Bilateral bidirectional cavopulmonary connection: a review of surgical techniques and clinical implications

Introduction

Systemic venous anomalies in the setting of a univentricular heart represent a complex issue that could influence the outcome of Fontan circulation and require specific surgical features. The presence of bilateral superior caval veins (bSCVs) is one of the most frequent systemic venous anomalies, which plays an essential and direct role in establishing the bidirectional cavopulmonary connection (Glenn operation). In a “standard bilateral Glenn” two similar mirror image anastomoses are constructed between each superior caval vein (SCV) and its ipsilateral pulmonary artery branch. Poor results in terms of Fontan completion and long-term outcome have been described in patients after the standard bilateral Glenn, mainly related to an increased risk of thrombus formation and insufficient growth of the intercaval portion of the pulmonary artery. Because of less-than-ideal results of the standard bilateral Glenn, alternative surgical techniques and therapeutic plans have been developed to improve the clinical outcome (1-3).

The purpose of this systematic review of the current literature is to analyze the pros and cons of the surgical techniques described for Glenn operation in presence of bSCVs. Moreover, the potential benefit of additional pulmonary blood and the role of computational flow simulation will be discussed to shape a prospective patient-individualized approach in this complex surgical strategy.

Methods

A review of the current literature was performed using published data from PubMed and Medline.

The search terms comprise: bilateral bidirectional Glenn, bSCVs, cavopulmonary connection, pulmonary artery growth, additional pulmonary blood, computational fluid dynamics simulations, virtual surgery, and combinations of the mentioned items. No articles were excluded based on the publication date. Case reports which described surgical technique specifically designed for bilateral bidirectional Glenn were included.

Studies not published as full-text or not written in English were excluded.

The articles selected for this review are summarized in Table 1.

Surgical techniques

The surgical techniques described to perform a bidirectional Glenn in the presence of bSCVs could be classified in five categories:

• The standard bidirectional Glenn performed bilaterally (Figure 1A);
• The modified bilateral Glenn through a “V-shape” anastomosis (Figure 1B);
• The modified bilateral Glenn through a “Y-shape” anastomosis (Figure 1C);
• The direct cavo-caval anastomosis (Figure 1D);
• The cavo-caval connection by means of an interposition-graft (Figure 1E).

Figure 1 Surgical techniques for cavopulmonary anastomosis in presence of bSCVs. (A) Standard bilateral bidirectional Glenn with two parallel anastomoses between each SCV and its ipsilateral pulmonary artery branch. (B,C) Modified bilateral Glenn techniques, respectively V-shape (B) and Y-shape (C). In the V-shape the cavopulmonary anastomoses almost touch each other. In the Y-shape the SCVs are merged to form a single combined vein with an end-to-side anastomosed to the pulmonary artery. (D,E) Cavo-caval anastomosis technique. One SCV is end-to-side anastomosed on the other one: directly (D) or by means of an interposition graft (E). SCV_R, right superior caval vein; SCV_L, left superior caval vein; RPA, right pulmonary artery; LPA, left pulmonary artery; SCV, superior caval vein; bSCV, bilateral superior caval vein.

The standard bilateral Glenn consists of two anastomoses between each SCV and its ipsilateral pulmonary artery branch, which let the SCVs run parallel (Figure 1A) and can be safely performed even with an off-pump technique (4,5). The modified bilateral Glenn techniques, known as “V- or Y-shape”, were designed to prevent central pulmonary artery thrombosis, involution, or failure to grow. In order to preserve the flow into the central pulmonary artery and at the same time preserve the symmetry of the flow distribution, the end-to-side anastomosis of the bSCVs was performed next to each other on the central portion of the pulmonary artery (6,7). In the V-shape technique described by Honjo (Figure 1B), the cavopulmonary anastomoses almost touched each other and were usually located posterior to the aorta (6). In the Y-shape technique described by Amodeo (Figure 1C) the SCVs were distally merged to form a single larger combined vein which was then end-to-side anastomosed to the pulmonary artery confluence behind the aorta (7,8).

The fourth and fifth surgical options consist in a cavo-caval surgical connection: one of the SCV could be end-to-side anastomosed on the other one in order to create a configuration similar to that one of a unilateral Glenn with or without an interposition-graft (9-12). The direct cavopulmonary anastomosis was performed on the side of the larger SCV (Figure 1D) and in case of equal size, on the same side as the inferior caval vein (9,10). In case of insufficient length of the SCV, a rolled autologous pericardial graft or a polytetrafluoroethylene graft have been used to elongate the SCV to perform the cavo-caval anastomosis (Figure 1E) (11,12). Even the creation of a “new innominate vein” by using an interposition Gore-Tex vascular prosthesis between the SCVs has been described in a case report by Vida et al. (13).

