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Ann Thorac Surg 2006;82:2139-2145
© 2006 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

Venovenous Extracorporeal Life Support After Pulmonary Endarterectomy: Indications, Techniques, and Outcomes

^a Division of Cardiothoracic Surgery, University of California, San Diego, San Diego, California
^b Division of Biostatistics, University of California, San Diego, San Diego, California
^c Division of Pulmonary and Critical Care Medicine, University of California, San Diego, San Diego, California

Accepted for publication July 6, 2006.

^_* Address correspondence to Dr Thistlethwaite, Division of Cardiothoracic Surgery, University of California, San Diego, San Diego, CA 92103-8892. (Email: pthistlethwaite{at}ucsd.edu).

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
BACKGROUND: Pulmonary endarterectomy is the accepted therapy for thromboembolic pulmonary hypertension. A recognized complication of this surgery is the postoperative development of reperfusion edema, a potentially fatal cause of respiratory failure. Because reperfusion edema can be a reversible process, temporizing support measures may be life saving.

METHODS: We retrospectively reviewed our experience with venovenous extracorporeal life support (V-V ECLS) from July 1990 to February 2006, in 20 adult patients (mean age 50.5 ± 14.5 years) presenting with potentially reversible respiratory failure after pulmonary endarterectomy. This subset of patients comprised 1.12% of our total pulmonary endarterectomy experience during that time (1,790 cases).

RESULTS: Overall in-hospital survival was 30.0% for patients requiring ECLS support after pulmonary endarterectomy versus 94.2% for patients who underwent pulmonary endarterectomy alone during the same timeframe. V-V ECLS was instituted at a mean of 86.8 hours after surgery. The mean duration of V-V ECLS was 123.4 ± 71.3 hours. The most common cause of death in ECLS patients after pulmonary endarterectomy was pulmonary hemorrhage. Survival was greater in patients cannulated within 120 hours of surgery (46.2% survival; 6 of 13 patients) compared with those cannulated after 120 hours (0 of 7 patients). Multiple logistic regression identified long duration of mechanical ventilation pre-ECLS and severity of preoperative pulmonary hypertension together as predictors of mortality.

CONCLUSIONS: A small subset of patients undergoing pulmonary endarterectomy develop temporary life-threatening respiratory failure secondary to severe reperfusion edema. In those patients with satisfactory hemodynamic outcome, V-V ECLS is a therapeutic option when all other conventional strategies have been exhausted.

	Introduction

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Reperfusion edema is a global term that has been applied to the condition of acute pulmonary edema after reinstitution of pulmonary blood flow to the lung, as seen in pulmonary endarterectomy or lung transplantation. This form of acute respiratory insufficiency has been reported to occur in between 5% and 20% of pulmonary endarterectomy patients [1] and between 10% and 20% of lung transplant patients [2]. From a clinical point of view, severe reperfusion edema has been associated with high short-term mortality, long periods of mechanical ventilation, and late decline in pulmonary function [3–5]. Although increased pulmonary arterial pressure, supranormal inspiratory oxygen, hypercarbia, ventilator mechanical volume, and barotrauma have all been linked to this disorder [6, 7], the exact cause of pulmonary capillary-alveolar membrane dysfunction leading to this disease is unknown. It is believed that the large amount of blood flow redirected to previously occluded pulmonary capillary beds in the postsurgical lung may be the catalyst for the development of this reperfusion phenomenon after pulmonary endarterectomy [8].

A number of patients who undergo pulmonary endarterectomy for chronic thromboembolic pulmonary hypertension manifest reperfusion edema in the early postoperative period. Individuals with this complication demonstrate early postoperative difficulty with carbon dioxide gas exchange and oxygenation and have chest radiographs, which demonstrate the development of progressive diffuse interstitial edema. In most cases, supportive care consisting of mechanical ventilation, diuretics, and avoidance of hypercarbia and supranormal levels of fraction of inspired oxygen allow for full lung recovery [9]. There are, however, a very small number of pulmonary endarterectomy patients who develop life-threatening reperfusion edema after operation despite good hemodynamic outcome. For such patients, the additional option of circulatory support should be considered to achieve immediate resuscitation.

