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Ann Thorac Surg 2006;82:138-145
© 2006 The Society of Thoracic Surgeons
a Joseph B. Whitehead Department of Surgery, Section of Pediatric Cardiothoracic Surgery, Atlanta, Georgia
b Division of Neonatology, Atlanta, Georgia
c Division of Cardiology in the Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia
d The Division of Critical Care Medicine at Children's Healthcare of Atlanta at Egleston, Atlanta, Georgia
e The ECMO and Advanced Technologies Center at Children's Healthcare of Atlanta at Egleston, Atlanta, Georgia
Accepted for publication February 4, 2006.
* Address correspondence to Dr Forbess, UT Southwestern Medical Center, Children's Medical Center, Dallas, TX 75235 (Email: joseph.forbess{at}utsouthwestern.edu).
Presented at the Fifty-first Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 2–4, 2004.
| Pediatric cardiac surgery:
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METHODS: Retrospective analysis of patients on VA-ECMO for cardiac failure was performed. Survival was defined as discharge from hospital.
RESULTS: Twenty-seven patients were supported with VA-ECMO (median age, 27 days; range, 1 to 640 days; median weight, 3.8 kg; range, 1.8 to 11.3 kg). Diagnoses were cardiomyopathy-myocarditis (CMM) in 8 (30%), systemic-to-pulmonary artery shunt-dependent single ventricle (SV) in 12 (44%), postcardiotomy for biventricular repair (BiV) in 6 (22%), and arrhythmia in 1 (4%). Sixteen of 27 patients survived (59%). Seven of 8 CMM patients survived (88%); 6 (75%) bridged to cardiac recovery, 1 to transplant (13%), and 1 death (13%). Seven of 12 SV patients survived (58%). The SV ECMO indications: post-Norwood ventricular dysfunction (n = 3, 2 deaths), postoperative cardiac failure (n = 6, 2 deaths), respiratory failure (n = 1, 1 death), and acute shunt occlusion (n = 2, 0 deaths). One of 6 BiV patients survived (17%). The BiV ECMO indications: failure to wean from CPB (n = 3, 3 deaths), postoperative cardiac failure (n = 2, 2 deaths), and pulmonary hypertension (n = 1, 0 deaths). Fifteen patients (56%) underwent cardiopulmonary resuscitation during ECMO cannulation. Eleven of 15 R-ECMO patients (73%) survived versus 5 of 12 non-R-ECMO patients (42%, p = 0.13). Median duration of R-ECMO: 66 hours (range, 18 to 179) versus 145 hours (range, 43 to 986, p = 0.01) for non-R-ECMO.
CONCLUSIONS: Resuscitation extracorporeal membrane oxygenation is an appropriate application in pediatric patients with cardiac disease. Single ventricle patients experiencing cardiopulmonary collapse and CMM patients have favorable outcomes. Failure to wean from CPB and postoperative ventricular failure are higher risk indications.
Acute cardiovascular collapse in pediatric patients with congenital heart disease (CHD) carries a dismal prognosis and has an estimated survival of 14% to 41% [1–3]. Although conventional pharmacologic intervention is the most common modality utilized in the resuscitation of these patients, the overall effectiveness remains bleak. Therefore, the employment of extracorporeal membrane oxygenation (ECMO) in this high-risk patient population has been applied. Since the initial reports in the 1970s by Baffes and colleagues [4] and Bartlett and colleagues [5], a more widespread application of ECMO has resulted in its use in neonates with a complex array of illnesses.
In the pediatric population with CHD, ECMO traditionally has been utilized for preoperative, intraoperative, or postoperative cardiac failure, or cardiomyopathies (with the hopes of recovery or bridge to transplantation). More recently, the indications for ECMO have expanded to include patients with acute cardiovascular decompensation. Duncan and colleagues [6, 7] have shown that pediatric patients with heart disease requiring ECMO for cardiac arrest had similar survival when compared with those requiring ECMO for all other indications.
