Chapter 1
Histology and Comparison of Arterial Grafts
Used for Coronary Surgery
J.A.M. van Son, F.M.M. Smedts, C.-Q. Yang, G.-W. He
Expanded use of the internal mammary artery for myocardial revascularization is based on the accumulating
data of superior late patency of the internal mammary
artery compared with venous conduits [1 – 9]. The primary consideration that has led to the gradual transition
of use of the internal mammary artery as the conduit of
choice is its relative freedom from atherosclerosis with
follow-up of up to 20 years. Since during the last decade
the frequency of coronary revascularization procedures
has increased considerably in patients with diseased or
absent greater and lesser saphenous veins, alternatives
to this arterial conduit have been sought. The right gastroepiploic artery and the inferior epigastric artery have
been advocated and used selectively or when traditional
conduits are unsuitable or unavailable [10 – 24]. Although the radial artery has been used in the past as a
conduit in myocardial revascularization and has been
abandoned because of its high failure rate [25 – 28], there
has been a recent resurgence of its use [29].
During the last 8 years we have performed histologic
research on the internal mammary artery, the right
gastroepiploic artery, the inferior epigastric artery, and
the radial artery and in this chapter we will summarize
our findings.
1.1
Internal Mammary Artery
1.1.1
Anatomy
The origin of the internal mammary artery, either right
or left, is on the concavity of the subclavian artery, just
opposite to the thyrocervical trunk, which is the second
branch on the convexity of the subclavian artery (the
first branch being the vertebral artery). The internal
mammary arteries line the sternum on both sides at a
distance of approximately 1 – 2 cm from the sternal border. The internal mammary arteries are accompanied
by a pair of internal mammary veins that unite to form
a single vessel, which ascends medial to the artery and
ends in the corresponding brachycephalic vein. The internal mammary artery lies on the chondral part of the
ribs and is covered by the parietal pleura. Between the
artery and the pleura is a deep fascial plane as far as the
third costal cartilage. Below this level the transversus
thoracic muscle separates the vessel from the pleura.
With one exception, there is no major difference between the right and left internal mammary arteries.
The proximal left internal mammary artery runs very
close to the chest wall, whereas on the right side there
can be up to 1 cm of connective tissue between the
proximal internal mammary artery and the ribs. This
may be due to the different anatomy of the subclavian
arteries, the left one originating from the aorta and the
right one from the innominate artery.
After the proximal medial thymic branch, the internal mammary artery anastomoses with the intercostal
arteries beyond each rib until it reaches the sixth intercostal space, where it divides into two major branches.
The craniocaudal branch, the superior epigastric artery, enters the sheath of the rectus abdominis muscle
through the interval between the costal and sternal attachments of the diaphragm. At first the superior epigastric lies behind the rectus muscle, but then perforates and supplies the muscle and thereby generally
anastomoses with the inferior epigastric artery, which
originates from the external iliac artery. The musculophrenic artery is directed obliquely downward and
laterally, behind the cartilages of the eighth, ninth, and
tenth ribs. It perforates the diaphragm near the eighth
or ninth costal cartilage, and ends, considerably reduced in size, opposite the last intercostal space. It gives
off anterior intercostal branches to the seventh, eighth,
and ninth intercostal spaces. Some other branches of
the musculophrenic artery course to the lower part of
the pericardium, dorsally to the diaphragm, and down
to the abdominal muscles.
