Angiographic Assessment of Collateral Connections in
Comparison With Invasively Determined Collateral
Function in Chronic Coronary Occlusions
Gerald S. Werner, MD; Markus Ferrari, MD; Stephan Heinke, MD; Friedhelm Kuethe, MD;
Ralf Surber, MD; Barbara M. Richartz, MD; Hans R. Figulla, MD
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Background—The evaluation of new therapeutic modalities to induce collateral growth in coronary artery disease require
improved methods of angiographic characterization of collaterals, which should be validated by quantitative assessment
of collateral function.
Methods and Results—In 100 patients with total chronic occlusion of a major coronary artery (duration ⬎2 weeks)
collaterals were assessed angiographically by the Rentrop grading, by their anatomic location, and by a new grading of
collateral connections (CC grade 0: no continuous connection, CC1: threadlike continuous connection, CC2: side
branch–like connection). The interobserver variability was 10%. Collateral function was assessed by Doppler flow
(average peak velocity) and pressure recordings distal to the occlusion before recanalization. A collateral resistance
index (RColl) was calculated. Recruitable collateral flow was measured during a final balloon inflation ⬎30 minutes after
the baseline measurement. The comparison of the anatomic location, the Rentrop, and the collateral connection grade
showed only for the latter an independent and significant relation with RColl. CC2 collaterals preserved regional left
ventricular function better than did CC1 collaterals and provided a higher collateral flow reserve during adenosine
infusion. CC0 collaterals were predominantly observed in recent occlusions of 2 to 4 weeks’ duration, with the highest
RColl. During balloon reocclusion, recruitable collateral function was best preserved with CC2 and least with CC0.
Conclusions—The angiographic grading of collateral connections in total chronic occlusions could differentiate collaterals
according to their functional capacity to preserve regional left ventricular function and was closely associated with
invasively determined parameters of collateral hemodynamics. (Circulation. 2003;107:1972-1977.)
Key Words: collateral circulation 䡲 angiography 䡲 occlusion
T
laterals. The aim of our study was to evaluate in a welldefined patient group of total chronic coronary occlusions
(TCO) whether such a semiquantitative assessment of collateral diameters would improve the prediction of collateral
function and be of clinical relevance. It should be compared
with established angiographic criteria by using the invasively
measured collateral function as the reference.
herapeutic approaches to induce collateral development
in humans1–3 require refined methods to assess collaterals in vivo.4,5 The most widely used method to assess
coronary collaterals is contrast angiography.4,6,7 The direct
measurement of collateral function with the use of miniaturized sensors of coronary flow and pressure distal to an
occlusion8 –12 is superior to angiographic assessment,13,14 but
it can be performed only during a coronary intervention. In
principal, this method can evaluate the induction of collateral
development, but it requires balloon occlusion to assess
collateral function,15 which limits its applicability.
A recently reported quantitative angiographic analysis of
collateral diameters on high-resolution cine films underscored the relevance of the collateral diameter for the collateral function. Aside from the complexity of this approach, its
applicability to modern digital storage standards with lower
resolutions is limited.16 Still, a semiquantitative assessment of
the collateral diameters as suggested three decades ago in this
journal17 may improve the angiographic assessment of col-
Methods
Patients
Collateral flow was analyzed in 103 patients during recanalization of
a TCO in one of the major coronary arteries. All TCOs had a
duration of ⬎2 weeks, TIMI grade 0 flow, and spontaneously visible
collaterals. The duration of the occlusion was defined by a prior
myocardial infarction (MI) or the onset of chest pain before the
diagnostic angiography. Three patients had been excluded from the
subsequent analysis because angiograms were of insufficient quality
to clearly define the collateral pathways as described below, leaving
100 patients for the data analysis. The study was approved by the
institutional ethics committee, and informed consent obtained from
all patients.
Received October 28, 2002; revision received January 28, 2003; accepted February 3, 2003.