Since July 2002, our institution has adopted an aggressive treatment strategy for resuscitative ECMO (R-ECMO) for pediatric patients with congenital heart disease and acute cardiovascular deterioration. The purpose of the present study was to review our institutional use of venoarterial (VA)-ECMO for cardiac diagnoses since the introduction of R-ECMO and to assess the impact of this aggressive treatment strategy.
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The indications for placement on ECMO included poor systemic perfusion and impaired ventricular function by transthoracic echocardiography (TTE) despite optimized fluid status, inotrope treatment, and ventilator management. Specifically, we have adopted the criteria by del Nido [8] in determining which patients are placed on R-ECMO: (1) witnessed arrest; (2) rapid institution of CPR; (3) no recovery of cardiac function within 20 minutes of the initiation of CPR; (4) no contraindications to mechanical support, such as sepsis, preexisting severe neurologic deficit, or multiorgan failure. The decision to discontinue ECMO was determined in conjunction with the family and a multidisciplinary team and was related to irreversible multisystem organ failure. The specific indications for ECMO were cardiomyopathy-myocarditis (CMM) in 8 patients (30%), systemic-to-pulmonary artery shunt-dependent single ventricle (SV) in 12 (44%), postcardiotomy for biventricular repair (BiV) in 6 (22%), and arrhythmia in 1 (4%). In those patients with postcardiotomy ventricular failure, ECMO was initiated if at least two attempts to wean the patient off bypass failed.
Extracorporeal Membrane Oxygenation Technique
A standard roller-head pump ECMO circuit (Stõckert S3, Sorine Biomedical Inc, Irvine, CA) with a membrane oxygenator (Medtronic, Minneapolis, MN), hemofiltrator (Asahi Medical Co, Ltd, Tokyo, Japan), and heat exchanger were utilized. Cannulation was performed either directly in the aorta and right atrium with left atrial (LA) venting or through the internal jugular vein and carotid artery using nonheparinized tubing. In those patients in the operating suite and who were unable to be weaned from CPB, the cannulae were already in place and patients were transferred from CPB to ECMO by switching the cannulae connections to the ECMO circuit. Appropriate cannulae were implanted to minimize, aggressively, right and (or) left ventricular distention. The VA-ECMO system was utilized so that the membrane oxygenator was in parallel configuration with the native lungs. This allowed us to support the oxygen content to the lungs and the cardiac output to the heart so that we could resuscitate patients with numerous etiologies.
A continuous heparin drip was maintained in all patients on ECMO to achieve an activated clotting time between 180 and 200 seconds. Administration of coagulation products were maintained such that platelet counts remained greater than 100,000 µL, fibrinogen levels greater than 100 mg/dL, and international normalized ratio less than 2.5.
An ECMO unit is primed with crystalloid and remains in storage in the cardiac intensive care unit (ICU). Packed red blood cells or crystalloid solutions were used for initiation of ECMO. Initial ECMO flows were implemented at 20 to 30 mL/kg per minute and were increased to achieve adequate oxygen delivery, generally between 80 and 120 mL/kg per minute. Measurement of serum lactate, arterial base deficit, and mixed venous oxygen saturation levels were utilized to ensure adequate systemic perfusion. In those patients with systemic-to-pulmonary shunts, the shunt was preserved and higher flows were generally necessary for adequate systemic perfusion.
Readiness to wean from ECMO was evaluated by clinical assessment of each surgeon and TTE at a reduced pump flow every 24 to 48 hours. Decannulation was performed after a satisfactory 1 to 2 hour interval on conventional support.
At our institution, a specialized team of fully trained, certified nurses and respiratory personnel manage the ECMO circuitry. These personnel are present within the hospital on a 24-hour basis. In the deployment of R-ECMO, initiation of circulatory support can be performed with the preprimed crystalloid circuit if blood products are not available. During CPR, ice was routinely applied to the patient's head and systemic cooling was not generally applied.
