Technical aspects of uniportal video-assisted thoracoscopic double sleeve bronchovascular resections

Summary

Double sleeve, bronchial and vascular reconstructions are challenging procedures indicated for centrally located tumours to avoid pneumonectomy. Traditionally, these resections have been performed by thoracotomy, but thanks to advances in imaging systems, better surgical instruments and the gained experience in video-assisted thoracic surgery (VATS), the scenario now is different. During the last decade, we have seen a rapid evolution of the uniportal VATS technique from simple lobectomies to advanced double sleeve bronchovascular procedures and carinal resections. The advantages of VATS over open surgery for major lung resections in terms of postoperative pain and morbidity, length of hospital stay and quality of life have prompted experienced surgeons to adopt uniportal VATS for cases requiring a sleeve resection. However, when a double bronchial and vascular sleeve resection is required, the adoption rate of minimally invasive surgery is still very low even for very experienced VATS surgeons. The difficulty of tumour mobilization, complexity of the suturing technique and the concern about possible uncontrolled massive bleeding during VATS are the main reasons for this low rate of adoption. In this article, we describe the technical aspects and tricks of this procedure when it is done by the uniportal VATS approach.

INTRODUCTION

Parenchyma-sparing double sleeve resections, when feasible, are recommended for the treatment of central tumours or lymph nodes involving the origin of a bronchus or artery or extending into the main bronchus or main artery [1]. Data accumulated over the past decades indicate that the same oncological outcome can be achieved, but with lower morbidity and mortality and improved postoperative quality of life [2]. Although technically more demanding, double sleeve resections can be performed with minimally invasive surgery. Thanks to advancements in imaging systems, instrument designs and experience in video-assisted thoracic surgery (VATS), these procedures can even be performed through a single incision in expert hands [3, 4]. Due to certain tumour characteristics such as central location or size, double bronchovascular reconstructions pose certain challenges not present during bronchial sleeve resections. The combined bronchial and vascular sleeve resections with an end-to-end anastomosis are the most complex procedures in minimally invasive thoracic surgery. In this article, we try to present a standardized way to treat such challenges by uniportal VATS, in an attempt to simplify the intraoperative decision-making process and strategy of the surgical team conducting such a complicated procedure.

LOCATION OF INCISION

The site of the incision is of utmost importance in uniportal VATS double sleeve resections, as it can facilitate or impair the efficacy of the suturing. Placing the incision at the 4th intercostal space at the anterior or middle axillary line provides a direct access to both ends of the bronchial tree and/or artery and enables suturing in an axis almost perpendicular to that of the anastomosis, similar as in open surgery [3]. For sleeve procedures, it is more convenient to place that incision higher than lower. A wrong location of the incision, for example at the 5th or 6th intercostal space, can make the vascular anastomosis extremely difficult through a uniportal approach. If this would happen, we recommend making another incision in a higher intercostal space throughout the same skin incision.

The only problem posed by using the 4th intercostal space on the left side is the difficulty of the stapler insertion to divide the upper vein. In addition, as in the case of large central tumours, the mobilization is normally not easy, which could make the vein transection even more difficult. We recommend different strategies to solve this issue: (i) using curved tip staplers with maximum angulation; (ii) opening the pericardium (allows more proximal and better dissection of the pulmonary vein); (iii) using a TA 30-mm vascular linear stapler for open surgery; or (iv) proximally ligating the vein with a double transfixive suture and then cutting the vein distally with scissors once the artery is occluded.

EQUIPMENT

Due to the complexity of these techniques, the use of high definition cameras is mandatory, as the bronchial and particularly the vascular anastomosis should be very precise. We recommend either a 5-mm or a 10-mm, 30° thoracoscope. Energy devices are important either for dissection or to accomplish a systematic lymphadenectomy. We do not recommend the use of polymer clips for small vessels in these procedures to avoid interference with the suture during the anastomosis. Curved tip staplers are also very helpful, especially for the division of the left upper lobe (LUL) vein. A wound protector and specifically designed instruments for thoracoscopic surgery with double joint articulation are also recommended. For the bronchial anastomosis, we recommend the use of a thoracoscopic curved tip needle holder, a long curved suction for retraction and exposure of the anastomotic site and a simple straight thoracoscopic knot pusher with the u-shaped tip. Also, needed for the vascular anastomosis is a curved thoracoscopic Debakey forceps to delicately grasp the edge of the artery during the reconstruction.

