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1 Lung Transplant Program, Department of Surgery, Toronto General Hospital, University of Toronto, Toronto, Ontario, Canada
Correspondence and requests for reprints should be addressed to Shaf Keshavjee, M.D., M.Sc., F.R.C.S.C., F.A.C.S., Division of Thoracic Surgery, Toronto General Hospital, 200 Elizabeth St. 9N-947, Toronto, ON, M5G 2C4 Canada. E-mail: Dr.Shaf.Keshavjee{at}uhn.on.ca
ABSTRACT
Patients with end-stage emphysema can be offered lung volume reduction surgery (LVRS), lung transplantation, or unilateral lung transplantation combined with contralateral LVRS if necessary, depending on multiple factors including age, lung function parameters, lobar predominance, and whether the disease is uni- or bilateral. Lung transplant is a complex and well-established therapeutic modality for patients with end-stage lung disease. The ideal candidate for LVRS is a patient with severe upper-lobe predominant emphysema and markedly impaired exercise capacity. Other groups may benefit from the procedure, but results are likely to be less good. The objective of this chapter is to describe the surgical techniques of bilateral lung transplantation and lung volume reduction surgery as performed at the University of Toronto.
Key Words: emphysema • transplantation • techniques
By the year 2020, chronic obstructive pulmonary disease (COPD) is predicted to become the third leading cause of death worldwide, exceeded only by heart disease and stroke (1). End-stage emphysema markedly limits the quality of life and survival of patients. Medical therapy and pulmonary rehabilitation are useful palliative measures and can temporarily improve symptoms. However, they do not alter the natural history of the disease.
Since end-stage emphysema is refractory to most medical treatment, surgery is often the only remaining option. Three surgical procedures are pertinent to the treatment of end-stage emphysema: giant bullectomy, lung volume reduction surgery (LVRS), and lung transplantation.
Patients with localized disease manifesting as a giant bulla that compresses adjacent healthy lung tissues can be offered bullectomy.
Patients with diffuse disease can be offered LVRS, lung transplantation, or unilateral lung transplantation combined with contralateral LVRS if necessary, depending on multiple factors including age, lung function parameters, lobar predominance, and whether the disease is uni- or bilateral.
The ideal candidate for LVRS is a patient with severe upper-lobe predominant emphysema and markedly impaired exercise capacity. Other groups may benefit from the procedure, but results are likely to be less good (2).
In selected patients with end-stage emphysema who are potential candidates for lung transplantation, LVRS can alleviate symptoms and improve lung function and quality of life to a degree that allows the postponement of transplantation for up to 4 to 5 years. In addition, LVRS has no adverse impact on outcome after lung transplantation and does not influence the patients' candidacy for transplantation (3).
Lung transplant is a complex and well-established therapeutic modality for patients with end-stage lung disease. It is complex because it is a multistage and multidisciplinary procedure. As a multistage procedure, its success relies on careful execution of each step: recipient selection, pretransplant care, donor selection, donor maintenance, organ retrieval and preservation, the transplant procedure itself, and postoperative care and follow up.
The objective of this article is to describe the surgical techniques of bilateral lung transplantation and LVRS as performed at the University of Toronto.
LUNG TRANSPLANT
Once a donor is available, the retrieval team is sent to evaluate the donor on site and the recipient is called in to be admitted. When the retrieval team arrives at the donor hospital, the donor is evaluated using the "ABCDEF" approach and the information is given to the recipient team:
Lung donation can be aborted in any of the described stages (A, B, C, D, E, F), but once we reach stages D/E and the lungs are judged adequate, the recipient team is told the expected flush time and the recipient is called to the operating room, taking into consideration flush time plus 1 hour for the retrieval team to leave the donor hospital and the length of time required for travel to the recipient hospital. We generally call the recipient to the operating room 2 hours before the expected arrival of the organs, so there is enough time for anesthesia, opening of the chest, and pulmonary dissection.
The retrieval technique includes administration of 500 µg of PGE1 into the main pulmonary artery, before aortic cross-clamping and lung perfusion with 4 L of 4°C Perfadex (Vitrolife, Gothenburg, Sweden) supplemented with PGE1 (500 µg divided into the bags with Perfadex) through a cannula inserted into the main pulmonary artery. The lungs are recruited before flushing, to assure that there is no atelectasis, using a sustained pressure no higher than 30 cm H2O. In this way, flush distribution is more homogeneous. During the flush one must observe the position of the tip of the cannula so that the flush is distributed equally to both lungs. For transport to the recipient hospital, lungs are kept inflated at mid-expiration with 50% oxygen in 2 L of cold Perfadex. Hyperinflation increases vascular permeability.