1.1.2
Histology
1.1.2.1
Morphologic Findings
The internal mammary artery was harvested in 11 individuals (aged 49 – 83 years; mean age, 67 years) and examined histologically at 1-cm intervals [30]. At the origin of the internal mammary artery, being a transition-
1
4
I Biological Characteristics of Arterial Grafts
al area between the elastic subclavian artery and the internal mammary artery proper, the media invariably
was elastic, containing 8 – 18 (mean, 10) elastic lamellae, including the internal and external elastic laminae
(Fig. 1.1). In 2 individuals the media of the entire internal mammary artery was elastic along its entire length,
with a number of elastic lamellae that varied from 8 to
12 (mean, 10). In the other 9 individuals an alternating
histological pattern was observed: the first 20 – 30 % of
the total length of the internal mammary artery was
elastomuscular. In this segment the smooth muscle
content in the media prevailed over a number of five to
seven (mean, six) elastic lamellae (Fig. 1.2). More
downstream in these internal mammary arteries we
observed a rather abrupt transition into an elastic pattern, which continued up to 70 – 80 % of the total length
of the internal mammary artery (Fig. 1.3). This elastic
segment was composed of 8 to 12 (mean, 9) elastic lamellae (Fig. 1.4). In all nine individuals we observed a
second elastomuscular segment with five to seven
(mean, six) elastic lamellae, analogous to the proximal
one, starting at 70 – 80 % of the total length of the internal mammary artery. In five of these nine individuals
this distal elastomuscular segment extended up to the
epigastric bifurcation, but in the remaining four it
abruptly (at 80 – 90 % of the total length of the internal
mammary artery) converted into a muscular pattern
with rare (mean, three) elastic lamellae (Fig. 1.5).
Fig. 1.1. The origin of the
internal mammary artery.
Note the multiple elastic
lamellae
Fig. 1.2. Proximal internal
mammary artery. The media
is elastomuscular. There is
mild intimal hyperplasia
1 Histology and Comparison of Arterial Grafts Used for Coronary Surgery
Fig. 1.3. Distribution of the mean number of elastic lamellae in
the media of the internal mammary artery along its downstream course
In seven individuals the elastic or elastomuscular patterns in the distal internal mammary artery continued
as an elastomuscular pattern in the proximal 1 – 2 cm of
the musculophrenic artery, with a mean number of
elastic lamellae of four; more distally the media became
muscular (Fig. 1.6). In the other four individuals with a
muscular pattern in the distal internal mammary artery, the latter continued into the musculophrenic artery. In all 11 individuals the media of the superior epigastric artery was predominantly muscular.
Fig. 1.4. Detail of elastic media at mid level of the internal mammary artery. Note
the intact internal elastic
lamina and the abundant
presence of elastic lamellae.
The intima consists of a thin
layer of endothelial cells,
which in this section, due to
fixation artifact, is not attached to the internal elastic
lamina
Quantitative Results. The mean cross-sectional luminal area of the proximal elastomuscular and elastic
segments of the internal mammary artery (both
1.9 mm2) was significantly greater than that of the distal
elastomuscular segment of the internal mammary artery (1.2 mm2) and that of the muscular segments of the
musculophrenic artery (0.9 mm2) and superior epigastric artery (0.7 mm2) (p < 0.01). The mean cross-sectional luminal area of the distal elastomuscular segment of the internal mammary artery (1.2 mm2) was
significantly greater than that of the distal purely muscular segments of the musculophrenic artery (0.9 mm2)
and superior epigastric artery (0.7 mm2) (p < 0.01),
whereas that of the latter two did not differ significantly
from that of the proximal segments of the musculophrenic and superior epigastric arteries with a muscular
media with rare elastic lamellae (1.0 mm2 and 0.8 mm2,
respectively). Although the cross-sectional luminal area of the internal mammary artery along its downstream course gradually decreased, this decrease
reached statistical significance only beyond the 90 %
segment. The small luminal diameter of the internal
mammary, musculophrenic, and superior epigastric
arteries in our study is mainly due to rigor mortis and
cross-linking contracture of the vessel wall, caused by
fixation in 4 % formaldehyde solution.
In the 30 – 70 % segment of the internal mammary
artery the number of elastic lamellae (mean, nine) did
not vary significantly at the various levels. Obviously,
in its primarily elastic segment the number of elastic lamellae was significantly greater than that in the proximal and distal elastomuscular segments of the internal
mammary artery (mean, six) (p < 0.01). The density of
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I Biological Characteristics of Arterial Grafts
Fig. 1.5. Distal internal mammary artery with a muscular
media. Note the considerable
degree of intimal hyperplasia
Fig. 1.6. Musculophrenic artery with a muscular media
containing rare elastic fibers.
There is marked intimal
hyperplasia
the elastic lamellae along the downstream course of the
internal mammary artery showed a similar pattern.