SURGICAL TECHNIQUE

For tumours involving both the central bronchus and the pulmonary artery (PA), bronchovascular sleeve resections are the only way to avoid pneumonectomy. Uniportal VATS technique represents the less invasive approach, but the technique poses certain challenges because all of the instruments are placed through a single small incision. The camera must always be located at the top of the incision, and the instruments need to be introduced below the camera through the lower part of the incision. The uniportal approach gives us an excellent panoramic view and an optimal exposure of the hilum with direct vision during suturing. Working with bimanual instrumentation in a sagittal plane (uniportal technique) could make the suturing technique easier and more ergonomic in expert hands.

The most frequent location of tumours suitable for double sleeve resections is in the LUL. Double sleeve resections on the right side are extremely rare and very challenging. This is because the deep location of the PA stump for the anastomosis is usually hidden by the superior vena cava (SVC).

Left-side double sleeve lobectomy

At the beginning of the procedure, it is advisable to perform a systematic lymph node dissection including stations 5, 6, 7, 8 and 9, as well as the release of the inferior ligament and opening of the pericardium. We also recommend starting with a careful evaluation of the artery in the fissure to rule out distal involvement and to confirm the viability of the procedure.

Not all the tumours seen in the computed tomography (CT) scan that look like they invade the artery require a complete vascular sleeve. If the tumour invades the main trunk, a proper circumferential arterial section proximally and distally is needed followed by an end-to-end anastomosis (vascular sleeve). However, if the tumour involves only one or more arterial branches up to their orifice, the involved tributary can be transected at its orifice with scissors and the main trunk sutured after the removal of the lobe (plasty) [5]. In both situations, proximal and distal occlusion is necessary.

Vascular control

One of the most important aspects when performing double sleeve procedures is appropriate vascular control. In the initial vascular procedures that we described in 2013, we used 2 vascular clamps through the incision, making the instrumentation more difficult than necessary as it took up unnecessary space [6]. In 2014, we described the first full uniportal double sleeve procedure using a vascular clamp for the main PA and a bulldog clamp for distal artery [7]. The use of bulldog clamps allowed us to have more space through the incision. However, the proximal placement of the vascular clamp on the main PA was not easy and the possibility of displacement was always a concern during the procedure. To improve the technique after gaining experience with these procedures, we developed at Shanghai Pulmonary Hospital the use of tourniquets to clamp the artery both at the proximal and distal edges [8, 9]. To ensure correct and safe clamping of the artery, we tied the tourniquet with 3 threads of number 0-silk and we left it inside the thoracic cavity. Once tied, the tourniquet must display a bent form to ensure proper occlusion. In the case of tumours with very proximal invasion of the artery, we use 2 tourniquets at the proximal level to ensure safer vascular control. To avoid displacement of the tourniquet, we use a wet gauze to keep it fixed in the apex and at the diaphragmatic face of the thoracic cavity. The main advantage of the tourniquets is the safety provided to the PA clamping, which also avoids the interference of excess instrumentation through the incision for the anastomosis.

In the case of large proximal tumours, it is sometimes advisable to perform intrapericardial control by dissecting the PA proximal to the ductus arteriosum to place the tourniquet in this position [10]. In this way, the ductus acts as a stop to prevent accidental displacement (Fig. 1). For tumours with a very central and proximal location, and when the length of the PA is short, the most advisable manoeuvre is to divide the ductus (prolongs the length of the artery >1 cm) [11] and use a thoracoscopic clamp. The thoracoscopic clamp should be placed outside the wound protector to decrease interference during the anastomosis (Fig. 2). It is very important to secure the clamp closure by tying a silk around the jaws to avoid the clamp from accidentally opening. We must also take special care with our movements during the surgery to avoid an abrupt displacement or traction on the clamp. We recommend using intravenous heparin before clamping to prevent thrombosis and subsequent pulmonary embolism. Doses could range from 1500 to 5000 IU [8–12].

One of the disadvantages of using a vascular clamp is that we cannot extract the tumour once the lobectomy is finished because the clamp interferes with removal through the incision. For this reason, we must be sure that the macroscopic surgical margins are free of tumour. If we are not sure about it, it is best to send an additional cut of the artery or bronchus for frozen section and wait for an intraoperative result. Once we have confirmation that the margins are free, we must position the lobe on the diaphragmatic side, begin the anastomosis and then extract the tumour at the end after the clamp is removed.

When the tumour extensively involves the fissure, dissection of the basal trunk and A6 branch independently with the use of 2 tourniquets is recommended to increase the length of the distal arterial stump. In the event dissection of distal artery is difficult, the inferior pulmonary vein may be clamped instead of the distal artery. Although this manoeuvre can suffice in preventing backflow coming from the distal PA, a little bleeding may still occur due to the collateral network between the bronchial arterial circulation and the pulmonary arterial circulation [12].

