1603
Impact of Compensatory Enlargement of
Atherosclerotic Coronary Arteries on
Angiographic Assessment of
Coronary Artery Disease
Georg M. Stiel, MD, MSc, Ludmilla S.G. Stiel, MD, MA, Joachim Schofer, MD,
Karl Donath, MD, DDS, and Detlef G. Mathey, MD
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To determine whether compensatory enlargement of atherosclerotic coronary arteries occurs
and to what degree it affects the angiographic assessment of coronary artery disease, we
performed postmortem coronary angiography of 30 human hearts with suspected coronary
artery disease and studied 70 histologic cross sections of the proximal left anterior descending
artery and proximal right coronary artery. Angiographic and morphometric analyses of 50
stenoses in proximal and middle sections of the left anterior descending artery, right coronary
artery, and left circumflex artery were performed. The control group of 10 human hearts
without suspected coronary artery disease was evaluated in the same way. For this purpose,
coronary arteries were filled with a methylmethacrylic radiopaque resin at a pressure of 100
mm Hg and closely embedded in a methylmethacrylic resin by use of which shrinkage and
mechanical artifacts could be avoided. The area circumscribed by the internal elastic lamina
was taken as a measure of the area of the arterial lumen if no plaque had been present. The
angiographic and corresponding morphometric degree of stenosis was assessed. A significant
correlation (r=0.85,p<O.0001) was found between the internal elastic lamina area and the area
of the plaque (lesion area), suggesting that coronary arteries may enlarge as lesion area
increases. With the morphometric degree of stenosis, the expected anatomic diminution of the
coronary artery was abolished (r=0.79, p50.0001), indicating compensatory enlargement in
atherosclerotic segments. Accordingly, the degree of stenosis assessed from in vitro angiograms
was underestimated. Compensatory coronary enlargement of the stenotic segment was the main
reason for angiographic underestimation. The underestimation factor of up to 3.50 for very
mild stenoses decreased to 1.37 at an angiographic degree of 50% area stenosis and 30%
diameter stenosis. In contrast, at higher degrees of stenosis, angiographic underestimation
resulted mainly from compensatory enlargement due to disease in the prestenotic reference
segment. The underestimation factor was 1.37. These studies show that compensatory enlargement in stenotic coronary artery segments occurs resulting in significant angiographic underestimation of coronary atherosclerosis during the early stage of coronary artery disease.
(Circulation 1989;80:1603-1609)
Coronary angiography is widely accepted as a
useful clinical and investigative tool to
assess coronary artery disease (CAD).
There are, however, some limitations of the techFrom the Department of Cardiology and Institute of Pathology
(K.D.), University Hospital Eppendorf, Hamburg, FRG.
Presented in part at the Tenth Congress of the European
Society of Cardiology, Vienna, Austria, August 29, 1988.
Address for reprints: Prof. Dr. Detlef G. Mathey, Priv. Doz.
Dr. Joachim Schofer, Innere Medizin/Kardiologie (Interventionelle Kardiologie im Allg. Krankenhaus Altona), Othmarscher
Kirchenweg 168, 2000 Hamburg 50, FRG.
Received October 18, 1988; revision accepted August 3, 1989.
nique that are important to recognize. Usually, the
extent of CAD is estimated as percent reduction of
luminal diameter determined by comparing the
diameter at the site of maximal reduction with the
diameter in adjacent areas that appear either normal or only minimally diseased. However, there
is significant intraobserver and interobserver variability in the conventional assessment of coronary
artery lesions.1 -4 Computer-based visual5 and
automated6-8 methods of luminal border definition from cine film images seem to improve the
reproducibility and accuracy of coronary diameter
measurements.
1604
Circulation Vol 80, No 6, December 1989
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On the other hand, several investigators have
shown a poor agreement of angiographic findings
with direct postmortem measurements.9-13 Recently,
Glagov et a114 studied the left main coronary artery
histologically and found compensatory enlargement
during the early stage of plaque formation. This new
morphological finding offers a logical explanation
why coronary angiography often underestimates
the severity of vessel stenosis. A controversial
discussion followed this report.15-19
In the present study, we were able to prove
conclusions of Glagov et a114 for the proximal
segments of the left anterior descending (LAD)
coronary artery and right coronary artery (RCA).