An alternative approach to create a configuration similar to that of a unilateral Glenn is banding or closure of one of the SCVs (14). This option is feasible only in presence of connecting veins somewhere (including intracranial) between the flow areas of the two SCVs. In fact, the purpose of the banding is to stimulate the growth of connecting veins. When the combined connecting veins reached a caliber similar to that of a usual innominate vein, a unilateral bidirectional Glenn could be performed with ligation of the involuted banded SCV.

Role of additional pulsatile pulmonary blood in presence of bSCVs

A source of additional pulsatile pulmonary blood flow (APPBF) represented by pulmonary stenosis or banding or by an aorto-pulmonary shunt can have positive effect on the main pulmonary artery growth, either after unilateral or bilateral Glenn (15-17). In fact, the pulsatility of the pulmonary blood flow creates semi-normal circumferential strain and shear stress, both known to be determinant factors in vascular homeostasis, endothelial integrity, and vessel remodeling (18-20). Therefore, pulsatile pulmonary blood flow could promote the regular growth of the pulmonary artery system and a preserved endothelial integrity could counteract thrombus formation. However, there is no consensus about the association between APPBF and pulmonary artery growth: some studies have described an improved main pulmonary artery growth in presence of APPBF (15,16), whilst other studies have not detected this finding (21,22). Moreover, a higher postoperative complication rate has been reported in presence of APPBF, especially longer chest tube drainage and higher incidence of chylothorax (16-21,23). A Blalock-Taussig shunt as source of additional pulmonary blood was associated with higher early mortality suggesting a relation with the quantity of APPBF (21). A recent study compared 110 patients without APPBF with 92 patients with APPBF after Glenn operation, including 43 patients after bilateral Glenn operation, confirmed the advantages of APPBF in terms of pulmonary artery size (23). Nevertheless, a sustained higher risk of death or transplant has been registered in the APPBF group and the incidence of events was prominent during interstage period (between Glenn operation and Fontan completion), making plausible the association with presence or absence of APPBF. However, all of these reports are non-randomized cohort studies, so that selection bias plays a role.

Contribution of computational fluid dynamics simulations to assess surgical strategy

Computational fluid dynamics simulations represent a new technological opportunity: surgeons and engineering team could create image-based models of operative results, obtained from magnetic resonance imaging or angiographic data. This “virtual surgery” has been used to predict the hemodynamic performance in single ventricle patients with or without bSCVs at time of bidirectional cavopulmonary connection, at time of total cavopulmonary connection and even at follow-up after Fontan completion (8,24-28).

Amodeo and colleagues compared the computational fluid dynamics simulations of modified bilateral Glenn by means of a Y-shaped technique (performed in seven patients) with the standard bilateral Glenn (8). The standard bilateral Glenn showed an evident directionally flow from each SCV towards the ipsilateral pulmonary artery with weak perfusion between caval veins anastomosis. Contrariwise, the Y-shaped showed symmetric and steady bilateral flow and absence of recirculation zones in the whole anastomosis.

Conflicting findings have been reported in two studies that analyze computational fluid dynamic simulation of total cavopulmonary connection after a standard bilateral Glenn. In fact, Sun and colleagues suggested that the connection of the extracardiac conduit from the inferior caval vein to the right pulmonary artery would be more favorable than a connection between the SCVs anastomosis (24). Conversely, the extracardiac conduit should be preferentially located between the two SCVs anastomosis to minimize the associated flow stasis of the main pulmonary artery, according to the results of Zélicourt and colleagues (25). It has to be mentioned that the simulation was performed based on respectively two patients (24) and just one patient (25) and no larger series of simulations have been reported.

Discussion

The presence of bSCVs and their sizes plays an essential role in the surgical strategies and in the clinical outcome of patients with single ventricle. We will review the evidence for three main issues which could be influenced by the presence of bSCVs: diminished growth of the central pulmonary artery, risk of thrombus formation and incidence of Fontan completion. The limited growth of the central portion of the pulmonary artery bifurcation described by standard bilateral Glenn is almost certainly related to limited blood flow to the ipsilateral lung with consequent flow stagnation in the connecting portion. Size discrepancy between caval veins and pulmonary artery branches could even amplify the thrombotic complications. Both unfavorable pulmonary artery growth and thrombotic events in turn affect the eligibility for Fontan completion.

