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A range of incisional techniques are available to lung transplant surgeons. Since the early 1990s, the standard for those undertaking bilateral lung transplant surgeries, particularly for septic disease, has been the clamshell incision or its anterior thoracotomy variants. There are potential problems of either incisional instability or reduced access. A relatively unused alternative that is very familiar to all cardiac and many thoracic surgeons is median sternotomy. Although pleural adhesions can cause a spectrum of difficulties, in their absence, the advantages of rapid opening and closure, combined with reliable stability and minimal discomfort, make this an attractive option. A series of evolved surgical maneuvers, with an emphasis of what can be done intrapericardially, facilitates this approach, and we describe them in this article.
Combined heart and lung transplantation, from its first description in 1981, has routinely been performed via a median sternotomy. Similarly, the first paired, isolated lung transplantations, the en bloc double lung,
were performed with the same approach. There was disillusion with the outcomes of this operation and, in particular, concerns regarding hemostasis, as the scope of transplantation extended to septic lung disease. An evolution in several centers, notably St Louis, culminated in the description of the clamshell incision combined with the sequential lung transplant, with hilar as opposed to central anastomoses, in 1990.
Available Incisional Techniques for Bilateral Lung Transplantation
The clamshell incision has become the standard approach to bilateral lung transplantation throughout the world. It gives marvelous exposure to pleural adhesions, permits good access to the hilum, and probably facilitates an off-pump approach. It is particularly good for training, as both the operating surgeon and the assistant have an excellent view of the key stages of the operation.
The disadvantages of this exposure are an increase in postoperative pain and potential for wound instability. The former requires measures such as epidural analgesia, which undoubtedly slows recovery and probably results in poorer early functional performance. The latter reflects the poor mechanical characteristics of the incision, with sternal union achieved across the few centimeters of apposed bone edges, supplemented by whatever support can be achieved with pericostal sutures on each side. The literature is awash with descriptions of the problem and a range of solutions of various successes. However, despite the poor mechanics, most of the patients achieve a stable wound.
The obvious alternative, that is, anterior thoracotomies with preservation of the sternum, was described in 1999.
It solves most of the stability issues, results in less pain than that with the full exposure, and has been adopted in many centers, particularly in Europe. However, access and particularly vision are limited, and this approach is not well suited to teaching. Unplanned bypass for sudden instability or abrupt bleeding can be challenging. Variations such as the axillary thoracotomy or the use of videothoracoscopic adjuncts may give even better cosmesis but have the same drawbacks.
Sternotomy
Sternotomy, despite a recent fashion for limited incisions, remains the standard approach in cardiac surgery. It is rapidly performed, gives all the exposure one would want for the heart, and is closed in a secure fashion. Pain control and chest wall function are much superior to that obtained with any of the intercostal incisions. These reasons, coupled with our near-routine use of cardiopulmonary bypass for bilateral lung transplants, have led our group toward increased use of sternotomy. We initially restricted ourselves to treating chronic obstructive pulmonary disease recipients, carefully screened to exclude those likely to have pleural adhesions, but now we have extended to treating recipients with pulmonary arterial hypertension and lung fibrosis.
Figure 1An entirely standard full-length sternal incision is made, and a retractor of choice is inserted after wound-edge hemostasis. The pericardium is opened in the midline and retraction stitches are attached to the pericardial edges. The next step is to examine the pleural spaces (Fig. 2) before heparinization and initiation of cardiopulmonary bypass. Our standard has been central aortic and separate caval cannulation, the latter with either straight or right-angled tubes. A cannula within the superior vena cava (SVC) is essential if obstruction to venous return during maneuvers around the right pulmonary artery and bronchus is to be avoided. We also routinely place a pulmonary artery vent. This is essential when our approach of bilateral lung extraction is followed by bilateral implantation. PA = pulmonary artery; RA = right atrium; Ao = aorta.
Figure 2With retraction of the pericardium to the opposite side of the chest, the pleural spaces are opened anteriorly. Care should be taken on both sides at the upper end of this incision, to avoid damage to either the phrenic nerve or the internal thoracic artery. The pleural spaces are explored, and any accessible pleural adhesions are divided with cautery. No other dissection is done at this stage. Access to the right is usually easy, except when the heart is large or the patient is intolerant of retraction, as may be the case in recipients with pulmonary arterial hypertension, when bypass may be required before any extensive pleural exploration.
Figure 3Once on bypass, the dissection at the root of the right lung proceeds easily. The assistant retracts the pericardium, taking care to avoid damage to the phrenic nerve. Similarly, the operating surgeon is always cognizant of the position of that nerve, initially close in front of the pulmonary veins, but progressively safer as the lung falls backward. It has been our habit to simply ligate and divide the vascular structures, but this can also be achieved with an appropriate stapling device. The inferior pulmonary ligament is divided while the assistant retracts the inferior vena cava (IVC) leftward, taking care to cut (usually with cautery) toward the lung and away from the esophagus. RIPV = right inferior pulmonary vein; RSPV = right superior pulmonary vein; RPA = right pulmonary artery.