We could also show that the compensatory enlargement occurs in the proximal circumflex (Cx) coronary artery and in the middle segments of the LAD
and RCA by determining the diminution ratio (DR)
of normal and diseased coronary arteries. In a next
step, we examined to what degree compensatory
coronary artery enlargement affects the angiographic assessment of CAD.
By conventional postmortem preparation of coronary arteries, shrinkage and mechanical artifacts
cannot be avoided. The results of postmortem angiographic studies, therefore, may reflect neither the
natural status of the coronary arteries nor the
results of coronary angiograms performed in vivo.
For our studies, we performed an angiographic and
morphometric analysis of postmortem human coronary arteries using a new method of preparation
that is free of these artifacts.22
Methods
Study Material
Forty human hearts were obtained at autopsy
within 24 hours of death. In the study group of 30
hearts, disease of left, right or left, and right coronary artery was demonstrated by postmortem angiography. The age of the subjects was 47-90 years
(67 + 18 years, mean + SD). Seventeen were men and
13 were women. The weight of the hearts before
fixation was 350-710 g (485±79 g, mean±SD).
The control group consisted of 10 hearts without
suspected CAD. The age of the subjects was 42-72
years (55±11 years, mean± SD). Four were men and
six were women. The weight of the hearts before
fixation was 310-390 g (345±28 g, mean±SD).
Study Methods
All hearts were prepared in an identical manner.
The hearts were weighed and examined for gross
changes. After the usual preparation,20,21 the coronary arteries were injected at a pressure of 100
mm Hg with a casting mixture consisting of barium
sulfate and methylmethacrylic resin.22 After coronary casting, the hearts were fixed in cold formalin
(40 C) and placed in a dummy thorax for the normal
x-ray recording simulation. Postmortem radiographs of the whole heart were made in several
standard projections (Figure 1); for each, a complementary perpendicular projection was obtained.
The morphometric analysis of 10 proximal and
nine middle segments of the LAD coronary artery,
nine proximal and 10 middle segments of the RCA,
and six proximal and six middle segments of the left
Cx coronary artery was performed for the study
group according to the method of Brown et al.5 By
this method, the angiographic percent-diameter stenosis and percent-area stenosis for 50 coronary
lesions were calculated.
After angiography of the whole hearts of the
study group and control group, the aforementioned
arterial segments were removed. The samples were
embedded in methylmethacrylic resin23 and reimaged by contact radiography to characterize the
state and configuration of the atherosclerotic plaques
(Figure 1). The acrylic samples were sawed exactly
in the area of minimal lumen diameter and the
corresponding "normal" lumen estimated by contact radiography. The distance between both cross
sections was the same as for the morphometric
analysis. In the control group, localization of and
distance between both cross sections were chosen
to be comparable with the study group. The cut
surfaces were ground and stained with the MassonGoldner trichrome procedure and with Weigert's
resorcin-fuchsine procedure for differentiation of
connective tissue (Figure 1).
For histologic measurements, a contour-tracing
system consisting of a microscope with a video
camera, a digitizer for semiautomatic measurements, a video monitor, and an IBAS 2000 computer system was used.
The lumen, the internal elastic lamina (IEL), and
the outer limit of the media in 38 proximal LAD and
32 proximal RCA diseased sections were traced as
proposed by Glagov et al.14
For the present study, the proximal LAD was
used before origin of the first diagonal branch and
the proximal RCA before origin of any major side
branch. In most adult hearts, these segments are
similar in diameter and lumen area.25 For 50 morphometric analyzed stenoses the cross sections
with a minimal lumen and corresponding prestenotic "normal" lumen could be defined and were
traced by the same method.
From these tracings, the actual cross-sectional
area of the lumen (lumen area), the lesion area (the
cross-sectional area occupied by plaque), and the
IEL area were determined from the contours (Figure 1). Using the same definition as Glagov et al,14
the IEL indicates the inner limit of the arterial wall
and describes an area that is nearly identical to the
lumen area when there is little or no intimal thickening. In the presence of plaque, the IEL area
represents the "potential" lumen area, that is, what
the actual lumen area would be if there was no
plaque. The diameter of a circular area equivalent
to each area traced was calculated. The IEL area
Stiel et al Compensatory Enlargement of Atherosclerotic Coronary Disease
1605
FIGURE 1. (A) Microphotograph ofLA 0 view ofpostmor
tern angiogram of left and
coronary artery.
. . ............right
.
