi-static T- curve.
Parenchymal strips were preconditioned, and 45-min stress adaptation
was allowed to occur as described above. Quasi-static T- curves were
measured as stress was increased from 0 to 6 kPa and back to 0 kPa in
stepwise increments of ~0.8 mm. At each step, tension was allowed to
decay for 3 min, at which point and T were measured. From the
quasi-static T- loop, we calculated quasi-static dT/d at stresses
of 1.5, 3, and 4.5 kPa on the unloading limb. We also calculated the
hysteresis ratio (HR) as follows
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(7) |
loop and × T is the area bordered by the
change in and the change in T (22). HR was first described as the
shape factor K by Bachofen and
Hildebrandt (1).
Data analysis.
To linearize and normalize the data, we transformed values of R, E, and
into their common logarithms. Three-way ANOVA (amplitude, frequency, and age) was performed for the three oscillatory variables. Age-frequency interactions were not significant; age-amplitude interactions were significant. Therefore, we proceeded to do a series
of two-way ANOVAs (frequency and age) at each amplitude, then we
performed Bonferroni tests for multiple comparisons. To test
differences in frequency dependence of the variables, a two-way ANOVA
(frequency and strip) and a test of linearity for each age group and
amplitude were performed. Inasmuch as linear relations between log(R)
or log(E) and log(frequency) were highly significant, linear regression
analysis was done to determine whether there were age-related
differences in frequency dependence. In other experimental data,
one-way ANOVA was used to compare the three age groups, and the
Bonferroni test was performed for multiple comparisons. In instances
where data were collected in only two groups, i.e., measurements of
stress relaxation and slow-cycling T- curves, Student's
t-test was used for comparison. Means
were considered significantly different at a probability level of 5% (P < 0.05). Values are means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Oscillatory mechanics.
Dynamic properties (R, E, and ) are shown in Figs.
2, 3, and
4, respectively. R and E of parenchymal
strips decreased with maturation (except at = 10%, at which
point R and E in baby strips were not significantly different from
those in young animals but were significantly different from those in
adults). Conversely, the values of in adult strips were larger than
those in the two other groups. Table 2
shows the results of the statistical analysis. In all cases, R and E
were significantly larger in baby than in adult strips. Values of R and
E in strips from young animals were intermediate between those in
strips from adult and baby animals. At = 1 and 3%, values of
were significantly larger in adult strips than in strips from the
immature animals; at = 10%, values of were significantly
smaller in young animals than in the other two groups.
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at different amplitudes was
observed for all groups. Linear relations between log(R), log(), or
log(E) and log(frequency) were highly significant (data not shown).
There were no significant differences in the slope of the regression
line between log(R) and log(frequency) among the three age groups. For
the relationship between log(E) and log(frequency), only the slope of
the regression line in strips from young animals at = 1% was
statistically different from the others.
Amplitude dependence of R, E, and at the different frequencies was
also observed (data not shown). There were, however, significant
differences in the age-amplitude interaction between strips from baby
animals and strips from the other two groups: in R between strips from
young and baby animals, in E between strips from adult or young and
baby animals, and in between strips from adult and baby animals.
This difference may relate to changes in
Tm during the experimental
protocol (Fig. 5). Although there was some
decline in Tm within all groups as
amplitude of oscillation was increased from 1 to 3 to 10%, the
decrease in Tm was significantly
greater in baby strips than in strips from the other two groups.
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Slow-cycling T- curve, stress relaxation, and
failure test.
The unloading limb of the T- curve is shown in Fig.
6. At > 1.5, values of stress were
larger in babies than in adults. At < 1.5, T was similar in the
two groups. E as a function of T is shown in Fig.
7. E increased almost linearly with T. Table 3 shows values of and E at a
stress of 3 kPa on the unloading limb before
(1) and after
(2) stress adaptation.
1 and
2 were lower in baby than in
adult strips; conversely, E1 and
E2 were lower in adult than in
baby strips.
