21/03/2024 23:36 Transjugular ductus venosus stent placement in an extremely premature, low birth weight neonate with infradiaphragmatic

ragmatic tot…

Progress in Pediatric Cardiology

Volume 67, December 2022, 101571

Transjugular ductus venosus stent placement in an

extremely premature, low birth weight neonate with
infradiaphragmatic total anomalous pulmonary venous
connection
Julian E. Cameron a b , Sarah Badran a b, John Cleveland b c, Neil D. Patel a b

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https://doi.org/10.1016/j.ppedcard.2022.101571
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Highlights
• Ductus venosus stent placement as palliation for high risk TAPVC

• Can be performed safely in low birth weight, premature neonates

• Procedural success dependent on the anatomy of the vertical vein to portal sinus

Abstract
Given the risks of cardiopulmonary bypass and general complications of surgical repair of total anomalous pulmonary
venous connection in low birth weight, premature neonates, there are limited palliative options for these patients when
obstruction occurs. This case presents successful transjugular stent placement in the ductus venosus in a 950 g neonate,
born at 26 weeks gestational age, with infradiaphragmatic total anomalous pulmonary venous connection. In addition, a
synthesis of previous case reports on this subject is discussed, with an emphasis on the anatomy of the portal sinus and
ductus venosus, relative to the location of vertical vein drainage.

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Keywords
TAPVC; TAPVR; Ductus venosus; Portal sinus

1. Introduction
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Infradiaphragmatic total anomalous pulmonary venous connection (TAPVC) is often associated with obstruction
secondary to the natural postnatal closure of the ductus venosus (DV) and insufficient capacity of the portal circulation to
accommodate pulmonary venous return. Obstruction may also occur within the vertical vein itself, particularly as it
descends across the diaphragm through the esophageal hiatus. Therefore, infradiaphragmatic TAPVC typically requires
prompt and often emergent surgical intervention. However, in select cases in which immediate surgical intervention is not
an option or the risk of surgery is unacceptably high, stenting of the DV has been utilized as a palliative measure [1], [2],
[3], [4], [5], [6], [7]. We present a case of transjugular DV stent placement in an extremely premature, low birth weight
neonate with postnatally diagnosed infradiaphragmatic TAPVC and provide a review of the literature. Informed consent
was obtained from the patient's legal guardian to describe the details of this case for publication.

2. Case history
The patient was born at 26 6/7 weeks gestational age with a birth weight of 935 g. He was supported with nasal non-
invasive ventilation until day of life (DOL) 9 at which point he required intubation for progressive respiratory failure. An
echocardiogram was performed demonstrating a pulmonary venous confluence posterior to the left atrium, draining into
a vertical vein coursing below the diaphragm, consistent with infradiaphragmatic TAPVC. A patent DV was visualized with
an initial gradient of 2.4 mmHg. By DOL 15, the gradient had increased to 5 mmHg (Fig. 1) with persistent pulmonary
edema and intermittent hypotension requiring dopamine infusion. Despite this, saturations remained consistently in the
upper 80s on 21 % FiO2.

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Fig. 1. Subcostal echocardiogram image in (A) 2D imaging and (B) color doppler demonstrating the stenotic ostium of the
ductus venosus relative to the portal sinus. The vertical vein can be seen entering at the left side of the frame. PS – portal
sinus, DV – ductus venosus, VV – vertical vein.

Given his size and degree of prematurity, it was unlikely that he would survive to an age and size at which the risks of
cardiac surgery with cardiopulmonary bypass and circulatory arrest would be minimized [8], [9]. Therefore, palliative DV
stent placement was offered while the patient was still relatively stable rather than performing an emergent procedure to
salvage the DV in the setting of acute decompensation. After discussing the risks and alternatives, parents opted to
proceed with transcatheter DV stent placement performed on DOL 17 at a weight of 1 kg.

4Fr sheaths were placed in the right internal jugular vein (RIJ) to access the ductus venosus and in the left femoral vein
(LFV) to concomitantly access the left pulmonary artery (LPA) for angiography of pulmonary venous return. A lower than
usual dose of heparin (20 U/kg) was given at the beginning of the case in anticipation of additional heparinized saline
flushes. An end-hole catheter was advanced prograde to the LPA from the LFV for angiography. This demonstrated that

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the left pulmonary veins drained to a vertical vein, which coursed caudally and entered the right portal vein. The DV was
only faintly seen given the lack of flow due to severe constriction (Fig. 2A).

