The Embryologic Origin of Vieussens’ Ring

Abstract: Vieussens’ ring is an embryologic remnant that acquires clinical significance as an intercoronary collateral vessel in advanced coronary artery disease. Its origin as a peritruncal structure early in embryologic development, and its association with congenital pulmonary artery fistula, provides a crucial insight into the early stages of the coronary circulation. This review describes the embryologic basis of Vieussens’ ring in relation to the formation of the coronary arteries, which explains its location, appearance, and clinical importance.

J INVASIVE CARDIOL 2019;31(3):49-51.

Key words: arteriogenesis, collaterals, embryology

In patients with a severe stenosis or total occlusion of the left anterior descending (LAD) coronary artery or right coronary artery (RCA), the conus artery may be the origin of a rich collateral network at the base of the heart circling the great vessels. The course of this collateral pathway appears to partially form a large, ring-shaped structure around the pulmonary outflow tract.¹ This structure is termed Vieussens’ ring, or the arterial circle of Vieussens2 (Figures 1 and 2), after its first description 300 years ago by anatomic dissection.^2,3 This collateral system connects the LAD to the RCA, allowing preserved flow despite significant obstruction in either vessel. In some cases, anomalous LAD to pulmonary artery fistula has been categorized as originating from Vieussens’ ring.^4-6 No other association with congenital heart disease has been described.

Since collaterals are generally considered to be the product of vascular remnants that have matured (arteriogenesis) rather than new vessels (neovascularization), the existence of this uniquely shaped structure instinctively raises the question of its origin. This review describes the embryologic basis of  Vieussens’ ring in relation to the formation of the coronary arteries, which elucidates its location and appearance, as well as its importance clinically.

Significance of Vieussens’ Ring Collaterals

Raymond de Vieussens (1641-1715) was a French physician and anatomist who contributed numerous original observations of cardiac and neurologic anatomy and physiology.^2,3 In 1706, he noted several important new cardiac findings, including a vascular connection of the conus branch of the RCA circling around the aorta to the left arterial system. Contemporary angiographic and computed tomographic (CT) imaging demonstrates the origin of Vieussens’ ring either in a conus branch of the RCA or as a separate conus artery. The vessel then passes anteriorly and superiorly to the right ventricular outflow tract, and joins the LAD before it enters the interventricular groove (Figures 1 and 2).^7-9 The defining features of the ring are: (1) the vessel passes around the conus, or infundibulum of the right ventricle; and (2) the vessel then anastomoses with the LAD in its proximal portion.

This vascular network is present most often in the context of LAD occlusion. It provides collateral blood flow to the myocardium distal to the occlusion, reducing ischemia and protecting the myocardium from infarction. It is present in about 5% of cases in some series^9,10 and is visualized by opacification through selective angiography of the conus artery or CT scanning. Its recognition may provide important diagnostic and therapeutic information in cases of chronic left main or LAD occlusion.

Vieussens’ Ring and the Embryologic Origins of the Coronary Arteries

The traditional theory of coronary artery development is that these vessels originate from a bud that evaginates in the cusps of the aortic root after septation of the truncus arteriosus and develop outward into the surrounding myocardium.^11-14 The hypothesized mechanism is that endothelial tissue grows out of the aortic wall and connects with the subepicardial vessel plexus during myocardial development.

However, recent findings suggest that coronary arteries develop from a peritruncal ring of coronary artery vasculature and grow inward toward the aortic sinuses.^11-14 In this theory, myocardial vessels arise in situ and connect retrograde with the aorta. The peritruncal ring is precisely in the location seen in adults as a collateral; thus, it is undoubtedly the embryologic origin of Vieussens’ ring, which re-emerges as a collateral network late in life with the occurrence of obstructive coronary artery disease.

The epicardial coronary arteries develop by angiogenesis, in which mesenchymal cells in the subepicardial space give rise to a network of vessels on the myocardial surface. Endothelial sprouts from this network approach the outflow tract and connect with the aortic root sinuses. Vessels that develop tunica media and adventitia persist, while those that do not develop media and adventitia regress.¹⁵

The ultimate course of the coronary arteries is determined by their formation from three vascular circles: (1) the atrioventricular circle, which forms the RCA and the left circumflex artery; (2) the interampullary circle, which gives rise to the anterior and posterior descending coronary arteries; and (3) the conotruncal circle, which persists as the circle of  Vieussens. The peritruncal plexus communicates with the lumen of the truncus arteriosus by way of the coronary ostia and also anastomoses with the other two coronary arterial circles, thereby establishing the definitive coronary arterial circulation.