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and T at the yielding
point in the failure test. Both were significantly lower in baby than
in adult strips. All four baby strips showed yielding at < 2.11. Only two of five adult strips demonstrated yielding
behavior at the highest imposed.
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Quasi-static T- curve.
Quasi-static E at various stresses calculated from the unloading limb
of the curve is shown in Fig. 9.
Quasi-static E was significantly higher in baby strips than in strips
from young and adult animals at T = 1.5 and 3 kPa. Quasi-static E at T = 4.5 kPa was not different among the three groups. The HR of the quasi-static T- loop was significantly higher in baby strips than in
young or adult strips (0.33 ± 0.04, 0.17 ± 0.02, and 0.13 ± 0.02, in baby, young, and adult strips, respectively,
P < 0.001).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The major findings of this experiment include the following. The lung
parenchymal strip of immature rats was stiffer than that of more mature
animals as a function of and T. Dynamic and static elastance and
resistance were higher in immature rat strips than in strips from more
mature rats. In addition, plastic change or tissue nonlinearities were
greatest in parenchymal strips from immature rats. Conversely, ,
which reflects the ratio of energy dissipated to that conserved (9),
was less in parenchymal strips from baby rats.
Before discussing the results, we should consider some potential
problems in the experimental approach. First, we think it is important
to consider the appropriate strain or stress to apply to the tissues.
In previously published reports in which oscillatory mechanics of
parenchymal strips were measured, Fredberg et al. (8) applied a
Tm of 1.1 and 2 kPa, Ludwig and
Dallaire (18) used 2.2 and 3.7 kPa, and Mijailovich et al. (20) chose
0.7 and 2.2 kPa. The actual T to which the tissue is exposed during physiological tidal breathing may be somewhat less. Resting lung volume, when transpulmonary pressure equals zero, is thought to be
~15% of total lung capacity (TLC) (2). Functional residual capacity
and tidal volume are roughly calculated as 0.41 and 0.14 TLC,
respectively, for a 250-g adult rat and 0.35 and 0.15 TLC, respectively, for a 27-g baby rat (17). If we assume that parenchymal strip scales as the cube root of lung volume ratio, then normal tidal lung deflation to functional residual capacity would correspond roughly to of 1.54 to 1.40 for the adult rat and 1.49 to 1.32 for
the baby rat, and TLC would correspond roughly to of 1.88. Therefore, according to our data, the physiological range of tidal volume should correspond to T < 1 kPa, at least in adult rats (Fig.
6). It is possible that the ratio of resting volume to TLC is somewhat
higher in baby rats than in adult rats, such that the corresponding
to tidal breathing may be less in baby rats than in adult rats. Because
the T- curve of the parenchymal tissue is nearly flat when the
stress is small, resting is difficult to determine and to measure.
Therefore, we chose to use a fixed T, rather than a fixed , around
which to perform oscillations. As stated above, this
Tm may be higher than under
physiological tidal breathing. However, applying a lower stress was
technically very difficult in our experimental setup, especially with
strips as small as those obtained from baby rats.
Although the conditions during oscillation measurements may not have reflected those during tidal breathing, they give important information regarding dynamic properties of the tissues, as well as their dependence on frequency and amplitude. Moreover, with this approach, it is not necessary to take into account effects of lung size, differences in breathing regimens related to age differences, or the effects of surface tension and atelectasis (32). All these variables need to be considered in an in vivo experiment when age-related differences are evaluated. Airway closure, for example, has been shown to occur more readily in newborn animals, and this may result in increased values of lung resistance and elastance (30). Therefore, it is difficult to be certain from intact lung experiments that differences in tissue properties are related to true differences in parenchymal structure.
It is possible that differences in strip size could affect the
mechanical data. Although
Lr of baby strips
was significantly smaller than that of adult strips (Table 1),
A0 was not
different. In those strips used for oscillation experiments,
A0 of young strips was smaller than that of adult strips. Nonetheless, the data
from young strips seem to be consistent, inasmuch as the values of R,
E, and were intermediate in value between those in adult and baby strips.
