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Ann Thorac Surg 2006;82:926-932
© 2006 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Ventricular Assist Device Support in Children and Adolescents as a Bridge to Heart Transplantation

Department of Cardiothoracic Surgery, The University of Pittsburgh School of Medicine, Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania

Accepted for publication February 27, 2006.

^_* Address correspondence to Dr Sharma, Department of Cardiothoracic Surgery, 200 Lothrop St, Suite C-700 PUH, Pittsburgh, PA 15213. (Email: sharmams{at}upmc.edu).

	Abstract

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BACKGROUND: Mechanical circulatory support using ventricular assist devices (VADs) is a life-saving option for children in heart failure refractory to maximal medical management. The aim of this study was to evaluate the efficacy of standard adult VADs in adolescents and children as well as report our early experience with miniaturized VADs in small children.

METHODS: A 15-year retrospective review was performed on all patients younger than 18 years of age undergoing insertion of a pulsatile VAD at our institution.

RESULTS: Eighteen patients underwent VAD placement during the study period. The mean age was 12 (range, 6 months to 18 years), with a mean body surface area of 1.48 (range, 0.25 to 2.3 m²). Diagnoses included dilated cardiomyopathy (n = 15), myocarditis (n = 2), and postcardiotomy ventricular failure (n = 1). Ten children underwent insertion of biventricular VADs, and 8 had implantation of left ventricular VADs. The mean support duration was 57 days (range, 2 to 175 days). Complications included bleeding requiring reoperation (n = 4), stroke (n = 5), and device-related infection (n = 2). Outcomes of VAD support were as follows: VAD explantation in 1 case, death while receiving mechanical support in 3 patients, and successful transplantation in 14 patients (77%). Survival at 6 months after orthotopic heart transplantation was 93% with 1-year and 5-year survival rates of 83%.

CONCLUSIONS: Currently available VADs are applicable for use as a bridge to orthotopic heart transplantation or in rare instances for myocardial recovery. The increasing accessibility of miniaturized devices allow for long-term support in smaller children and infants while awaiting orthotopic heart transplantation. Although the perioperative morbidity and mortality of VAD placement is not insignificant, survival for those who receive a heart transplant is excellent.

	Introduction

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Despite improvements in the treatment of children with heart disease, a small number of patients will experience refractory myocardial failure. For the most severe forms of heart failure, orthotopic heart transplantation (OHT) has emerged as the only effective therapy affording longevity and quality of life. In an effort to keep the patient alive until a suitable organ becomes available, mechanical circulatory support is often necessary. Historically, nonpulsatile devices such as extracorporeal membrane oxygenation (ECMO) and centrifugal pumps have been the mainstay of circulatory support technology [1–2]. Extracorporeal membrane oxygenation has the advantage of providing immediate cardiopulmonary support in patients with pulmonary hypertension, hypoxemia, and ventricular failure secondary to congenital heart disease [3]. However, with the shortage of donor hearts and requisite waiting times, the use of these devices may be hazardous. Support with ECMO and centrifugal ventricular assist devices (VADs) for more than 2 weeks is associated with increased bleeding risk, sepsis, and neurologic complications [4]. Also, the intricate circuits require patient immobilization, which has a detrimental impact on rehabilitation.

The successful use of VADs as a bridge to transplant in adults has led to the introduction of such technology for children awaiting OHT [5]. In 1991, Warnecke and colleagues [6] reported the first successful bridge to transplantation using a pulsatile paracorporeal left ventricular VAD in an 8 year-old boy. Despite worldwide use with pulsatile pediatric VADs, centers in the United States have relied on adult-sized devices because of a lack of U.S. Food and Drug Administration–approved miniaturized VADs [7].

We describe our single-center experience since 1990 with 18 children who were supported with pulsatile VADs as a bridge to OHT. Moreover, we include in this series our early experience with pediatric-sized VADs.

	Material and Methods

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Data
We conducted a retrospective review of all patients younger than 18 years of age who underwent insertion of a VAD at Children's Hospital of Pittsburgh, The University of Pittsburgh Medical Center. Our pulsatile VAD program for children and adolescents was initiated in April 1990, and data collection was completed in November 2005. Demographic and clinical outcome data including adverse events and information regarding pump performance and device malfunction were collected prospectively on all VAD recipients at the time of device implantation or on listing for transplantation. Patient data were prospectively collected into the Web-based Transplant Patient Management System. This database was designed to function as both a clinical database and a research registry and operates under protocols for these purposes that are approved by the University of Pittsburgh Institutional Review Board for the use of patient management, quality assurance reports, and clinical research. Integrity of the database and quality assurance of the data are maintained by one of the investigators (J.R.B.).