The absence of elastic lamellae in the media had a
profound effect on the degree of intimal hyperplasia:
the intima was significantly thicker in the purely muscular segment (25.6 % degree of intimal hyperplasia)
than in the elastic (16.7 %), elastomuscular (15.3 %),
and muscular (with rare elastic lamellae) (17.5 %) segments (p < 0.01). Although the degree of intimal hyperplasia varied along the downstream course of the internal mammary artery (being slightly greater in the proximal and distal elastomuscular segments than in the
elastic segments), these differences were not signifi-
cant. These data are in agreement with the fact that the
number of discontinuities in the circumferential internal elastic lamina increases from the elastic (median,
21; interquartile range, 7) to the elastomuscular (median, 4; interquartile range, 11) and muscular (median,
89; interquartile range, 12) segments [31].
In another morphometric analysis of the internal
mammary artery and other arterial conduits we measured a mean combined width of the intima and media
in the flaccid internal mammary artery of 350 ± 92 mm
(Table 1.1) [32]. In all instances the vasa vasorum were
confined to the adventitia.
1 Histology and Comparison of Arterial Grafts Used for Coronary Surgery
Table 1.1. Combined width of intima and media in various arterial conduits and left anterior descending coronary arterya
Arteries
(n = 17)
Width of intima and media (± SD) (µm)
Fixation in flaccid
Fixation at pressure
state
of 100 mm Hg
LAD
IMA
RGEA
IEA
RA
320 ± 63
350 ± 92
291 ± 109
249 ± 87
529 ± 52
313 ± 209
303 ± 100
284 ± 136
LAD left anterior descending coronary artery, IMA internal
mammary artery, RGEA right gastroepiploic artery, IEA inferior epigastric artery, RA radial artery
a
Kruskal-Wallis analysis of variance
1.2
Right Gastroepiploic Artery
1.2.1
Anatomy
The right gastroepiploic artery is the larger of the two
terminal branches of the gastroduodenal artery, the
other being the superior pancreaticoduodenal artery.
The right gastroepiploic artery passes from right to left
along the greater curvature of the stomach at a somewhat variable distance from the border of the organ. It
lies between the two layers of the gastrocolic ligament
or the ventral two layers of the greater omentum when
these are not adherent to the colon. It gives off a large
ascending pyloric branch near its origin and at its termination usually anastomoses with the left gastroepiploic branch of the splenic artery. It supplies a number
of ascending gastric branches to the stomach and descending branches to the greater omentum.
a
1.2.2
Histology
In a histological study of the gastroduodenal and right
gastroepiploic arteries, harvested in 28 patients (mean
age 73.2 years), the former demonstrated mild to moderate intimal hyperplasia (Fig. 1.7) [33]. Its thickness in
the immediate vicinity of the origin of the right gastroepiploic artery was highly variable: 95 ± 107 µm. The
media of the gastroduodenal artery was muscular
with rare dispersed elastic fibers; its thickness was
395 ± 85 µm.
The mean luminal diameter of the right gastroepiploic artery was 2.7 ± 0.3 mm at its origin, 2.2 ± 0.4 mm
at 10 cm, and 1.8 ± 0.5 mm at 15 cm. The right gastroepiploic artery generally showed mild intimal hyperplasia at its origin (intimal thickness 50 ± 49 µm), with
a gradually decreasing degree of intimal hyperplasia
along its course (distal intimal thickness, 10 ± 17 µm)
(p = 0.003). The media of the right gastroepiploic artery was muscular with rare dispersed elastic fibers
(Fig. 1.8). The thickness of the media varied from
380 ± 116 µm at the origin of the right gastroepiploic
Table 1.2. Combined width of intima and media of the right
gastroepiploic artery at its proximal, mid, and distal segments
Layer
Width (µm)a
Proximal
Mid
Distal
p
Valueb
Intima
Media
58.9 ± 41
245.9 ± 107
40.8 ± 33
187.1 ± 38
NS
NS
37.3 ± 22
253.7 ± 103
NS not significant
a
Data are shown as the mean ± standard deviation
b
Student’s t-test
b
Fig. 1.7a, b. Gastroduodenal artery at origin of the right gastroepiploic artery. a Overview; b detail showing moderate intimal hyperplasia and muscular character of the media
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I Biological Characteristics of Arterial Grafts
a
c
b
e
d
Fig. 1.8a–e. Right gastroepiploic artery. a Overview and b detail at origin from the gastroduodenal artery; c at 1 cm; d at 9 cm; and
e at 18 cm. Note mild intimal hyperplasia a with focal moderate hyperplasia b at origin of the artery, decreasing intimal hyperplasia from proximal to distal, and muscular character of the media
artery to 155 ± 70 µm distally (p = 0.0001). The number
of discontinuities in the circumferential internal elastic
lamina was rather constant, varying from 86 ± 30
at the origin to 93 ± 29 at 5 cm, and 58 ± 17 distally
(p = 0.79). The vasa vasorum were confined to the
adventitia.