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Fig. 2. Angiography with AP 0 projection. A – Contrast injection into the left pulmonary artery demonstrating drainage of
the vertical vein predominately to the right portal vein; B – Following DV stent placement, contrast injection into the
portal sinus demonstrates filling of the left portal veins, but no significant antegrade flow though the DV or flow into the
right portal vein; C – Final contrast injection into the portal sinus with robust drainage through the second DV stent. PS –
portal sinus; DV – ductus venosus; iLPV – inferior left portal vein; sLPV – superior left portal vein; RPV – right portal
vein; VV – vertical vein.

From the RIJ sheath, the DV was accessed using a 1.8F FineCross MG microcatheter (Terumo Medical, Somerset NJ) and
a 0.014″ Asahi Sion Blue wire (Asahi Intecc USA, Tusint CA). Angiography demonstrated that the DV constricted to
<1 mm. The wire was positioned in the superior left portal vein and angioplasty of the DV was performed using a
3 × 8 mm Takeru balloon (Terumo Medical, Somerset NJ), followed by placement of a 4 × 12 mm Resolute Onyx
Zotarolimus drug-eluting stent (Medtronic Inc., Santa Rosa CA).

However, on follow-up angiography in the LPA and portal sinus, it was apparent that the stent crossed and jailed the
rightward part of the portal sinus where the vertical vein was draining. The initial wire course across the stenotic DV for
stent positioning was looped in the most anterior region of the portal sinus into the left portal veins. This anterior region
of the portal sinus would have been the location of previous umbilical venous drainage providing the most streamlined
course of fetal blood flow from umbilical vein to right atrium across the DV (Fig. 3, Fig. 4). The region of portal sinus
connecting the right portal vein and vertical vein was more posterior compared to where the wire was positioned, and not
as easily accessible or visualized on initial angiography (Fig. 2, Fig. 4). Therefore, the FineCross MG microcatheter and
0.014″ Asahi Scion Blue wire were utilized to cross the side cell of the existing stent and access the right portal vein and
vertical vein. Angioplasty of the side cell was performed using a 3 × 8 mm Takeru balloon and the 4 mm balloon from the
previously placed stent. During catheter and sheath manipulation, it was noted that the existing stent distorted with
residual obstruction in the DV. A 4 × 16 mm Formula 418 stent (Cook Medical, Bloomington IN) was implanted across the
DV, extending into the right side of the portal sinus allowing for unobstructed return from the vertical vein.

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Fig. 3. Generalized fetal portal sinus anatomy in the setting of anomalous pulmonary venous return with a vertical vein
draining to the right portal vein, using adopted nomenclature standards [10]. The proximal, anterior PS can be defined as
the region of UV drainage, and the distal, posterior PS as the region draining into the RPV. UV – umbilical vein; PS –
portal sinus; DV – ductus venosus; mLPV – medial left portal vein; iLPV – inferior left portal vein; sLPV – superior left
portal vein; RPV – right portal vein; PV – portal vein; VV – vertical vein; IVC – inferior vena cava.

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Fig. 4. AP (A) and Lateral (B) projections of distal VV angiography following intentional fracture of initial DV stent with
corresponding landmark identification and particular attention to the location of VV drainage directly into the RPV The
arrow marks the direction of umbilical venous flow through the portal sinus. DV – ductus venosus; PS – portal sinus;
RPV – right portal vein; VV – vertical vein; sLPV – superior left portal vein.

Follow-up angiography demonstrated robust flow from the vertical vein to the right atrium via the stented DV (Fig. 2C).
The systemic arterial pressure markedly increased after placement of the second stent corresponding to adequate

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drainage of pulmonary venous return. At the end of the procedure, there was a 3 mmHg gradient from the right portal
vein to right atrium and a mean pulmonary artery pressure of 17 mmHg. Post-procedure, the patient had significant
improvement in lung compliance and pulmonary edema. He was anticoagulated with low dose heparin for 72 h (goal anti-
xa 0.2), followed by aspirin monotherapy due to elevated risk of intraventricular hemorrhage with prematurity. He was
also maintained on rifaximin to normalize elevated ammonia levels in the setting of the patent portosystemic shunt.

One month following the initial intervention, the patient developed lactic acidosis. There was concern for inadequate
atrial shunting, so the patient underwent balloon atrial septostomy. Two weeks later, he developed frequent desaturations
with elevated right ventricular pressure by echo. He returned for cardiac catheterization where a 6 mmHg gradient was
noted across the stent and underwent balloon dilation of the stent with 4 and 5 mm balloons with reduction to a 4 mmHg
gradient.

