1. 3
Division of Pediatric Cardiology, Department of Pediatrics, MedicalUniversity of South Carolina, Charleston, South
Carolina
Although the structure and function of the coronary vasculature has been exhaustively
studied, it still holds significant elements of mystery for the researcher and clinician.
This is particularly true regarding the structure and function of the human collateral coronary
circulation. Controversy still exists concerning the pathways of collateral vessels as well as their
function. Contro- versies also exist relative to the methods used to delineate the pathways,
these being additionally compounded by the lack of standardization of the studies and
measurements. In this review, we summarize our current knowl- edge of this functionally
significant vascular network. Clin.Anat. 22:146–160,
2009. V
C 2008 Wiley-Liss, Inc.
Key words: arteriogenesis; angiogenesis; collateral circle of Vieussens; artery
of Kugel; myocardial infarction
Confirmation of the existence of collateral circula- tion,
however, left several unanswered questions. Queries sprouted
regarding the physiological func- tion of these vessels as well
as their distribution, histology, and anatomy. Early hypotheses,
due to limited techniques and knowledge, were vague. With
time, and advancing technology, more accurate assessments have
been made, albeit that, as we will discuss, much still remains
unanswered.
INTRODUCTION
It was Richard Lower who first demonstrated, in the 17th
century, the presence of anastomoses between the coronary
vessels, when he made the astute observation that fluid injected
into one coro- nary artery would inevitably become present in
the other (Tubbs et al., 2008). Although his observation was
endorsed in the 18th century by Albrecht von Haller, a Swiss
anatomist, subsequent investigators of the 19th century, using
human cadavers for their studies, wrongly declared that
2. interventricular artery.
An artery joining the infundibular branch of the right
coronary artery to the anterior interven-
tricular artery.
An artery passing between a diagonal branch of the
anterior interventricularartery and the distal
part of anterior interventricular artery.
An artery running from the inferior interventric- ular
branch of the right coronary artery and extending
around the cardiac apex to join the
anterior interventricular artery.
Anastomoses between the inferior interventricu- lar branch
of the right coronaryartery and the
anterior interventricular artery through the ven- tricular
septal arteries.
Levin (1974) relied on the arteriograms obtained from
patients with significant coronary arterial dis- ease when making
his classification. On the basis of these studies, he compiled a
list of 22 anastomoses. Several of the identified collateral
arteries are simi- lar, being mentioned twice because they were
visual- ized in patients with different coronary arterial occlu-
sions. His study also excluded many collateral origi- nating from
the circumflex coronary artery, as they could not be well
visualized. He noted the following collateral arteries in
patients with significant occlu- sion of the right coronary artery
(Fig. 1):
•
•
•
Collateral channels from the anterior interven- tricular
artery to the inferior interventricular branch of the right
coronary artery via septal branches.
Distal collateral arteries joining the circumflex to the right
coronary artery.
Collateral arteries running from the obtuse mar-
ginal branch of the circumflex artery to the infe- rior left
ventricular branches of the right coro- nary artery.
• •
He also noted additional collateral unions in indi- viduals
with severely stenosed circumflex arteries (Fig. 3 ):
•
•
Collateral union of the left atrial circumflex branch to the
distal part of the circumflexartery. Collateral arteries
running from the proximal obtuse marginal branch of
the circumflexartery to a more distal obtuse marginal
branch. Collateral communications between a diagonal
branch of the anterior interventricular artery and the
obtuse marginal branch of the circum- flex artery.
Arteries running between the distal parts of the right and
the circumflexarteries.
A collateral artery running from the inferior
interventricular branch of the right coronary ar-
tery to the obtuse marginal branch of the cir- cumflex
artery.
•
•
A proximal
marginal or
communication from the acute
infundibular branches of the right
•
coronary artery to a more distal acute marginal branch.
Kugel's Artery, which runs from the proximal
parts of the right or left coronary artery along the
anterosuperior margin of the oval fossa to anastomose
with the distal part of the right cor-
onaryartery.