1.3
Inferior Epigastric Artery
1.3.1
Anatomy
The inferior epigastric artery (IEA) arises from the medial side of the external iliac artery just proximal to the
inguinal ligament, and at first lies in the midst of the extraperitoneal tissue at the medial side of the abdominal
inguinal ring, in intimate relation with the posterior
wall of the inguinal canal. The ductus deferens, as it enters the abdomen, hooks around the lateral side of the
artery. Accompanied by its satellite veins, the inferior
epigastric artery ascends obliquely superiorly and me-
dially toward the umbilicus; after piercing the transversalis fascia, it enters the rectus compartment by passing
in front of the linea semicircularis (semilunar fold of
Douglas). It then pursues a cephalad vertical course.
Grossly demonstrable direct arterial communications
between the superior and inferior epigastric arteries
may exist in approximately 40 % of cases [34].
1.3.2
Histology
In a histological study of the inferior epigastric artery
harvested in 28 individuals (mean age, 73.2 years), the
mean luminal diameter of the inferior epigastric artery
was 2.0 ± 0.4 mm at its origin, 1.9 ± 0.5 mm at 10 cm,
and 1.1 ± 0.5 mm at 15 cm. At all three levels, the luminal diameter of the inferior epigastric artery was significantly smaller than that of the right gastroepiploic artery (p < 0.05). In contrast to the findings in the right
gastroepiploic artery, there was substantial intimal hyperplasia in the first 1-cm segment of the inferior
epigastric artery (intimal thickness, 134 ± 131 µm)
1 Histology and Comparison of Arterial Grafts Used for Coronary Surgery
a
c
b
d
e
Fig. 1.9a–e. Inferior epigastric artery. a Overview and b detail at origin from the external iliac artery; c at 1 cm; d at 8 cm; and e at
16 cm. Note severe intimal hyperplasia in the first 1-cm segment, gradually decreasing degree of intimal hyperplasia beyond the
first 1-cm segment, and muscular character of the media
(p = 0.01); the width of the intima decreased to
57 ± 78 µm at 1 cm and then gradually decreased to trivial values distally (p = 0.01) (Fig. 1.9). The media of the
IEA was muscular with rare dispersed elastic fibers.
The thickness of the media varied from 316 ± 86 µm at
1 cm to 165 ± 70 µm distally (p = 0.0001). The number of
discontinuities in the circumferential internal elastic
lamina was rather constant and varied from 82 ± 25 at
3 cm to 35 ± 11 distally (p = 0.039). In all instances, the
vasa vasorum were confined to the adventitia.
1.4
Radial Artery
1.4.1
Anatomy
Opposite the neck of the radius, approximately 1 cm
below the bend of the elbow, the brachial artery terminates in two branches, the radial and ulnar arteries. The
radial artery is smaller in caliber than the ulnar artery.
The radial artery passes along the radial aspect of the
forearm to the wrist. The proximal part of the artery is
covered by the belly of the brachioradialis muscle,
while the rest of the artery is superficial, being covered
only by skin and the superficial and deep fasciae. The
radial artery has numerous collateral branches, particularly in its distal segment. The vessel is accompanied
by a pair of veins throughout its whole course.
