#3 Veno-venous Collaterals in Glenn and Fontan Physiology

Veno-venous collaterals are abnormal systemic venous channels that connect one venous territory to another. In patients with single-ventricle physiology, particularly after bidirectional Glenn or Fontan palliation, these vessels may become clinically important because they divert systemic venous blood away from the intended cavopulmonary pathway. The essential physiologic consequence is a reduction in effective pulmonary blood flow, resulting in systemic desaturation despite an anatomically patent cavopulmonary connection [1, 2].

In Glenn physiology, the SVC is directly connected to the pulmonary arteries. Therefore, SVC return should ideally pass through the pulmonary vascular bed before returning to the single ventricle. When a veno-venous collateral develops, a portion of this venous return escapes through an alternative systemic venous route, often toward the IVC, azygos system, hemiazygos system, hepatic veins, atrium, or pulmonary venous atrium. This creates a functional right-to-left shunt at the venous level.

1. Definition and Core Concept

Veno-venous collaterals are systemic venous bypass channels that allow blood to flow from a higher-pressure venous territory into a lower-pressure venous pathway.

In the setting of a Glenn circulation, this usually means:

Expected Glenn pathway:

SVC → Pulmonary arteries → Pulmonary veins → Single ventricle

With veno-venous collateral runoff:

SVC → Collateral vein → IVC/systemic venous pathway → Single ventricle

→ bypasses the lungs

This distinction is central. The Glenn anastomosis may be widely patent, but the effective amount of blood reaching the lungs can still be reduced because part of the SVC return is diverted through collateral channels.

A useful conceptual equation is:

Effective pulmonary blood flow = Glenn flow − veno-venous collateral runoff

2. Anatomic Pathways

Veno-venous collaterals often develop through pre-existing systemic venous networks that enlarge in response to altered pressure relationships. The azygos and hemiazygos systems are particularly important because they naturally form longitudinal connections between the upper and lower systemic venous territories.

Common pathways include:

1. SVC-to-IVC systemic venous connections
• Azygos vein
• Hemiazygos vein
• Intercostal veins
• Lumbar veins
• Paravertebral venous plexus
• Mediastinal venous channels
2. Systemic venous-to-pulmonary venous collaterals
• From the SVC, innominate vein, azygos system, or IVC territory
• Draining into pulmonary veins or the pulmonary venous atrium
• Particularly relevant after Fontan completion because they may cause direct systemic desaturation [3]
3. Cavopulmonary-to-systemic decompressive pathways
• These collaterals may act as “pop-off” channels when SVC, Glenn, or Fontan pressure is elevated.

The clinical significance depends not only on the size of the collateral but also on its origin, drainage site, pressure gradient, and whether it bypasses the pulmonary vascular bed.

3. Why Veno-venous Collaterals Develop

Veno-venous collaterals should not be interpreted as random vascular anomalies. They are often a marker of unfavorable cavopulmonary hemodynamics.

The major driving mechanism is a pressure gradient between the cavopulmonary pathway and a lower-pressure venous chamber. After bidirectional cavopulmonary anastomosis, systemic venous collateral development has been associated with elevated SVC or cavopulmonary pressure and a significant pressure gradient between the SVC and atrium [2].

Important promoting factors include:

• Elevated Glenn or Fontan pressure
• Elevated pulmonary artery pressure
• Increased transpulmonary gradient
• Pulmonary vascular resistance elevation
• Branch pulmonary artery stenosis or distortion
• Pulmonary artery hypoplasia
• Ventricular diastolic dysfunction
• Atrioventricular valve regurgitation
• Obstruction within the cavopulmonary pathway
• Long interval between staged palliations

In more recent large-cohort data, systemic venous collaterals between Glenn and Fontan were associated with higher pre-Glenn pulmonary artery pressure and higher transpulmonary gradient, supporting the concept that collateral formation reflects a hemodynamically stressed cavopulmonary circuit [4].

4. Hemodynamic Consequences

The primary consequence of veno-venous collateral flow is a reduction in effective pulmonary blood flow.

In Glenn circulation, pulmonary blood flow is passive and depends on unobstructed venous return from the SVC into the pulmonary arteries. If a portion of SVC blood escapes through a collateral, that blood does not participate in gas exchange.

This produces several downstream effects:

• Reduced SVC contribution to pulmonary blood flow
• Reduced pulmonary venous return
• Lower systemic arterial oxygen saturation
• Persistent or progressive cyanosis
• Potential underestimation of Glenn adequacy if only the anastomosis is assessed
• Possible reduction in ventricular preload through the pulmonary venous pathway

The patient may therefore appear cyanotic even when the Glenn anastomosis is anatomically open and unobstructed. This is the key teaching point: desaturation after Glenn does not always mean Glenn obstruction; it may reflect loss of effective pulmonary blood flow through collateral runoff [1].

5. Prevalence and Clinical Impact

The reported prevalence of veno-venous or systemic venous collaterals varies widely depending on patient age, stage of palliation, imaging method, and definition used.