From the Clinic for Internal Medicine III, Friedrich-Schiller-University Jena, Jena, Germany.
Correspondence to Gerald S. Werner, MD, Klinik für Innere Medizin III, Friedrich-Schiller-Universität, Erlanger Allee 101, D-07740 Jena, Germany.
E-mail [email protected]
© 2003 American Heart Association, Inc.
Circulation is available at http://www.circulationaha.org
DOI: 10.1161/01.CIR.0000061953.72662.3A
1972
Werner et al
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Figure 1. A, Collateral connection through septal branches from
the left anterior descending artery (LAD) to branches of the posterior descending artery (PDA; arrow) is not continuously visible
and is interrupted at arrowheads: CC0. B, Continuous threadlike
connections of septal branches from PDA to LAD (arrows): CC1;
similarly sized connections from right ventricular branch to distal
LAD (arrowheads): CC1. C, Patient with LAD occlusion and
numerous collateral connections from PDA, some side branch
size (arrows: CC2), some of smaller size (arrowheads: CC1). D,
Continuous threadlike connections of marginal side branches of
the left circumflex artery (LCX) to diagonal branches of proximally occluded LAD (arrows): CC1. E, Patient with LAD occlusion and supply through right ventricular branch of RCA
(arrows), with threadlike collateral connection (arrowhead: CC1).
F, Continuous side branch–like connection (arrows) between
LCX and marginal branch of occluded RCA (arrowhead): CC2.
Angiographic Assessment of Collaterals
All angiographic studies were done with a Philips biplane cine
system (DCI or Integris), with a 7-inch field size. The view with the
least foreshortening of the collateral connection was selected for
analysis. Angiograms were stored on digital media in DICOM
format (512⫻512 matrix) and analyzed as follows:
(1) The collateral filling of the recipient artery was assessed
according to Rentrop and Cohen.7 All collaterals in TCOs were
either Rentrop grade 2 (partial epicardial filling of the occluded
artery) or 3 (complete epicardial filling of the occluded artery).
(2) The anatomic pathways were categorized according to Levin’s
26 different pathways6 and then summarized in 4 categories: septal,
intra-arterial (bridging), epicardial with proximal takeoff (atrial
branches), and epicardial with distal takeoff.16 In the case of
coexisting collateral pathways, the principal pathway was defined as
the one that was the first to opacify the occluded epicardial segment.
(3) The size of the collateral connection (CC) diameter was
assessed by 3 grades: CC0, no continuous connection between donor
and recipient artery; CC1, continuous, threadlike connection; and
CC2, continuous, small side branch–like size of the collateral
throughout its course (Figure 1). To provide a size estimate, the
collaterals were measured with an electronic caliper on enlarged still
images: CC1 collaterals had diameters ⱕ0.3 mm and CC2 ⱖ0.4 mm.
Interobserver Variability for Collateral
Connections Size
The two best views of the collaterals supplying an occluded segment
were selected by one investigator and then reviewed independently
by two others. The physiological data on collateral function were not
known to the investigators at the time of review. The agreement in
grading was 88%, 92%, and 91% among the 3 investigators.
Doppler and Pressure Recordings
The recanalization procedure was done as previously described.12,18
After the lesion was crossed by a guidewire, an exchange catheter
(Transit Cordis) or a low-profile over-the-wire balloon catheter
Angiographic Assessment of Coronary Collaterals
1973
(Bandit, Scimed) was passed distal to the occlusion. The guidewire
was exchanged for a Doppler guidewire (FloWire, EndoSonics
Corporation). The first 21 patients of this consecutive series were
assessed by Doppler measurements only and subsequent patients by
both Doppler and pressure measurements. In these patients, the
Doppler wire was exchanged for a pressure wire (PressureWire,
RADI Medical Systems). After these recordings, the occlusion was
dilated and treated by stent implantation. Finally, the Doppler
guidewire was reintroduced and the antegrade coronary flow was
recorded.
