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The ligament of Marshall (LOM) is an epicardial vestigial fold that contains the oblique vein of Marshall (VOM), autonomic nerves, and myocardial sleeve, ie, the Marshall bundle (MB),1 that serves as a terminal portion of the inferior interatrial pathway.² The left lateral ridge, an endocardial structure located in between the LAA and left PVs, is known to be important to AF ablation.³ The LOM is located in the epicardial aspect of the left lateral ridge. The MB can develop automatic rhythm during isoproterenol infusion,⁴ can serve as a source of paroxysmal AF,^5,6 and is known to activate rapidly during sustained AF.⁷ A worldwide survey in 2005 showed that 22.8% of the clinical EP laboratories target LOM in their AF ablation sessions.⁸ The LOM is a frequent source of paroxysmal AF in a young man with a history compatible with adrenergic AF,⁹ ie, AF induced by exercise or a high catecholaminergic state. In the EP laboratory, a high dose (10 to 20 mcg/min) of isoproterenol is used to trigger AF in these patients. Ectopic beats from the MB often show biphasic or negative P waves in surface ECG lead II. The intracardiac recordings from the mid-CS may show double potentials. If the earliest activation of ectopic beats or AF is in the mid- or distal CS, and double potentials are present at those sites, the MB mapping should be considered. In addition, if the earliest endocardial activation is located inside the left PVs but the PV potential during triggered beat precedes the LA potential by < 45 ms, the LOM mapping should be considered. Finally, if EP study after complete PV isolations shows that a left PV site-premature complex seems to have triggered AF, but no left PV trigger can be found despite careful mapping, LOM mapping may be needed to identify the focus.

The Anatomy of Ligament of Marshall

The LOM can be divided anatomically into proximal, mid, and distal portions. The proximal portion directly connects to the muscle sleeve of the CS. The mid portion of the MB connects to the LA or the left PVs. The distal portion, which is often fibrotic and shows no electrical activity, extends beyond the left PVs. There are significant variations of the morphologies of the LOM on the epicardium. The postmortem histopathological studies of the proximal and the mid portions of the MB demonstrated multiple connections with the LA.^10,11 The major connections between the MB and the LA are located in the CS juncture, LA–left PV junction, and LA in between CS and PVs with wide multiple connections. At the CS junction, the MB completely encircles the VOM and inserts directly into the CS musculature or more distally into the posterior wall of the LA. At the middle or distal portions of the LOM, the MB gradually changes into multiple muscle fibers and then disappears or inserts into the epicardium of the anterior wall of the LA and left PVs, dominantly in the LIPV. There are 3 distinct groups of anatomical connections between MB and LA: single connection in the juncture of the CS, double connections in CS and LA–PVs, multiple connections in between CS and PVs. Typical examples of the LOM in human hearts are shown in Figure 21.1.¹² In addition to MBs, immunohistochemical studies of the LOM confirmed the presence of sympathetic nerve fibers and ganglion cells.^4,11 A more recent study by Ulphani et al¹³ documented that, in addition to sympathetic nerves, the LOM is abundantly innervated by the parasympathetic nerves as well. These nerve structures may be responsible for the vagal responses observed during MB ablation and may contribute to the initiation and perpetuation of AF.

Electrophysiological Characteristics of the Marshall Bundle

Scherlag et al2 first characterized the electrical activities of the LOM. The investigators reported that the MB was part of the inferior interatrial pathway that connects the left and right atria. A recent study showed 3 different EP characteristics of the MB in humans based on anatomical connections.¹³

Single Connection

This type of connection was documented in the beginning of the MB research.⁵ In patients with a single connection, the activation from the sinus node crosses to the LA via Bachmann’s bundle and the inferior interatrial pathway and activates the MB from a proximal-to-distal direction. Because there is no other connection between the MB and LA, the MB is not preexcited by the sinus wavefront from the Bachmann’s bundle. The EGM recording during sinus rhythm shows a typical proximal-to-distal activation sequence (Figure 21.2A) and the same sequence of activation occurs during AF (Figure 21.2, B and C). Note that these activations are relatively regular as compared with the activations within the LA. This electrical activity of the MB during AF is much slower and more organized than in the other 2 types of connections. Because the MB only connects to CS muscle sleeves, the communication between the LA and MB is indirect. It is possible that delayed conduction with the CS muscle sleeves has prevented some of the AF wavefronts from reaching the MB. Therefore, the MB activation is slow. Some of this type of patients show additional ectopic activity from the distal MB during AF. Those activities (downward arrows in Figure 21.2, B and C) activate the MB in a distal-to-proximal direction with slower rate than passive activation of the MB. Although MB of this type may initiate AF through ectopic activity,⁵ the slow activation during persistent AF suggests that it may not be a major contributor to AF maintenance.