1.4.2
Histology
In a histological study of the radial artery, harvested in
11 individuals (mean age 64 years), the media was
purely muscular (Fig. 1.10) [32]. A mild to moderate
degree of intimal hyperplasia was observed. The mean
number of discontinuities in the circumferential internal elastic lamina of the radial artery (45 ± 28) was similar to that found in the elastomuscular segments of the
internal mammary artery. The mean width of the intima and media of the flaccid radial artery was
529 ± 52 mm (Table 1.1). The vasa vasorum were confined to the adventitia.
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I Biological Characteristics of Arterial Grafts
Fig. 1.10. Radial artery. Note
the width of the muscular
media
Fig. 1.11. Proximal intercostal
artery. Note the multiple
elastic lamellae in the media
1.5
Intercostal Artery
The potential suitability of the intercostal artery as a
conduit in myocardial revascularization was assessed
[35]. In 11 patients three combinations of histological
patterns were observed along the course of the fourth
to ninth intercostal arteries: a proximal elastic segment
(Fig. 1.11) followed by subsequent elastomuscular
(Fig. 1.12) and muscular segments (n = 3) (Fig. 1.13), a
proximal elastomuscular segment with the remainder
of the artery being muscular (n = 6), and a completely
muscular pattern (n = 2). The mean luminal diameter
of the fifth intercostal arteries varied from 1.4 ± 0.3 mm
at the origin to 0.9 ± 0.2 mm at 30 cm. The mean intimal
thickness at these locations was 54 ± 38 mm and
25 ± 16 mm, respectively, and the mean thickness of the
media was 205 ± 38 mm and 70 ± 45 mm, respectively.
The histological findings, mean luminal diameter, and
mean diameter of the intima and media were similar in
the intercostal arteries other than the fifth. An anatomic study concluded that it is feasible to use the intercostal artery as an in situ graft in myocardial revascularization [36].
1 Histology and Comparison of Arterial Grafts Used for Coronary Surgery
Fig. 1.12. Mid segment of intercostal artery. The media is
elastomuscular
Fig. 1.13. Distal intercostal
artery. The media is muscular
1.6
Comment
1.6.1
General Considerations
Over the long term, there is a striking difference in the
late development of atherosclerosis in internal mammary artery bypass conduits compared with venous
conduits. Comparison of internal mammary artery and
vein graft patency reveals a highly significant difference at every interval [7]. Accelerated vein graft closure
because of progressive intimal hyperplasia and athero-
sclerosis begins in the fifth year and approximates 5 %
per year, with a 10-year patency rate varying between
41 % and 56 % (3). In contrast, the 10-year patency rate
of the internal mammary artery has been reported to
be greater than 80 % [3, 7]. It is intriguing that the internal mammary artery, a vessel comparable in cross-sectional diameter to the coronary artery and acclimated
to the same biochemical environment, has such a low
incidence of atherosclerosis. Although the cause of the
apparent protection of the internal mammary artery
from intimal thickening and atherosclerosis remains
obscure, a few conclusions can be made on the basis of
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I Biological Characteristics of Arterial Grafts
our studies and accumulated evidence from research in
vascular pathology.
Histological research has established that the first
stage of intimal thickening is caused by invasion of
smooth muscle cells from the media through the fenestrated internal elastic lamina [37]. In the first decade of
life this intimal thickening can already be observed.
Sims [38, 39] pointed out that the internal elastic lamina has a key role in arterial wall structure. His observations suggest that the occurrence of discontinuities in
the internal elastic lamina provokes early and progressive intimal hyperplasia. Stimuli that trigger smooth
muscle cell proliferation are most likely complex and
may include leakage of blood constituents and exertion
of stress forces on the smooth muscle cells [40]. Operation of these processes over a long period may contribute to progressive intimal hyperplasia. If, as the accumulated evidence suggests, damage to the internal elastic lamina in the presence of smooth muscle cells in the
media has a determining role in the initiation of intimal
thickening, as a result of the proliferation of smooth
muscle cells from the media, it is intriguing to consider
that elastic arteries may be less prone to intimal hyperplasia than muscular arteries. In the former, intimal hyperplasia develops at a considerably delayed rate because proliferative smooth muscle cells are present only
to a moderate extent. In addition, the multiple elastic
lamellae and the internal elastic lamina form barriers
to their invasion. Moreover, elastin, the basic component of the elastic tissue of the media, is a bradytrophic,
relatively inert tissue with a low metabolic rate. The
media of the elastic artery therefore has a lower intrinsic demand for oxygen and substrates than the media of
the muscular artery. Also, the abundant lymphatic
drainage as present in the internal mammary artery
may delay intimal hyperplasia [41].