Venovenous extracorporeal life support (V-V ECLS; also known as extracorporeal carbon dioxide removal; ECCO₂R) is a well-established technique for providing emergent gas exchange support for patients with respiratory failure [10]. The V-V ECLS has several advantages: (1) the percutaneous and small incision approaches are technically simple, rapid, and can be done at the bedside; (2) it provides respiratory support for hypercarbic and moderately hypoxic patients; (3) it preserves physiologic pulsatility; (4) it does not alter preload or stroke work of the heart; (5) it avoids a sternotomy or redo-sternotomy incision; and (6) it is less costly than other forms of mechanical circulatory support. Despite these advantages V-V ECLS support has several disadvantages that limit its widespread use, including the significant risk of bleeding, the high incidence of infectious and thromboembolic complications with prolonged support (ie, more than 7 days), and often the limited rehabilitation potential of patients who have undergone long-term support [11].

The application of extracorporeal life support for immediate resuscitation from life-threatening respiratory failure after successful pulmonary endarterectomy may be a useful strategy for improvement of patient survival. We reviewed our experience over a 15 year period with 20 adult patients who required V-V ECLS after pulmonary endarterectomy, with the goal of determining whether this approach would improve survival in this critically ill subset of patients.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Patient Selection
From July 1990 to February 2006, 1,790 patients underwent pulmonary endarterectomy at our institution. Twenty patients (1.12%) exhibited severe respiratory failure in the early postoperative period and were placed on V-V ECLS at the bedside, utilizing a percutaneous or small incision vascular access technique. Criteria for institution of V-V ECLS in a patient with improved hemodynamic parameters postoperatively and with potentially reversible respiratory failure included the following: (1) partial pressure of oxygen, arterial to fraction of inspired oxygen (PaO ₂/FIO ₂) ratio less than 60%; (2) partial pressure of carbon dioxide, arterial (PaCO₂) greater than 60 mm Hg; (3) static lung compliance less than 0.5 mL/cm H₂O/kg or less than 30 mL/cm H₂O at tidal volume of 10 mL/kg; (4) peak inspiratory pressures greater than 30 mm Hg with pneumothorax. We considered these patients likely to die without mechanical gas exchange support, as has been previously reported by Vasilyev and colleagues [12] for patients with similar clinical criteria in a prospective, multi-institutional evaluation of pulmonary failure. Review of patient data that comprises this paper was approved by the University of California, San Diego (UCSD) Institutional Review Board (IRB) in February 2006. The UCSD IRB has waived the requirement for individual patient consent for this retrospective analysis.

Venovenous ECLS Characteristics and Insertion Technique
Our venovenous ECLS system consisted of a Medtronic heparin-bonded circuit (Carmedia 3/8-inch tubing; Medtronic Inc, Minneapolis, MN) with a centrifugal pump. For gas exchange, two hollow-fiber microporous membrane oxygenators with an integrated heat exchanger (Maxima PRF or Silicon Membrane Oxygenation System I-4500, both from Medtronic Inc) were placed in parallel. Gas regulation to the oxygenators was achieved using a blender (Sechrist Industries, Inc, Anaheim, CA). A thin-walled, wire-wound polyurethane venous catheter (19-23 French; heparin-coated from Biomedicus, Eden Prarie, MN), typically 37 cm in length, was inserted into the right jugular vein utilizing a small neck incision and a modified Seldinger technique. A second heparin-coated cannula (21–27 French; Biomedicus) 40 to 50 cm in length was inserted into either femoral vein using a percutaneous or open approach. The cannulae were positioned into the mid-right atrium and the inferior vena cava near the confluence of the common iliac veins, respectively.

