Various innovative surgical techniques have been proposed to improve outcomes of pediatric liver transplantation (LT) because vascular complications can occur in a not negligible proportion of pediatric LT recipients. Pediatric recipients, especially infants, are vulnerable to vascular complications because their graft and recipient vessels are much smaller than those of adult LT. Once graft inflow or outflow vein stenosis occurs, it is difficult to treat it effectively [1-4]. Insertion of an endovascular stent can be a rescue treatment in pediatric patients, but such a stent may not expand sufficiently during physical growth of the recipient from infant to adolescent [5]. Consequently, endovascular stent-associated vascular insufficiency can lead to retransplantation later [6]. Therefore, graft vascular reconstruction requires a secure surgical design in pediatric LT recipients, particularly in infant patients.

Secure graft outflow vein reconstruction is essential for successful LT, especially in infant patients because they have definite demerits vulnerable to hepatic vein outflow obstruction (HVOO). Small size of the recipient vein and size mismatch during hepatic vein reconstruction can induce anastomotic stenosis. Extrinsic compression due to large-for-size graft can result in functional obstruction of the outflow vein. Laparoscopic donor hepatectomy often results in very short hepatic vein stumps, which is not suitable for direct anastomosis [7,8]. To minimize the risk of HVOO, it is necessary to perform individually designed reconstruction customized to each pediatric LT operation. Although various surgical techniques have been used for hepatic vein reconstruction in pediatric LT, their main principle can be expressed as making anastomosis as large as possible. We present our tailored surgical techniques for hepatic vein reconstruction in pediatric LT with the following six topics.

The usual left lateral section (LLS) graft has one left hepatic vein (LHV) trunk with complete preservation of the middle hepatic vein trunk at the donor side. The orifice size of this donor LHV trunk is often as small as the diameter of the retrohepatic inferior vena cava (IVC) of an infant recipient, thus this graft outflow vein orifice is often considered to be too small to perform direct anastomosis even in an infant recipient. It is important to make both graft and recipient hepatic vein orifices large enough by widening unification venoplasty to compensate such surgical procedure-related stenosis (Fig. 1).

Figure 1. Illustrations of unification venoplasty of the recipient hepatic veins to make their stumps thick and long. (A) The hepatic vein stumps are transected, leaving a bulk of the hepatic parenchyma. (B) The intervening septum between the left and middle hepatic vein openings is cut. (C) The intervening septum between the right and middle hepatic vein openings is transected. (D) Three hepatic vein openings are unified to make a wide single orifice.

After the recipient native liver is completely dissected, the hepatic parenchyma is incised with a surgical knife, by which a bulk of hepatic parenchyma is left around the hepatic vein trunks. A longitudinal incision is applied at the hepatic parenchyma between the right hepatic vein (RHV) and the middle hepatic vein (MHV) trunks. The attached hepatic parenchyma is then separated into two parts. The hepatic parenchyma is forcefully pulled out to detach from the hepatic vein stumps, which makes the hepatic vein stump walls long and thick. The IVC wall septa between the RHV and the MHV stumps and between the MHV and the LHV stumps are incised consecutively to make a single large hepatic vein orifice. The V-shaped anterior wall defect between the RHV and the MHV stumps at the hepatic vein orifice is repaired with a continuous suture. This unification procedure makes the transverse diameter of the recipient hepatic vein orifice twice larger than that of the retrohepatic IVC. It also makes the stump of hepatic vein orifice thick and long enough (Fig. 2) [9].

Figure 2. Unification venoplasty of the recipient hepatic vein stumps. (A) The native liver of the recipient is completely dissected and the hepatic parenchyma is then incised with a surgical knife. (B) A bulk of the hepatic parenchyma is left around the hepatic vein stumps. (C) A longitudinal incision is applied at the hepatic parenchyma between the right and middle hepatic vein trunks, by which the attached parenchyma is separated. (D) The hepatic parenchyma is forcefully pulled out to detach from the hepatic vein stumps. (E) The septa between the right and middle hepatic veins and between the middle and left hepatic veins are incised. (F) The defect at the anterior wall between the right and middle hepatic vein stumps is repaired with continuous sutures. (G) The size of the unified hepatic vein orifice is twice larger than the diameter of the inferior vena cava. (H) The size of the unified hepatic vein orifice is well matched with that of the graft hepatic vein orifice.

A small proportion of patients with biliary atresia show biliary atresia-polysplenia syndrome, which can manifest agenesis of the IVC. Since there is no retrohepatic IVC, the graft hepatic vein has to be directly anastomosed with the suprahepatic confluence of the recipient hepatic veins (Fig. 3) [10].