When the recipient is in the operating room, a peripheral venous line and a radial artery line are inserted while the patient is awake. Five-lead ECG and pulse oximeter are also required. At Toronto General Hospital (TGH), epidural catheter is not placed routinely.
Anesthesia is induced and the recipient is intubated. In patients with septic pulmonary diseases such as cystic fibrosis and bronchiectasis, we first use a single lumen tube and bronchoscopy is performed for airway toilette and bronchial washing for microbiological cultures. A left-sided double lumen tube is then inserted to allow one-lung ventilation.
For induction, propofol, penthotal, midazolam, and ketamine have been used at TGH in combination with narcotic analgesics such as fentanyl (10–15 µg/kg) or sufentanyl. Pancuronium is the most frequently used relaxant. Nitrous oxide is never used because it increases pulmonary vascular resistance (PVR) and expands intravascular gas emboli, which may be entrapped in the graft. Isoflurane or sevoflurane are used initially for maintenance of anesthesia, but the patient may not tolerate well once he or she becomes hemodynamically unstable due to mediastinal manipulation or vasodilatory hypotension. Propofol infusion at a rate of 50 µg/kg/min ensures amnesia. Supplemental doses of fentanyl are administered every 2 to 3 hours (5 µg/kg) (4).
After the anesthesia is induced, a Swan-Ganz catheter is inserted through the right jugular vein and a central venous catheter is inserted into the jugular or subclavian vein.
A nasopharyngeal temperature probe and Foley catheter are also inserted. A warming blanket is used to cover the upper thorax and the legs (4).
Transesophageal echocardiogram is used to monitor the right ventricular function and biventricular filling. It may also be used to evaluate the venous pulmonary blood flow at the end of the transplant procedure (4).
In severe pulmonary hypertension, one-lung ventilation is not attempted. Increased expiratory time is necessary in patients with severe obstructive airway disease to avoid gas trapping and auto-PEEP (4).
Permissive hypercarbia is usually required, and pH is a better determinant of the inability to ventilate than is PaCO2 (4).
In the following sections we present the technique for bilateral lung transplantation, step by step.
Step 1: Patient Position
For bilateral lung transplant, the recipient is positioned supine with the arms abducted (Figure 1). In patients with emphysema, who have a bigger anterior-posterior diameter, the arms can be positioned alongside.
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It is important to watch the position of the arms so they are not overstretched during the whole procedure, avoiding brachial plexus injury. Proper padding of the arms and legs is also important. Thrombo-embolic deterrent (TED) stockings and compressive device are used for prophylaxis of deep venous thrombosis.
Step 2: Clamshell Incision
Our incision of choice is the clamshell incision, with sternal transection. Others have performed bilateral lung transplantantion through median sternotomy or anterolateral thoracotomies with sternal sparing (5). Two separate posterolateral incisions have also been used.
After prepping and draping, the skin incision is performed in the mammary fold. A short skin flap is raised with cautery to the level of the fourth intercostal space, and the pectoralis muscle is cut at this level.
The fourth intercostal space is entered laterally, and a rib spreader can be placed to aid in the dissection of the mammary vessels, close to the sternum (Figure 2).
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scan. For the purpose of illustration, in the next steps we will show the transplant procedure done on the right side.
The lung is collapsed and the pleura over the pulmonary hilum and the inferior pulmonary ligament are incised. Hypoxia is common during one-lung ventilation due to intrapulmonary shunt in the nonventilated lung and improves considerably when the pulmonary blood flow to the nonventilated lung is stopped by occluding the pulmonary artery (PA) (4). The superior pulmonary vein, pulmonary artery, and inferior pulmonary vein are dissected and divided (Figures 5 and 6).
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Patients with idiopathic pulmonary fibrosis also have an increased need for cardiopulmonary bypass support (4).
If CBP is required for hemodynamic or ventilatory support, the heart remains warm and beating. If cardiac repair is necessary, such as for atrial septal defect or ventricular septal defect, the heart is arrested and moderately cooled (4).
Cardiopulmonary bypass unloads the right side of the heart and improves hemodynamic stability. On the other hand, CPB may cause (1) coagulopathy due to hemodilution, heparinization, and platelet dysfunction; (2) hemolysis due to red blood cell trauma; or (3) activation of complement, neutrophils, and systemic inflammatory response, which may contribute to allograft injury at reperfusion (4).