In the most currently widely accepted theory, the coronary arteries have a dual origin – both proximally and distally. The distal vascular network appears first in the interventricular and atrioventricular grooves and then communicates with the extracardiac great vessels. With persistence of some vessels and regression of others, the final coronary arterial pattern develops.

Ando¹⁵ demonstrated in embryonic quail heart studies that the proximal coronary arteries form as a result of angiogenesis (rather than neovascularization), wherein endothelial strands originate from the peritruncal ring, which penetrate the aortic sinuses. Tian¹⁶ found that this process of vascular remodeling of peritruncal endothelial cells also takes place in mammalian heart models. In both of these studies, the peritruncal ring was found to connect with subepicardial sinusoidal structures, which encircled both the pulmonary and aortic trunks.

The distal coronary vascular network induces the formation of coronary buds in the truncus arteriosus in the embryo by 9 weeks.^3-5 The epicardial coronary plexus grows proximally with the coronary network, forming a ring around the truncus arteriosus. The formation of the connections to the coronary buds in the truncus occurs rapidly; the attachment preferentially involves those that arise from the sinuses of  Valsalva in the aortic positions adjacent to the pulmonary trunk as the truncus partitions. These locations are most common, possibly as a consequence of the particular morphologic configuration of the bud at these sites.

Anomalous pulmonary artery fistulas are likely the result of a connection to a bud arising close to the anatomically correct ones, but that are partitioned into the pulmonary artery. It is notable that the posterior pulmonary artery sinus is directly adjacent to the left aortic sinus. The presence of such vessels connecting to a ring structure at the base of the heart is an extraordinary clue into the origin of coronary arterial embryogenesis.^4,17

The Conus Coronary Artery

Descriptions of  Vieussens’ arterial ring in adults, including the original description, depend on the presence of the conus artery giving rise to the structure. The conus artery is often a minor branch of the RCA, but has a separate origin in 50% of adults. Previous studies have suggested that it is embryologically a “third coronary artery.”^7,18,19 The conus artery begins anteriorly, either as a proximal branch of the RCA or as a vessel with an independent ostium, and courses anteriorly and superiorly to provide coronary perfusion to the pulmonary infundibulum. It anastomoses with the LAD to form the peritruncal ring. This circle (or ring) in the embryo communicates with the lumen of the truncus arteriosus and anastomoses with the atrioventricular and interampullary circles.^19,20 Vieussens’ ring is not angiographically demonstrable in most adults, but has been reported in the majority of adults by careful post mortem dissection.¹² Collateralization via this network to a clinically meaningful extent has been reported^1,7-10 when coronary artery disease is present.

Mechanism of Collateral Vessel Formation

The formation of collateral coronary vessels is a multifactorial process, influenced by the severity of coronary artery stenosis and duration of ischemia. As a response to these physiologic triggers, collaterals arise from a combination of arteriogenesis and angiogenesis. Angiogenesis is the development of new coronary capillaries induced by ischemia. Arteriogenesis, by comparison, is the remodeling of pre-existing pathways that were present in the sinusoids of the embryologic myocardium. During development, the majority of the heart muscle is a sponge-like meshwork of interwoven myocardial fibers. As normal development progresses, these trabeculated structures undergo significant compaction that transforms them from spongy to solid. The sinusoidal pathways therefore never disappear, but exist in a vestigial state, which can later serve as the origin of collateral pathways.

The process of collateralization is driven by increased shear stress within the vessels caused by a pressure gradient resulting from main branch stenosis. The increased shear stress results in activation of collateral arteriolar endothelium cytokines (NO, EDGR1, ICAM) that promote vascular proliferation.²¹ Once formed, these vessels conduct flow on the basis of classical pressure and resistance hemodynamics. In Vieussens’ ring, the embryologic conotruncal plexus therefore re-emerges as a collateral with clinical significance.

Conclusion

Vieussens’ ring is an embryologic remnant that acquires clinical significance as a collateral vessel in advanced coronary artery disease. Moreover, its origin as a peritruncal structure early in embryologic development and its association with congenital pulmonary artery fistula provide crucial insights into the early stages of the coronary circulation.

