During the radical resection of hepatobiliary and pancreatic (HBP) cancer, direct invasion of cancer into major vessels, especially the portal vein (PV) and superior mesenteric vein (SMV), poses a significant challenge for achieving curative surgery (Fig. 1). In such clinical scenarios, the role of a vascular surgeon is crucial to ensure safe and successful oncovascular surgery (OVS) [1,2]. The concept of OVS has become popular and is now considered an integral component of curative surgery for advanced cancers [3,4]. An OVS can be defined as a cancer resection with concurrent ligation or reconstruction of a major vascular structure.

Figure 1. Pancreas cancer invading PV and SMV near the splenic vein confluence. PV, portal vein; SMV, superior mesenteric vein; CHA, common hepatic artery.

Portomesenteric vein (PMV) reconstruction is frequently required during HBP surgery. However, the procedure presents several challenges for a vascular surgeon, including size discrepancies between the PV and SMV, lack of suitable autogenous conduits, and the risk of complicated fluid collections and infections. Inappropriate PMV reconstruction may result in immediate complications, such as thrombosis, which can cause bowel swelling and make intestinal anastomoses very difficult, as well as venous hypertension, bleeding, or infection. Furthermore, PMV stenosis or occlusion can result in late atypical variceal bleeding, which is hard to manage [5,6].

PV occlusion after pancreatic surgery is common and often related to inflammation due to complicated fluid collection or increased OVS with vessel reconstruction during tumor resection [1]. Kang et al. [7] showed that PV steno-occlusion is common after pancreatoduodenectomy (PD), particularly after PV resection or chemoradiotherapy. Although the most common cause was tumor recurrence, 17.3% of the patients developed PV steno-occlusion without recurrence.

Although the role of arterial resection in borderline resectable and locally advanced pancreatic cancers remains controversial, PMV resection is generally accepted [8]. Neoadjuvant therapy for locally advanced cancers has improved resectability and yielded satisfactory long-term outcomes [8]. Consequently, the current recommended approach involves administering neoadjuvant therapy, followed by a reassessment of resectability before surgical intervention [9]. This strategy increases the feasibility of achieving curative R0 resection and improves long-term survival. A recent multicenter study in Korea and Japan [10] showed that PMV and jejunal vein resection for pancreatic cancer can be safely performed. Adjuvant therapy and R0 resection were independent prognostic factors.

The advent of preoperative chemoradiotherapy coupled with innovations in surgical devices and techniques has contributed to improved survival rates following periampullary cancer surgery. Paradoxically, this improvement led to an increased incidence of atypical variceal bleeding due to PV occlusion. Atypical hepatico-jejunostomy bleeding is very difficult to treat [6]. Therefore, meticulous PV reconstruction during the initial surgery is essential to prevent this fatal complication. Herein, various techniques to reconstruct the PMV will be discussed with a literature review.

The International Study Group of Pancreatic Surgery (ISGPS) published a consensus statement on borderline resectable pancreatic cancer, including the classification of venous resections [11].

- Type 1. Partial venous excision with direct closure by suture (venorrhaphy)

- Type 2. Partial venous excision using a patch (patch repair)

- Type 3. Segmental resection with primary veno-venous anastomosis (end-to-end anastomosis, EEA)

- Type 4. Segmental resection with an interposed venous conduit and at least two anastomoses (interposition graft)

The National Comprehensive Cancer Network guidelines proposed the anatomic definition of borderline pancreatic cancer as “no contact with the most proximal draining jejunal branch into the SMV” [12]. Because it is often difficult to identify jejunal vein invasion, alternative definition can be “tumor contact 180° or greater or invasion of SMV/PV with bilateral narrowing or occlusion, and not exceeding the inferior border of the duodenum.”

In pancreatic head cancers, vascular invasion typically occurs in the 7-9 o’clock direction. If the circumferential invasion is mild (<20%), the PMV can be repaired with a longitudinal elliptical incision followed by primary lateral venorrhaphy. For moderate invasion (<60%), patch repair is recommended to prevent stenosis (Fig. 2A). If the invasion is greater than 60%, the EEA is generally the preferred approach.

Figure 2. Bovine patch repair techniques for PMV invasion. (A) Patch repair for moderate PMV invasion. (B) Complex patch repair for extensive PMV involvement, encompassing more than 50% of the vessel circumference, with splenic vein reimplantation. PMV, portomesenteric vein; SMV, superior mesenteric vein.