The ventilator was maintained at rest settings: peak airway pressures less than 30 cm H20; peak end-expiratory pressures between 8 and 12 cm H20; ventilator rate of 10 to 15 breaths per minute; and fraction of inspired oxygen of 0.21 to 0.40. Fluids, electrolytes, and renal function were monitored using patient care initiatives. All patients received either enteral or parental nutrition. Prophylactic antibiotics were administered to all patients with an open chest.
Statistics
Data are expressed as mean ± standard deviation, median, and range. Differences between groups (R-ECMO vs non-R-ECMO) were determined with the Student t test for continuous data and the Fisher exact test for categorical data. These analyses were performed using a commercially available statistical package (Sigma Stat 2.03, San Rafael, California). Statistical significance was defined as a p value of 0.05 or less.
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Specific patient characteristics and outcomes are listed for all 27 patients (Table 2). Seven of 8 cardiomyopathy-myocarditis (CMM)-arrhythmia patients (88%) survived their hospital course with 6 patients (75%) bridged to cardiac recovery, 1 (13%) bridged to cardiac transplant, and 1 (13%) death. Seven of 12 (58%) systemic-to-pulmonary artery shunt-dependent single ventricle (SV) patients survived their hospitalization. Indications for ECMO in this group included post-Norwood ventricular dysfunction (n = 3, 2 deaths), loss of previously normal postoperative cardiac function (n = 6, 2 deaths), respiratory failure (n = 1, 1 death), and acute shunt occlusion (n = 2, 0 deaths). One of six patients (17%) with biventricular repair (BiV) survived. Indications for ECMO in this group included failure to wean from cardiopulmonary bypass (n = 3, 3 deaths), postoperative cardiac failure (n = 2, 2 deaths), and pulmonary hypertension (n = 1, 0 deaths). Patients treated with R-ECMO included 5 patients with CMM-arrhythmias (all patients alive at hospital discharge and late follow-up), 9 with SV (6 of 9 [66.7%] alive at hospital discharge and 4 of 9 [44.4%] alive at late follow-up), and 1 with BiV (none alive at hospital discharge).
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While the precise indication for ECMO support has significant bearing on patient outcome, most studies do not provide distinction in the survival among these indications. The current study is unique in that it provides in-hospital and late survival for all subcategorized patients undergoing ECMO; cardiomyopathy, myocarditis, arrhythmia, single ventricle physiology, biventricular physiology, and resuscitative.
In a retrospective review, Morris and colleagues [10] evaluated 137 patients managed with ECMO in a pediatric cardiac ICU over six and a half years. They noted that although 58% of patients survived greater than 24 hours after decannulation, only 39% survived to hospital discharge. A multivariate analysis of patients requiring ECMO after cardiac surgery revealed that age less than 1 month and male gender significantly affected hospital survival. They did not find any significant independent predictors in the nonsurgical ECMO group. Furthermore, they did not find that failure from separation from cardiopulmonary nor cardiac physiology alterations (single ventricle) correlated significantly with hospital survival.
The duration of ECMO has been shown to affect survival. While some have shown that most patients who survive recover contractile function within 48 to 72 hours [11–13], others have noted that minimal survival exists after 144 hours [14]. In the current study, 9 of 16 (56.3%) survived hospitalization when on ECMO for greater than 72 hours compared with 7 of 11 (63.6%) surviving with less than 72 hours of ECMO (p = not significant [NS]). In those patients on ECMO less than 144 hours, 13 of 19 patients (68.4%) survived, while only 3 of 8 (37.5%) survived with greater than 144 hours of ECMO (p = NS). Despite these differences, statistical significance was not achieved due to the inadequate power of this study. In contrast, Aharon and colleagues [12] have shown that 56% of patients requiring ECMO less than 72 hours were successfully discharged to home compared with only 36% who required ECMO greater than 72 hours. Kulik and colleagues [15] summarize by noting that ECMO support 200 hours or greater is very unlikely to result in survival in pediatric cardiac patients.