When lung transplant is performed through the clamshell incision or through a right thoracotomy, the right atrium and the ascending aorta are cannulated for CPB.
When left single lung transplant is performed through a left thoracotomy, the main pulmonary artery and the descending aorta are cannulated. Others prefer to perform a left single lung transplant by means of a left anterolateral thoracotomy with sternal division and to cannulate the ascending aorta and atrium, if CPB is necessary.
At TGH, we have also used bicaval cannulation instead of a double-stage cannula inserted through the right atrium. We have noticed less systemic hypotension during mediastinal manipulation when we use the bicaval cannulation.
The last structure to be divided is the bronchus. Hemostasis is carefully obtained, chiefly in patients with cystic fibrosis and bronchiectasis who may have enlarged bronchial arteries and enlarged lymph nodes as well. The bronchus is divided immediately proximal to the upper lobe bronchus takeoff.
Step 4: Hilar Dissection for Allograft Implantation
Before implanting the allograft, the pulmonary hilum has to be prepared for the anastomoses. The pulmonary hilum is prepared in the following sequence: bronchus 
pulmonary veins pulmonary artery, as depicted in the Figures 7, 8, and 9. It is extremely important not to devascularize the recipient bronchial stump during dissection to avoid ischemic complications.
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Then, two Judd-Allis clamps are applied to the pulmonary artery, and the adventitial tissue around PA is carefully dissected. The mediastinal tissue posterior to PA will be used to cover the bronchus together with the donor peribronchial tissue, after the bronchial anastomosis is completed.
Step 5: Allograft Separation and Dissection (Back Table)
The lungs to be implanted are separated and dissected on a back table, at the recipient hospital (Figures 10, 11, and 12). If two single lung transplants are to be done for two recipients, the separation can be done at the donor hospital and the allografts can then be transported separately to the recipient hospital(s).
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The donor PA is cut appropriately short, so there will be no kinking at the anastomotic site (Figure 13). At least 5 mm of atrium is left around the pulmonary veins. The left atrium is dissected very close to its wall on the anterior aspect of the hilum so that the pericardium over the bronchus is not dissected, preserving its vascularization (Figure 14).This is an important step to avoid ischemic bronchial complications.
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Step 6: Implantation
Once the allograft is dissected and ready to be implanted, the bronchus is opened with a # 15 blade scalpel. The allograft is then placed on the cooling jacket in the pleural cavity.
The anastomoses start from the most posterior to the most anterior hilar structure (bronchus pulmonary artery atrial cuff).
At the end, the bronchial anastomosis is covered. The peribronchial tissue is sutured to the mediastinal tissue behind the pulmonary artery (Figures 15 and 16).
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In the next figures, we show step by step how to perform a running everting mattress suture for the atrial anastomosis (Figures 21, 22, and 23).
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If hypoxia occurs in the presence of systemic hypotension, improving hemodynamics may improve the gas exchange. Systemic hypotension due to mediastinal manipulation and vasodilation are common in lung transplantation. Norepinephrine infusion at a rate of 0.05 µg/kg/minute and titrated to effect is used to treat systemic hypotension due to low systemic vascular resistance (SVR). Vasopressin 1 to 4 units/hour may be added if not responsive to escalating doses of norepinephrine. Phenylephrine may also be used (100–200 µg bolus) (4).
Arrhythmias are common during mediastinal manipulation, allograft implantation, or after allograft reperfusion. Atrial fibrillation is usually poorly tolerated and requires cardioversion. Nonsustained ventricular tachycardia is frequent, and sustained ventricular tachycardia is usually due to acute electrolyte abnormalities or systemic air embolism from the allograft, after releasing the atrial clamp. Hyperkalemia may ensue after prolonged surgery with hypercapnia, acidosis, and low urine output and should be treated with glucose, insulin, and calcium. Magnesium supplementation may be necessary, and hypomagnesemia may be worsened by calcineurim inhibitors (4).
After the implantation and reperfusion is completed, hemostasis is confirmed. The implantation of the left lung follows the same principles.
At the end of the operation, two 28F chest tubes are inserted on each pleural cavity, one apical (straight chest tube) and one basal (curved chest tube).
Step 7: Clamshell Incision Closure
Four pericostal sutures (VICRYL #2, figure of eight) are placed on each hemithorax. After that, three #5 wires are placed in the sternum.