After PV resection, a deeper invasion of the posterior wall may be discovered, rendering simple venorrhaphy unfeasible. In such cases, a custom-trimmed bovine patch is used to match PV defects. The posterior wall suture starts from the far side, followed by anterior running sutures. Patch repair is particularly valuable when invasion occurs near the splenic vein (SV) confluence because it facilitates SV preservation and mitigates the risk of stenosis (Fig. 2B).

An autogenous vein, bovine pericardial patch (BPP), or prosthetic graft can be used as the patch material. While the autogenous vein is the best conduit, I prefer to use a BPP because it is easily available off-the-shelf and more infection-resistant than a prosthetic graft, saving time and additional incision for vein harvest, and the saphenous vein can be reserved for a longer arterial bypass in the future.

In previous studies, bovine patches are more infection-resistant than prosthetic grafts. McMillan et al. [13] reported that BPP provides a durable alternative to the saphenous vein for arterial reconstruction following the removal of infected arterial grafts, including arteriovenous grafts, femoral-distal bypasses, and femoral endarterectomy.

A meta-analysis reported that different patch materials, including autogenous veins, BPP, and synthetic grafts, showed similar short- and long-term outcomes [14]. Noronen et al. [15] reported that BPP is a good alternative to autogenous vein patches in femoral angioplasty, with similar outcomes in patency, restenosis, and infection rates. Moreover, patch ruptures occurred significantly more frequently in the autogenous vein patch group. Previously, we reported the outcomes of vein reconstruction using BPP [16], which showed no infectious complications after BPP repair.

The most basic and ideal reconstruction of the resected PMV is a direct EEA without a conduit (Fig. 3). However, EEA is almost impossible without tension if the cancer invasion extends beyond 3 cm [17]. To ensure long-term patency, EEA should be performed without tension, torsion, or kinking. Fortunately, in most cases, PV resection can be performed using the EEA. If tension-free anastomosis is not guaranteed, tension can be relieved by further dissection of the proximal PV and distal SMV or by right colon mobilization [18].

Figure 3. SMV resection and EEA. SMV, superior mesenteric vein; EEA, end-to-end anastomosis; SV, splenic vein; PV, portal vein.

The first important step before the resection of the PV is to confirm its orientation. If uncertain, marking the PV at the 12 o’clock position with a pen is helpful (Fig. 4). For surgeons who prefer not to use marking pens because of concerns regarding vein wall degeneration, the orientation of the vascular clamps can serve as a guide to prevent torsion. I always clamp the PV and SMV from the 9 to 3 o’clock direction, and an assistant holds and approximates both clamps for the anastomosis.

Figure 4. Marking the 12 o’clock direction of the portal vein with a sterile marking pen is useful to prevent a twist or torsion.

The PV is resected using Metzenbaum scissors to ensure clear gross margins. To minimize the size discrepancy, the SMV can be cut obliquely and more proximally at the 3 o’clock position. After PMV resection, frozen biopsies from both cut ends were obtained to confirm clear resection margins. Occasionally, after preoperative radiotherapy, the PMV may thicken due to inflammation without cancer invasion. The SMV end may need to be tailored obliquely or beveled-off to overcome this size mismatch.

Continuous running sutures with 6-0 polypropylene are applied from the far side to the near side of the posterior wall. Given the difficulty of repairing posterior wall bleeding post-anastomosis, posterior wall stitches should be sewn closely. Posterior wall suturing can be performed from the luminal side while avoiding inversion of the vein wall. After suturing 1/2 or 2/3 of the circumference, the anterior wall is sutured using the other end of a polypropylene suture. Before knotting the sutures, anastomotic tightness should be relieved. Otherwise, anastomotic stenosis is inevitable because of the elasticity of the vein. You can provide a growth factor (intentional loosening of the knot by 3-5 mm) or let the venous flow dilate and expand the anastomosis to its full diameter. I prefer the latter method; before making the final suture, the clamps are released to ensure that there is no thrombus inside and to mitigate anastomotic tightness, followed by gentle tensionless ties of the final suture. Additional sutures could be applied to any bleeding site. A loosened anastomosis is easier to correct than a tight stenotic anastomosis.