In our histological studies we showed that there may
be a correlation between the absence of elastic lamellae
in the media and an increased number of discontinuities in the internal elastic lamia and, as a potential result of this, increased intimal thickening [30, 32]. The
intima was significantly thicker in the purely muscular
segments of the musculophrenic and superior epigastric arteries than in the internal mammary artery. Although one may argue that these findings may be coincidentally related but not causally, similar findings are
reported by Sims and Gavin [42] in a comparative histological study between the muscular coronary artery
and the primarily elastic internal mammary artery, in
which the number of discontinuities in the internal
elastic lamina and the degree of intimal thickening
were significantly greater in the former vessel. Based on
their and our observations we conclude that elastic lamellae in the media may protect against the occurrence
of discontinuities in the internal elastic lamina and,
secondarily, against intimal thickening, even if the
number of lamellae is small. The study by Sims and Gavin [42] also suggests that gaps in the internal elastic
lamina allow smooth muscle cells of the media to proliferate into the intima and that the rate of this growth
reflects the response of medial smooth muscle cells to
tension on the arterial wall. Other studies by Sims [43,
44] confirm the structural importance of the internal
elastic lamina and its relationship to intimal thickening. Research in vascular pathology has shown that medial smooth muscle cells are mesenchymal cells capable
of changing from a contractile to a synthetic type in response to damage of the internal elastic lamina and increasing tangential tension on the vessel wall [45]. This
process leads to active cell division and synthesis of collagen, elastin, and proteoglycan matrix [46, 47]. After
penetration from the media into the intima, the proliferating smooth muscle cells produce elastin, often as a
coherent reduplicated internal elastic lamina, which
can be seen as single or multiple thin sealing layers on
the luminal aspect of the defective internal elastic lamina. This phenomenon was frequently observed in our
specimens, especially in arteries with a purely muscular media. Almost invariably such repair is imperfect,
and with the passage of time, breakdown of the reduplicated internal elastic lamina occurs, leading to serious
impairment of attachment of endothelial cells, cell loss,
and the development of bare areas. Such bare areas may
enhance the infiltration of macromolecules of all sizes,
including lipoproteins, and cells of the circulating
blood, thus accelerating the development of atherosclerotic lesions [48, 49].
Due to the effect of pulsatile stress on the proliferation of smooth muscle cells from the media into the intima, the rate of intimal thickening may be enhanced in
the central aorta and its branches in comparison with
the internal mammary artery, in which the hemodynamics are less vigorous [50, 51]. Such proliferative
smooth muscle cell response has been observed in systemic and pulmonary hypertension and in the culture
of medial cells from hypertensive animals and from experimental atherosclerosis [52 – 55]. We observed a
considerably greater degree of intimal thickening in the
subclavian artery and the first centimeter of the internal mammary artery than in the remainder of it.
The findings as presented in our studies may have
implications with regard to selection of the anastomotic site in the internal mammary artery. We observed a
considerable interindividual variability with regard to
the extent of a primarily elastic media in the internal
mammary artery. In seven patients the distal segment
of the internal mammary artery was either elastic or
elastomuscular, whereas in four patients the distal
10 – 20 % segment was muscular with rare elastic lamellae. These findings suggest that, based on the assumption that use of an elastic or elastomuscular conduit is
superior to use of a primarily muscular one in myocar-
1 Histology and Comparison of Arterial Grafts Used for Coronary Surgery
dial revascularization, it may be beneficial not to use
the distal 10 – 20 % segment of the internal mammary
artery. This strategy has the additional advantage that
the internal mammary artery cross-sectional luminal
diameter proximal to or at the 80 – 90 % level may better
match the diameter of the coronary artery than the
more distal segment. Selection of the anastomotic site
in the musculophrenic or superior epigastric arteries is
not encouraged because of the potentially increased
risk of intimal thickening and the significantly smaller
luminal diameter of these vessels.