An anastomosis from the distal part of the ante- rior
interventricular artery that extends around
the cardiac apex to join the inferior interventric- ular
branch of the right coronary artery.
•
•
•
•
•
Since this extensive compilation of collateral arteries
3. Fig. 1. Collateral pathways in right coronary (RC) obstruction.
RAO ¼ right anterior oblique projection; LAO ¼ left anterior
oblique projection; LC ¼ left coro- nary artery; AM ¼ acute
left anterior descending artery (anterior interventric- ular artery); C
¼ circumflex artery; OM ¼ obtuse mar- ginal branch of the
circumflex artery, D ¼ diagonal branch of the left anterior
4. Fig. 2. Collateral pathways in the left descending artery
obstruction. RAO ¼ right anterior oblique projec- tion; LAO ¼ left
anterior oblique projection; LC ¼ left coronary artery; AM ¼
left anterior descending artery (anterior interventric- ular artery); C
¼ circumflex artery; OM ¼ obtuse mar- ginal branch of the
circumflex artery, D ¼ diagonal branch of the left anterior
5. Fig. 3. Collateral pathways in circumflex artery obstruction.
RAO ¼ right anterior oblique projection; LAO ¼ left anterior
oblique projection; LC ¼ left coro- nary artery; AM ¼ acute
marginal branch of the right coronary; PD ¼ posterior descending
branch of the right coronary (inferior interventricular artery); PLV
¼ posterior left ventricular branch of the right coronary (inferior
left ventricular branch of the right coro- nary); A-V ¼ artery to the
atrioventricularnode; LAD ¼
left anterior descending artery (anterior interventric- ular artery); C
¼ circumflex artery; OM ¼ obtuse mar- ginal branch of the
circumflex artery, D ¼ diagonal branch of the left anterior
descending (diagonal branch of the anterior interventricular
artery). Bold captions in the parenthesis indicate the attitudi- nally
correct nomenclature of the coronary arteries (with permission
from Levin, 1974, Circulation 50:831-
837).
between the proximal parts of the right and left coronary
arteries. These collateral arteries also figures among those identified
by Levin (1974) (Figs. 8–12).
ate the sensibility in the assumption that there is no need to
name all the collateral arteries (James,
1965). The downside of this assumption lies in the danger
of bypassing information of clinical signifi-
cance. The location and function of common collateral patterns
can assist in both prognosis and surgical
intervention. Surgically, preservation of large, and
The artery to the sinus node also commonly pro-
vides a communication between the proximal parts of the right and
left coronary arteries. According to James (1965), this connection is
also comparable with one of those identified by Levin (1974).
6. connections between two independent arteries as anastomoses
(Schaper, 1971; Waltenberger,2001).
Paster (1977) divided the collaterals arteries into
four distinct groups, concentrating attention on aspects
often not considered within the normal scheme of the
collateral coronaryt arterial circula-
tion. His first group included the arteries traditionally described
as collateral arteries and included homo- coronary and
intercoronary variants. He emphasized that these arteries are
found throughout the myocar- dium, but not in the subepicardial
area. The second group consisted of arterioluminal vessels,
which con- nect coronary arteries to the cardiac chambers. He
designated his third class as extracardiac vessels. These are
derived from the arteries supplying the ar- terial trunks, the so-
called vasa vasorum and serve to join the cardiac circulation
with bronchial and mediastinal arteries. He named his last
group the transepicardial collateral arteries. These vessels arise
from pericardial adhesions or surgical granulations (Paster,
1977).
Another system, proposed by Rockstroh et al. (2002), also
divided the collateral arteries into four categories. He named
the arteries according to the
flow from the donor to the recipient artery and rec- ognized
septal, atrial, ventricular parietal, and bridg- ing patterns. He
also rated the diameters of the arteries on an arbitrary
numericalscale from one to three.