V-V ECLS Management
The ECLS pump flow was initiated at a rate of 50 to 60 mL/kg per minute and then titrated to increase oxygen delivery without allowing recirculation between the drainage (inferior vena cava) and reinfusion (right atrial) cannulae. Support was monitored by the use of continuous venous saturation measurements in the drainage line (Terumo Medical Corp, Ann Arbor, MI) and continuous blood gas measurements postoxygenator (Terumo Medical Corp) within the ECLS circuit, and by continuous pulse oximetry monitoring of the patient. Radial artery blood gas measurements were taken hourly until PaCO ₂ levels were measured to be less than 45 mm Hg. With 100% oxygen used as the sweep gas, blood flow was adjusted to maintain arterial blood oxygen saturation at or greater than 80%. If possible, ventilator settings were diminished to 4 to 6 breaths per minute with a FIO ₂ of 30% to 40%, with peak inspiratory pressures less than 20 cm H₂O and end-expiratory pressures less than 10 cm H₂O to allow for lung rest. Hemofiltration, if needed, was achieved by the circuit.

Patients were anticoagulated with heparin (initial dosage 100 U/kg, followed by an intravenous drip) to maintain an activated clotting time between 150 and 200 seconds. A perfusionist was present at the bedside during all periods of V-V ECLS.

Weaning Procedure
For weaning, patients’ chest radiographs were evaluated daily for improvement and compliance of the lungs evaluated. Once clearing of interstitital edema commenced on radiograph, patients were tested for weaning. Oxygen and CO₂ clearance provided by the ELCS circuit was reduced in stepwise increments while blood gas measurements and hemodynamic variables were observed. Ventilator support was increased on demand. Acceptable PaO ₂ (>60 mm Hg), PaCO ₂ (<50 mm Hg), and stable pH for a period of 2 to 3 hours with the reduced device support demonstrated the improvement in respiratory function and represented indication for removal of the device. For device removal, patients received 100 U/kg of intravenous heparin and the flow rate was reduced in stepwise increments of 1 L/minute to off over a period of 30 to 60 minutes. The removal of the V-V ECLS circuit was performed either at the bedside in the intensive care unit or in the operating room.

Statistical Analysis
For Tables 1 through 3, continuous variables were expressed as mean ± standard deviation of the mean. Means were compared by a two-sample 2-tailed Wilcoxon rank sum test. Nominal variables were expressed as percentages and were analyzed by a 2-tailed Fisher exact test.

	Results

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Twenty adult patients required V-V ECLS support after pulmonary endarterectomy in the last 15 years. Since 1990, UCSD has averaged 1.3 cases per year of severe reperfusion injury requiring V-V ECLS after pulmonary endarterectomy, with a maximum of 3 cases in 1 year. Successful weaning off V-V ECLS was 40% (8 of 20 patients), and survival to hospital discharge was 30% (6 of 20 patients). Of the 20 patients placed on V-V ECLS after pulmonary endarterectomy, 18 had been referred from hospitals outside of California in the United States (16 patients) or from Europe (2 patients), 1 was transported to our hospital on a ventilator, and 1 was inotrope-dependent prior to surgery. All but one patient, who required ECLS support, was found to have type 3 or type 4 thromboembolic disease at the time of surgery (Table 1).

Characteristics of patients treated for severe reperfusion injury after pulmonary endarterectomy are listed in Table 1. In general, patients who required V-V ECLS support after surgery had very high preoperative pulmonary vascular resistance (mean PVR 1148.7 + 450.0 dynes/sec/cm^–5) and manifest large reductions in pulmonary vascular resistance after pulmonary endarterectomy (mean decrease in PVR 660.7 ± 407.1 dynes/sec/cm^–5). There was no correlation between preoperative respiratory function, as measured by PaO ₂ and PaCO ₂ and survival after V-V ECLS support. Surgical variables such as cardiopulmonary bypass time and circulatory arrest time in patients requiring ECLS after surgery were similar to recorded values for patients who underwent uncomplicated pulmonary endarterectomy during the same time frame. Mean time of ventilation for all patients before V-V ECLS cannulation was 86.8 ± 80.0 hours with a median of 48 hours. Although not statistically significant by itself, there was a clear-cut trend of longer periods of ventilatory support prior to initiation of ECLS support in patients who did not survive versus those who did. For example, we found that survival was greater in a patient cannulated within 120 hours of surgery (46.2%; 6 of 13 patients) compared with those cannulated after 120 hours (0 of 7 patients).