Heparin is usually not injected during anastomosis because PD is a high-risk procedure for bleeding and transfusion. The maximal clamping time for PMV anastomosis is unknown; however, immediate thrombosis is uncommon. Before completing the anastomosis, any thrombus at the site should be confirmed by temporary declamping and flushing under direct vision.

In cases of cancer invasion near the SV confluence, EEA can be performed as described above, followed by re-implantation of the SV (Fig. 5). Although the SV can be safely ligated without immediate complications, preserving it prevents left-sided portal hypertension, which can cause variceal bleeding and hypersplenism-associated thrombocytopenia [8,19]. In cases of subsequent PMV stenosis or occlusion, the patent SV serves as a crucial pathway for collateral development and percutaneous intervention.

Figure 5. After the end-to-end anastomosis of the PV and SMV, SV can be reimplanted to the PV. PV, portal vein; SMV, superior mesenteric vein; SV, splenic vein.

When the PV invasion exceeds 3 cm, EEA cannot be performed without tension, necessitating the use of an interposition graft. The conduit can be an autogenous vein, bovine patch or homograft. I avoid prosthetic grafts due to a higher risk of infection and thrombosis, and homografts due to poor availability and potential aneurysmal degeneration. Although autogenous veins are ideal, identifying compatible large veins is challenging. Saphenous vein can be used, however, it is troublesome to make another operation field and incision. Additionally, size mismatch requires back table tailoring with spiral or longitudinal sutures, and sacrificing the long saphenous vein seems to be a waste for a short 2-3 cm interposition. Though an option, the femoral or external iliac veins can cause postoperative leg edema. Therefore, a bovine tube graft that can be easily fabricated with a bovine patch is preferred.

A long, large bovine tube graft can be made on the back table using a tube-like structure or syringe of the desired size. Fig. 6A, B show a 6-cm long bovine tube graft and a good-looking interposition graft. However, it thrombosed during the early postoperative period. Consequently, the bovine tube interposition grafts were limited to a maximum length of 3 cm (Fig. 6C). Usually, cancer invasion is no longer than 5-6 cm, and the EEA can be performed up to 3 cm in length; therefore, only a graft–2-3 cm in length is necessary for interposition.

Figure 6. Bovine graft interposition. (A) A bovine tube graft is sewn on the back table over a tube. (B) A 6-cm long bovine tube graft was interposed. (C) A short bovine tube graft was sewn in situ. (D) Schematic diagram of in situ interposition graft with a bovine patch. PV, portal vein; SMV, superior mesenteric vein; SMA, superior mesenteric artery common hepatic artery; CHA, common hepatic artery; BPP, bovine pericardial patch.

Recently, I preferred to use an interposition tube graft in situ. After resecting the PV, both clamps are approximated, and a tube graft is created in situ to match the distance and diameter differences (Fig. 6D). First, proximal anastomosis begins at the 6 o’clock position on the posterior wall, followed by distal anastomosis, leaving the open patch end on the anterior wall, usually at the 12 o’clock position. The patch graft is then trimmed for longitudinal sutures. The short-tube grafts exhibited good long-term patency. Previously [16], we reported 36 cases of major venous reconstruction using bovine patch angioplasty, with no infections and a thrombotic occlusion rate of 13.9%. Risk factors for thrombosis include tube-shaped repair and emergency surgery due to iatrogenic injury.

Burla et al. [20] also reported good outcomes with intraoperative self-made bovine pericardial grafts for portomesenteric reconstruction in pancreatic surgery.

Various autogenous vein options can be considered in selected cases as substitutes for a large PV (1-2 cm diameter). These include the internal jugular, left renal, external iliac, and femoral vein [21-23], although their availability may be limited. The great saphenous vein (GSV) is a more commonly used option. However, owing to the size mismatch, GSV tailoring is required to achieve a larger diameter suitable for PV reconstruction. The GSV can be modified on the back table using two primary techniques: a spiral vein graft (Fig. 7A) and a longitudinal panel graft (Fig. 7B). After harvesting the GSV of the desired length, a longitudinal venotomy is performed, and the valves are resected. Using a tube-like device with the desired diameter, the GSV can be sutured in a spiral or longitudinal fashion [24,25]. If the GSV is extremely small, three longitudinal pieces can be combined. Again, a 2-3 cm conduit is generally sufficient for the interposition.