Anastomosis

In a double sleeve procedure, the transection of the artery usually precedes that of the bronchus, while reconstruction of the bronchus precedes that of the artery to avoid tension on the vascular anastomosis. After the transection of the superior pulmonary vein with a stapler, the main PA can be sectioned proximally by using scissors (Fig. 3A), then the distal PA (Fig. 3B) and finally the bronchus. It should be taken into account that whenever we cut the artery, there is considerable proximal retraction. Therefore, it is important to not pull the lobe too much to avoid tearing the artery proximally and to cut as distal as possible (when the tumour allows) (Fig. 4, Video 1).

The bronchial anastomosis of the LUL is a relatively easy sleeve due to the lateral orientation of the bronchial stumps and the absence of the PA, which is snared with a tourniquet. Occasionally, when the invasion of the PA is very extensive, it is advisable to perform a bronchial sleeve even in the absence of endobronchial involvement to reduce tension on the vascular anastomosis.

The idea is to perform a 360° circumferential suture using 1 thread and 2 needles for knotting only once at the most anterior portion of the suture [8]. An absorbable 3–0 PDS double-armed suture for every bronchial sleeve anastomosis is recommended (monofilament Prolene non-absorbable suture is also an alternative) (Fig. 5A, Video 1).

Once the bronchial anastomosis has been completed, we recommend using a hook to adjust the tension, pulling each point along the entire visible part of the anastomosis. We check for leakage with water while insufflating the lobe up to a pressure of 30 mmHg. If there is an isolated point of leakage, we can use an interrupted suture for its closure. The anastomosis can be covered with a pleural flap, pericardial tissue, thymus or an intercostal muscle flap. It is not clear that this manoeuvre prevents bronchoarterial fistula, but it can nevertheless be useful to cover a small leak that has gone unnoticed [12].

For a vascular reconstruction, the suturing technique we apply is the same as the one described for the bronchus (360° circumferential suture) (Fig. 5B). A 4–0 or 5–0 double needle (no >16 mm) Prolene suture is preferred (Fig. 4C and D) [8]. It is recommended to irrigate both stumps of the artery with a heparin solution before starting the reconstruction, to wash away debris from the endothelium to prevent a possible pulmonary embolism.

During the vascular anastomosis, it is very important to be extremely careful to avoid pulling the thread abruptly as it could tear the wall of the artery. Once the vascular anastomosis is finished, we recommend irrigating back into the artery with heparin to avoid small thrombi. Before knotting, we must first release the distal tourniquet gradually to favour the return flow and allow air to escape and prevent embolism. Once we see bleeding coming from the distal site, we can tie the knots (Video 1). If after tying there is no bleeding, presumably there will be no bleeding from the proximal site (it does not work in all cases). The last part is the release of proximal tourniquet.

Right-sided double sleeve resections

Right-sided double sleeve procedures are very rare and more challenging than the left side due to the relation of the main PA with the SVC. In case this procedure is needed, and to avoid a pneumonectomy, a bilobectomy is usually required.

It is recommended to divide the azygos vein and fix both stumps with a stitch to the parietal pleura at the anterior and posterior levels. This manoeuvre retracts the superior cava vein anteriorly, allowing better visualization to obtain more proximal control of the PA. If mobilization of the tumour allows good exposure of the paratracheal and subcarinal stations, we recommend the removal of all the lymph nodes at the beginning of the procedure. In the case of large tumours with difficult mobilization, removal of the lymph nodes should be performed after the tumour is removed.

Opening the pericardium is almost mandatory in right-sided double sleeve resections to achieve more proximal control of the PA.

We recommend dissection from the anterior aspect of the right hilum, using a hook cautery or energy device to gently open the anterior mediastinal pleura. The superior and middle lobe pulmonary vein can be dissected and divided first. If we clearly detect that the main PA is involved at its origin, the pericardium must be opened initially to allow encircling of the main PA intrapericardically to get more margin for clamping.

If the oblique fissure is good, the lower artery should be dissected and encircled. In the case of a bad fissure, we must divide it from the hilum following the tunnel technique to expose the lower artery.

Adequate PA control requires careful dissection of the main PA and removal of the lymph nodes surrounding the hilum. On the right side, we always use tourniquets for clamping the artery because the use of a clamp for the main PA would interfere with the anastomosis due to the location of the SVC. Once the proximal and distal arteries are occluded, the sequence could be as follows: we first cut the distal portion of the artery with scissors, then the intermedius bronchus, then the main PA and finally the main bronchus (Fig. 6A and B).