Seven articles compared the results of the standard bilateral Glenn with those of the bidirectional Glenn with just one SCV, the “unilateral” anatomy (1-3,29-32). An increased risk of postoperative pulmonary artery thrombus formation (1,2) and an unfavorable growth in the central pulmonary arteries (2) have been reported by the bilateral subgroup.

However, in two studies from Japan thrombus formation and poor development in the central pulmonary artery were not observed, for no stated reason (29,30). In these studies, the standard postoperative therapy with Aspirin (29) and the presence of additional source of pulmonary flow in all patients (30) may have prevented these events. Even an increased risk of SCV obstruction after bilateral Glenn has been reported in two studies (1,30), although this complication appeared not to be a risk factor for mortality or Fontan completion. Shuler and colleagues suggested to delay elective Glenn operation in presence of bSCVs until at least 120 days of age to reduce the risk of prolonged intensive care and hospital length of stay (31). It seems logical to delay the operation to allow the maximum growth of both SCVs and to perform the Glenn operation with the largest obtainable size of both caval veins. If the size of the SCVs would remain small and unsuitable for a Glenn operation, a primary extracardiac inferior cavopulmonary connection could be considered and the timing of a secondary successive Glenn operation could be assessed depending on the improving of SCVs anatomy and size. This reverse order of Fontan completion, also known as “Southern Glenn”, has been described in a case of unfavorable upper-body systemic venous anatomy and at follow-up the diminished SCV had grown making a Glenn operation feasible (33,34). Therefore, the diminutive SCV in small infancy, which may occur in presence of bSCVs, may grow to normal size by childhood and the “southern Glenn” could be a feasible approach to achieve an acceptable size and anatomy for the “northern Glenn”.

The reported rate of Fontan completion after bilateral Glenn can vary from a range of 80–90% (29,30) to a significantly lower percentage (39%) (2). Even when the patients underwent completion of their Fontan circulation, a previous bilateral Glenn can affect the postoperative outcome after total cavopulmonary connection, as recently published (32). In fact, the comparison between 365 patients with a unilateral Glenn with 40 patients with a bilateral Glenn showed a longer intensive care unit stay and a lower survival rate in the bilateral group. The higher incidence of late Fontan failure reported by Keizman et al. confirmed the negative influence of bilateral Glenn even after the Fontan completion (3).

The modified bilateral Glenn with the creation of a “new innominate vein” could allow decompression of the SCVs and could be then helpful in case of small caliber of SCVs (13). However, this technique does not improve the flow distribution in the central portion of the pulmonary artery and the Gore-Tex prosthesis could even represents an additional source of thrombosis.

Because of the unfavorable outcome of the standard bilateral Glenn, alternative surgical techniques which could guarantee a better pulmonary artery growth and prevent thrombus formation have been designed: the modified bilateral Glenn either with Y- or V-shape (6-8).

Compared to 37 patients after standard bilateral Glenn group, 24 patients after modified V-shape technique showed a better pulmonary artery growth at the pre-Fontan completion study: higher central pulmonary artery index and Nakata index. In both groups the small size of the SCVs was predictor for re-intervention and thrombosis.

From a technical point of view, it can be speculated that a large ascending aorta could increase the divergence between the caval veins and might compress the confluence of the caval veins or the cavopulmonary anastomosis, representing a potential contraindication to this approach. However, Honjo et al. performed 24 consecutive V-shape Glenn between 1999 and 2007 and no anatomical contraindications were described (6). Up to now, the potential influence of the ascending aorta size on the surgical feasibility of this technique has not been supported by the published data.

A surgical technique with a different principle consists in the cavo-caval anastomosis (9-12). The aim of this technique is to create a configuration similar to that one of the unilateral bidirectional Glenn by means of an end-to-side anastomosis of one SCV with the other one: one of the SCVs will work as an innominate vein. This technique is feasible even in case of large distance between the caval veins because a rolled pericardial graft or a polytetrafluoroethylene graft can be used to connect the SCVs (11,12). However, overall, only 13 cases of this technique have been reported and the follow-up has not been published yet.