Double Connections

If the MB has connections with both the CS and the LA (or PVs), the wavefronts from the CS and LA (or PVs) compete for MB activation.¹⁴ As a result, the MB EGMs might not be clearly visible. Figure 21.3A shows the recordings during sinus rhythm. Note that the MB EGM and the local LA EGM are very close to each other at the distal MB and most of the MB EGMs are indistinguishable from the local LA EGM in sinus rhythm. However, by the premature complex from the LSPV (dashed arrow, Figure 21.3B), multiple MB potentials are revealed. The activation in the MB is distal to proximal, consistent with the existence of a distal connection within the LSPV. After successful RF catheter ablation of the distal MB–LA (PV) connection, only one connection (MB–CS) is left conducting. The MB activity should then be visible in sinus rhythm. In this situation, the propagation is proximal to distal (solid arrows, Figure 21.3C), simulating the activation patterns of a single connection. In this type, the MB may serve as a bypass tract that connects the CS to the left PVs without any LA involvement. This connection might provide a substrate for macroreentry. The rapid electrical interaction between the left PVs and the MB has been shown to participate in reentry during electrically induced AF in canine models.¹⁵ An important clinical implication of this finding is that the PV–MB connection provides an epicardial conduit between PV and LA through the CS muscle sleeves. If this epicardial conduit (accessory pathway) is not eliminated, electrical stimulation within the PV would be followed by LA activation and vice versa. A clinical electrophysiologist performing AF ablation might interpret these findings as failed PV isolation. In half of the patients of this type, the MB is directly connected to the muscle sleeves of the left PVs. Direct ablation inside the PVs is needed to eliminate these distal connections and to achieve complete antral isolation. The sites of successful ablation within the PV may be either at the origin of MB ectopy or at the site of earliest activation during MB pacing.

Multiple Connections

In case of multiple MB–LA connections, the electrical activation patterns depend on the earliest MB–LA breakthrough sites and the number of MB–LA connections. In these patients, the electrical potentials from the MB are generally small due to thin muscle bundle, and they do not propagate in a uniform proximal-to-distal activation pattern as in a single connection or distal-to-proximal activation pattern during premature complex in double connections. Rather, both central and peripheral sites could serve as an independent early site, and the earliest MB activation is not at either end of the MB (Figure 21.4, A and B). Due to the presence of these additional connections, the interval between the local atrial EGMs and the MB may be either short or nonexistent. Therefore, distinct MB potentials are often difficult to identify during sinus rhythm. In patients with multiple connections, we might observe a premature MB activity breakthrough into the middle of the LA earlier than into either end of the LA. An example of the latter phenomenon is shown in Figure 21.4C, where the bold arrow points to the earliest LA activation. Due to conduction delay, there is a clear separation between MB and LA. During AF, rapid and complex fractionated activations of the MB are noted in all patients with multiple connections (Figure 21.5A). After isolation of the MB, some of this type of patient shows dissociated MB potentials and MB tachycardia under isoproterenol infusion (Figure 21.5B). Experimental studies showed that the dominant source of AF maintenance might be the rotors that generate high-frequency spiraling waves and create spatially distributed frequency gradients.^16–18 Clinical studies demonstrated the existence of a hierarchical distribution of the rate of activation in the different regions during AF.^19,20 Ablation of the highest-frequency site was associated with slowing and termination of AF.²⁰ Thus, a very rapid focus producing fibrillatory conduction may be a driver of AF, and these drivers are often the targets of the catheter ablation.^21,22 Animal and human studies have shown that the MB had the highest dominant frequency during sustained AF.^7,23 The complex pattern of the electroanatomical connections between the MB and the LA can provide a substrate for reentry, leading to complex and fragmented MB activities. After isolating the MB from LA, localized MB tachycardia could be induced by sympathetic stimulation while the atria remain in sinus rhythm. These findings document that MB is capable of independent rapid activation and is not always activated passively by the neighboring AF wavefronts.

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