Patients
The prospectively collected data from the Transplant Patient Management System were evaluated retrospectively in patients younger than 18 years of age who underwent insertion of a VAD at Children's Hospital of Pittsburgh, The University of Pittsburgh Medical Center from April 1990 through November 2005. Data points are summarized in tabular format and expressed as a mean value with range when appropriate. The median value is reported when statistically relevant.

Children and adolescents with intractable heart failure who received pulsatile paracorporeal VADs were included in this study. Patient demographics are summarized in Table 1. The study included 10 boys and 8 girls with a median age of 12 years (range, 6 months to 18 years) with 5 children younger than 8 years of age. Body surface area ranged from 0.25 to 2.3 m² (mean, 1.48 ± 0.6 m²). The cause of heart failure was dilated cardiomyopathy in 15 patients: idiopathic (n = 13), peripartum (n = 2). One patient had a concomitant intracardiac fibroma. Two children suffered from acute myocarditis, and 1 child underwent repair of recurrent supravalvular aortic stenosis at another institution requiring postoperative ECMO. He was transferred to Children's Hospital of Pittsburgh, The University of Pittsburgh Medical Center, and subsequently had biventricular VAD placement.

View larger version (73K): [in this window] [in a new window]   Fig 1. Device type stratified by patient age. (gray bar = Thoratec ventricular assist device; black bar = Novacor left ventricular assist system; white bar = Berlin Heart Excor.)

Berlin heart excor ventricular assist device
Recently, 4 small children (body surface area, 0.25 to 1.0 m²) underwent placement of an appropriate sized (10 to 30 mL) blood pump (Berlin Heart AG Berlin, Germany) for left-ventricular support on a compassionate-use basis. The Berlin Heart consists of a paracorporeal pneumatically driven polyurethane blood pump with a multilayer flexible membrane that separates the blood and air chambers. Silicon cannulas connect the blood pump to the patient, and a triple-leaflet valve prevents blood reflux. All blood-contacting surfaces are heparin-coated (Carmeda, Inc, San Antonio, Texas). The pump is driven by a pulsatile electropneumatic system. The drive unit (IKUS 2000) has a triple operational control and pneumatic system, with synchronous and asynchronous operating modes. The synchronous mode was used in all cases.

Anticoagulation
Our anticoagulation protocol consisted of full systemic heparinization during insertion on cardiopulmonary bypass. Aprotinin was used at implant and removal. In adolescent patients, postoperative anticoagulation was started with Dextran 40% at 25 mL/h 6 hours after admission to the intensive care unit if bleeding was less than 100 mL/h. Subsequently, heparin was started when postoperative bleeding from the chest tubes was less than 50 mL/h for 3 consecutive hours. The goal for the partial thromboplastin time was 40 to 51 seconds for at least the first 72 hours or until the risk of bleeding from more aggressive anticoagulation was thought to be acceptable. Heparin was then increased to maintain a partial thromboplastin time of 50 to 70 seconds. Warfarin sodium (Coumadin; Bristol-Myers Squibb Company, Princeton, NJ) was introduced around postoperative day 10 to keep the international normalized ratio at 2.5 to 3.5. Heparin was discontinued after obtaining an international normalized ratio of at least 2.5.

The philosophy of anticoagulation was to maintain heparin until the patient demonstrated a low risk for bleeding complications and after there had been a period of stable gastrointestinal tract function and diet. This usually was found to occur around 10 to 14 days after implant. In our early experience, we did not add aspirin unless there was a specific concern about thromboembolism. Recently, we have altered our protocol to include use of aspirin. After discharge, the international normalized ratio was assessed at a minimum of 2 times per week for stable patients. Infants and small children were maintained on heparin alone with a target partial thromboplastin time range of 60 to 80 seconds followed by the addition of aspirin after 72 hours. Clopidogrel was added if there was visible fibrin or thrombus in the pump or thrombocythemia. We routinely monitored the efficacy of anticoagulation with thromboelastograms.

	Results

Top Abstract Introduction Material and Methods Results Comment References

 
The primary end points included the rates of survival to OHT and survival after transplantation. Outcomes based on the cause of end-stage heart failure are depicted in Figure 2. Overall, 15 of the 18 patients (83%) who received VADs survived the support period (Fig 3). A 16-year-old adolescent with cardiomyopathy died 16 days after VAD placement of severe biventricular failure with end-organ dysfunction. This death was early in our experience and resulted from delayed institution of support. A 7-year-old boy died as a result of unsuccessful attempt at postcardiotomy support. He was transferred to our institution 10 days after an attempted repair of a congenital defect on ECMO support. He died 2 days after biventricular VAD implantation. Postmortem examination revealed findings consistent with multisystem organ failure. Although he did have a 0.5-cm infarct in the adenohypophysis, pathologic examination revealed a subacute infarct, suggesting his stroke was likely a result of ECMO support. A third death occurred in a 12-year-old child with idiopathic dilated cardiomyopathy. She underwent left ventricular VAD implantation with immediate evidence of right ventricular dysfunction. It was believed that her right heart failure would be transient. Therefore, a centrifugal right ventricular VAD was placed, which was explanted on the fifth postoperative day. However, she died 45 days later secondary to multiple embolic events. A 17-year-old girl with peripartum cardiomyopathy demonstrated full recovery after 95 days of support and underwent VAD explantation. The remaining 14 patients were successfully bridged to OHT.