Prior to the initiation of ECLS, patients manifest deterioration in oxygenation and carbon dioxide clearance, despite high levels of inspiratory oxygen (100% oxygen for all patients), high peak inspiratory pressures (mean 41.7 ± 9.1 cm H₂O), and high positive end-expiratory pressures (mean 12.5 ± 3.4 cm H₂O) (Table 2). Five patients suffered pneumothorax prior to ECLS cannulation. Progressive respiratory failure was accompanied by an average increase in pulmonary artery pressures and pulmonary vascular resistance. The combination of deteriorating gas exchange, nonphysiologic ventilator settings, and worsening pulmonary hypertension were the constellation of factors that prompted initiation of V-V ECLS. Despite aggressively instituting V-V ECLS when severe reperfusion injury was anticipated, two patients suffered cardiopulmonary arrest prior to initiation of support.

All patients on ECLS had a significant blood transfusion requirement, necessitating support with packed red blood cells (pRBC), fresh frozen plasma (FFP), and platelets (Table 3). Although not statistically significant, nonsurvivors received a higher mean and median number of each of these types of blood products. Multiple logistic regression identified severity of preoperative pulmonary artery systolic pressure (p = 0.0855) and pre-ECLS ventilation time greater than 120 hours (p = 0.0942, odds ratio = 3.75, 95% confidence interval = [0.342 and 41.082]) as predictors of mortality. Of the 8 patients who survived to decannulation, 6 survived to discharge and 2 succumbed to sepsis (1 fungal, 1 bacterial; 5 and 18 days after cessation of V-V ECLS) while on intravenous antibiotics and antifungal drugs.

Pulmonary endarterectomy with subsequent V-VECLS support was associated with numerous perioperative complications (Table 4). Pneumonia was the most common complication found (75%; 15 of 20 patients), with concomitant high incidence of renal failure-dialysis (9%), bacteremia (7%), and bleeding necessitating surgical re-exploration (3%). The most common cause of death was massive endobronchial bleeding leading to pulmonary hemorrhage through the endotracheal tube (25%; 5 of 20 patients). For each of these patients, endobronchial bleeding occurred within 48 hours of systemic anticoagulation for ECLS (with a mean 98.6 hours after pulmonary endarterectomy), despite maintenance activating clotting time levels of 150 to 200 seconds. Individuals who were terminally weaned from ECLS also died from multiorgan failure (4 patients), persistent right heart failure from pulmonary hypertension (1 patient), sepsis (1 patient), and nonhemorrhagic stroke (1 patient).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

Despite refinements in operative technique and improvements in perioperative care, severe reperfusion-induced lung injury remains a significant cause of early morbidity and mortality for a very small number of patients after pulmonary endarterectomy. The syndrome typically occurs within the first 48 hours after operation and is characterized by nonspecific alveolar damage, lung edema, hypercarbia, and hypoxemia. The clinical spectrum can range from mild hypoxemia and hypercarbia associated with little interstitial edema on chest radiograph to a syndrome of progressive opacification of the lung fields on chest radiograph with concomitant acute respiratory failure, leading to inability to provide adequate ventilation by conventional strategies. In the more severe cases, strategies such as administration of neutrophil adhesion inhibitors [14], high dose steroids [15], and inhaled nitric oxide [16] have been tried to limit reperfusion edema after pulmonary endarterectomy with variable success. Despite aggressive measures to treat this process and provide adequate gas exchange, a small subset of patients after operation progress to fulminant respiratory failure requiring ECLS support. It is our belief that if these patients could have adequate gas exchange support during their period of lung injury-recovery, that some may be saved from inevitable death.