Once the specimen is removed, an end-to-end bronchial anastomosis must be performed first because the right main bronchus is anatomically beneath the main PA from a uniportal view, and also to diminish the tension on the vascular anastomosis to be performed later. Both anastomoses are performed following the same technique as on the left side (Figs 6C and D and 7, Video 2).

What to do in case of bleeding after the anastomosis

One of the biggest concerns of this procedure is the accidental displacement of the tourniquet during the anastomosis. It is very important to place the tourniquet proximal to the ductus to act as a barrier and avoid displacement (Fig. 1). We recommend using 3 threads of size 0-silk. We then thread these tourniquet sutures through a small plastic tube to push the tourniquet and fix it strongly on the base to constrict the artery. We must see that the tourniquet plastic tube has bent to be sure it is safely fixed. Using a vascular polymer clip to create traction on the tourniquet thread is another option, but it is not safe in the case of a total vascular sleeve.

When the anastomosis has been completed, we release the distal tourniquet first. If bleeding happens along some point of the anastomosis after tying the knot, we need to place an additional stitch. The use of the angiorrhaphy technique is very useful in this situation, using the tip of the suction to compress the hole and rolling it around the suture line that is bleeding (Fig. 8A) [13, 14]. In the event of important bleeding, we recommend reclamping the distal site using another tourniquet or using a vascular thoracoscopic clamp on the distal part of the artery (Fig. 8B).

If bleeding occurs after releasing the proximal tourniquet, we must try to place a stitch using the same technique. The only disadvantage of using a silk tourniquet is that, at the end of the procedure when we cut the silk and release the tourniquet, we cannot tighten it again with the same thread and need to use a new tourniquet (for this reason, it is advisable to encircle the main artery with an additional silk at the beginning of the procedure) (Video 1). A vascular clamp should always be ready to control the artery proximally in case of important bleeding.

Summary

We can summarize the following tricks:

• Open the pericardium for safe vascular control in the case of a blocked hilum or very proximal tumours;

• Ensnaring the artery is preferred over clamping because the tourniquets can be placed inside the chest, thus sparing the space at the single incision access for the use of instrumentation and the camera;

• Transect the ductus ligament if very proximal arterial control is needed in the left hemithorax;

• If a thoracoscopic clamp is used, place it out of the wound protector;

• Release the inferior pulmonary ligament to ensure a tension-free anastomosis. if tension is still an issue, make an intrapericardial release;

• When the tumour extends into the fissure, distal vascular control on the left side is better managed by ensnaring the superior and basal arterial branches separately;

• Clamp the inferior pulmonary vein whenever the tumour involves the fissure and distal arterial control is difficult;

• In the right side, transect the azygos arch at the level of the azygos–SVC junction, fix the stumps to pleura and open the pericardium; and

• Release the distal tourniquet first before tying to remove air inside the vessel. In case of bleeding, always have a thoracoscopic clamp ready and be prepared to use the angiorraphy technique for suturing.

RESULTS (SINGLE SURGEON)

The personal experience of the corresponding author of this article includes as follows: 24 cases performed since 2014 (22 left side, 2 right side), mean age 58 ± 6.1 years (20 males, 4 females), mean surgical time 225 ± 55 min, median length of stay 7 days (5–26) and no perioperative mortality. One patient presented prolonged air leak of 18 days, which was solved with conservative treatment. Another patient showed thrombosis on the anastomotic site (main artery occluded in a CT scan control) and was treated with anticoagulation with no clinical repercussions.

DISCUSSION

Even though the benefits of performing bronchovascular reconstructions to prevent pneumonectomy are not questionable, most of these procedures are still performed by thoracotomy due to their complexity [15]. However, the technical advances and experience gained in VATS during the last years have encouraged surgeons to expand the applications for complex bronchovascular reconstructions to include multiportal VATS [16] or even the uniportal single incision approach [7].

The geometrical characteristics of the uniportal approach, working in a sagittal plane and performing bimanual instrumentation, are suitable for sleeve procedures [17]. Since the first uniportal VATS sleeve resection reported in 2013 [18], many groups have adopted this technique for bronchial sleeve anastomosis [19]. However, the end-to-end anastomosis of both the artery and the bronchus is extremely difficult procedures by minimally invasive surgery and very few surgeons can successfully perform it through a uniportal VATS approach [8–11]. There are very few reports in the literature of series for double sleeve resections performed by uniportal VATS [11, 20].