;0
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.;.1,
0t; ti:0
and RCA demonstrate several
:;F o
irregularities oflumen. Arrow
f 00 >
point -i
to lesions
'heads
t E inprox'
g:g<;jin
Acrylic blocks of left and right
.......
..........
.t
......im
A
A........
;*'~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.
c
for distal and proximal cross sections of 30 control
samples was determined by the same method.
D
.sJ
. .....
coronary artery are shown.
Involved segments are sawed,
revealing slices as shown in
lower part of (B). Contact
angiograms of acrylic blocks
(B) with right (C) and left (D)
coronary artery. Microphoto~~~~graphs ofground and stained
~~~~~~~~cross-sections of stenotic segments of right (E) and left
coronary artery (F). Intimal
surface demarcates actual
lumen area (Lu). Area occupied by lesion (Le) is surrounded by internal elastic
lamina. "Potential" lumen
is defined as area encom
~~~~~~~~~~~~~~~~~area
internal elastic lamin~~
~~~~~~~~passedby
~ ~ (arrow
~ ~a s).
The degree of stenosis as calculated from the
cross section of an artery was defined as the extent
1606
Circulation Vol 80, No 6, December 1989
to which the lesion area occupies the "potential"
lumen area, and the morphometric percentage of
stenosis was expressed as: %ASm=(1 -lumen area/
IEL area)x 100.
Analyses of the coronary angiograms and of the
pertinent histologic slices were performed by two
independent observers, each of whom was unaware
of the other's results.
The corresponding angiographic and morphometric measurements were compared using leastsquares regression analysis and Pearson's correlation coefficient. Statistical significance was assigned
when p was less than or equal to 0.05.
Results
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Because a methylmethacrylic resin was used to
fill and embed the coronary arteries, no shrinkage
artifacts could occur. By the sawing and grinding
technique, mechanical artifacts were avoided. With
this new method of preparation, the anatomy of
distended coronary artery was well preserved,
thereby offering comparable conditions for angiographic and histologic evaluations.
The IEL area in 38 proximal LAD and 32 proximal RCA, diseased cross sections was 3.0-20.0
mm2 (9.8±3.3 mm2, mean±SD). The smallest measured lesion area was 1.1 mm2, and the largest was
15.2 mm2 (6.0±3.8 mm2, mean±SD). The actual
lumen area was 0.0-9.0 mm2 (4.4±2.0 mm2,
mean±SD).
Ten proximal and nine middle stenotic segments
of the LAD, nine proximal and 10 middle stenotic
segments of the RCA, and six proximal and six
middle stenotic segments of the Cx coronary artery
were analyzed angiographically and histologically.
The percent-area stenosis by angiographic measurements was 10.0-95% (41.6±24.7%, mean± SD)
and by morphometric measurements, 18.3-96%
(61.1 ± 24.5%, mean±+ SD). The morphometric
percent-area stenosis in the prestenotic region (normally the reference for angiographic measurements)
was 10.9-59.9% (28.7+9.1%, mean±SD).
The examined arterial sections of the control
group were chosen to be identical in number and
location with those of the study group.
IEL Area (mm2)
20 _
DIMINUTION RATIO
=
Internal elastic lamina area in stenotic segment
Internal elastic lamina area in prestenotic segment
DR
Reference
=
1.3
DR
z
1.8
FIGURE 3. Definition of diminution ratio for anatomical
diminution of coronary artery and diagrammatic representation of changes in internal elastic lamina (IEL) area
for minimal and more severe lesion (Le).
In the control group, the proximal IEL area was
5.5-10.6 mm2 (8.9+1.2 mm2 mean+SD) and the
distal IEL area was 5.4-10.5 mm2 (8.3±1.2 mm2,
mean+SD). The mean distance and its variation
was almost identical for the study and the control
group (range, 5-25 mm; mean 12±5 mm).
IEL area increased with the lesion area (r=0.85,
p<O.OOO1) (Figure 2). The standard error of the IEL
area in relation to the lesion area along the regression line was 2.0 mm2.
The anatomical diminution of the coronary artery
was expressed as the ratio of the distal to the
proximal IEL area (Figure 3). A DR 0.93+±0.05 was
found in the arterial segments of the control group.
If the IEL area does not change with growth of the
lesion, no increase of the DR would have been
expected. Figure 3 shows the diagrammatic representation of the changes in the IEL area if the lesion
is only minimal and later more severe, resulting in
different DRs.