ECMO for Cardiomyopathy, Myocarditis, or Arrhythmia
In the pediatric population, mechanical ventricular assist devices (VADs) for circulatory support in intractable or acute heart failure as a bridge to recovery or transplantation have limited availability. Therefore, ECMO support remains the most used modality for circulatory support in this pediatric patient population [16, 17]. Mehta and colleagues [18] describe 8 nonsurgical patients (3 with acute myocarditis and 5 with end-stage dilated cardiomyopathy), but requiring ECMO for cardiac failure. Of these patients, all 5 patients with end-stage dilated CM underwent ECMO followed by heart transplantation and 4 survived (80%). Similarly, of the 4 patients in the current study with idiopathic cardiomyopathy, 3 (75%) survived their hospital stay. In these 3 patients, ECMO was utilized as a bridge to heart transplantation in one patient and as a bridge to recovery in two patients.
In the 3 patients with acute myocarditis, Mehta and colleagues [18] noted only one patient (33%) was weaned from ECMO and discharged to home. In contrast, all 4 patients (100%) in our series were successfully weaned from ECMO and were discharged.
In an earlier paper, del Nido and colleagues [11] describe 6 children (dilated cardiomyopathy: 3 patients; viral myocarditis: 3 patients) who underwent ECMO as a bridge to heart transplantation. One patient with myocarditis recovered without a heart transplant, while the other 5 underwent transplantation. Of these 5 patients, 4 (80%) survived to hospital discharge and 1 died secondary to sepsis. In agreement with Mehta and colleagues [18] and del Nido and colleagues [11], we feel that survival in patients undergoing ECMO for CMM is favorable.
del Nido and colleagues [11] also note the importance of preventing severe left ventricular distention, which commonly presents as pulmonary edema. In those with ECMO cannulation through the neck, as is usual for patients with myocarditis or cardiomyopathy, left ventricular decompression can be performed in the catheterization laboratory by balloon atrial septostomy (BAS) with or without the placement of an atrial stent. In our patients with CM, 3 of 4 patients underwent BAS and stenting after ECMO for left ventricular decompression (1 patient recovered, 1 underwent a heart transplant, and 1 died from sepsis). In 4 patients with myocarditis, 2 underwent post-ECMO balloon atrial septostomy (both bridged to recovery).
ECMO for Patients With Single Ventricle Physiology
Controversy still surrounds the use of ECMO in patients with single ventricle physiology, where mortality is generally greater than 50% [14, 19, 20]. The higher mortality in this subset of patients with incomplete repair has been hypothesized as an imbalance between systemic and pulmonary blood flow and associated suboptimal coronary perfusion and increased probability of ventricular distension [21]. Pizarro and colleagues [21] have described 12 patients undergoing ECMO after stage I Norwood surgery. They noted that 8 patients (67%) were weaned from ECMO and 6 (50%) survived hospitalization. Aharon and colleagues [12] noted that infants with single-ventricle physiology who required ECMO support had improved in-hospital survival when compared with those with biventricular physiology (11 of 18 patients [61%] vs 14 of 32 patients [43%]). Similarly, in the current series, patients with single ventricle physiology had an improved survival when compared with BiV physiology (58% vs 17%, p = 0.152), albeit not statistically significant.
Similar to Jaggers and colleagues [22], Pizarro and colleagues [21] noted a much better outcome in those patients placed on ECMO in the operating room or early in their failure. In the current study, 12 patients undergoing ECMO had SV physiology, with 7 surviving (58%). Of the 4 patients with ECMO intraoperatively or within 24 hours of surgery, 3 (75%) survived hospitalization. Of the 7 patients undergoing ECMO after 24 hours of surgery, 3 (42.8%) survived hospitalization. We agree with Jaggers and Pizarro that ECMO support for pediatric patients with SV physiology is efficacious when performed early in the postoperative course.