Patients who developed life-threatening reperfusion injury after pulmonary endarterectomy were distinguished by several clinical characteristics. First, although the patient numbers are small, there is no apparent sex or age predilection toward the development of this complication. Second, all patients who required ECLS support manifest extremely high preoperative pulmonary vascular resistance (mean 1,148.7 dynes/sec/cm^–5; range, 464 to 1,892 dynes/sec/cm^–5) and preoperative pulmonary artery systolic pressures (mean 87.0 mm Hg; range, 65 to 110 mm Hg), on the high side of the spectrum for which we operate on this disease. Perhaps most interesting is the observation that all but two of these patients had type 3 thromboembolic disease [17] (fibrosis, intimal webbing, and thickening with or without organized thrombus within distal segmental arteries only) identified at the time of surgery. We speculate that removal of disease from small subsegmental pulmonary vessels (rather than main or lobar vessels) may, in some patients, trigger a vascular leak-like syndrome that results a severe reperfusion response. This response may be due to increased flow through new small areas of open vessels, leading to significant ventilation-perfusion mismatch.

In this study we retrospectively looked at our experience over 15 years with V-V ECLS in the postoperative treatment of pulmonary endarterectomy patients. In almost 1,800 pulmonary endarterectomies performed at our institution during this timeframe with a survival rate 94.2%, only 20 patients have required ECLS support, with a survival rate of 30.0%. Our results demonstrate that V-V ECLS may be used to salvage patients with fulminant reperfusion injury after pulmonary endarterectomy, although the rate of success is limited and the perioperative morbidity is high. We have chosen a strategy of V-V ECLS, in contrast to venoarterial ECLS (V-A ECLS; extracorporeal membrane oxygenation [ECMO]) for these patients, because failure after pulmonary endarterectomy is usually due to inadequate gas exchange rather than need for cardiovascular circulatory support. Numerous previous studies have also suggested that V-V ECLS is associated with a lower complication rate than V-A ECLS [18].

Since the first report of venovenous cardiopulmonary bypass to manage severe respiratory failure in adult patients was reported by Gattinoni and associates in 1979 [19], this method of support has been used to salvage adult patients with respiratory failure from trauma [10], mechanical airway obstruction [20], postcardiotomy shock [21], diffuse alveolar hemorrhage from granulomatous disease [22], and adult respiratory distress syndrome [23]. Success rates for survival and hospital discharge after V-V ECLS support in series of more than 20 patients ranges from 15% to 52%. Individuals who have undergone pulmonary endarterectomy present a unique challenge for V-V ECLS support, as they are more prone to several specific complications not found in other types of ECLS patients. For example, we found that 25% of ECLS patients suffered massive pulmonary hemorrhage, manifest by endotracheal bleeding, leading to death after anticoagulation with heparin. Although this complication is extremely uncommon in routine pulmonary endarterectomy patients, we suspect that hemorrhage came from significant coagulopathy that may be associated with ECLS as well as potential technical difficulty resulting in the disruption of vascular interface during the actual endarterectomy. In addition, a small cohort of V-V ECLS patients (5%) never recover right ventricular function after pulmonary endarterectomy. We suspect that persistent right ventricular failure represents the persistence of pulmonary hypertension from small vessel-microvascular (undiagnosed type 4) disease, despite surgical attempt at correction. Although it is difficult to separate complications of the pulmonary endarterectomy surgery (reperfusion injury, persistent pulmonary hypertension, etc) from complications of ECLS (bleeding, end-organ dysfunction, etc), we did find a common theme of pneumothorax (pre-ECLS), pneumonia, and renal failure requiring dialysis in many of the patients who were supported by ECLS.