Whether the strips of different age groups were taken from an
equivalent part of the lung is also an important question. Because the
immature lung is much smaller than the mature lung, immature strips
might sample a more proximal portion of the lung. Salerno et al. (26)
reported that, under baseline conditions, oscillatory mechanics of
parenchymal strips were not dependent on anatomic makeup. According to
their data, volume fractions of blood vessel wall and bronchial wall in
strips obtained from a more proximal location were significantly higher
than those in strips obtained directly from the subpleural location.
However, no correlation was found between the baseline values of the
oscillatory parameters, E, R, and , and the relative proportion of
these anatomic constituents.
The results of this study clearly show that immature rat lung tissue
was stiffer than more mature tissue, whether stiffness was assessed
during tissue oscillation at a wide range of frequencies and
amplitudes, during slow cycling at various T and , or during quasi-static unloading at T 
3 kPa. Tissue R was also shown to be
larger in immature rat tissue than in tissue from more mature animals.
Finally, was less in strips from immature animals than in strips
from more mature animals. Previous investigators have examined
maturational changes in tissue resistance and elastance in vivo and
found that they decreased with age (6, 22). Because the absolute value
of resistance and elastance decreases with lung volume and airway
closure occurs more readily in newborn animals (30), it is difficult to
be certain from in vivo experiments that differences in tissue
properties are related to true differences in parenchymal structure.
The data from the present experiment suggest that these in vivo changes
reflect actual alterations in parenchymal makeup.
We also found that R, E, and showed frequency and amplitude
dependence. These results are in agreement with previous studies in
adult lungs from different species. A number of investigators have
shown in parenchymal strips that R decreases hyperbolically with
frequency (15, 20, 23), E increases linearly with log(frequency) (15,
20), and is frequency invariant (9) or decreases modestly with
frequency (20). Amplitude dependence of R, E and has been shown in
guinea pig lung strips (32). Finally,
Tm dependence of R, E and has
also been demonstrated in several previous studies (18, 20, 23, 32).
We found no systematic difference in the frequency dependence of these
parameters in parenchymal strips from the different age groups.
However, there were differences in amplitude dependence in the baby
strips. R and E decreased with , and increased with
much more markedly in baby strips than in mature strips. One possible
explanation relates to the relatively greater fall in
Tm in baby strips, as amplitude
was increased from 1 to 3 to 10%
Lr. Amplitude
dependence could include a component of
Tm dependence. A second
explanation relates to a greater plastic change or nonlinearities in
strips from baby animals. Plastic change refers to a residual deformation in the tissue that does not reverse when the distorting force is removed (28). Measurements of the failure curve showed an
increased vulnerability to yielding in baby strips (Table 4), and
quasi-static measurements showed a higher HR in baby strips. Both of
these results are consistent with an important plastic change. This
large plastic change in baby strips may also explain the somewhat
curious observation that calculated from the HR is quite different
from that measured during oscillation. {The shape factor
K is related to as follows: = [(/4K)2 
1]
1/2
(1).} Whereas HR was measured during a quasi-static maneuver over a large range of , during the dynamic maneuver was measured over a relatively small length amplitude. The plastic change or nonlinearities would more likely contribute in an important way to the
calculated from the quasi-static curve compared with that measured
during the dynamic oscillation. Previous investigators have also shown
that the hysteresis or stress-strain behavior measured during dynamic
and quasi-static maneuvers can be markedly different (23, 25).
However, this does not explain why k
gives a different result from derived during dynamic oscillation. A
larger k means the tissue is more
viscous and should be greater. Although
k values were highest in baby tissue,
was lowest in baby tissue. One explanation may be that certain
nonlinearities in the tissue are evident during stress relaxation that
are not apparent during small length oscillations. Alternately, the
difference may lie in the fact that during stress relaxation the tissue
is moving in only one direction, as opposed to during oscillation, when the tissue is forced in two directions.