In presence of a connecting vein the banding and then ligation of the smallest SCV could also be considered and results in an almost usual unilateral Glenn (16). The feasibility of this technique is by definition limited by the presence of a connecting vein and the rate of eligible patients is not known.

Regardless of the surgical technique of choice, if allowed by the anatomy, a source of APPBF could stimulate the growth of the central pulmonary artery. In fact, pulsatile pulmonary blood can influence the endothelium regulation promoting the pulmonary artery growth, therefore opposing against the flow stagnation of the central pulmonary artery in case of standard bilateral Glenn. Furthermore, APPBF can increase postoperative oxygen saturation during the critical period of brain growth in the infant (15-17,21). However, this benefit on pulmonary artery size has not been always demonstrated and this discrepant effect of APPBF on the pulmonary artery growth could be related to different amount of APPB. The amount of APPBF in the setting of a partial cavopulmonary connection can be difficult to calibrate because of the lack of measurement tools. Moreover, the increased amount of pulmonary blood flow could determine an increase of central venous pressure, which in turn could explain the increased rate of postoperative chylothorax and prolonged pleural effusion. The impact of APPBF on long-term outcomes has been reported to be unfavorable in terms of transplant-free survival and could be associated to the progression of atrioventricular valve regurgitation and ventricular dysfunction (23). In fact, the overload of the single ventricle related to the APPBF could worsen valve and ventricular function and should be accounted. The quantification of the ideal amount of APPBF could allow to benefit from the advantages of pulsatile pulmonary blood in terms of pulmonary artery growth stimulation and to minimize the “collateral damage” of postoperative and long-term complications which are presumably related to an excessive amount of it. The theoretical quantification of additional pulmonary blood flow in the context of a bidirectional cavopulmonary shunt formulated by Ebels and colleagues can be applied in vivo to assess the desired level of APPBF (35). The perspective to predict the hemodynamic performance and operative results by means of image-based models and virtual surgery is encouraging the application of computational fluid dynamics simulations in single ventricle patients. Computational fluid dynamic simulations have confirmed the more favorable flow distribution of the modified bilateral Glenn with V-shape, compared to the standard bilateral Glenn (8). However, the limited number of patients (seven) of this study does not allow to draw definitive conclusions and these results should be interpretated and accounted with their intrinsic limitations. Similarly, the conflicting findings reported in the computational fluid dynamic simulation of total cavopulmonary connection after a standard bilateral Glenn could derive from the extremely limited cohort of patients and do not allow to identify the most favorable model. Computational fluid dynamic simulations are a promising tool to identify the best hemodynamical performing strategy prior to surgery, especially in complex anatomical connection by single ventricle, as in presence of bSCVs. Further studies are needed to enlarge the cohort of patients and acquire enough data to support stronger conclusions.

Conclusions

In the light of our findings a standard bilateral Glenn operation could impede the normal growth of the connected portion of the main pulmonary artery and a higher risk of thrombus formation has been reported. These sequels may interfere with the future Fontan completion. When a standard bilateral Glenn is performed, postoperative therapy with anti-platelet or anticoagulation drug could be advisable to prevent thrombo-embolic complications and whenever possible, it could be reasonable to postpone this technique as long as is clinically feasible to decrease postoperative morbidity and optimize SCVs size.

The modified Glenn operations, V- or a Y-shape anastomosis and the cavo-caval anastomosis should be considered feasible alternative surgical techniques. Despite the limited cohort of patients described and the lack of the long-term results, these modified procedures should be estimated counting the provided distribution of blood flow to the pulmonary artery, which can promote a good-balanced growth of the pulmonary system.

The benefit on pulmonary artery size of APPBF is logically dependent on the quantity of flow. Excessive APPBF can be associated with a higher rate of postoperative complications and unfavorable long-term outcomes. Therefore, a source of adjusted APPBF can be considered. The amount of APPBF in vivo could be quantified intra-operatively and its calibration is essential to maximize the benefit and minimize the postoperative risks.

Computational fluid dynamic simulations and virtual surgery are promising tools and a progressive increase of its application in complex single ventricle, as in presence of bSCVs could be expected. The scientific merger of surgical and engineering insights could strongly improve the processing and analysis of the surgical strategy and should be explored further.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Antonio F. Corno & Ali Dodge-Khatami) for the column “Pediatric Heart” published in Translational Pediatrics. The article has undergone external peer review.

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-24-28/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-24-28/coif). The column “Pediatric Heart” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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