Figure 4As these patients do not, in general, have septic disease, we are happy to simply divide the bronchus, as the last stage, and remove the lung. The airway is divided distally, here separately through the upper lobe and bronchus intermedius segments, to avoid inadvertent damage to the vagus. This structure may be pulled laterally with the lung and then severed if the airway is cut short. The cut edge of the longer bronchus can be retracted upward, and the vagus is safely cleared off the underside, using metal clips to secure any bronchial arteries. The bronchus is then trimmed back flush with the mediastinum and at an angle that gives a good size match to the donor airway. RMSB = right mainstem bronchus.
Figure 5The safest way to develop a recipient cuff of pulmonary veins and left atrium on the right is to move back into the pericardium, retracting the right atrium and heart to the left. The pericardium is open just in front of the superior vein—this is the closest to the phrenic nerve, and as the incision is taken down over the inferior vein, the nerve is at progressively less risk. Working again within the pericardium, the inferior vein can be completely freed from its attachments. Tissue between the inferior vein and the IVC is divided to give access to the pericardial space behind the veins and the left atrium. Attention then switches to the outer side of the pericardium, and the recipient venous cuff can be completely mobilized. A trial clamping with a large Satinsky-type clamp confirms adequacy of mobilization. IVC= inferior vena cava; RAA = right atrium appendage; SVC = superior vena cava.
Figure 6With the right hilum prepared, attention switches to the left. It is useful to have a second assistant, standing to the right of the surgeon and using his or her right hand to retract the heart. The operating surgeon should again be cognizant of the situation of the phrenic nerve, on the left farther from the front of the hilum.
Figure 7Here the hand of the second assistant is outside the pericardium, pulling it and its contents to the right, allowing good exposure of the vascular structures. These are again ligated and divided on the outer side of the pericardium. LSPA = left subclavian-left pulmonary artery anastomosis.
Figure 8After dealing with the vessels, the airway is again divided distally. The same maneuvers to protect the phrenic nerve and then trim back the airway are followed as on the right. LMSB = left mainstem bronchus; PA = pulmonary artery; LSPV = left superior pulmonary vein; LIPV = left inferior pulmonary vein; LPA = left pulmonary artery.
Figure 9The complete dissection of the left lung has so far been performed outside, ie, on the pleural aspect, of the pericardium. Attention now switches to the inner side of the pericardium, again aided by the hand of the second assistant, but now retracting only the heart to the right. The pericardium is opened in front of the veins, and this dissection is carried on up over the pulmonary artery. As the divided stumps of the vessels come into sight, they are completely mobilized from their pericardial reflections. This enables the recipient׳s pulmonary venous or left atrial cuff to be completely freed. Division of a band of tissue running between the superior vein and the underside of the left pulmonary artery is a key step here. LAA = left atrium appendage; PA = pulmonary artery.
Figure 10As the vessels are fully mobilized and, in particular, the pulmonary artery is completely freed of its attachments to the pericardium, the bronchus comes into sight, from within the pericardium. If not already divided, this step can be performed now, and the lung is removed from the chest. To facilitate exposure of the bronchus, a retraction stitch is placed on the ligated pulmonary artery, pulling it to the right. A similar stitch can be used for the left atrial appendage and also the superior vein, to further improve exposure of the airway. LPA = left pulmonary artery; LMSB = left mainstem bronchus; LSPV = left superior pulmonary vein; LIPV = left inferior pulmonary vein.
Figure 11The donor lung is prepared in an entirely standard fashion (not shown). We have emphasized the need to cut the bronchus as close as possible to the lung parenchyma, to within one cartilaginous ring of the lobar divisions. The lung is then placed, surrounded by cold saline–soaked swabs, into the pleural cavity, having confirmed correct orientation. Working within the pericardium, the donor bronchus is identified and pulled up from the donor lung hilum, into which it tends to retract. Access to the recipient airway is excellent, facilitated by retraction sutures (shown here on the pulmonary artery stump) and a curved retractor blade, protected by a gauze swab, shown here as an alternative to the assistant׳s hand, around the heart. Suturing commences on the membranous section. Our standard is to use 3 lengths of running 4-0 monofilament nonabsorbable polypropylene. The material is probably irrelevant compared with the importance of a short donor bronchus, rigorous avoidance of devascularization, and meticulous end-to-end airway apposition.
Figure 12Anastomosis of the 2 ends of the pulmonary artery is similarly done intrapericardially. Because there is a pulmonary artery vent, the Satinsky clamp on the recipient side can be dispensed with if desired. We retain the dimple indicating the position of the ligamentum arteriosum on the donor left pulmonary artery to aid orientation. It aligns with the most superior part of the recipient vessel. In practice, the section containing the dimple is often resected, to avoid a redundant PA and the risk of kinking, but its role in orientation is important. Behind the artery, there are interrupted sutures pulling peribronchial tissue over the airway—the airway anastomosis suture line is completely covered, a step we believe is important. PA = pulmonary artery.
Figure 13Following completion of the venous anastomosis on the left (not shown) attention switches to the right lung. Access is much better; a drainage cannula in the SVC is an essential part of exposing the pulmonary artery without causing venous obstruction. The bronchus has been completed, and we can see the 2 vascular anastomoses. That on the vein is left incomplete to allow deairing at the time of reperfusion. SVC = superior vena cava; PA = pulmonary artery; RPA = right pulmonary artery; RPV = right pulmonary vein.