Mortality in our series was directly related to longer durations (>120 hours) of mechanical ventilation before the institution of ECLS. Patients who underwent delayed V-V ECLS manifest extremely poor gas exchange with hypoxemia and hypercarbia, systemic hypotension, and longer periods of ventilatory barotrauma than patients who were rapidly supported. We speculate that prolonged hypercarbia contributes to pulmonary small vessel vasoconstriction, worsening pulmonary hypertension, and consequent exacerbation of reperfusion injury after pulmonary hypertension. The relationship between the long periods of mechanical ventilation and mortality is consistent with progressive alveolar damage with fibroproliferative changes that occurs in the injured lung and current knowledge regarding the adverse sequelae induced by pressure injury, distension trauma, and supranormal levels of ventilatory oxygen [24]. Early postoperative hypotension may be the catalyst for multisystem organ failure, leading to death. All 12 patients terminally withdrawn from ECLS died from either pulmonary hemorrhage with progressive pulmonary dysfunction, multiorgan failure, persistent right ventricular failure, sepsis, or stroke.

In our experience, during mechanical circulatory support special attention has to be given to the following points. First, infection (predominantly pneumonia) is common and contributes to the poor outcome in these patients. This warrants aggressive prophylactic antibiotic and antimycotic therapy. Second, bleeding complications, like pulmonary hemorrhage and mediastinal bleeding, are associated with a high mortality. Vigilance in monitoring activated clotting time, fibrinogen, antithrombin III, hematocrit, white blood cell, and platelet count is essential to everyday maintenance while on V-V ECLS. Finally, in order to avoid fluctuations in systemic venous return and stroke work of the heart during the period of mechanical circulatory support, the central venous pressure should be kept relatively constant, and fluid balance should be kept close to even or slightly negative. Diuresis during V-V ECLS support aids in decreasing lung interstitial edema.

Our study is limited by several factors: it is a retrospective, single-center experience over 15 years, lacking any form of randomization. Concurrently, the surgical technique of pulmonary endarterectomy has improved, management protocols and drug treatments for thromboembolic pulmonary hypertension have evolved during the time of this study, and postoperative care has become more focused on aggressive diuresis, avoidance of hypercarbia that can precipitate pulmonary hypertension in the immediate postoperative period, and avoidance of ventilator barotrauma with oxygen toxicity. Nonetheless, we have seen approximately 7 cases of life-threatening reperfusion injury every 5 years (from 1990 to 1995, 1996 to 2000, and 2001 to 2005) regardless of these changes in surgical and medical management.

In conclusion, we believe that the unique potential of V-V ECLS to support gas exchange without causing further lung damage from positive pressure ventilation makes it an appropriate treatment option in adults with fulminant respiratory failure after pulmonary endarterectomy. Patients who are appropriate for this level of support include the following: (1) those with good hemodynamic response after pulmonary endarterectomy; (2) those with potentially reversible, life-threatening reperfusion injury; and (3) those without other significant comorbidities or end-organ failure. Although not clearly evident in the patient population included in our study, with increasing experience we have become more vigilant about selecting only the appropriate patients whom we believe may benefit from this technique. Typically these patients have had significant improvement in their hemodynamic parameters with an ideal residual PVR that is less than 600 dynes/sec/cm^–5. We would also consider V-V ECLS as the last therapeutic option in a young patient with severe life-threatening reperfusion edema who despite modest reduction in PVR, may still have significant residual pulmonary hypertension with PVR levels greater than 600 dynes/sec/cm^–5. Obviously in such patients the prognosis still remains poor and will not improve if reperfusion injury has not recovered within the first seven days. We believe that further refinements in this technique and appropriate timing of its application will lead to a higher rate of survival in patients with life-threatening reperfusion edema after a successful pulmonary endarterectomy.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Patricia A. Thistlethwaite, MD, is supported by NIH grant R01 HL70852 and a grant from the Cardiovascular Medical and Research Education Fund.

	References

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 

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