1.6.2
Internal Mammary Artery
To expand the benefits of the elastic and elastomuscular internal mammary artery, the shortest possible
route to the heart should be established [56 – 59]. For
the same reason bilateral grafting with the internal
mammary artery may be beneficial [60 – 62]. To gain
additional length of the internal mammary artery,
transection of the pleura and fascia beneath it may be a
valuable technique [63]. However, we do not favor its
complete or partial skeletonization, as advocated by
Sauvage and associates [60] and Keeley [64], respectively, because this technique has an increased risk of
iatrogenic disruption of the internal elastic lamina.
This may be especially deleterious in segments with a
high muscular content because it may provoke enhanced intimal thickening [65].
A reported patency rate of free, pedicled internal
mammary artery grafts approximating that of in situ
grafts [66] is consistent with our supposition that the
intima and media of the nondiseased internal mammary artery are nourished entirely from the lumen. Therefore, any discrepancy in patency rate between in situ
and free internal mammary artery grafts may be attributable primarily to the proximal anastomosis.
1.6.3
Right Gastroepiploic Artery
The number of discontinuities in the internal elastic
lamina in the muscular right gastroepiploic artery is
greater than that in the elastic segments of the internal
mammary artery [33]. This observation probably reflects the absence of a protective effect of elastic lamellae in the media against the development of discontinuities in the internal elastic lamina in the former. Therefore, we believe that some skepticism toward the longterm patency of the right gastroepiploic artery is warranted, especially if this conduit is used as a free graft.
The muscular character of the media of the right gastroepiploic artery may find expression in an increased
vulnerability toward intimal thickening and, ultimately, atherosclerosis of the former once its wall is exposed
to the forceful mechanical stretching of the central aortic circulation (if used as a free graft) and (to a lesser
extent) the coronary circulation. Thus, although Suma
and associates [67, 68] and we found only a mild to
moderate degree of intimal thickening in the right gastroepiploic artery, this finding must be interpreted with
caution, because it reflects the situation at the time of
harvesting of the artery in its natural environment. Future clinical studies with regard to the long-term patency rate of the right gastroepiploic artery as a coronary
artery bypass graft will prove whether our skepticism is
justified or not.
1.6.4
Inferior Epigastric Artery
The number of discontinuities in the internal elastic
lamina of the inferior epigastric artery is similar to that
of the right gastroepiploic artery and elastomuscular
segments of the internal mammary artery. Based on the
lower elastic content of the media of the inferior epigastric artery as compared to the internal mammary artery, we hypothesize that the former may have an increased tendency toward intimal thickening. Although
early patency rates of the inferior epigastric artery
ranging from 88 % to 97 % have been reported [20, 22,
23], based on our observations, we predict less superior
long-term patency rates of this arterial conduit.
A study by Perrault and coworkers [69] who performed immediate postoperative angiographic evaluation in 14 patients who had received one inferior epigastric artery graft each to the right coronary artery, a
marginal circumflex coronary artery, and a diagonal
coronary artery, showed that only eight grafts (57 %)
were patent. Although the less superior results in this
report may partially have been due to the technical
learning curve, a word of caution is needed against indiscriminate use of the inferior epigastric artery in
myocardial revascularization until satisfactory longterm patency rates of this conduit have been established.