Still another system classified the arteries into four
categories, namely, bypass, interarterial, trans-
arterial, and scar arteries. Bypass arteries were described as
extending around a segment of arther-
oma to an area further down the same vessel. Inter- arterial
collaterals were those joiningbranches of the
same coronary artery. Transarterial arteries were those coursing
between the right and left coronary arteries, while scar arteries
Fig. 4. Artery of Kugel in a corrosion cast specimen. The Great
Cardiac Vein (CGV) joins the Middle Cardiac Vein (MCV) in the
Coronary sinus (Cs) and empties into the right atrium. The
Circumflex coronary artery (1) gives off several atrial branches (2)
which supply the right atrium. A prominent atrial branch crosses over
the coronary sinus (3) formingthe artery of Kugel.
1998). Additionally, collateral arteries arising from the anterior
interventricular artery are commonly damaged during the
7. Fig. 5. Artery of Kugel (**) in a coronary angio- gram. An
atrial branch originating from the proximal portion of the right
coronary artery anastomoses with a
branch of the inferior interventricular artery. Interest- ingly, the
artery of Kugel is best seen during coronary angiography or
corrosion cast techniques.
8. PHYSIOLOGICAL SIGNIFICANCE
As the quest continues to create a clear anatomi- cal map
of the collateral coronary arterial system, the question of its
physiological significance remains
unanswered.
arteries have
function, but
Since their initial recognition, the been
presumed to offer a protective evidence
supporting this notion has
been inconsistent. The vessels were ignored for sev- eral years
after their discovery, owing to presumed clinical insignificance.
Today, there is renewed inter-
Fig. 6. The right conal artery, branch of the right coro- nary artery
anastomoses with the left conal artery, branch of the anterior
interventricular artery forming the arterial circle or vascular ring of
Vieussens, a typical collateral ar- tery. est in their role along with numerous functional
assessment studies (Shaper and Shaper, 2004).
9. Early on, it was noted that highly developed col- lateral
arterial systems were more commonly found in autopsied hearts
from individuals with long-stand- ing coronary arterial disease,
suggesting the devel- opment of the collateral arteries to be
strongly corre- lated with slowly developing coronary arterial
obstruction (Maxwellet al., 1987; Rockstroh et al.,
2002; Koerselman et al., 2003; Baroldi et al., 2005). Large
numbers of collateral arteries have also most often been
observed in patients with severe coronary arterial narrowing
(Baroldi et al., 1956). A strong
correlation of slowly developing coronary obstructive
disease and extensive collateral development has been noted
in several studies. The conclusion reached by several
investigators is that a slowly forming occlusion allows for the
time collaterals need to form a functional nutritive bypass
(Maxwellet al.,
1987; Rockstroh et al., 2002; Koerselman et al.,
2003; Baroldiet al., 2005).
The arteries are presumed to form when its lumen becomes
constricted, usually because of the forma-
tion of atherosclerotic plaques. As the pressures increase
proximalto the constriction, preexistent col-
lateral vessels are forced open and begin to receive nutritive
flow. Constrictions developing slowly are
superior for development of collateral arteries, pre- sumably
because of the extended period during which the
myocardium retains its function. Con-
versely, infarction is usually the consequence of acute
occlusion, preventing the development of col- lateral arteries,
which require several days to
appear. In this sense, atherosclerosis can play a pro- tective role,
the subsequent appearance of the col-
lateral circulation protecting against infarction (Max- well et al.,
1987). This also raises doubt, however, regarding the long-
held belief that ischemia is
can skew results and make comparisons difficult. In addition,
the stages, sizes, and relative
dispersion of the collateral arteries have been proven to result in
significantly different functional effects.
As has been emphasized, the collateral arteries
develop slowly, and their function, reciprocally in- creases
with an enlarged diameter. In attempts
more fully to appreciate the significance and function of the
collateral channels, their mode of development achieves
significance. This process is unique and
highly specified. The different stages of development may well
impact on function, and hence be worthy of further discussion.
DEVELOPMENT OF THE COLLATERAL
CORONARY ARTERIAL CIRCULATION
The collateral arteries are derived from the same components
as the native coronary arteries during embryonic development,
and as such are histologi- cally indistinguishable.