Figure 3. Graft hepatic vein reconstruction in a patient with agenesis of the inferior vena cava (IVC). (A, B) There is agenesis of the retrohepatic IVC. (D) The portal vein is continued with the azygos vein (arrow). (C) The orifices of the three hepatic veins at the suprahepatic confluence are unified. (D) The suprahepatic confluence of the recipient hepatic veins is directly anastomosed with the graft hepatic vein.

LLS grafts can be divided into four groups, based on the type of donor surgery (open or laparoscopic) and the presence or absence of a superficial LHV branch (Fig. 4) [11].

Figure 4. Pathways to choose the hepatic vein venoplasty method for left lateral section grafts. LHV and sLHV indicate the orifices of the left hepatic vein and its superficial branch, respectively. Incision indicates an incision on the medial side of the left hepatic vein wall. Vein patches are applied to the semicircular area or to the full circumference.

For an open-recovered LLS graft not having a superficial LHV branch, a small incision is made and a semicircular vein patch is attached to the medial end of the LHV orifice (incision-and-patch venoplasty). If the graft LHV orifice appears to be large enough (≥2 cm for infant recipients), venoplasty is not applied. For an open-recovered LLS graft containing a superficial LHV branch, an incision is made over this vein. The LHV and this branch is then unified to widen the outflow vein orifice. If this unified vein orifice is large enough (≥2 cm for infant recipients), no vein patch is attached (Fig. 5). Otherwise, a semicircular vein patch is attached at the lateral end of the LHV orifice (Fig. 6). If the graft LHV orifice per se appears to be large enough (≥2 cm for infant recipients), venoplasty is not performed [11].

Figure 5. Hepatic vein reconstruction of a left lateral section graft without patch venoplasty. (A) A small superficial left hepatic vein branch is located at the left end of the left hepatic vein stump. (B) This vein branch is incised to expose the lumen. (C) A septum between the two vein orifices is incised. (D) The two graft vein openings are unified with a continuous suture.

Figure 6. Hepatic vein reconstruction of a left lateral section graft with patch venoplasty. (A) A small superficial left hepatic vein branch is not recognized at a glance. (B) A very small branch is identified through a thorough examination and incised to expose the lumen. (C) The two vein openings are unified with a continuous suture. (D) A vein homograft patch is attached over the periphery of the incised superficial branch.

For a laparoscopically-recovered LLS graft, a small incision is made at the medial end of the LHV orifice in the absence of a superficial LHV branch or at this branch if it is present, and then a circumferential vein patch is attached because the graft LHV stump is usually too short to anastomose directly (Fig. 7) [7,11].

Figure 7. Hepatic vein reconstruction of a left lateral section graft with incision and circumferential patch venoplasty in a laparoscopically recovered graft. (A) A small superficial left hepatic vein branch is not recognized at a glance. (B) The medial wall of the left hepatic vein trunk is incised first. (C) A vein patch is attached at the medial half of the left hepatic vein opening. A very small superficial left hepatic vein branch is incidentally identified and incised. (D) A vein patch is attached at the lateral half of the opening, resulting in a completely circumferential patch.

The anatomy of the LHV is diverse, but the majority of graft LHVs are suitable for direct anastomosis to the recipient hepatic vein stumps or directly to the IVC. However, in rare instances, the LLS outflow drains through both LHV and MHV or the LHV flow drains directly through the MHV trunk (Fig. 8) [12,13]. In donors with such variant LHV anatomy, it is necessary to preserve the MHV trunk for the safety of the living donor or for securing split extended right liver graft.

Figure 8. Classification of the hepatic vein anatomy in the left lateral section based on the patterns of the left lateral section graft hepatic vein openings. Type 1 makes a single opening. Type 2 makes two widely spaced openings. Type 3 makes two large and small adjacent openings. Type 4 makes two widely spaced openings. Crossed circles indicate the location of the umbilical portion.

If a sizable anomalous hepatic vein branch is present at the graft liver cut surface in addition to the orthodox LHV opening, a wedged unification venoplasty is necessary to facilitate hepatic vein reconstruction (Fig. 9) [12]. If the graft LHV opening is located at the cut surface of the LLS graft instead of at the cephalic apex, a customized venoplasty using a funneling patch venoplasty is necessary to make it suitable for graft hepatic vein reconstruction (Fig. 10) [13].

