Comparison of Medial Growth of Human Thoracic and Abdominal

Comparison of Medial Growth of Human
Thoracic and Abdominal Aortas
By Harvey Wolinsky, M.D., Ph.D.
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ABSTRACT
Recent morphologic studies of adult mammalian thoracic and abdominal
aortic segments have shown that the adult human abdominal aorta deviates
significantly from the usual pattern of medial lamellar architecture. In the
present study medial growth of these two aortic segments from prenatal life to
adulthood was compared in terms of medial architecture and calculated tangential tension levels. During prenatal life, these parameters were very similar
in the two segments. However, the postnatal increase in the medial thickness
of the thoracic segment was due mainly to the addition of lamellar units which
increased in number from 35 to 56; only a minor contribution was made by
increased thickness of each unit which changed from 0.012 to 0.017 mm. The
converse was true for the abdominal segment; the number of lamellar units
increased only from 25 to 28, but lamellar unit thickness increased strikingly
from 0.012 to 0.026 mm. Calculated wall stress was similar in the two segments
throughout growth, but tension per lamellar unit became disparate in the
segments during the first decade of life, culminating in unusually elevated values
in the adult human abdominal aortic media.
ADDITIONAL KEY WORDS
lamellar unit
fetus
• Segments of the vascular tree differ
greatly in their susceptibility to disease. For
example, the abdominal- aorta of man has a far
greater predilection for arteriosclerotic involvement than the thoracic segment (1, 2).
Alterations in medial morphology of susceptible vessels commence shortly after birth (3).
These include development of a fibromuscular
subintimal layer (3-5), progressive fraying
and fragmentation of medial elastin lamellae
(6) and an increase in stainable collagen in
the media (7, 8). From birth until old age, the
aortic media becomes progressively thicker (9,
10), and its distensibility diminishes progressively during pre- and postnatal development
(11). Studies of the fibrous protein composiFrom the Department of Medicine and the Unit for
Research in Aging, The Albert Einstein College of
Medicine, Bronx, New York 10461, and the
Department of Pathology, University of Chicago
School of Medicine, Chicago, Illinois 60637.
This work was supported in part by U. S. Public
Health Service Grants HE-12766 and HD-00674 and
by the Health Research Council of New York,
Contract U-2041.
Received March 3, 1970; accepted for publication
August 3, 1970.
Circulation Research, Vol. XXVU, October 1970
comparative anatomy
wall stress
tional changes corresponding to these morphological changes during growth and aging have
given conflicting results. Some have reported
only an increase in elastin (12), others have
shown an increase in collagen and decrease in
elastin content (13, 14); most recent studies
indicate a constant collagen content but a
slight decrease in elastin content (15-18).
These differences probably reflect acknowledged variations in methodology and sampling and the use of relative content rather
than the absolute amount of each component (19).
Recent morphologic studies of adult
mammalian thoracic and abdominal aortic
media have shown that the adult human
abdominal aorta deviates significantly from
the usual pattern of medial lamellar architecture (20). Thickness of this avascular segment
is appropriate for its diameter but is far
greater than the avascular zone or the
avascular media of any other mammalian
aorta studied. Also, this segment has a relative
deficiency of medial lamellar units, which
results in an elevated estimated value for
531
532
tension per lamellar unit compared to the
abdominal segment of other species. It was
not determined in that study how this
deviation came about or when it appeared in
this segment.
The present study compares the growth of
the human abdominal aortic media to the
thoracic aortic media from prenatal life to
adulthood in terms of medial lamellar
architecture and calculated tension levels. It
will be shown that the characteristic structural
deviation of the adult abdominal segment is
not present at birth but appears during the
first decade of postnatal life.
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Materials and Methods
A total of 59 segments was studied, 37 thoracic
and 22 abdominal. These included 19 fetal
vessels, 5 newborn aortas, 18 segments from
children and 17 from adults. The fetuses,
products of spontaneous abortions, were not
macerated, were free of obvious congenital
diseases, and were of body weight and length
appropriate for the estimated length of gestation.
Newborn infants were born alive and died within
48 hours, though usually within minutes of birth.
They were free of all obvious congenital diseases
and had the body parameters of term infants.