The relation between the DR of the coronary
artery and the degree of stenosis (percent-area
stenosis and percent-diameter stenosis obtained by
DR
2.0
-
1.8
-
1.6
-
1.4
-
1.2
**
*
a
*
*
00
0
.. * * * y = ~~~~~~33.72 +1.06 x- 0.004x2
S*
-
16
*
r
0.79
p < 0.0001
SEE = 12.3 %
= 50
_________________SE
___12.3
1.0 -
0.93p+0.05
12
z
0.8 -
8
2W
*'
C.
4
I
y
0.84 x + 5.51
r =0.85
p c0.0001
SEE = 2.0 mm2
n = 70
l
0
0
2
4
6
8
=
10 12 14 16
LESION Area (mm2)
FIGURE 2. Scatterplot of comparison of internal elastic
lamina area (IEL Area) ("potential" lumen area) with
lesion area (Lesion Area). Linear regression.
0
0
40
20
60
80
I
I
*
a
10
20
30
40
l
l
l
100
%ASm
a
50
...5
11
70 100
% DSm
FIGURE 4. Scatterplot of diminution ratio of coronary
artery (DR) plotted against morphometric degree of
stenosis (percent-area stenosis [%oASmJ and percentdiameter stenosis [%DSmJ. Polynominal regression.
Expected diminution ratio is indicated by broken line.
Stiel et al Compensatory Enlargement of Atherosclerotic Coronary Disease
%ASa
100 - - 29.55
y
80
-
r
-
p
SEE
<
-
40
-
20
-
r. I
v-I
n
/
50
n
60
+ 2.53 x -..04 x2 + 0.0003 x3
0.93
0.0001
9.2#%
1
1
1
-
1
80
60
40
20
0
/ ,
*
100
%ASm
FIGURE 5. Scatterplot ofangiographic percent-area stenosis (%oASa) versus morphometric percent-area stenosis
(%oASm). Polynominal regression.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
morphometric measurements) is shown in Figure 4
(r=0.73,p<0.0001, SEE=0.12). The regression line
approximates the DR of 2.0 at higher degrees of
stenosis.
Figure 5 shows the relation between the cineangiographic and morphometric degree of stenosis.
The line of best fit expressed as polynominal regression gives a high coefficient of correlation (r=0.93,
p'0.0001, SEE=9.2%) between the angiographic
percent-area stenosis and the morphometric percentarea stenosis. Cineangiography significantly underestimates coronary atherosclerosis at all degrees of
stenosis.
The factor of angiographic underestimation is
defined as the ratio of morphometric percent-area
stenosis to angiographic percent-area stenosis. The
angiographic underestimation factor (UF) for each
of the stenoses studied with respect to the angiographic degree of stenosis is shown in Figure 6. The
line of best fit shows the following course: a hyperUF
3.5
-
.
r
3.0
SEE
\
-
2.0
-
0.80
-
_p C
-
2.5
3.68 -0.11 x + 0.002 X2-0.00001 X3
y =
n
a n.I.
0.uuui
0.37
50
*S
0~~~~
*\
1.5
-
1.0
-
-*eo
*
a
0
.0
0.*
.
*.
*~~~~.0i
.
I
40
20
80
60
[-100
% ASa
0
10
l
20
30
l
40
50
liii
70 100
% DSa
FIGURE 6. Scatterplot of variability of angiographic
underestimation of coronary atherosclerosis (UF) depending on angiographic degree of stenosis (percent-area
stenosis [%ASal and percent-diameter stenosis [%DSa]).
Polynominal regression.
1607
bolic slope with an angiographic UF between 3.50
and 1.37 for angiographic percent-area stenoses
smaller than 50% and angiographic percentdiameter stenosis smaller than 30%, followed by a
linear course with an approximately constant UF of
1.37 for angiographic area stenoses ranging 50-75%
and diameter stenoses ranging 30-50%, then followed by a downward slope to an UF of 1.00 for
stenoses of more than 75% area stenosis and 50%
diameter stenosis. The horizontal broken line at an
UF of 1.37 mainly indicates the degree of angiographic underestimation due to disease in the prestenotic area averaging 28.7±9.1% area stenosis,
which corresponds to an underestimation of 0.29.