The pericostal sutures are tied first so that the sternal wires can be secured without undue tension. The muscle, subcutaneous tissue, and skin are sutured in layers with absorbable suture. The anesthetist switches the double lumen to a single lumen tube, and a bronchoscopy is performed for toilet and to recheck the bronchial anastomoses.
LUNG VOLUME REDUCTION SURGERY
LVRS can be performed either unilaterally or bilaterally. Clinical conditions for which unilateral LVRS may be appropriate are summarized in Table 1.
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Bilateral LVRS can be achieved through a median sternotomy, staged anterolateral thoracotomies, or VATS LVRS.
When performing bilateral surgery, consensus opinion is to operate on the worst side first (6). VATS LVRS is our choice.
ANESTHETIC MANAGEMENT
Most authors avoid sedative premedication to avoid respiratory depression in this group of severely ill patients. Others use light sedation with midazolam during invasive pre-anesthetic procedures (6).
Standard monitoring includes invasive arterial monitoring before induction, central venous pressure, pulse oximetry, capnography, core temperature, and ECG. The use of Swan-Ganz catheter and transesophageal echocardiogram (TEE) is more controversial (6).
A thoracic epidural catheter is placed before surgery for optimal postoperative analgesia, if there are no contraindications. Hypotension may ensue when local anesthetics are administered through the epidural catheters due to sympathetic blockade (7). Invasive arterial blood pressure monitoring, vasoactive agents, and fluid administration are necessary (7). It is important to avoid fluid overload to allow early extubation (7). We use both epidural analgesia and preemptive local anesthesia. Nonsteroidal agents are also used postoperatively to supplement analgesia (7).
Before induction of anesthesia, the patient is preoxygenated in a partial sitting position. Intravenous induction with all commonly used agents has been reported. Pancuronium is not a good option once early extubation is planned. The use of both volatile agents or propofol has been described for anesthesia maintenance. Use of short-acting intravenous agents is the key consideration. Propofol preserves the hypoxic pulmonary vasoconstriction, thus avoiding an increase in oxygen shunt fraction (7). Nitrous oxide has been avoided. Due to the severity of the bullous disease and associated dead space, uptake and distribution of inhalational agents is unpredictable, and delayed awakening may occur (7).
Emphysema, with its severe airflow obstruction coupled with the need of positive-pressure ventilation during general anesthesia and one-lung ventilation, can lead to severe gas trapping or dynamic hyperinflation and pneumothorax, with hemodynamic instability. Disconnecting the ventilator circuit from the endotracheal tube leads to rapid resolution of systemic hypotesion in that situation. Ventilating the patient with small tidal volumes and allowing longer expiratory times can avoid dynamic hyperinflation (auto-PEEP, air trapping) and its deleterious effect on venous return and systemic hypotension. Both pressure-controlled or volume-controlled ventilation have been successfully used. A ventilator capable of measuring auto-PEEP is helpful. Pressure-controlled ventilation limits airway peak pressure and may decrease the chance of barotrauma. Volume-controlled ventilation can minimize auto-PEEP when using low tidal volumes (5 ml/kg during one-lung ventilation). Inspiratory time:expiratory time ratios of 1:3 to 1:5 and low respiratory rates are used (7). Hypercarbia is a consequence of low–tidal volume ventilation, and maneuvers to increase minute ventilation must be used when pH falls below 7.2: (1) increase of ventilatory rate, (2) aspiration of secretions, (3) adequate muscle relaxation, and (4) aggressive treatment of bronchospasm. When hypoxia occurs during one-lung ventilation, one can: (1) increase FIO2, (2) apply PEEP in the dependent lung, and (3) temporarily occlude PA flow to the nonventilated lung (7).
Patients with emphysema may also have occult coronary disease, which can manifest abruptly in the operating room. Careful assessment of cardiac disease before selection for LVRS is necessary. LVRS carries a risk of significant cardiac stress, and intraoperative myocardial infarction has been reported. A pharmacologic stress test is recommended to screen for occult cardiac ischemia, and a coronary angiogram may be necessary. The use of β-blockers and nitrates during the perioperative period should be considered. The occurrence of bronchospasm should be monitored (7).
Air leak is an important potential complication of LVRS, due to disruption of the suture line or adjoining lung tissue. Because of that, low–tidal volume ventilation, longer expiratory times to avoid hyperinflation during LVRS, and early extubation in the operating room are desired. To accomplish early extubation, the anesthesiologist must use short-acting anesthetic agents, provide excellent postoperative pain control, and maintain the patient in a euvolemic and normothermic state (7).