Doppler flow signals were analyzed as described previously.18 A
collateral flow index (CFI) was obtained before and after PTCA as
the ratio of average peak velocity (APVD) distal to the occlusion and
antegrade APV recorded after completion of PTCA.11 From the ratio
of the mean distal coronary pressure (PD) and the mean aortic
pressure (PAo), obtained through the fluid filled guiding catheter, the
collateral pressure index (CPI) was calculated at baseline and during
balloon reocclusion9,11 (Figure 2). The collateral resistance index
RColl was calculated, assuming steady laminar flow and constant
vessel diameters, as (PAo⫺PD)/APVD10,12,19,20 (with a physical dimension of mm Hg/cm per second).
Assessment of Recruitable Collateral Function
The above-described recordings were repeated during reinflation of
the stent balloon to obtain the recruitable collateral flow in 87
patients with Doppler and in 72 with additional pressure recordings.
These measurements were done 38⫾13 minutes after the baseline
recording. The identical location of the sensor wires for all recordings was ascertained by fluoroscopy.
Collateral Flow Reserve
In 51 patients, collateral flow was assessed before balloon dilation
during intravenous administration of adenosine (140 ␮g/kg per
minute) over a period of 3 minutes by Doppler and pressure
recording, as previously described.21 The ratio of APV during
adenosine and APV at baseline was the collateral flow reserve, a
value ⬍0.95 indicated coronary steal.
Quantitative Angiography
Biplane left ventricular (LV) angiograms were obtained in all
patients at the time of the baseline diagnostic angiography. The
quantitative LV analysis was done with standard software (LVA 4.0,
Pie Medical Imaging). LV ejection fraction (LVEF) was calculated,
and the centerline method was applied to analyze the territory of the
occluded artery by the regional wall motion severity index (SD/
chord) and the extent of regional dysfunction (number of chords).22
Statistics
Data are mean⫾SD if not indicated otherwise. Group differences of
continuous variables were evaluated by ANOVA and of categoric
variables by Fisher’s exact test. A GLM ANOVA was used to
analyze covariate effects of the angiographic criteria of collateral
grading on quantitative parameters of collateral function. Post hoc
analysis was done with the Scheffé test. A level of P⬍0.05 was
considered significant. All calculations were done with SPSS for
Windows (Version 10, SPSS Inc).
Results
Angiographic Assessment of Collateral Pathways
In 100 patients, 211 different collateral pathways were
identified; 86% of patients had more than one distinct
pathway (Table 1). The subsequent analysis included only
one principal pathway per patient, which was through septal
connections in 44%, atrial epicardial connections in 32%,
distal interarterial connections in 18%, and bridging connections in 6%. Collateral connection grade CC0 was observed in
14%, CC1 in 51%, and CC2 in 35%. CC2 was observed less
1974
Circulation
April 22, 2003
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Figure 2. Angiography of collateral connections,
Doppler, and pressure recordings (PAO and PD)
distal to TCO. A, Patient with proximal LAD
occlusion collateralized from right ventricular
branch of the RCA (arrows: CC2) and additional
septal and proximal connections (arrowheads:
CC1); predominantly diastolic Doppler flow pattern, high amplitude PD. B, Patient with occluded
RCA and filling of PDA (arrowheads) through
septal branches from LAD with discontinuation of
connections (arrows: CC0); predominantly systolic, retrograde Doppler flow pattern, and low
amplitude PD.
frequently in septal than in epicardial pathways (23% versus
45%) and CC0 more frequently (23% versus 7%; ␹2 P⫽0.02).