Figure 9. Interposition-wedged unification venoplasty to join the two anomalous hepatic vein openings. (A) Design of customized venoplasty techniques to unify a widely spaced segment III hepatic vein (V3) orifice to the left hepatic vein (LHV) trunk is illustrated. (B) A separate V3 orifice is located at the liver cut surface (arrow). A cryopreserved ilio-femoral vein allograft is prepared. (C) End-to-side anastomosis is performed to the V3 orifice. (D) The interposed vein is attached to the incised left hepatic vein trunk. Some interposed vein cuffs are preserved for later size matching to the recipient hepatic vein orifice.

Figure 10. Customized funneling venoplasty for an anomalous graft left hepatic vein opening. (A) Illustrations show the design of funneling venoplasty. Arrow indicates a slit incision. (B) The small left hepatic vein orifice is partially incised to increase the diameter and a vein patch is attached to make a funnel-shaped conduit. Arrow indicates a slit incision. (C) The hepatic vein openings at the recipient inferior vena cava and the graft are well matched in size.

A left liver graft has two outflow veins, the LHV and MHV. In a left liver graft harvested through an open surgery, the shape of the graft outflow vein orifices appears to be a single orifice or similar to a figure of 8, thus requiring simple unification venoplasty with or without excavation of the intervening hepatic parenchyma (Fig. 11) [12].

Figure 11. Hemodynamically compliant techniques of wedged unification venoplasty commonly used for left liver grafts. (A) Some liver parenchyma between two hepatic vein orifices is excavated. If necessary, additional crossing septotomy (bidirectional arrow) can be performed to deepen this common channel portion. When two hepatic vein openings are separated by a substantial distance, the intervening parenchyma should be removed to facilitate approximation. An excavated portion such as this is simply repaired by central approximation tying and bidirectional suturing with a monofilament. (B) After graft regeneration/remodeling, the inferior vena cava (IVC) portion is expected to be compressed. Maintenance of the common channel within the hepatic parenchyma (arrows) is beneficial to preserve hepatic outflow into the IVC.

In contrast, in a left liver grafts harvested through a laparoscopic surgery, the stumps of the LHV and the MHV are usually separate completely [8,14]. Thus, a complex unification venoplasty is often necessary to achieve secure hepatic vein reconstruction. The surgical technique of unification venoplasty for laparoscopically harvested left liver grafts is different from that for laparoscopically harvested LLS grafts. The intervening hepatic parenchyma between the LHV and MHV openings is excised through septotomy. A unification septoplasty is then performed. An incision is made at the medial wall of the MHV trunk and a vein homograft patch is attached to make the graft outflow vein orifice large enough (Fig. 12) [8].

Figure 12. Patched unification venoplasty for two separate hepatic vein openings used in a laparoscopically recovered left liver graft. (A) There are two separate openings of the left hepatic vein (LHV) and middle hepatic vein (MHV). (B) The intervening hepatic parenchyma between these openings is excised through septotomy. (C, D) A unification septoplasty is performed. (E) An incision is made at the medial wall of the MHV trunk. (F) A vein homograft patch is attached, making the graft outflow vein orifice large enough.

Replacement of the retrohepatic IVC after concurrent resection of hepatoblastoma and IVC or in Budd-Chiari syndrome is an optional technique of living donor LT, as in adult living donor LT for managing hepatocellular carcinoma around the IVC or Budd-Chiari syndrome [15-18]. In pediatric patients, synthetic vascular grafts cannot be used because of ongoing physical growth. Because the IVC is a large vein, a large-sized vein homograft such as IVC (Fig. 13) and iliac vein (Fig. 14) depending on the body size of the recipient and the availability of vein homograft should be used for replacing the recipient IVC [17,18].

Figure 13. Inferior vena cava (IVC) replacement with IVC homograft in a pediatric patient with hepatoblastoma. (A) The middle and left hepatic vein orifices of the left liver graft are unified. (B, C) An IVC homograft is anastomosed to the left liver graft. (D) The graft IVC is anastomosed to the recipient IVC stump.

Figure 14. Inferior vena cava (IVC) replacement with IVC homograft in an infant patient with hepatoblastoma. (A) The left hepatic vein orifice of the left lateral section graft is enlarged with patch venoplasty. (B) A common iliac vein homograft is attached to the graft to replace the retrohepatic IVC. (C, D) The supra- and infra-hepatic ends of the recipient IVC are anastomosed with the graft IVC conduit.

The retrohepatic IVC is quite small in infant recipients, thus conventional techniques used in adult LT with a whole liver graft should not be used in infant LT. The modified piggyback anastomosis technique is a mixed form of the conventional piggyback technique using the recipient hepatic vein orifice and the conventional double IVC technique (Fig. 15). The dorsal wall of the graft IVC is incised longitudinally close to the infrahepatic stump of the graft IVC. The operation field for IVC anastomosis is very narrow in infant patients. Thus, the caudal apex of the anastomotic triangle should be sutured first. Side walls are then gradually sutured toward the hepatic vein orifices (Fig. 16) [19].