Surgery is performed under general anesthesia with left-sided double-lumen endotracheal tube to allow single-lung ventilation (2). A bronchial blocker may also be used. Regardless of the method for one-lung ventilation, the tube position must be assured by bronchofibroscopy. Low–tidal volume during exposure and apneic oxygenation during stapling the diseased lung may be used when one-lung ventilation is problematic. Due to severe obstructive lung disease and decreased elastic recoil, deflation of the operative lung takes longer. The lung may not deflate even during one-lung ventilation. Suctioning of secretions and gentle pressure exerted on the operative lung by the surgeon may help with deflation of the lung (7).
VIDEO-ASSISTED LUNG VOLUME REDUCTION SURGERY
VATS LVRS can be performed sequentially on two lungs under the same anesthetic procedure.
SURGICAL TECHNIQUE
We use supine positioning for upper lobe disease (Figures 24a and 24b). For lower lobe and if we anticipate adhesions, lateral positioning is used but troublesome. A 30-degree video-telescope enhances visualization in either patient position. The technique used at the Toronto General Hospital is depicted in Figures 25 and 26.
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No clear differences in outcome between median sternotomy and bilateral video-assisted thoracoscopic surgery have been shown (2). NETT surgeons found that the two approaches resulted in similar early and late mortality, similar types and rates of complications, and produced similar improvements in spirometry, exercise capacity, and quality of life extending to 24 months of follow-up (5). The operative results alone are impressive, with a 90-day mortality in NETT between 4.6% (VATS) and 5.9% (sternotomy) versus the pre-NETT Medicare 90-day mortality rate of 14.4% (8).
Regardless of the approach, LVRS is achieved by resecting 20 to 30% of each lung or as high as 60% of hemithorax volume. The staple lines are often buttressed with bovine pericardial or polytetrafluoroethylene strips to reduce air leaks.
POSTOPERATIVE MANAGEMENT AND OUTCOMES
LVRS carries a high morbidity, with complication rates up to 85 to 100% in some series, and up to 60% excluding air leaks (2). Aggressive management of early postoperative complications, including air leaks, respiratory failure, arrhythmias, and hemorrhage, can also be expected to improve outcomes (9).
Early extubation is beneficial to avoid coughing or gagging and to minimize the duration of positive-pressure ventilation of the fragile, operated lungs. The PaO2 is maintained close to baseline because a high PaO2 may be deleterious in a patient with preoperative CO2 retention (11). Szekely and coworkers (cited by Brister and coworkers, Reference 7) found that a resting PaCO2 greater than 45 mm Hg together with a six-minute-walk distance less than 200 m are risk factors for poor outcome, defined as death within 6 months or a hospital course of greater than 3 weeks. O'Brien and colleagues (cited by Brister and coworkers, Reference 7) found no increased mortality in 15 patients with hypercapnic emphysema (PaCO2 = 58 ± 7 mm Hg) compared with a population with eucapnea. Keenan and coworkers found increased mortality when PaCO2 was greater than 50 mm Hg (10).
Thoracic epidural analgesia is maintained for 4 to 5 days after surgery. Oral opioids are avoided until the epidural catheter is removed. Early mobilization and aggressive chest physiotherapy are also critically important (11).
Nebulized bronchodilators should be administered for at least 48 hours before resuming usual bronchodilator therapy. Retained secretions may require nasotracheal suctioning; fiberoptic bronchoscopy may be needed up to twice daily for retained secretions, and a 5.4 F minitracheostomy tube can be inserted through the cricothyroid membrane if more frequent suctioning is necessary (2).
Table 2 shows the common postoperative complications encountered in LVRS (2, 7).
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Patients spend significant time recovering after LVRS, with nearly 30% of patients still hospitalized or in rehabilitation facilities 1 month postoperatively and 15% still not at home 2 months after the operation (13).
ACKNOWLEDGMENTS
The authors are grateful to Matthew Villagonzalo for his excellent drawings done for this manuscript.
FOOTNOTES
Conflict of Interest Statement: None of the authors has a financial relationship with a commercial entity that has an interest in the subject of this manuscript.
(Received in original form August 15, 2008; accepted in final form October 18, 2008)
REFERENCES
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6–7 sutures), as shown on the left. When there is a size mismatch we perform a telescoping anastomosis (