Children were free of chronic disease and had
died from a trauma or an acute illness. Adults
were between 20 and 50 years of age and had
been free of apparent cardiovascular disease
during life and had died from a trauma or a brief
acute illness; only aortas with little or no gross
atherosclerosis were used. All vessels were
obtained within 24 hours of death; both segments
were not obtained from every case either because
thoracic segments alone had been obtained as
part of another study (21) or because one
segment had been damaged during removal and
rendered unsuitable for distention.
The thoracic segment was defined as that
portion delimited by the left subclavian artery
and coeliac artery; the abdominal segment was
that portion between the left renal artery and the
iliac bifurcation. All segments except those of the
fetuses were distended as follows; All branches of
the segment were ligated in situ and the
adventitia was marked with a row of dots, using a
gentian violet solution. The segment was then
cannulated at both ends, excised and attached to
a special frame. After re-extension of the segment
to its in-vivo length, the proximal cannula was
connected to a closed pressure system as
previously described (21). Segments from
newborns were distended to 60 mm Hg, the
WOLINSKY
approximate mean pressure at birth (22).
Pressures used to distend segments from young
children were taken from reference tables of
normal mean values (23, 24). Vessels from older
children and adults were distended to mean
pressures obtained from their clinical records.
Fetal vessels were not distended because of the
unavailability of accurate blood pressure data.
Each segment was first flushed with normal
saline at 37°C and was distended briefly at the
appropriate mean pressure; it was then perfused
with a mixture of barium sulfate, gelatin, and
india ink in the same proportions as described in
previous studies (21). After closure of the distal
cannula, the distending pressure was adjusted to
the appropriate mean pressure; vasa vasorum
filled with the perfusion mixture. With pressure
maintained in the segment, the entire apparatus
was immersed in 10% buffered formalin at 4°C.
Gelling of the distending mixture occurred in 1 to
2 minutes, permitting removal of the segment
from the pressure system. Special holding clamps
maintained extension of the segment during
formalin fixation over the following 48 hours. The
entire procedure up to the beginning of fixation
was completed in 20 minutes.
After fixation, the luminal diameter of each
segment was measured from x-rays; details are
described elsewhere (21). Cross-sectional rings
were taken from the midpoint of each segment
and were prepared for light microscopy.
Histological sections were 7/JL thick and were
stained with hematoxylin and eosin and Weigertvan Gieson stains.
Micrometric methods for measurement of wall
thickness and lamellar composition have been
previously described (21). Fetal vessels were not
distended so that only the lamellar complement of
the media was measured in these vessels. Tissue
shrinkage amounted to 14% after fixation and an
additional 16% after dehydration and paraffin
embedding; all reported values have been
appropriately corrected.
The estimated tangential tension exerted on the
wall at the midpoint of each segment was
expressed both in terms of tension per lamellar
unit as described previously (20) and as wall
stress, using the following equation: T = P-^in
o
which T = waII stress in dyn/cm 2 at the site in
the vessel wall, P = blood pressure in dyn/cm2,
r = radius in cm, and S = wall thickness in cm
(25).
The significance of differences between means
was determined by use of Student's t-test;
significance was considered to be present at the
5% level.
Circulation Research, Vol. XXVII. October 1970
533
GROWTH OF HUMAN AORTIC MEDIA
16-
THORACIC AORTA
•
ABDOMINAL AORTA o
NEW BORN
i
•
•
•
*
o
•
o °o
1 12
*
S
<
LAMELLAR UNITS AND BODY WEIGHTS
o
•
*
8
4 -
i
A
i
12
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o
x
5
points was seen (Fig. IB); the relationship
between thicknesses of the two segments at
any age was similar to the relationship of their
respective diameters.
8
The complement of medial lamellar units
could be easily determined in undistended as
well as distended aortic segments. In Figure 2
the relationship of medial lamellar units to
body weight is shown for aortas of humans
ranging in age from early fetal life to
adulthood. During the prenatal period, the
number of lamellar units appeared to increase
at a similar rate for both segments. The
relative number of lamellar units in the two
segments at any point during this age period
corresponded to their relative diameters and
wall thicknesses as described above.