View larger version (72K): [in this window] [in a new window]   Fig 2. Outcome of ventricular assist device support based on cause of heart failure. (black bar = death; CHD = congenital heart disease; gray bar = weaned off support; white bar = bridged to transplantation.)

View larger version (10K): [in this window] [in a new window]   Fig 3. Actuarial survival curve (Kaplan–Meier) of patients on ventricular assist device (VAD; censored at time of transplantation).

View larger version (11K): [in this window] [in a new window]   Fig 4. Actuarial survival (Kaplan–Meier) of ventricular assist device–supported patients after orthotopic heart transplantation.

	Comment

Top Abstract Introduction Material and Methods Results Comment References

The decision as to which device to use for a particular situation in children is complex. Extracorporeal membrane oxygenation has certain advantages in the pediatric population in that it is relatively rapid, inexpensive, and readily available. Moreover, it allows the flexibility of peripheral and central cannulation and can provide total cardiopulmonary support. Our philosophy is to support children in the acute setting with ECMO as a bridge to recovery. Historically, we have also relied on ECMO for postcardiotomy support beyond 72 hours because of a lack of other options. Lengthy waiting times for donor organs, however, make extended support with ECMO and centrifugal VADs hazardous. Children on these devices are immobilized and become deconditioned. Extracorporeal membrane oxygenation and centrifugal pumps require high levels of anticoagulation, increasing the risk for hemorrhagic complications. Therefore, children with postcardiotomy heart failure who do not exhibit any recovery within 72 hours should be considered for conversion to a VAD.

The indications for pediatric VAD usage are evolving. Furthermore, there has been no fixed selection criteria such as those proposed for adults in whom indications and optimal timing of device implantation have been better defined. Our strategy for those children with significant biventricular failure caused by myocarditis or cardiomyopathy has been planned biventricular VAD implantation. Currently, however, we agree with Stiller and colleagues [15] that left ventricular VAD alone in this group may suffice. Left ventricular VAD therapy allows for maximal unloading of the left ventricle, which reduces the afterload of the right ventricle by up to 15 to 25 mm Hg. Combined with pharmacologic right heart support, the need for additional mechanical assistance is more limited. Studies in adult VAD recipients have shown that patients who do not exhibit signs of secondary organ malfunction have the greatest benefit from mechanical support, supporting the strategy of early intervention [16, 17]. Nevertheless, implantation of a VAD too early exposes the patient to unnecessary surgery and device-related morbidity. The importance of patient selection and timing of device implantation is illustrated in a study published by Stiller and colleagues [18] from the German Heart Center in Berlin. Of the 45 pediatric patients who received VADs during the period of 1990 to 2002, only 18 children underwent OHT, for a total survival rate of 51%. After careful analysis of their outcomes in this series, the authors concluded that most of these implantations occurred too late. Recently, the same group reported improved survival (67%) in postcardiotomy infants when compared with their historical control group [15]. The authors attribute this improvement in survival to earlier VAD implantation, exclusion of children with prolonged cardiopulmonary resuscitation, and refinements in device design, anticoagulation protocols, and intensive care unit management.

In the United States, lack of government approval for existing miniaturized VADs has necessitated the obligatory use of standard pulsatile devices in children. Although the Thoratec VAD has been used by several centers successfully in small children, specific concerns of using "oversized" devices in children have been documented [19]. These include (1) large stroke volumes (65 mL in volume mode) into a small aorta, leading to systolic hypertension and subsequent intracranial hemorrhage; (2) stasis in the device that can cause thromboembolic complications; and (3) obligatory use of multiple adult-size cannulas in a limited pericardial space. To compensate for these mechanical limitations, VADs in pediatric patients (25 kg, body surface area, 1.0 m²) may be run using the fixed mode with higher rates (80 to 90 beats/min) and partial stroke volumes. This diminishes the effect of the large volumes in small children. Although this mode causes the VAD chamber to fill submaximally, physical inspection of the device at end systole can confirm complete emptying of the pneumatic chamber. The smallest patient to date supported with this device was a 7-year-old girl (body surface area, 0.77 m²) with biventricular failure from myocarditis. She was successfully bridged to OHT using a fixed-rate mode of 90 to 120 beats/min [20].