Figure 15. Modified piggyback anastomosis of a graft inferior vena cava (IVC). The matched IVC walls at the graft and recipient are incised with unification of the recipient hepatic vein orifices. Three corners of two inverted triangles are sutured for anchoring to adjust the suture lines (dotted bidirectional arrows).

Figure 16. Modified piggyback anastomosis of a graft inferior vena cava (IVC) in infant-to-infant whole liver transplantation. (A) The dorsal wall of the graft IVC is incised longitudinally close to the infra-hepatic stump of the graft IVC. (B) The anchoring suture starts at the apex of the inverted triangles. (C) The operation field for IVC anastomosis is very narrow in infant patients, thus the caudal apex of the anastomotic triangle should be sutured first, and then the side walls are gradually sutured toward the hepatic vein orifices. (D) More than three-fourth of the graft IVC are anastomosed in the side-to-side fashion.

Secure graft outflow vein reconstruction is the most important step for successful pediatric LT. Once HVOO occurs, it is difficult to treat it effectively [1-4] and the sequences of treatment are often intractable. Endovascular stenting in infant patients should be the last life-saving procedure because it can induce stent-associated vascular insufficiency according to physical growth of the recipient from infant to adolescent [5,6].

We have reported the sequence of triple LTs performed in a 13-year-old girl as a typical example of endovascular stenting-associated catastrophic events [6]. The patient was diagnosed with biliary atresia-polysplenia syndrome. She underwent living donor LT using a LLS graft at 9 months of age. The first liver graft failed due to stenosis of the portal vein. She underwent the second LT using a split LLS graft. Endovascular stenting was performed for portal vein stenosis at 2 months and for hepatic vein stenosis at 9 months after the second LT. During the next 9 years, 11 sessions of balloon angioplasty to treat HVOO were performed. Ten years after the second LT, she underwent the third LT using a whole liver graft. A double IVC technique was used for outflow vein reconstruction and the graft portal vein was anastomosed with the stent-containing portal vein stump because it was impossible to remove the stent and the inner diameter of the portal vein stent was large enough. We presume that such graft failure might not happen if our customized techniques for hepatic vein reconstruction had been used.

There are three features in our techniques for graft hepatic vein reconstruction. The first feature is the maximal usage of the recipient hepatic vein stumps. The intrahepatic portions of the three hepatic vein trunks are used for recipient-side hepatic vein patch, making the diameter of recipient hepatic vein orifice twice larger than that of the retrohepatic IVC. They also make the stump of hepatic vein orifice thick and long enough.

The second feature is the maximal widening of the graft outflow vein orifice through unification and patch venoplasty. The shape and size of the LLS and the left liver grafts are uniformly wide through meticulous benchwork. The transverse diameter of hepatic vein anastomosis is more than 2 cm even in very young infant patients. The actual cross-sectional area of the hepatic vein anastomosis is much smaller than the transverse diameter of hepatic vein anastomosis because a considerable portion of the enlarged vascular cuffs is buried during anastomosis. Considering this sequence, it is essential to make the diameter of hepatic vein anastomosis as large as possible.

The third feature is the frequent use of vein homografts. Since synthetic vascular grafts cannot be used for pediatric patients due to their ongoing physical growth, vascular homografts should be used. We have maintained an institutional tissue bank for more than 20 years to supply various vascular homografts. If an adequate vein homograft for pediatric living donor LT is not available from the tissue bank, we often delay the LT operation until obtainment of a suitable vein homograft. All human tissues stored at the tissue bank were donated after informed consent was obtained from the donors’ family members. All procedures for vascular tissue procurement and processing were in compliance with Korean legislation. They conformed to ethical and safety concerns for therapeutic use [20]. Currently, cryopreserved homografts of the femoral vein and artery, and the greater saphenous vein are commercially available through the Korea Public Tissue Bank.

In conclusion, secure graft outflow vein reconstruction is the most important step for successful pediatric LT. Thus, every effort should be done to minimize the risk of HVOO. We strongly suggest that the diameter of graft hepatic vein anastomosis should be made as large as possible regardless of recipient age and body size.

None of the authors was supported financially for this study.

All authors have no conflicts of interest to declare.

Conceptualization: SH. Data curation: SH, JMN. Methodology: SH, JMN. Visualization: SH. Writing - original draft: SH. Writing - review & editing: SH.