References

1. O’Leary EL, Garza L, Williams M, McCall D. Images in cardiovascular medicine. Vieussens’ ring. Circulation. 1998;98:487-488.
2. Parker J. Raymond de Vieussens (1641-1715) French neuroanatomist and physician. JAMA. 1968;206:1785-1786.
3. Loukas M, Clarke P, Tubbs RS, Kapos T. Raymond de Vieussens. Anat Sci Int. 2007;82:233-236.
4. Klein LW. A new hypothesis of the developmental origin of congenital left anterior descending coronary artery to pulmonary artery fistulas. Catheter Cardiovasc Interv. 2008;71:568-571.
5. Hirzallah MI, Horlick E, Zelovitzky L. Coronary artery to main pulmonary artery fistulae via a Vieussens’ arterial ring. J Cardiovasc Comput Tomogr. 2010;4:339-341.
6. Lee HY, Cho SH. An unusual form of coronary artery fistula: a small aneurysm of Vieussens’ arterial ring communicating with the pulmonary artery. Korean J Thorac Cardiovasc Surg. 2014;47:152-154.
7. Yamagishi M, Haze K, Tamai J. Visualization of isolated conus artery as a major collateral pathway in patients with total left anterior descending artery occlusion. Cathet Cardiovasc Diagn. 1988;15:95-98.
8. Deora S, Shay S, Patel TM. “Arterial circle of Vieussens” – an important intercoronary collateral. Int J Cardiol Heart Vessel. 2014;3:84-85.
9. Germing A, Mugge A. Images in cardiology: Vieussens’ ring. Clin Cardiol. 2003;26:441.
10. Singla R, Sasidharan B. Vieussens’ ring from isolated conus artery. Indian Heart J. 2013;65:482-483.
11. Loukas M, Groat C, Khangura R, Owens DG, Anderson RH. The normal and abnormal anatomy of the coronary arteries. Clin Anat. 2009;22:114-128.
12. Chiu IS, Anderson RH. Can we better understand the known variation in coronary arterial anatomy? Ann Thorac Surg. 2012;94:1751-1760.
13. Silva GO Jr, Miranda SWS, Lacerda CAM. Origin and development of the coronary arteries. Int J Morphol. 2009;27:891-898.
14. Hutchins GM, Kessler-Hanna A, Moore GW. Development of the coronary arteries in the embryonic human heart. Circulation. 1988;77:1250-1257.
15. Ando K, Nakajima Y, Yamagishi T, Yamamoto S, Nakamura H. Development of proximal coronary artery in quail embryonic heart. In: Cardiovascular Development and Congenital Malformations. Artman M, Benson DW, Srivastava D, Nakazawa M (eds). Blackwell Publishing: 2005.
16. Tian X, Hu T, He L, et al. Peritruncal coronary endothelial cells contribute to proximal coronary artery stems and their aortic orifices in the mouse heart. PLoS One. 2013;8:e80857.
17. Latson LA. New look at an old ring. Catheter Cardiovasc Interv. 2008;71:572.
18. Schlesinger MJ, Zoll PM, Wessler S. The conus artery: a third coronary artery. Am Heart J. 1949;38:823-836.
19. Stankovic I, Jesic M. Morphometric characteristics of the conal coronary artery. MJM. 2004;8:2-6.
20. Corone P, Corone A, Dor X, Binet JP. Coronary arteries and their variations. An embryologic explanation. C R Acad Sci III. 1984;299:451-458.
21. Meier P, Schirmer SH, Lansky AJ, Timmis A, Pitt B, Seiler C. The collateral circulation of the heart. BMC Med. 2013;11:143.

From the Advocate Illinois Masonic Medical Center and Rush Medical College, Chicago, Illinois.

Disclosure: The authors have completed and returned the ICMJE Form for Disclosure of Potential Conflicts of Interest. The authors report no conflicts of interest regarding the content herein.

The authors report that patient consent was provided for publication of the images used herein.

Manuscript submitted November 8, 2018 and accepted November 19, 2018.

Address for correspondence: Lloyd W. Klein, MD, FACC, 1953 North Clybourn Avenue, Suite #R-221, Chicago, IL 60614. Email: lloydklein@comcast.net