Earlier series reported systemic venous collateral development in approximately 20–33% of patients after Glenn or Fontan procedures [1, 5]. In adults with single-ventricle physiology after cavopulmonary palliation, systemic-to-pulmonary venous collaterals have been reported more frequently, with one adult catheterization cohort identifying collaterals in more than half of patients [6]. A large contemporary cohort between Glenn and Fontan reported a prevalence of 12.3%, emphasizing that clinically recognized collaterals remain common even in modern staged palliation [4].

Clinically, veno-venous collaterals may present as:

• Lower-than-expected systemic oxygen saturation
• Progressive cyanosis
• Exercise intolerance
• Discrepancy between acceptable Glenn/Fontan anatomy and poor saturation
• Recurrent desaturation after otherwise successful palliation

However, the presence of a collateral does not automatically mean that it should be closed. Its clinical role must be interpreted in relation to the patient’s hemodynamics.

6. Diagnostic Evaluation

Evaluation should answer two questions:

1. Where is the collateral?
2. Why did it develop?

The first question is anatomic. The second is physiologic and often more important.

Imaging and catheter-based assessment

Echocardiography

Echocardiography is useful for assessing ventricular function, atrioventricular valve regurgitation, pulmonary venous return, and gross Glenn or Fontan pathway flow. However, small or complex collateral pathways may be difficult to visualize.

CT angiography and cardiac MRI

Cross-sectional imaging can define the systemic venous anatomy, collateral course, and drainage site. MRI may also provide information about flow distribution, although quantification of collateral flow remains technically challenging.

Cardiac catheterization

Cardiac catheterization remains central when intervention is being considered. It allows direct measurement of pressures, angiographic definition of the collateral pathway, test occlusion when needed, and transcatheter closure if appropriate.

Important hemodynamic data include:

• SVC/Glenn pressure
• Fontan pressure
• Pulmonary artery pressure
• Transpulmonary gradient
• Pulmonary vascular resistance
• Ventricular end-diastolic pressure
• Atrial pressure
• Pulmonary venous saturation
• Systemic arterial saturation
• Branch pulmonary artery anatomy

A veno-venous collateral should therefore be considered a hemodynamic signal, not merely an anatomic target.

7. Management Principles

The management of veno-venous collaterals requires balancing two competing physiologic realities.

First, the collateral can be harmful because it bypasses the lungs and worsens cyanosis. Second, the collateral may be protective because it decompresses a high-pressure cavopulmonary circuit.

Therefore, the correct management question is not simply:

“Can we close this collateral?”

The more appropriate question is:

“Can this circulation tolerate closure of this collateral?”

When closure may be beneficial

Transcatheter closure may be appropriate when:

• The patient has clinically significant desaturation.
• The collateral is large and clearly responsible for right-to-left venous shunting.
• Glenn or Fontan pressure is acceptable.
• Pulmonary vascular resistance is not significantly elevated.
• There is no untreated branch pulmonary artery obstruction.
• Ventricular filling pressure is acceptable.
• The collateral is not functioning as a necessary decompressive pathway.

Percutaneous coil or vascular plug occlusion can improve systemic oxygen saturation in selected patients. Adult Fontan series have demonstrated improved resting saturation after closure, supporting the role of catheter-based treatment in carefully selected patients [6, 7].

When closure may be harmful

Closure should be approached with caution when:

• Glenn or Fontan pressure is elevated.
• Pulmonary vascular resistance is high.
• There is significant pulmonary artery stenosis or distortion.
• Ventricular diastolic pressure is elevated.
• Atrioventricular valve regurgitation is significant.
• The collateral appears to serve as a decompressive “pop-off” pathway.

In such patients, occluding the collateral may increase systemic venous pressure, worsen venous congestion, and potentially unmask Fontan or Glenn failure physiology.

This concern is not theoretical. In a Fontan cohort, embolization of veno-venous collaterals was associated with decreased 5-year survival, particularly in patients with atriopulmonary Fontan connections and elevated Fontan pressures [8]. This finding does not mean that closure is always harmful, but it strongly supports individualized decision-making based on hemodynamic profile rather than saturation alone.

8. Glenn versus Fontan Physiology

The interpretation of veno-venous collaterals changes depending on the stage of palliation.

After bidirectional Glenn

In Glenn physiology, the SVC is the primary source of pulmonary blood flow from the upper body. A collateral from the SVC system to the IVC system can substantially reduce effective pulmonary blood flow. Therefore, desaturation after Glenn may reflect diversion of SVC blood away from the lungs.

In this setting, closure may improve saturation if the Glenn pressure is acceptable and there is no significant downstream obstruction.

Between Glenn and Fontan

During the interstage period, systemic venous collaterals may influence oxygen saturation and Fontan candidacy. Contemporary data suggest that these collaterals are associated with lower oxygen saturation and less favorable pre-Glenn or pre-Fontan hemodynamics, but they do not necessarily preclude Fontan completion [4].

The key clinical task is to determine whether the collateral is primarily:

• A cause of desaturation,
• A marker of elevated cavopulmonary pressure, or
• A compensatory decompressive pathway.