When performing a VATS double sleeve lobectomy, a surgeon has to face the same challenges as those that occur during open surgery. These are generally related to large-sized tumours accompanied by inflammatory changes in the pleural cavity and hilum, and strong adhesions after neoadjuvant chemoradiotherapy [15]. To perform such difficult procedures, the surgeons must have a large experience in uniportal VATS and also be experienced with a considerable number of bronchoplastic procedures. The vascular reconstruction is much more difficult than the bronchial part. The LUL bronchial sleeve suture is relatively easy because there is no interference with the PA. It will usually take ∼15–20 min, while the vascular anastomosis may take up to 40–50 min even in expert hands. We must be extremely careful with every stitch and traction to avoid tears of the vessel wall that could be complicated to repair if the tear goes proximally. One of the most important points is to be sure about the correct alignment of both vascular edges to avoid malrotation. We must be more careful with every stitch in the posterior wall (the most difficult part), and in the posterior angle because bleeding from a hole located in the posterior aspect is difficult to repair by uniportal VATS. The superior wall of the artery is the easiest part, and normally, we can suture both edges with a single movement in every stitch.

In bronchovascular reconstructions, it is crucial to understand and visualize the extent of tumour invasion in the hilum and in the fissure. A careful confirmation of the absence of a tumour involving the lower artery or bronchus on the left side must be performed from the beginning to define the viability of the procedure. Usually, tumours requiring double sleeves are large tumours. In these cases, opening the pericardium and intrapericardial upper pulmonary vein division are advised [10].

One of the disadvantages in the early period of the uniportal technique for double sleeve procedures was the need to use a vascular clamp through the incision [6, 7]. However, thanks to the use of tourniquets, we have sorted out this issue and avoid interference with the clamp during the instrumentation. The use of a vascular clamp is still recommended in the case of tumours extending too deep into the main trunk of the PA. The transection of the ductus arteriosus enlarges the artery and allows safer placement of the arterial clamp [11].

Compared with our previous reports, we have also improved our technique for suturing. Even though there are no clear data in the literature favouring interrupted or continuous sutures (one over the other), we clearly prefer a running suture to achieve a tension-free anastomosis. In the period of open surgery, Tronc et al. [21] suggested that anastomotic complications can be reduced using interrupted absorbable sutures, but other authors demonstrated the safety of a continuous suture anastomosis using a non-absorbable monofilament suture [22]. Some studies [23] compared the interrupted with the continuous suturing technique in terms of anastomotic-related complications and found no difference. The running suture saves time, allows a more uniform distribution of the tension over the bronchial and vascular anastomoses and is being adopted by most of the experienced teams performing sleeve resections by VATS.

Some authors argue that the use of the robot improves and facilitates bronchial or vascular reconstructions due to 3-dimensional vision and the greater range of movements. Qiu et al. [24] reported the robotic technique using a clamp for proximal control and a Reliance bulldog clamp for the distal artery. The use of a short continuous suture is preferred because of the lack of tactile (haptic) feedback. This is especially true when pulling from the distal suture while using 5–0 Prolene, as it can easily break if too much traction is exerted. The authors perform the vascular anastomosis first to reduce vascular clamping time. In our opinion, the vascular anastomosis should be performed last to reduce tension to the suture, especially in uniportal VATS where doing the bronchial anastomosis first for the LUL makes the procedure much easier without the interference of the artery.

In the era of minimally invasive surgery, uniportal VATS double sleeve is a feasible technique that requires an experienced team for it to be safely performed and it extends the current limits of uniportal VATS. We expect further developments in robotic uniportal technology to make these procedures more precise and easier to adopt.

Conflict of interest: none declared.

Author contributions

Diego Gonzalez-Rivas: Conceptualization; Investigation; Methodology; Project administration; Resources; Supervision; Validation; Visualization; Writing—original draft; Writing—review & editing. Alejandro Garcia: drawings. Chang Chen: Conceptualization. Yang Yang: Supervision. Lei Jiang: Supervision. Dmitrii Sekhniaidze: Conceptualization. Gening Jiang: Supervision; Validation. Yuming Zhu: Supervision.

Presented at the 7th Asian Single Port VATS Symposium, Nagoya, Japan, 24–25 May 2019.

REFERENCES

ABBREVIATIONS

 
• CT

  Computed tomography

 
• LUL

  Left upper lobe

 
• PA

  Pulmonary artery

 
• SVC

  Superior vena cava

 
• VATS

  Video-assisted thoracic surgery