Vasculogenesis is the process by which angioblasts form the
primary plexus, com- posed primarily of endothelial cells
(Koerselman et al., 2003). It is from this precursor that the
mature vasculature, including the collateral arteries, will arise.
The endothelial channels of the primary plexus grow via
sprouting and intussusceptions, eventually recruiting surrounding
mesenchymal cells and forming the mature coronary
vasculature (Shaper and Shaper, 2004).
The native coronary arteries develop in a clear pattern
from proximal to distal, mimicking the pat- tern of blood flow
through these vessels. Larger arteries develop first, and
successive branches fol- low. The collateral arteries do not
follow this pattern, as these unique bridging vessels can
10. Fig. 8. In this corrosion cast specimen, there are evident three
collateral arterial anastomoses. At the area of the subpulmonary
infundibulum the right conal artery, branch of the right coronary
artery anastomoses with the left conal artery branch of the
anterior inter- ventricular artery forming the arterial circle or
of the right coronary artery and the anterior interven- tricular artery
are forming a second collateral pathway (**). Finally, the marginal
artery of the right coronary artery, as well as the distal ventricular
branches of the right coronary artery anastomose with
ventricular branches of the op the distal portion of the anterior
11. Fig. 9. In this coronary angiography, there are evi- dent three
collateral arterial anastomoses. At the area of the subpulmonary
infundibulum the right conal ar- tery, branch of the right coronary
artery anastomoses with the left conal artery branch of the
anterior inter- ventricular artery forming the arterial circle or
vascular ring of Vieussens (*). As a result, there is contrast me-
dium at the proximal portion of the anterior interven-
tricular artery. Ventricular branches of the right coro- nary artery
and the anterior interventricular artery are forming a second
collateral pathway (**). Finally, ven- tricular branches of the
inferior interventricular artery anastomose with ventricular branches
of the distal por- tion of the anterior interventricular artery
(***).As a result, there is contrast medium at the distal portion of
the anterior interventricularartery.
12. Fig. 10. In this coronary angiography, there are evident two
collateral arterial anastomoses. At the area of the subpulmonary
infundibulum the right conal ar- tery, branch of the right coronary
artery anastomoses with the left conal artery branch of the
anterior inter- ventricular artery forming the arterial circle or
vascular
ring of Vieussens (*). Proximal ventricular branches of the right
coronary artery anastomose with the anterior interventricular artery
are forming a second collateral pathway (**). As a result of these
two pathways, there is contrast medium at the distal portion of the
anterior interventricular artery.
bypass vessels is determined by prevailing pressures and thus
moves toward the lower pressures located distal to obstructions.
Extended obstructions allow for more extensive vascular
remodeling. Larger obstructions, involving obstructions of up
tively slow process, producing low grade collaterals within 10
to 15 days following substantially reduced blood flow
(Bourassa et al., 1974, Werner et al.,
2004). As a result this mechanism is ineffective in protecting
13. Fig. 11. In this coronary angiography, there are evident three
collateral arterial anastomoses. At the area of the subpulmonary
infundibulum the right conal artery, branch of the right coronary
artery anastomoses with the left conal artery branch of the
anterior inter- ventricular artery forming the arterial circle or
vascular
ring of Vieussens (*). Ventricular branches of the right coronary
artery anastomose with the proximal (**) and distal portion (***) of
the anterior interventricular ar- tery forming two collateral pathways.
As a result, there is contrast medium at the anterior
interventricular artery.
respond to shear stress varies based on their level of
development when regression first occurred. Smaller vessels
nearly collapse after obstruction relief and require some time to
reopen. Larger, on the other hand, retain their responsiveness
and can reopen quite quickly in response to increased
mation of the new arteries is induced by ischaemia, rather than
pressure. The extent to which newly formed angiogenic
vessels assist in the formation of the collateral circulation
remains to established (Wal- tenberger, 2001; Helisch et al.,
2003).