Two months after the initial intervention, at a corrected gestational age of 37 weeks and weight of 2 kg, he underwent
successful surgical TAPVC repair. At 4 months of age, he remained on rifaximin due to intermittently elevated ammonia
levels and underwent cardiac catheterization to embolize the stented ductus venosus with a 4 × 4 mm Amplatzer Piccolo
Occluder (Abbot Medical, Plymouth MN). His right ventricular systolic pressure was 26 mmHg and mean pulmonary
artery pressure was 19 mmHg. Angiography demonstrated that the left portal vein was occluded as a consequence of prior
intervention. He was ultimately discharged from the hospital at 5 months of age. On most recent follow-up at 19 months
of age, the patient continues to do well. His echocardiogram demonstrates unobstructed pulmonary venous return, and
right ventricular pressures are estimated to be normal.

3. Discussion
While this is not the first report of ductus venosus stent implantation for infradiaphragmatic TAPVC, this case emphasizes
several of the challenges associated with this procedure with a particular emphasis on the importance of delineating portal
sinus anatomy in relation to the vertical vein and DV which has not been extensively described. Ten prior cases of DV
stenting have been reported in the literature, which were performed in both premature and term neonates of a variety of
sizes (Table 1). This strategy has been used successfully to palliate patients with isolated infradiaphragmatic TAPVC as
well as patients with complex single ventricle anatomy, although transcatheter re-intervention for either stent dilation
and/or ductus venosus device closure following surgical repair is common, being reported in half of the currently
published cases in addition to the present study. From an anatomic perspective, the portal sinus can be defined as an L-
shaped, intrahepatic venous confluence with the umbilical vein at its proximal end and the origin of the right portal vein
at its distal end (Fig. 3). The primary left portal veins branch off the proximal portal sinus followed by the ductus venosus
with its ostium typically aligned with the outlet of the umbilical vein. The portal sinus, which becomes the left portal vein,
courses at a near right angle after the ductus venosus towards the right portal vein [10]. In the setting of
infradiaphragmatic TAPVC, the vertical vein usually drains into the portal system, but is variable [11] with one series of
autopsy cases reporting 68 % draining into the portal venous system, 14 % to the IVC, 7 % directly to the ductus venosus,
7 % to the left hepatic vein, and 4 % unknown [12]. The precise location of vertical venous drainage into the portal system
– whether directly to the portal sinus, left, or right portal vein – has not been well described, although one case report
demonstrated the VV draining directly into the DV [5].

Table 1. Summary of all 10 previously reported cases of ductus venosus stent placement. Only one case specifically
identified the location of vertical venous drainage directly to the ductus venosus [5], all others did not report the location
of the vertical vein in relation to the portal sinus. TAPVC – total anomalous pulmonary venous connection; DOL – day of
life; UV – umbilical vein; RIJ – right internal jugular; RFV – right femoral vein; DV – ductus venosus; VV – vertical
vein.

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Gestational Birth Diagnosis Age Access Stent Anti- Stent Additional Stat
age weight at coagulation stenosis interventions DV p
Cath surg

Meadows Term 3900 g Isolated DOL UV Pre- No Spon

et al. 2006 infradiaphragmatic 3 mounted closu
TAPVC stent in DV
and VV

Kitano et 38 weeks 2400 g Heterotaxy, single DOL LIJ, Two bare Yes Stent dilation
al. 2009 ventricle, mixed 12 RFV metal stents with 7 mm
type TAPVC in the DV balloon at 2, 5,
and 8, 11, and
ascending 15 months
VV

Higaki et al. 39 weeks 3000 g Heterotaxy, single DOL UV 3 × 24 mm Heparin/ Yes Stent dilation
2009 ventricle, 6 and two Aspirin at 5 weeks of
infradiaphragmatic 3 × 18 mm age
TAPVC bare metal
stents

38 weeks 2580 g Heterotaxy, single DOL UV 8 × 24 mm No No

ventricle, 0 bare metal
infradiaphragmatic stent
TAPVC

Rothman et 32 weeks 1700 g Mixed TAPVC DOL UV 4 × 20 mm Heparin drip Yes IV urokinase at Spon
al. 2011 2 coronary 2 weeks for closu
stent stent
thrombosis

30 weeks 1500 g Isolated DOL UV 3.5 × 13 mm Heparin drip No No Spon

infradiaphragmatic 13 coronary closu
TAPVC stent

3200 g Isolated DOL UV 4 × 24 mm Heparin drip No No Devi

infradiaphragmatic 2 coronary occlu
TAPVC stent due t
hype
amm

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Gestational Birth Diagnosis Age Access Stent Anti- Stent Additional Stat
age weight at coagulation stenosis interventions DV p
Cath surg

Oonishi et Heterotaxy, single DOL Two bare Yes Balloon

al. 2012 ventricle, 0 metal stents dilation of
infradiaphragmatic stent at 35 days
TAPVC of age