Figure 7. Autogenous tailored saphenous vein grafts. (A) Spiral vein graft. (B) Longitudinal saphenous vein panel graft. PV, portal vein; SMV, superior mesenteric vein.

Vuorela et al. [26] reported 69 spiral vein graft reconstructions and concluded that spiral grafts using the GSV are safe and feasible for PMV reconstruction. Lee et al. [22] reported that 15 PMV reconstructions using the femoral vein showed good patency with minimal leg complications.

When autogenous veins are unavailable, alternative autogenous materials can be used as substitutes [27]. Viable options include parietal peritoneum [28,29], falciform ligament [30], and ligamentum teres hepatis [31], which can be safely used as vein substitutes. The mesothelium of the peritoneal covering serves as the endothelium of the vein wall, resulting in a frictionless thrombo-resistant conduit. However, long-term results and possible limitations, such as durability, risk of adhesions, and late thrombosis, need to be further investigated.

Contemporary practice for PMV reconstruction during HBP surgery with vein resection involves various graft options, including autografts, allografts, xenografts, and synthetic grafts, used either as conduits or patches. Prosthetic grafts are associated with a higher incidence of graft thrombosis and potential risk of infection [32]. Allografts offer survival rates comparable to those of EEA, albeit with lower primary patency [33]. However, allografts are not easily available at every center and carry the risk of late degeneration [34].

In the absence of an autogenous vein, a prosthetic graft can be used as a conduit. Garnier et al. [35] reported the results of 19 PMV reconstructions using 10-12 mm ringed polytetrafluoroethylene grafts. The 6-month graft patency rate was 68%, with no reported graft infections. Heparin and low-molecular-weight heparin were administered postoperatively and switched to antiplatelet therapy. Interestingly, the late graft thrombosis rate was higher after distal pancreatectomy than after PD (50% vs. 8%, P=0.049).

The ISGPS classification of venous resection and reconstruction correlates with the severity of tumor invasion and complexity of vein reconstruction. Theoretically, the patency of the reconstructed PMV is better in types 1 and 2 than in types 3 and 4.

Roch et al. [36] reported that SMV/PV thrombosis varied according to the reconstruction technique: 12.8% after venorrhaphy, 13.2% after EEA, 22.6% after autologous vein graft interposition, and 83.3% after synthetic graft interposition (P<0.0001). PMV thrombosis developed in 16% at a median of 15 days and PMV thrombosis was associated with increased 90-day mortality (16.7% vs. 4.9%, P=0.02).

Interposition grafting of the resected PMV can be safely performed using various conduits, including autogenous veins (internal jugular, saphenous, femoral, external iliac, inferior mesenteric, left renal, or gonadal vein), autogenous substitute grafts (parietal peritoneum, falciform ligament, or ligamentum teres hepatis), cryopreserved allografts, xenografts (bovine patch), and prosthetic grafts [27].

Labori et al. [32] conducted a systematic review of patency after PMV reconstruction in 603 patients. Early graft thrombosis (<30 days) developed in 5.6% of the autologous veins, 6.7% of the autogenous peritoneum/falciform ligament, 2.5% of the allografts, and 7.5% of the synthetic grafts. Overall, graft thrombosis developed in 11.7% of the autologous veins, 8.9% of the autogenous peritoneum/falciform ligaments, 6.2% of the allografts, and 22.2% of the synthetic grafts. Notably, synthetic grafts are associated with a higher incidence of graft thrombosis. However, no synthetic graft infections were reported in 158 patients.

PMV can be safely reconstructed during HBP surgery using various conduits, including autogenous veins, peritoneum, allograft, bovine patches, and prosthetic grafts. Meticulous surgical techniques are essential to ensure long-term patency of the reconstructed PMV and prevent thrombosis and resultant variceal bleeding.

None.

Seung-Kee Min has been the editorial board member of the VSI since 2019. Ahram Han and Sanghyun Ahn have been the editorial board members of the VSI since 2023. They were not involved in the review process. Otherwise, no potential conflict of interest relevant to this article was reported.

Concept and design: SKM. Writing the article: SKM. Critical revision of the article: all authors. Final approval of the article: all authors. Statistical analysis: none. Obtained funding: none. Overall responsibility: SKM.