The remaining underestimation of 0.08 has methodologic reasons related to the formula used to calculate the angiographic degree of stenosis.
Discussion
This study provides evidence that the compensatory enlargement of human atherosclerotic coronary arteries occurs during the early stage of
plaque formation and demonstrates its impact on
the in vitro angiographic underestimation of coronary atherosclerosis.
Arterial size measured as the cross-sectional area
enclosed by the IEL correlated significantly with
the cross-sectional area of the plaque (Figure 2).
This result is in agreement with previous studies.14
Glagov et a114 interpreted this observation as evidence for the compensatory enlargement in the
stenotic coronary artery segments of equal size.
Using a different approach, we could prove compensatory enlargement in the present study. Normally, the coronary artery becomes smaller along
its course, both in lumen diameter and in size.25
This results in the DR of 1.0 or less if IEL area
remains constant when the lesion increases (Figure
3). As shown in Figure 4, the DR increases with the
degree of stenosis indicating that the normal anatomical diminution in arterial size is abolished by
compensatory enlargement in the stenotic coronary
arterial segment. For mild CAD (stenoses less than
35-40%) no change in lumen area was found,
because IEL area significantly increased.14,25 The
projected relation between the DR and the degree of
stenosis for this range of mild stenosis is shown by
the broken line in Figure 4. These observations
relate to measurements in the proximal and middle
segments of the coronary artery tree. As suggested
by Zarins et al,30 different segments of the same
coronary artery can respond differently.
The compensatory enlargement has a significant
influence on the in vitro angiographic underestimation of stenosis up to an angiographically determined degree of approximately 50% area stenosis
and 30% diameter stenosis (Figure 6). This important observation shows that compensatory enlargement is a major source of error in the assessment of
coronary lesions by angiography up to the aforementioned degree of stenosis. At a higher degree of
1608
Circulation Vol 80, No 6, December 1989
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stenosis, compensatory enlargement is a less important factor for angiographic underestimation. The
UF for lesions ranging from 50% to 75% area stenosis and from 30% to 50% diameter stenosis is relatively constant (UF= 1.37). In this range of stenoses,
in vitro angiographic underestimation is mainly the
result of two opposing factors, compensatory enlargement in the stenotic and the prestenotic reference
segment. In stenoses of more than 75% area and 50%
diameter reduction, no compensatory enlargement
could be observed in both segments.
Beyond that, a well-known methodical underestimation resulting from the formula used to calculate percent stenosis influences the in vitro angiographic assessment steadily but insignificantly
independent of the degree of stenosis.
In previous studies, it was shown that the assessment of CAD by angiography does not predict the
severity of atherosclerosis.9-13,26-29 Our study provides evidence that coronary angiography underestimates the degree of coronary atherosclerosis over
the entire range of stenoses (Figure 5). The mechanism of compensatory enlargement in a stenotic
coronary arterial segment is recognized as a new
factor of underestimation in addition to the wellknown methodical factors. Compensatory enlargement has its greatest impact on the angiographic
measurement of CAD during the early stage of
plaque formation, leading to a significant underestimation of the disease in this low range of stenoses.
The explanation of the mechanism of the compensatory enlargement in stenotic coronary arteries
is unknown. Glagov et a114 explained this mechanism as a two-step process.14 In the early stage of
CAD, the atherosclerotic plaque is usually eccentric. The stenosis might enlarge in the area of the
plaque or in the uninvolved wall segment. In the
first instance, atrophy of the wall or degradation of
mural connective tissue fibers could result in an
outward bulging of the plaque and the underlying
wall. In the second instance, narrowing of the
lumen would result in an increased flow velocity,
thereby leading to expansion of the uninvolved
segment of the wall.
As a clinical consequence of these findings, the
accuracy of coronary angiography to determine the
early stage of CAD has to be questioned. In view of
the ongoing and future angiographic studies to determine progression and regression of CAD in clinical
trials, our findings are very important for the interpretation of these data.
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KEY WORDS * arteriosclerosis * angiography * coronary
vessels * stenoses
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Impact of compensatory enlargement of atherosclerotic coronary arteries on
angiographic assessment of coronary artery disease.
G M Stiel, L S Stiel, J Schofer, K Donath and D G Mathey
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
Circulation. 1989;80:1603-1609
doi: 10.1161/01.CIR.80.6.1603
Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1989 American Heart Association, Inc. All rights reserved.
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