Conventionally, the Kelvin body has been used to model viscoelastic
material such as lung tissue (3). This model can account for much of
the observed mechanical behavior. Recently, Hantos et al. (10-12)
described the "constant phase model" first introduced by
Hildebrandt (13). In this model, frequency dependence of R and E are
more accurately formulated than in the Kelvin body, and the time domain
expression [p(t) = Atk,
where p(t) is pressure and
A is a constant] predicts stress relaxation nearly perfectly (4). The applicability of this model was
confirmed by our results.
The amount of collagen and elastin in the rat lung increases with maturation (22). Turino (31) reported that elastic fibers contribute as a stress-bearing element over the physiological range of the pressure-volume curve, whereas the mechanical properties of collagen become more prominent at higher lung volumes. That the collagen content is relatively small in the immature parenchymal strip has been proposed as the reason immature strips are more vulnerable to yielding (31). Inasmuch as collagen and elastin are thought to be largely responsible for the elastic behavior of the tissues, it seems counterintuitive for elastance modulus to decrease with maturation. Nonetheless, we found a significant decrease in E and quasi-static elastance with increasing age. The alveolarization process occurs throughout early postnatal life, i.e., the number, size, and thickness of alveoli change markedly (5). Hence, differences in fiber structure, orientation, or alveolar geometry, rather than the absolute amount of collagen and elastin per se, may be more important in determining tissue viscoelastic behavior. The decrease in R with maturation is also difficult to reconcile. Again, changes in the alignment or structure of matrix fibrils may be important.
The one dynamic measure that did increase with age was . is a
measure of the mechanical friction in the tissue and reflects the
energy dissipated to that conserved in the system during dynamic oscillation. Mijailovich et al. (21) postulated that energy dissipation
in the tissues is related to fiber-fiber interactions. Suki and
co-authors (29) invoked the concept of reptation, i.e., a process
whereby fibers disengage from the surrounding matrix, to explain
mechanical friction in tissues. One could speculate that is
increased in lungs of more mature animals, because the absolute number
of fibers interacting with each other increases. Alternately, the
increase in may reflect changes in the ground substance. The concentration of hyaluronic acid and the
amount of chondroitin sulfate proteoglycans have been shown to be
higher in neonatal rats than in more mature animals (16, 27).
Proteoglycans are macromolecules containing many hydrophilic
glycosaminoglycan side chains; the latter have the capacity to attract
ions into the tissue and thereby alter tissue turgor. In addition, they have been shown to coat individual collagen and elastic fibers (7, 27);
as proteoglycans and glycosaminoglycans become less plentiful with
maturation, the fiber-matrix interaction may be altered. One could
postulate that proteoglycans and glycosaminoglycans act as a
"lubricant" between adjacent fibers. As their relative amount
decreases, the energy required for fibers to move within the matrix may
be increased.
Finally, plastic changes or tissue nonlinearities were greatest in parenchymal strips from babies. Again, this may reflect changes due to "immature" collagen and elastic fibers, immature alveolar structure, or the intrinsic mechanical properties of excess proteoglycans. Further studies need to be directed at determining precisely which matrix components are altered with maturation, the time course of those changes, and how those changes modify parenchymal tissue mechanics.
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ACKNOWLEDGEMENTS |
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This study was supported by the J. T. Costello Memorial Research Fund and the Medical Research Council of Canada. R. Tanaka was supported by a research fellowship from the Montreal Chest Hospital Research Institute. M. S. Ludwig is a research scholar of the Fonds de la Recherche en Santé du Québec.
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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: M. S. Ludwig, Meakins-Christie Laboratories, 3626 St. Urbain St., Montreal, PQ, Canada H2X 2P2 (E-mail: Mara{at}meakins.lan.mcgill.ca).
Received 23 October 1998; accepted in final form 7 August 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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