ECMO for Postcardiotomy Cardiac Failure
In a recent report by Chaturvedi and colleagues [23] in 81 children placed on ECMO after cardiac surgery, they noted that the initiation of ECMO in the operative theater improved the odds of survival when compared with those patients in which ECMO was started in the ICU (30 of 47 patients [64%] vs 10 of 34 [29%], respectively). In the latter group, the median interval from cessation of CPB to ECMO was 21.9 hours. In the current series, 17 patients required ECMO after pediatric cardiac surgery; 5 required ECMO within the operative theater, and 12 required ECMO at a median of 17 days after surgery. In contrast to Chaturvedi and colleagues [23], we had a dismal survival of patients requiring ECMO during surgery (1 of 5 patients, 20%), compared with those requiring ECMO postoperatively (6 of 12 patients, 50%).
In a series of 11 patients, del Nido and colleagues [24] reported early survival of 64% and long-term survival of 55% after sudden cardiac arrest in the postoperative period. In that series, cardiac arrest ensued 39 ± 15 hours after cardiac surgery, the mean duration of CPR before the start of ECMO support was 65 ± 9 minutes, and the average length of ECMO support was 112 ± 18 hours.
Not all reports regarding ECMO have been positive. In a report of nine children requiring ECMO postoperatively, Langley and colleagues [19] noted an overall weaning from ECMO and decannulation in 44% of patients with hospital survival of 22%. Furthermore, they noted that of seven children requiring ECMO in the operating theater after failure to wean from corrective surgery, only one patient survived (14%).
Resuscitative ECMO
The outcome of children after out-of-hospital cardiac or respiratory arrest remains dismal and is estimated at approximately 15% survival to hospital discharge [25]. In this high-risk patient population, the median time from CPR to R-ECMO has ranged from 42 to 65 minutes and hospital survival from 44% to 80% [7, 8, 10, 12, 26]. The distinct advantages of R-ECMO include prompt institution of cardiac output, regulation of systemic temperature, and diminution of oxygen delivery without the deleterious consequences of high-dose inotropic medications and high-inspired fractioned oxygen.
In an eloquent paper, Duncan and colleagues [7] retrospectively reviewed 11 pediatric patients with heart disease treated by rapid-resuscitation ECMO. They noted that 10 patients (91%) were weaned successfully from ECMO, while 7 (64%) were discharged from the hospital. In the current series, 15 patients underwent R-ECMO. The overall in-hospital survival was 11 of 15 patients (73.3%), with 9 patients (60%) alive at late follow-up. We agree with Duncan and colleagues [7] that the expedient restoration of cardiac output most likely improves survival in this high-risk pediatric population.
The time interval from CPR to R-ECMO has been noted as a limiting factor in the effectiveness of any rescue during acute cardiac and pulmonary failure. At the Children's Hospital of Pittsburg, survival was 100% in patients with CPR times less than 15 minutes, whereas survival was 55% in those who underwent CPR for more than 42 minutes [26]. Similarly, Aharon and colleagues [12] have shown that patients with CPR duration greater than 45 minutes tended to have poorer survival. Morris and colleagues [10] have noted that the duration of chest compressions prior to the initiation of ECMO did not differ significantly between survivors and nonsurvivors. In agreement with Morris and colleagues, we did not note a decrease in survival in those patients with substantial CPB times.
Late Follow-Up
A paucity of literature exists on late follow-up for pediatric patients with congenital heart disease undergoing ECMO. Ibrahim and colleagues [27] performed late follow-up in 26 patients who had been previously supported on ECMO. At a median follow-up time of 43 months, only one patient died after hospital discharge. Similarly, we noted an 81% survival of those patients surviving their hospitalization at a median of 17 months.
Limitations
The current series has limitations that are inherent to retrospective, observational studies. Furthermore, the small cohort size precludes sophisticated statistical analyses and lacks the power to detect clinically significant outcome differences.