Studies examining pediatric bridge to transplant experiences report bridging success rates of 51% to 66% [18, 21–23]. Our reported bridging success rate of 78% with no early deaths after OHT is favorable when compared with other centers using VADs for those children with heart failure as a result of cardiomyopathy or myocarditis. It is important to note that when VADs are used in the postcardiotomy setting or for complex congenital heart disease, survival on VAD is poor, ranging from 20% to 25% regardless of device [12, 23]. In an analysis of Thoratec VAD–supported children, Reinhartz and colleagues [23] demonstrated that congenital heart disease and failure to wean off bypass were independent risk factors for death (p < 0.05).

When comparing adverse events in this study with the literature, bleeding requiring reoperation, infection, and device malfunction occurred with similar frequency to our series [18, 21–23]. Neurologic events, defined as transient ischemic attack or stroke, varied from 11% to 45%. A subgroup analysis of our series reveals a stroke rate of 21% in the Thoratec group, which is less than a recent multicenter report in which the neurologic event rate was 35% [23]. Possible explanations for this include (1) a high percentage (24%) of children requiring left atrial or intraatrial groove cannulation, a demonstrated risk factor for stroke; (2) some centers using volume mode in smaller children, which expels a stroke volume of 65 mL into a relatively small aorta rather than a fixed-volume mode maintaining higher drive line pressures to ensure complete emptying of the pump; and (3) variations in anticoagulation protocols.

Both the Berlin Heart Excor and Medos HIA blood pumps are manufactured in multiple sizes, obviating large stroke volumes in small children. Device design includes the use of polyurethane valves instead of mechanical valves, which may be less thrombogenic, and transparent blood chambers and ports allowing visual control of filling and emptying and transillumination detection of thrombotic deposits. Nevertheless, neurologic event rates using these devices ranged from 11% to 45% in the literature with centers using a combination of left atrial and apical inflow cannulation and varied anticoagulation schemes [12, 21]. Pump exchanges owing to thrombus formation were not infrequent (28%) in the Berlin Heart group despite heparin coating of all blood-contacting surfaces [12]. Recent data may support the use of a modified anticoagulation protocol with heparin dose depending on a partial thromboplastin time of 60 to 80 seconds, antithrombin III substitution when less than 70%, and use of aspirin and dipyridamole depending on platelet number and function tests [15]. Of the 4 patients in our series supported with the Berlin Heart, 2 patients suffered a neurologic event. One patient had an underlying neoplasm and another patient suffered from a bloodborne infection that is known to enhance clotting potential.

Reports of 1-year and 5-year posttransplant survival in VAD-supported children vary from 62% to 88% and 47% to 72%, respectively [18, 21–23]. Post-OHT survival after VAD support in this series was excellent, with 93% of children alive at 6 months. One-year and 5-year survival after OHT was 83% (Fig 4). Despite these favorable results, there exists concern regarding the effect of sensitization in VAD-supported patients because sensitized untreated left ventricular VAD recipients have been noted to have both a prolongation of waiting time to transplantation and an increased risk of acute rejection [24, 25]. The impact of elevated panel reactive antibody (PRA) in children awaiting OHT was addressed in a recent article that demonstrated that 30-day mortality was higher with elevated PRA versus those with PRA levels of less than 10% [26]. However, this difference did not reach statistical significance. In this report, 14% of patients showed evidence of sensitization after VAD support. These children all had negative donor cross-match results at OHT. Use of a VAD in our series does not appear to significantly increase antibody sensitization before transplantation and did not appear to have a negative impact on posttransplantation survival.

Improvements in patient selection, medical optimization, and surgical technique have improved outcomes for children suffering from heart failure. Nevertheless, a subset of these patients will have refractory myocardial dysfunction requiring mechanical circulatory support. Pulsatile paracorporeal VADs have been validated as an effective strategy to keep children alive while awaiting heart transplantation. The timing of implementing VAD support is critical. The success of our bridge to transplantation experience demonstrates the feasibility of VAD support in adolescents and older children. In addition, our limited use of miniaturized VADs to successfully bridge 4 small children to OHT underscores the need for continued development and implementation of this life-sustaining technology.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mahesh S. Sharma Victor O. Morell Sanjiv K. Gandhi Peter D. Wearden Robert L. Kormos Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Sharma, M. S. Articles by Kormos, R. L. Search for Related Content PubMed PubMed Citation Articles by Sharma, M. S. Articles by Kormos, R. L. Related Collections Mechanical Circulatory Assistance Transplantation - heart