The filling of the occluded epicardial segment was graded as
Rentrop grade 2 in 22% and grade 3 in 78%. There was a
TABLE 1. Clinical Characteristics of 100 Patients With Chronic
Total Coronary Occlusions
Age, y
Male gender, %
63.4⫾10.4
76
No. of diseased arteries, 1/2/3
40/40/20
Occluded coronary artery, right/LAD/LCX
57/38/5
Previous MI, %
65
Angina pectoris (CCS 0–4)
0/4/40/55/1
Heart failure (NYHA 0–4)
2/37/42/19/0
Diabetes, %
37
Hypertension, %
67
significant but weak correlation between CC grade and the
Rentrop grading (r⫽0.32; P⬍0.001).
Collateral Pathways and LV Function
The relation of regional LV function and the collateral size
could be assessed in 35 patients in whom the collaterals had
prevented a Q-wave MI. None had CC0 collaterals, and the
duration of occlusion tended to be longer in CC2 collaterals
(P⫽0.13). Patients with CC2 collaterals had less severe wall
motion abnormalities than with CC1 collaterals (Figure 3). In
patients with prior Q-wave MI, the extent of regional wall
motion abnormality was not related to the CC grades. In the
latter patients, the CC grade was closely related to the
duration of TCO, with CC0 observed predominantly in TCOs
of ⬍4 weeks’ duration and CC2 predominantly in TCOs of
⬎12 weeks’ duration (Table 2).
Hypercholesterolemia, %
73
Collateral Pathways and Collateral Function
History of smoking, %
44
The parameters of collateral function were characteristically
different in the three CC grades (Table 3). The Doppler
parameter APV and CFI were lowest in CC0 but comparable
between CC1 and CC2, whereas the pressure parameter PD
and CPI were comparable between CC0 and CC1 but highest
Ejection fraction, %
56.6⫾17.8
CCS indicates Canadian Cardiovascular Society classification of chest pain;
LAD, left anterior descending; LCX, left circumflex; and NYHA, New York Heart
Association classification of heart failure.
Werner et al
Angiographic Assessment of Coronary Collaterals
1975
patients with CC2 collaterals and in 61% with CC1 collaterals
(P⫽0.16).
Recruitable Collateral Function and Collateral
Connection Size
The recruitable collateral function after recanalization
showed considerable and specific differences between the
collateral connection grades (Table 3). The APV that had
been similar for CC1 and CC2 at baseline decreased significantly in CC1, and it was further decreased in CC0. The
recruitable RColl increased in all three groups as compared
with baseline, but the amount of increase was lowest with
CC2 and highest with CC1 (Figure 5).
Discussion
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The present study analyzed the relation of collateral pathway
anatomy, the collateral diameter, and the recipient artery filling
with the invasively assessed collateral function in TCOs. We
propose a visual grading of the size of collateral connections that
discriminates collaterals with different functional capacity.
Figure 3. Relation between collateral connection grade and
regional wall motion abnormalities in patients without prior MI
(top) and with prior MI (bottom). Note different scales for subgroups. Columns to the left represent extent and to the right
severity of wall motion abnormality. Values are mean⫾SEM;
patient numbers are shown in brackets.
in CC2. RColl was highest in CC0 and lowest in CC2 (Figure
4). A potential influence of the LV end-diastolic pressure on
intracoronary pressure measurements was unlikely because it
was similar in the 3 groups (CC0: 16⫾7; CC1: 14⫾8; CC2:
14⫾10 mm Hg; P⫽0.7).
A univariate ANOVA comparing the influence of Rentrop
grades, CC grades, and anatomic location on RColl showed that
the CC grade was a better predictor of a low RColl (r2⫽0.32;
P⬍0.001) than Rentrop grade (r2⫽0.10; P⫽0.12) or anatomic
location of the collaterals (r2⫽0.07; P⫽0.65). The number of
individual collateral connections within each CC group did
not further improve the prediction based on the CC grade.