After Fontan completion

After Fontan completion, both SVC and IVC return are routed to the pulmonary arteries. Veno-venous collaterals may still develop and may drain into pulmonary veins or the pulmonary venous atrium, causing systemic desaturation [3, 6]. Recent studies also suggest that post-Fontan veno-venous collaterals may be associated with Fontan complications, including plastic bronchitis, although their impact on survival may vary across cohorts [9].

Thus, post-Fontan collaterals require careful interpretation within the broader context of Fontan pathway pressure, ventricular function, lymphatic complications, and end-organ status.

9. Distinction from Aortopulmonary Collaterals

Veno-venous collaterals should be distinguished from aortopulmonary collaterals.

Veno-venous collaterals divert systemic venous blood away from the pulmonary vascular bed and usually worsen cyanosis by reducing effective pulmonary blood flow.

Aortopulmonary collaterals arise from systemic arteries and supply blood to the pulmonary circulation. They may increase pulmonary blood flow but can also create volume load, increase ventricular work, and complicate Fontan physiology [10].

Both types of collaterals are common in single-ventricle palliation, but their physiology is fundamentally different:

• Veno-venous collateral: systemic venous runoff → desaturation
• Aortopulmonary collateral: systemic arterial runoff → volume load and pulmonary overcirculation

This distinction is important when interpreting angiography, oxygen saturation, pulmonary blood flow, and ventricular loading conditions.

10. Practical Clinical Framework

A structured approach is useful when evaluating veno-venous collaterals.

Step 1: Define the anatomy

• Origin: SVC, innominate vein, azygos vein, hemiazygos vein, IVC, hepatic vein
• Drainage: IVC, atrium, pulmonary vein, pulmonary venous atrium, hepatic venous system
• Size: small incidental channel versus large decompressive pathway
• Number: single dominant vessel versus multiple diffuse collaterals

Step 2: Define the physiology

• Is systemic saturation significantly reduced?
• Is cavopulmonary pressure elevated?
• Is pulmonary vascular resistance acceptable?
• Is there branch pulmonary artery obstruction?
• Is ventricular diastolic pressure elevated?
• Is the collateral helping or hurting the circulation?

Step 3: Decide whether closure is appropriate

Closure is most attractive when the collateral is a major source of desaturation and the cavopulmonary circuit is otherwise low pressure and unobstructed.

Closure is potentially dangerous when the collateral is decompressing a high-pressure Glenn or Fontan pathway.

11. Key Teaching Concept

Veno-venous collaterals in Glenn and Fontan physiology should be understood in two complementary ways:

1. They are a cause of cyanosis.

They divert venous return away from the pulmonary vascular bed and reduce effective pulmonary blood flow.

2. They are a marker of abnormal cavopulmonary hemodynamics.

They often develop because the Glenn or Fontan pathway is under elevated pressure.

Therefore, the presence of a veno-venous collateral should trigger a deeper physiologic assessment. The question is not only whether the vessel can be occluded, but whether occlusion will improve the overall circulation.

Summary

Veno-venous collaterals are abnormal systemic venous channels that develop after Glenn or Fontan palliation and may connect the SVC, innominate, azygos, hemiazygos, or IVC systems to other systemic or pulmonary venous pathways. Their principal effect is diversion of venous return away from the pulmonary circulation, causing reduced effective pulmonary blood flow and systemic desaturation. However, these collaterals may also function as decompressive pathways in patients with elevated cavopulmonary pressure. Management must therefore be individualized. Transcatheter closure can improve oxygen saturation in selected patients, but closure may be harmful when the collateral is acting as a protective pop-off pathway in a high-pressure Glenn or Fontan circulation.

References

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[3] Sugiyama H, Yoo SJ, Williams W, Benson LN. Characterization and treatment of systemic venous to pulmonary venous collaterals seen after the Fontan operation. Cardiol Young. 2003;13(5):424-430.

[4] Nguyen Cong MBH, Schaeffer T, Osawa T, Palm J, Niedermaier C, Piber N, Matsubara M, Heinisch PP, Georgiev S, Hager A, Ewert P, Hörer J, Ono M. Systemic venous collaterals between Glenn and Fontan: prevalence, therapy, and impact on outcomes. Cardiol Young. 2025;35(3):497-504.

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[8] Poterucha JT, Johnson JN, Taggart NW, Cabalka AK, Hagler DJ, Driscoll DJ, Cetta F. Embolization of veno-venous collaterals after the Fontan operation is associated with decreased survival. Congenit Heart Dis. 2015;10(5):E230-E236.

[9] Nguyen Cong MBH, Schaeffer T, Osawa T, Palm J, Georgiev S, Di Padua C, Niedermaier C, Heinisch PP, Piber N, Hager A, Ewert P, Hörer J, Ono M. Impact of veno-venous collaterals on outcome after the total cavopulmonary connection. Int J Cardiol. 2024;410:132229.

[10] Triedman JK, Bridges ND, Mayer JE Jr, Lock JE. Prevalence and risk factors for aortopulmonary collateral vessels after Fontan and bidirectional Glenn procedures. J Am Coll Cardiol. 1993;22(1):207-215.