14. Fig. 12. In this coronary angiography, there are evident three
collateral arterial anastomoses. Ventricu- lar branches of the right
coronary artery anastomose with the proximal (*), middle (**), and
distal portions
(***) of the anterior interventricular artery forming three
collateral pathways. As a result, there is contrast medium in the
anterior interventricularartery.
been elucidated, attempts to instigate the growth and
formation of new arteries have been fruitless (Helisch et al,
2003; Koerselman et al., 2003). Some factors that negatively
affect collateral growth and angiogenesis, such as diabetes, have
been identified. Perhaps increased understanding of these mecha-
nisms will allow for greater therapeutically relevant success
promised myocardium. Cardiovascular disease is a leading
killer in the developed world, and as such its vasculature bears
full comprehension.
REFERENCES
15. their branches. I. Arteria anastomotica auricularis magna. Am
Heart J 3:260–270.
Levin DC. 1974. Pathways and functional significance of the coro- nary
collateral circulation. Circulation 50:831–837.
Loukas M, Clarke P, Tubbs RS, Kapos T. 2007. Raymond de Vieus- sens. Anat
Sci Int 82:233–236.
May AM. 1960. Surgicalanatomy of the coronaryarteries. Dis Chest
38:645–657.
Maxwell MP, Hearse DJ, Yellon DM. 1987. Species variation in the coronary
collateral circulation during regional myocardial ischae- mia: A critical
determinant of the rate of evolution and extent of myocardial infarction.
Cardiovasc Res 21:737–746.
Meier P, Gloekler S, Zbinden R, Beckh S, de Marchi SF, Zbinden S, Wustmann
K, Billinger M, Vogel R, Cook S, Wenaweser P, Togni M, Windecker S,
Meier B, Seiler C. 2007. Beneficial effect of recruitable collaterals: A 10-
year follow-up study in patients with stable coronary artery disease
undergoing quantitative col- lateral measurements. Circulation 116:975–983.
Miller RR, Mason DT, Salel RF, Massumi RA, Amsterdam EA. 1972.
Determinants and functional significance of the coronary collat- eral
circulation in patients with coronary artery disease. Am J Cardiology
29:281.
Miyamoto S, Fujita M, Sasayama S. 2000. Bidirectional function of coronary
collateral channels in humans. Int J Cardiol 75:249–252.
Paster SB. 1977. The coronary collaterals: Their development, mor- phology,
function, and classification. CRC Crit Rev Diagn Imag- ing 9:51–76.
Tubbs RS, Loukas M, Shoja MM, Adralan MR, Oakes WJ. 2008. Rich- ard Lower
(1631–1691) and his early contributions to cardiol- ogy. Int J Cardiol
128:17–21.
Wainwright RJ, Maisey MN, Edwards AC, Sowton E. 1980. Functional
significance of coronary collateral circulation during dynamic exercise
evaluated by thallium-201 myocardial scintigraphy. Br Heart J 43:47–55.
Werner GS, Ferrari M, Heinke S, Kuethe F, Surber R, Richartz BM, Figulla
HR. 2003. Angiographic assessment of collateral connec- tions in comparison
with invasively determined collateral func- tion in chronic coronary
occlusions. Circulation 107:1972–1977.
Werner GS, Surber R, Ferrari M, Fritzenwanger M, Figulla HR. 2006.
The functional reserve of collaterals supplying long-term chronic total
coronary occlusions in patients without prior myocardial in- farction. Eur
Heart J 27:2406–2412.
Waltenberger J. 2001. Impaired collateral vessel development in di- abetes:
Potential cellular mechanisms and therapeutic implica- tions. Cardiovasc Res
49:554–560.
Werner GS, Jandt E, Krack A, Schwarz G, Mutschke O, Kuethe F, Ferrari M,
Figulla HR. 2004. Growth factors in the collateral circulation of chronic
total coronary occlusions: relation to dura- tion of occlusion and collateral
function. Circulation 110:1940–
1945.
Yacoub MH, Klieverik LM, Melina G, Edwards SE, Sarathchandra P, Bogers AJ,
Squarcia U, Sani G, van Herwerden LA, Takkenberg JJ.
2006. An evaluation of the Ross operation in adults. 15:531–539.