Pharmacological Modulation of Collateral Flow
Maximum decrease of the peripheral microvascular resistance during adenosine infusion in 51 patients did not change
APV with CC0 collaterals. Adenosine caused a decrease of
APV with CC1 collaterals from 10.0⫾5.4 to 8.8⫾4.3 cm/s
and an increase with CC2 collaterals from 11.7⫾5.5 to
13.6⫾9.4 cm/s (ANOVA: P⫽0.06). A collateral flow reserve
⬍0.95 indicating coronary steal was observed in 33% of
TABLE 2. Collateral Connection Grades and Duration of
Occlusion in 65 Patients With Prior Q-Wave MI
The most accurate way to assess collaterals would be a
quantitative angiography, which is not applicable to modernday digital storage media with a resolution limit ⬎0.2 mm
given the small diameter of collaterals and the often tortuous
course of the collateral connections.16 In TCOs with welldeveloped, spontaneously visible collaterals, the widely used
Rentrop grading lacks further differentiation because most
collaterals are grade 3. A measure of the collateral diameter
should enhance the semiquantitative assessment as first suggested by Carroll et al.17 Therefore a visual grading of the
diameter of collateral connections was used in our study, with
an interobserver variability of about 10%.
The Rentrop grading shows only a weak correlation with
invasive parameters of collateral function.13,14 Other methods
for the angiographic assessment of collaterals such as the
bifurcation count, collateral length estimation, and collateral
frame count have not been compared with invasive methods.4,23 A frame counting of contrast medium washout distal
to a balloon occlusion by recruitable collaterals was shown to
correlate well with invasive collateral function, but it requires
an interventional procedure.24 The goal of the present study
was instead to evaluate an angiographic grading that would
be applicable during diagnostic angiography. Furthermore,
attempts to induce collateral development will aim at vascular
territories in need of constant collateral perfusion distal to
TCOs not accessible to revascularization, and the TCOs of
our study represent a model for this situation.
Clinical Relevance of the Collateral Connection Grade
Duration of Occlusion
2– 4 Weeks
⬎4 –12 Weeks
⬎12 Weeks
CC grade 0
12
2
CC grade 1
9
9
䡠䡠䡠
8
CC grade 2
5
2
18
␹2 Value⫽23.4; P⬍0.001.
Angiographic Assessment of Collaterals
Well-developed collaterals should preserve LV function in
the incidence of an occlusion, but many collaterals develop
after an occlusion had already caused an acute MI.25,26
Therefore, we assessed the prediction of collateral adequacy
to preserve LV function by this new grading system in a
subgroup of patients without a prior MI. Only CC1 and CC2
collaterals were found in these patients, and the regional wall
motion was best preserved with grade CC2 collaterals.
1976
Circulation
April 22, 2003
TABLE 3. Quantitative Assessment of Collateral Function in Chronic Total
Coronary Occlusions With Different Collateral Size Grades Before and
After Recanalization
Collateral Connection
Grade 0
Grade 1
Grade 2
11.9⫾6.5
11.8⫾5.0
Baseline
APV, cm/s
6.3⫾3.6*§
PD, mm Hg
35⫾12‡
41⫾11‡
54⫾13
0.32⫾0.26
0.44⫾0.27
0.44⫾0.27
CPI
0.33⫾0.09‡
0.39⫾0.11‡
0.52⫾0.09
RColl, mm Hg/cm per second
14.5⫾7.1*‡
7.2⫾4.4
5.2⫾3.0
3.5⫾2.3‡
5.6⫾2.7‡
8.7⫾5.6
CFI
Reocclusion
APV, cm/s
PD, mm Hg
CFI
26⫾9‡
32⫾10‡
45⫾14
0.17⫾0.11§
0.19⫾0.11‡
0.33⫾0.26
0.44⫾0.12
CPI
0.25⫾0.08‡
0.29⫾0.09‡
RColl, mm Hg/cm per second
33.9⫾21.7*†
16.8⫾9.2储
9.5⫾6.1
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PD indicates distal coronary pressure; RColl, collateral resistance index. Significant differences
compared with grade 1: *P⬍0.001, †P⬍0.05; compared with grade 2: ‡P⬍0.001, §P⬍0.01,
储P⬍0.05.