Burkhardt 38 weeks 1270 g Isolated DOL RIJ 4.5 × 9 mm Heparin/ Yes Stent dilation
et al. 2014 infradiaphragmatic 16 coronary Aspirin with 5 mm
TAPVC stent balloon at
2 months of
age

Hope et 28 weeks 940 g Double outlet right DOL UV, 5 mm No No Spon

al. 2020 ventricle, 6 RIJ Zotarolimus- closu
infradiaphragmatic eluting stent
TAPVC

Given this variability in the vertical vein, adequate visualization and mapping of the portal sinus, and vertical vein is
necessary to determine optimal approach and location of stent implantation. During our procedure, angiography from the
LPA did not provide clear delineation of the portal sinus anatomy and DV. Given that the DV was nearly closed and the
normal direction of blood flow in the portal system is into the liver parenchyma, the anatomy could not be well delineated.
Umbilical venous access would have been advantageous by allowing for better definition of the portal venous anatomy as
it related to the DV and vertical vein through direct angiography and could have been utilized for the intervention, as
others have described [2], [3], [4]. Pre-preprocedural CT angiography may be considered to better define the anatomy [5],
[6], however the risks of radiation and transporting an extremely low birth weight infant must be considered.

Although not described in previous cases of infradiaphragmatic TAPVC anatomic location of VV drainage relative to the
portal veins and DV may contribute to the clinical severity at presentation. Our patient was able to maintain relatively
high oxygen saturations and adequate cardiac output initially. Even in the setting of near complete occlusion of the DV,
the patient did not suffer from cardiovascular collapse. We suspect that this is secondary to the ability of the portal venous
system to ultimately allow for return of pulmonary venous blood back to the heart.

During most of fetal life, only a fraction of umbilical venous flow enters the DV. During the first half of pregnancy, flow
through the DV may account for >40 % of total umbilical venous return on average [13]. The relative flow through the DV
subsequently decreases with gestational age as the portal and hepatic circulation mature. After 20 weeks, the relative DV
flow stabilizes to an estimated 20–30 % of umbilical venous flow, with 70–80 % draining intrahepatic. Though there is
considerable variance in this percentage due to various factors that may affect hepatic vascular resistance [14], [15], and it
is unknown if TAPVC affects this flow distribution. Prematurity may also be protective by prolonging DV patency
compared to term infants [16], [17].

In addition to delineation of the venous anatomy, there are several other procedural considerations which include optimal
stent size, anticoagulation strategy, and natural history of a persistent portosystemic shunt, which may affect the need for
additional non-surgical intervention after the initial palliative procedure. Previously reported cases (Table 1) demonstrate
that there is considerable variation in practice. While most cases utilized coronary stents ranging in diameter from 3 to

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5 mm, a larger 8 mm stent was used in a 2.6 kg term neonate. We initially chose a 4 mm diameter drug eluting stent based
on our patient size, and stent sizes that had been used in prior cases. A stent with drug eluting properties was chosen to
minimize the risk of in-stent stenosis, which was reported in four cases that required reintervention. In our case, there
was minimal in-stent stenosis at the time of re-intervention, and the primary factor was somatic growth of the patient.

The optimal anticoagulation following DV stent placement remains unclear. Use of only heparin [3] or both heparin and
aspirin [4], [7] have been reported, and in one case of heparin monotherapy, there was stent occlusion, which was treated
with urokinase [3]. We elected to continue a low dose heparin infusion for only 72 h, followed by aspirin monotherapy.
While our method of anticoagulation was more conservative given the risk of intraventricular hemorrhage with this
degree of prematurity, thrombotic occlusion of the DV stent did not occur.

Finally, once surgical repair is performed, a patent DV could potentially be problematic given the associated complications
of portosystemic shunts including hyperammonemia with or without encephalopathy and galactosemia [18]. In four of the
prior cases, spontaneous closure occurred, however in one case the patient developed hyperammonemia and required
transcatheter embolization as our patient did [3]. This potential complication requires close monitoring by ultrasound
with color Doppler to assess for persistent patency of the DV.

4. Conclusions
Ductus venosus stent placement can be performed safely in low birth weight, premature infants <30 weeks gestational age
as a palliative measure until adequate age and weight to undergo surgical repair is achieved, although transcatheter re-
intervention may be necessary during the interim and post-surgical periods. The anatomy of the L-shaped portal sinus
relative to the drainage of the vertical vein is a significant factor to be considered in determining whether a transumbilical
or transjugular approach is most optimal to ductus venosus stenting. Adequate delineation of the portal venous anatomy
as it relates to the DV and vertical vein is crucial for successful stent placement.

Declaration of competing interest

There are no known financial interests or personal relationships of the authors which may have influenced the work of
this paper.

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