In a study of ours not presented above [70], we did a
morphometric comparison between the right gastroepiploic and inferior epigastric arteries. We reported
only mild to moderate intimal thickening in the gastroepiploic artery (GEA) its natural state. Based on our results and those of previous studies, we hypothesize that
although the muscular character of the media of the
GEA may increase its vulnerability to intimal thickening (as compared with the primarily elastic IMA), the
development of intimal hyperplasia may be slow – following a pattern that approximates that of the GEA in
its natural environment – if it is used as an in situ graft
and thus is protected by retention in its usual physiologic environment. This hypothesis is corroborated by
the clinical studies [15]. In this study, we observed that
13
14
I Biological Characteristics of Arterial Grafts
at its origin, the intima of the IEA is significantly thicker (175 ± 131 µm) than that of the GEA in the corresponding segment (64 ± 50 µm) (p < 0.01). Beyond
1 cm, there was only low-grade intimal hyperplasia in
the IEA. This finding leads us to conclude that it may be
better not to use the origin of the IEA because of the
high likelihood of substantial intimal hyperplasia in
this segment.
1.6.5
Radial Artery
Reports from the 1970s have unanimously condemned
further use of the radial artery as a conduit for myocardial revascularization on the basis of an alarmingly
high early occlusion rate [25 – 28]. It may be true that
the observed discrepancy in early patency between the
previous and current experience with the radial artery
conduit [29] may partially have been caused by accelerated intimal hyperplasia as a result of dilation of the
vessel with graduated probes and by stripping of the
vessel of surrounding tissue in the past. Such focal
damage, which is more likely to occur in muscular conduits such as the radial artery than in elastic segments
of the internal mammary artery, may trigger a cascade
of events and may ultimately enhance progressive intimal thickening [31]. Vasospasm is also significantly related to the abandened use of this conduit in 1970s (see
Chapter 9 and 17).
In our studies we measured a mean width in the media of the radial artery of approximately 500 mm, as opposed to 330 mm for that of the internal mammary artery, 280 mm for that of the right gastroepiploic artery,
and 240 mm for that of the inferior epigastric artery. In
addition, nutrition of the thick media of the radial artery is mainly through diffusion from the lumen, as we
did not observe any penetration of vasa vasorum into
its media. Although the thick media of the radial artery
may be advantageous with regard to ease of performance of the proximal anastomosis (as opposed to the
technically more challenging proximal anastomosis
when the internal mammary artery and especially the
right gastroepiploic and inferior epigastric arteries are
used as free grafts), it may also predispose the conduit
to a potentially greater degree of ischemia (and potentially fibrosis), especially in the outer layer of its media.
Because the right gastroepiploic and inferior epigastric
arteries have a considerably thinner media, a less critical relationship exists between metabolic demand and
supply of the media, and therefore the potential for ischemia in these vessels may be less.
In addition, we have found a considerable number of
discontinuities in the internal elastic lamina of the radial artery harvested in its natural environment, with
mild to moderate intimal hyperplasia. Based on these
findings and the presence of a thick muscular media,
we think that the potential for intimal hyperplasia may
be considerably more pronounced in the radial artery
conduit than in the internal mammary artery conduit,
which has the protective effect of multiple elastic lamellae in its media. This hypothesis was proven correct in
the internal mammary artery, the elastic and elastomuscular segments of which had significantly less intimal thickening than the muscular superior epigastric
and musculophrenic arteries.
A second major concern regarding use of the radial
artery as a conduit in myocardial revascularization is
the potentially deleterious effect on the vascular supply
of the forearm and hand, which must not be underestimated. The occurrence of claudication in the hand and
(transitory) dysesthesia of the thumb in patients in
whom the radial artery was used as a conduit in myocardial revascularization has been reported [71]. In the
case of thromboembolism or injury of the ulnar artery,
major catastrophes may ensue. In view of these complications, the radial artery is much less dispensable an artery than are the internal mammary, right gastroepiploic artery, and inferior epigastric arteries.
In view of the potentially serious drawbacks of the
radial artery as a conduit in myocardial revascularization, use of bilateral internal mammary arteries or, alternatively, the right gastroepiploic or inferior epigastric arteries should be emphasized, rather than use of
the radial artery, which in our opinion should not be
used as a conduit of primary choice.
In summary, arterial grafts have similarities and differences in structure and histology. The structural differences may account for the different biological behavior such as long-term patency rates. Careful choice of
optimal arterial grafts is critical in the success of arterial grafting. The details of the functional assessment of
arterial grafts and the clinical choice will be introduced
in separate chapters.
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