In patients with a prior MI, collaterals had not been
sufficient to prevent the MI and most likely developed fully
after the occlusion. We have recently shown that collateral
function improves between 4 and 12 weeks after an acute
MI.12 This is further supported by the present study, which
contained also patients 2 to 4 weeks after an occlusion. There
was a significant relation between the collateral connection
grade and the duration of the occlusion with CC0 collaterals
representing early stages of collateral development and CC2
collaterals representing mature collaterals.
The relevance of the collateral connection grades was
further supported by the differential response to adenosine.
An increase of collateral flow by adenosine occurred predominantly in CC2 collaterals. However, these changes showed
wide variations, which is explained by the multiple factors
influencing the adenosine response such as the donor artery
resistance and the peripheral vasodilation of the donor and
recipient vascular beds.21
Collaterals in TCOs lose part of their functional capacity
immediately after recanalization.12,18,27 The observation that
patients who had CC2 collaterals before recanalization had
the best and those with CC0 collaterals had the lowest
recruitable collateral function is further support for the
clinical relevance of this new grading. In CC2 collaterals,
invasive function indexes remained above the values reported
to prevent ischemia.9,11 In analogy to animal studies, CC2
collaterals probably will have a well-developed vascular wall
structure, whereas CC0 collaterals represent those with only a
rudimentary wall structure.28,29 CC2 collaterals retain their
responsiveness to influences such as increased shear stress
during reocclusion, whereas CC0 collaterals probably collapse after recanalization and do not immediately reopen
during reocclusion.
Limitations of the Study
The RColl is not identical to the collateral resistance derived
from quantitative angiographic data,16 but it describes the
resistance of the combined collateral network including the
donor artery segment proximal to the collateral takeoff. The
majority of patients show multiple collateral pathways, and
the location of the Doppler sensor distal to the occlusion will
detect flow that may enter this segment at various locations
Figure 4. Individual data and group
mean⫾SD of average peak velocity (left),
collateral pressure index (middle), and
collateral resistance index (right) for the
three collateral size grades.
Werner et al
Figure 5. Increase of RColl from baseline to reocclusion
(mean⫾SEM). RColl increased more with CC0 compared with
CC1 and CC2 (repeated-measures ANOVA: *P⬍0.001). It
increased least with CC2 compared with CC1 (†P⫽0.019).
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and will not be the result of one but rather the sum effect of
all relevant collaterals. Therefore, the interindividual variability (Figure 4) may be explained by this collateral interference.
During reocclusion, a lower APV was recorded, which may
be influenced by a changed vascular diameter at the site of
measurement both at baseline and during reocclusion. However, the drop of PD supports the conclusion of genuine
differences in recruitability. A limitation of the pressurederived indexes is that we did not simultaneously record the
central venous pressure.
We used only one principal pathway with the highest CC
grade of the coexisting multiple pathways to categorize our
patients. Theoretically, the 2 to 3 largest collateral connections would determine the collateral conductance,16 but the
additional consideration of the number of collaterals within
each CC grade did not further improve the discrimination of
collateral function parameters.
Conclusions
The angiographic collateral connection grades provide an
additional parameter to describe spontaneously visible collaterals in TCOs. This grading showed a close association with
clinical determinants of collateral adequacy. It could be also
of clinical relevance because CC2 collaterals identified patients with well-recruitable collaterals, which may protect
myocardium in the case of an acute reocclusion. These
observations were made in TCOs, and the applicability of this
angiographic method to collaterals in nonocclusive lesions
and to the assessment of pharmacologic agents or growth
factors on collateral function is not yet established.
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Circulation. 2003;107:1972-1977; originally published online March 24, 2003;
doi: 10.1161/01.CIR.0000061953.72662.3A
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