In summary, the current series has shown that ECMO is a viable treatment modality in pediatric patients with congenital heart disease and cardiopulmonary collapse. Furthermore, we have shown that SV patients experiencing sudden cardiopulmonary collapse and CMM patients have favorable outcomes. We have shown that R-ECMO is an appropriate application of VA-ECMO. Nevertheless, failure to wean from CPB and postoperative ventricular failure are higher risk indications for VA-ECMO.
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DR THOURANI: Thank you, Dr. Ungerleider, for the comments and also the question. During that time period we did not use VADs. In my experience, we have used VADs infrequently, and as Dr. Pennington mentioned this morning, the new advent of VADs may increase our use during that time period. We do use an oxygenator for those, and that is a good point. Of the patients that we had with single ventricles, as far as I can remember, all patients had oxygenators.
DR D. GLENN PENNINGTON (Johnson City, TN): A great presentation. I was curious as to why the biventricular patients did poorly. Certainly ECMO doesn't really support the left ventricle and in fact may have a negative effect on the left ventricle if you are doing just venoarterial bypass, and many times it has been necessary to either place an extra cannula into the left ventricle or the left atrium to provide biventricular support. Was that a factor in those patients, you think?
DR THOURANI: That is an excellent question. There were a handful of patients that required an extra cannula in the left atrium to help decompress the left ventricle, and I think early in our series when we were doing those biventricular patients that may be one of the reasons that they failed. If you noticed, most of those patients were intraoperative patients, where we had access to the left atrium, and I think that that may be one of the reasons that there was a higher mortality in that group, and we have changed our philosophy that we are doing that more often. There was one patient who did survive in the biventricular group that we actually put a direct left ventricular decompression cannula, and that actually was successful.
DR ERLE H. AUSTIN III (Louisville, KY): I enjoyed this and think it is important to make everyone realize that it is important to have ECMO available for emergency resuscitation. You have shown that those patients actually do relatively well. My question relates to what appear to be two groups of ECMO patients. There appears to be a group with cardiomyopathy to which you compared this cardiopulmonary resuscitation group. It is interesting to me that the length of time on ECMO is significantly different. How do you decide when a patient on ECMO is not going to survive, and can you go over what you used to decide when to discontinue support in a patient that wasn't going to survive?
DR THOURANI: Thank you, Dr. Austin, for that question. The indications for removing ECMO mainly depended on the entire physiological status of the patient; for instance, sepsis, overwhelming sepsis, but also neurologic conditions. There were a few patients who had severe neurologic conditions, which were thought to be completely unrecoverable, and after discussions with the family they were discontinued.
As you saw, the majority of the patients, 20 out of 27, were weaned from ECMO; not all of them survived. In fact, we lost four patients from discontinuation of ECMO to survival. So the majority of patients did get weaned from ECMO, but the patients who had severe neurologic or severe sepsis, those patients did not successfully get weaned from ECMO. For the most part, we were able to get them off ECMO.
DR JAMES A. QUINTESSENZA (St. Petersburg, FL): Regarding the single ventricle shunt occlusion patients, presumably they had very low oxygenation while they were getting CPR. How did they do neurologically after? I know there were no deaths in that group, there were just two patients, but how did they do neurologically?
DR THOURANI: A very good question also. Currently, one of our cardiology staff, Dr. Bill Mahle, is actually looking through all the neurologic patients in follow-up on these patients. So although I have no data for that, these patients are being followed currently and we are about halfway going through all the neurologic status for those patients. So hopefully that will be forthcoming.
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) and late (
) survival of pediatric patients with congenital heart disease undergoing venoarterial extracorporeal membrane oxygenation (VA-ECMO) by pre-ECMO diagnosis. In-hospital survival: CM/Myo/Arr vs BiV (p = 0.011); late survival: CM/Myo/Arr vs BiV (p = 0.041). (Arr = arrhythmia; BiV = postcardiotomy failure after biventricular repair; CM = cardiomyopathy; Myo = myocarditis; SV = systemic-to-pulmonary artery shunt-dependent single ventricle.)