During the period of growth from birth to
adulthood, however, the rate of increase of
lamellar units for the two segments was
disparate. The lamellar units of the thoracic
aorta nearly doubled over this period of time,
whereas the number of abdominal aortic
B
looo
IQOOO
10QO0O
BODY WEIGHT (Grams)
THORACIC AORTA
ABDOMINAl AORTA
NEW BORN
FIGURE 1
•
O
t
A. Relationship of diameters of thoracic and abdominal
aortic segments to body weight during human growth
from birth to adulthood. B. Relationship of medial
thicknesses of thoracic and abdominal aortic segments
to body weight during human growth from birth to
adulthood. See text for details.
» .
i i
I 1
Results
AORTIC WALL THICKNESS AND DIAMETER
The relationships of diameter and wall
thickness to body weight of thoracic and
abdominal segments are compared in Figure
1. The diameters of both segments increased
throughout the period from birth to adulthood; in general, diameter of the abdominal
segment was 30 to 403! less than that of the
thoracic segment (Fig. 1A). Medial thicknesses of both segments also increased steadily
over the same period, though more scatter of
Circulation Research, Vol. XXVll,
October 1970
10
100
1000
BODY WEIGHT ( G w m s )
IQOOO
100.000
FIGURE 2
Relationship of number of aortic medial lamellar units
to body weight during human growth. The rates of
growth in the two segments are similar during fetal
life; over the period from birth (arrows) to adulthood,
however, accretion of units is much more rapid in the
thoracic segment than in the abdominal segment.
534
WOLINSKY
lamellar unit thickness would be expected.
This is confirmed by calculations of lamellar
unit thickness: This value is 0.012 ± 0.004 mm
(SD) and 0.012 ±0.002 mm in the newborn
thoracic and abdominal aortic segments,
respectively; in the adult it is increased to
0.017 ±0.003 mm and 0.026 ±0.001 mm for
the same segments, respectively. The difference between lamellar unit thicknesses of
newborn segments was not significant
(P>0.9); that between the adult values was
highly significant (t = 8.63, P<0.001).
4000
2
2 3000
THORACIC AORTA
•
ABDOMINAL AORTA o
NEW BORN
I
o
1
«
2000
O
1000
iffDownloaded from http://circres.ahajournals.org/ by guest on June 16, 2017
1000
10,000
BODY WEIGHT (Grom»)
MEDIAL TENSION
I
100,000
FIGURE 3
Relationship of calculated tangential tension per
lamellar unit of thoracic and abdominal aortic segments to body weight during human growth from birth
to adulthood. Over the range of body weights of 15
to 40 kg, corresponding to the ages of 4 to 10 years,
values for tension per lamellar unit become greater
in the abdominal than in the thoracic segments.
lamellar units increased much less. In the
aortic segments of a 12-g fetus, the youngest
studied, 25 to 30 lamellar units were already
present in the thoracic portion, compared to
15 to 20 units in the abdominal portion. In the
adult, this number had increased to about 56
units for the thoracic segment, but in the
abdominal segment only an average of 28
medial lamellar units was present. This latter
number is of importance for it has been shown
by us to be the maximum number of lamellar
units which are found in the avascular medias
of both segments in mammals and that when
more than 28 lamellar units are present, vasa
vasorum are present in those units located
between the inner 28 and the adventitia
(26).
It was seen in Figure IB that increases in
wall thicknesses of thoracic and abdominal
segments were generally similar during the
period of postnatal growth: Taken together
with the different rates of accretion of lamellar
units in these two segments during the same
period, a progressively greater difference in
During postnatal growth, increases in
calculated tangential tension reflected increases of both blood pressure and diameter
(23). Calculated tension per lamellar unit was
significantly elevated in the adult human
abdominal aorta compared to other avascular
aortas, thoracic or abdominal, of many adult
mammalian species (20). The development of
this unusual situation is traced in Figure 3.
Newborn human thoracic and abdominal
segments had comparable levels of tension per
lamellar unit (arrows). As growth proceeded,
• THORACIC SEGMENT
O ABDOMINAL SEGMENT
>o
2
x
a)
c
>.
to
to
I NEWBORN
*0
15
10
-
i
LU
I—
••
o •
to
*
i
1,000
10,000
100,000
BODY WEIGHT (grams)
FIGURE 4
Relationship of calculated wall stress of thoracic and
abdominal aortic segments to body weight during postnatal human growth. Values in both segments are
similar during the entire period from birth (arrows) to
adulthood.