Figure 14Both the lungs have now been implanted. The use of bypass enables simultaneous, controlled ventilation and perfusion. The pulmonary artery vent is replaced with a pressure-monitoring line. Bronchial toilet is performed, facilitated by the large, single-lumen endotracheal tube, and the lungs are then ventilated with room air. At this stage, there are clamps on the proximal venous cuffs on both the sides. The right heart is allowed to fill, while pulmonary artery pressure is monitored, and the lungs are deaired via the untied venous suture lines. When this has been done, the lungs remain ventilated and are reperfused with a PA pressure of less than 20 mmHg for 5-10 minutes. Hemostasis is checked, the patient is fully rewarmed, and any metabolic defect is corrected. The inspired oxygen is then typical increased to 40% and then the patient weaned off bypass. The pulmonary artery monitoring line reassures the surgeon of low pressures and hence good anastomoses. A transesophageal echo probe confirms complete deairing and good flow out of pulmonary veins on both the sides. All that remains is reversal of heparin, placement of apical and basal drains, and closure of the chest. PA = pulmonary artery; Ao = aorta; SVC = superior vena cava.
Although anecdotes suggest that this approach is used in several centers, particularly in France and the United Kingdom, published information is scant. Machiarrini et al
described a short series of sternotomies (for both heart-lung and bilateral lung) and made comparisons with a contemporaneous cohort undergoing a clamshell incision. They reported development of much more chronic pain after clamshell incision. There were significantly better spirometry readings and peak expiratory flow at the same time after transplant. The only other publication is of a short series from Denmark.
Kohno M, Steinbruchel DA. Median sternotomy for double lung transplantation with cardiopulmonary bypass in seven consecutive patients. Surg Today 42:406-409.
Our own experience has been similar to that of the authors of the French article, with a shorter median time for ventilation and length of intensive therapy unit stay, albeit the patients were carefully selected.
The advantages of sternotomy are clear: rapid chest opening and closure, with very good pain control afterward. However, there are clearly some disadvantages. Most important in the current era is the need for cardiopulmonary bypass. Bypass is an important risk factor for primary graft dysfunction.
Diamond JM, Lee JC, Kawut SM, et al. Clinical risk factors for primary graft dysfunction after lung transplantation. Am J Respir Crit Care Med 187:527-534.
Many centers seek to avoid its use, particularly for the sort of straightforward patient we have in the past selected for the sternotomy approach. It may be that the near–simultaneous controlled reperfusion into the whole vascular bed and injury-sparing ventilation that our approach allows diminishes some of the deleterious effects of bypass.
More recently, we have adopted an extracorporeal membrane oxygenation-type circuit for recipients with pulmonary hypertension and adapted the sternotomy approach—this includes no reservoir, no cardiotomy suction, and minimal heparinization (activated clotting time: 18-220 s). There is no pulmonary artery vent, and we revert to a sequential single-lung philosophy, implanting the left lung first. In a small series, we have appreciated the reduced bleeding and almost no need for blood products, as well as excellent immediate function of the lung.
Finally, the tricks learned from this evolution of the sternotomy approach can also be applied to other unique situations. One of these is the setting of lung transplant after previous pneumonectomy. Bypass is mandatory, and anatomical distortion is often extreme. The largest published experience is from a French group
Le Pimpec-Barthes F, Thomas PA, Bonnette P, et al. Single-lung transplantation in patients with previous contralateral pneumonectomy: technical aspects and results. Eur J Cardio-Thorac Surg 36:927-932.
that enrolled 14 patients, with 4 patients undergoing sternotomy.
In conclusion, the sternotomy incision, with some of the technical approaches described in this article, permits straightforward lung transplantation, albeit with a mandatory use of cardiopulmonary bypass. It is particularly suited to surgical and anesthetic teams with cardiac rather than thoracic surgical expertise. The approach is very good for teaching, with excellent vision during all stages of the operation. Benefits to the patient of a reliably healing and, compared with lateral thoracotomy, almost pain-free incision may overcome some of the other disadvantages. It can be adapted to the use of extracorporeal membrane oxygenation-type technology, exemplified by recipients who have pulmonary arterial hypertension who inevitably need cardiopulmonary bypass. Familiarity with the techniques also equips the surgeon for some rare and complex recipients who need novel thinking.
References
Patterson GA CJ
Dark J.H.
et al.
Experimental and clinical double-lung transplantation.
Kohno M, Steinbruchel DA. Median sternotomy for double lung transplantation with cardiopulmonary bypass in seven consecutive patients. Surg Today 42:406-409.
Diamond JM, Lee JC, Kawut SM, et al. Clinical risk factors for primary graft dysfunction after lung transplantation. Am J Respir Crit Care Med 187:527-534.
Le Pimpec-Barthes F, Thomas PA, Bonnette P, et al. Single-lung transplantation in patients with previous contralateral pneumonectomy: technical aspects and results. Eur J Cardio-Thorac Surg 36:927-932.
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