Circulation Reiearcb. Vol. XXVII.
October 1970
535
GROWTH OF HUMAN AORTIC MEDIA
Wll
AORTIC W A U
iKUU
Ml
wn wn mums
W Nb I I I I II I
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", I I 1 1 :
2
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A
i
3Ad[
1
28
35 0.012
28
56 0.017
25
25 0.012
28
28 0.02J
i
DISTANCE FROM INTIMA (mm)
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FIGURE 5
Semidiagrammatic representation of medial growth of
human thoracic and abdominal aortic segments. Adult
wall thickness of the thoracic segment is attained
mainly by elaboration of more lamellar units whereas
final wall thickness of the abdominal segment is accomplished primarily by the thickening of existing
lamellar units. See text for details. Nb = newborn;
Ad = adult.
however, with its attendant increases in blood
pressure and diameter, the points representing
abdominal vessels separated from those
representing thoracic segments; a clearcut
difference in tension per lamellar unit was
seen by about 10 years of age (or
approximately 40 g body weight); the
transition seemed to occur between approximately 4 years and 10 years of age (or
between 15 kg and 40 kg body weight).
Unlike medial lamellar complements, wall
thicknesses of the thoracic and abdominal
segments were related to each other in a
similar manner throughout the period from
birth to adulthood. It would be expected,
therefore, that tension levels per unit wall
thickness, i.e., wall stress, would remain
similar in both segments over the same period.
This is confirmed in Figure 4, where wall
stress is related to body weight. Points
representing thoracic and abdominal segments
overlapped at all ages; the regression
coefficient between wall stress and body
weight was 0.63 (P < 0.01) and was the same
when calculated separately for abdominal
vessels or for all segments.
Circulation Research, Vol. XXVII, October 1970
Discussion
The findings of the present study are
summarized in the semidiagrammatic representation shown in Figure 5. Medial
thicknesses of thoracic and abdominal aortic
segments were increased more than twofold in
the adult compared to the newborn. In the
human thoracic segment growth is accomplished mainly by an increase in number of
lamellar units with only a relatively minor
contribution from an increase in the thickness
of individual units. The converse is true for
the abdominal segment; most of the increase
in postnatal thickness of this segment results
from prominent thickening of existing
lamellar units; very few new units are added.
Stated differently, of the net increment in wall
thickness of the thoracic aorta which occurs
after birth, two-thirds is due to more units,
one-third to increased unit thickness; corresponding figures for the increase in abdominal
segment thickness are one-fifth due to new
units, four-fifths due to thicker units. Note also
in Figure 5, that thoracic aortic segments of
newborn and adult humans have an outer
zone which contains vasa vasorum (dark
ellipses). The inner avascular zone contains 28
lamellar units, regardless of age, and is about
0.5-mm thick in the adult; both of these values
are characteristic for this zone in mammalian
aortas as established previously (26). In
contrast, the human abdominal aortic media
normally contains no vasa vasorum at any age;
the lamellar complement of 28 of this adult
vessel, while appropriate for an avascular
vessel, is at the maximum value found in
totally avascular aortas or avascular zones of
vascularized aortas. Thickening of the media
which corresponds to somatic growth and
which is associated with rising tension levels
results in an avascular abdominal segment in
the adult human which greatly exceeds the
maximum thickness of the avascular zones of
vascularized aortas of other mammals. The
implications of this discrepancy in the adult
abdominal vessel have been discussed recently
(20). A striking finding of the present study is
that this segmental difference in the nature of
medial growth of the human aorta arises in
536
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the postnatal period of growth; no difference
is morphologically detectable before birth.
One possible explanation for the different
mode of growth of the avascular abdominal
segment is that it reaches a total maximum
lamellar complement of 28 shortly after birth;
as tangential tension continues to rise, no
outer vascularized zone is present to elaborate
more units; the only alternative is to thicken
each unit. Parenthetically, this same course is
taken by the avascular rat aorta under
conditions of hypertension (19). In contrast,
the human thoracic aorta has an outer
vascularized zone at birth; the postnatal
increase in tension is attended by the
elaboration of many more lamellar units in the
outer vascularized zone, a zone which has
been shown to be capable of more structural
adaptation than avascular inner medial zones
or completely avascular vessels (unpublished
observations). In retrospect, it is apparent
from a previous study by us of vasa vasorum
in mammalian aortas that the totally avascular
aortas of the several smaller species studied
added few, if any, units during postnatal
growth but that the lamellar unit complement
of vascularized outer medial zones of larger
species increased considerably at a rate characteristic for each species (26). The presence
of an outer vascularized zone seems to confer
an adaptability not seen in avascular aortas or
avascular zones.
The findings of this study also confirm our
previous observations that no species with
fewer than 28 medial units at birth exceeded a
total of 28 units at any time thereafter (26).
Conversely, all species with more than 28
medial units, i.e., with a vascularized outer
zone in a segment as an adult, already had at
least 28 units present at birth. It is intriguing
that others have reported that when complete
elastin lamellae first appear in the fetal human
aorta (14 weeks gestation), "30 to 33 definite
concentric layers" are seen (27). The youngest
fetuses in our study were also of about this
age and similarly had approximately 25
medial lamellae in the thoracic aorta. An
explanation for this finding might be either
that the avascular inner zone forms as a unit in
WOLINSKY
those portions of the vascular tree destined to
have an outer vascularized zone, or that the
vascularized outer zone is found only in those
segments in which development of the
avascular zone is completed at an early stage
of gestation. The finding that a "limit" of 28
lamellar units is reached early in postnatal life
and that tension per unit rises inordinately
thereafter because no vascularized outer zone
develops may reflect the well-described lag in
human growth during the final 2 months of
gestation (28), or the more general finding
that all primates have a significantly slower
rate of intrauterine growth than nonprimates
(29).
Previous experimental work (30) and
autopsy studies of acardiac infants (31)
showed that two influences are operative in
cardiovascular development: (1) differentiation, which is of genetic origin; and
(2) functional adaptation, which is presumably regulated by chemical and mechanical
factors. The sharp increase in number of
medial lamellar units, wall thickness, and
vessel diameter seen during pre- and postnatal
periods can probably be attributed to several
factors acting concurrently. During these
periods of very rapid body growth, aortic
dimensions would be expected to keep pace
with increasing body mass. To this point, we
have noted that total medial lamellar units
reached adult levels in the late teens and
certainly by age 20, by which time adult body
configuration had been attained; no further
increases were seen between 20 and 50 years
of age in the adults studied.
The level of blood pressure may be an
important mechanical factor which influences
the relative degree of lamellar accretion
during pre- and postnatal growth periods. The
pictograms by Dawes and his associates of
blood pressure levels of several mammals
during intra- and extrauterine life indicate
that each species has a characteristic rate and
pattern of rise (32): Wall thickness has been
shown to correspond closely to pre- and
postnatal blood pressure levels in the
pulmonary and systemic circulations (33). It
has also been noted that thoracic aortic wall
Circulation Research, Vol. XXVII. October 1970
537
GROWTH OF HUMAN AORTIC MEDIA
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thickness of man increases steadily from birth
until death (9, 10); in middle life it is twice as
thick as at birth and in advanced age nearly
three times as thick (9). Humoral factors,
including the dramatic changes in arterial
oxygen saturation and levels of circulating
estrogens and other hormones which are
associated with birth (34) may also influence
vascular development.
Studies of humans and other mammals have
shown that the characteristically different
adult patterns of elastin and collagen
composition of thoracic and abdominal
segments are already present to some degree
at birth (16, 18). In the present study we
found that the morphologic appearance of the
two segments was very similar in the prenatal
period and that calculated tension levels per
lamellar unit were also very similar in the
newborn. It is possible that these data are not
conflicting and that fibrous protein composition reflects changes in amplitude of, rather
than mean levels of, tension in these segments
(16). However, the importance of eliminating
adventitia completely before determining the
"true" fibrous protein composition of the
media and intima has recently become
apparent (35); many chemical data obtained
without this precaution, including the above,
should therefore be accepted with reservation
until they are confirmed.
4.
of coronary arteries in newborn infants. Amer J
Path 23: 90, 1947.
5.
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Circulation Research, Vol. XXVII, October 1970
Comparison of Medial Growth of Human Thoracic and Abdominal Aortas
HARVEY WOLINSKY
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Circ Res. 1970;27:531-538
doi: 10.1161/01.RES.27.4.531
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