Venoarterial extracorporeal membrane oxygenation using magnetic levitation centrifugal pumps for fulminant myocarditis in infants, children and young adults

Introduction

Fulminant myocarditis (FM), is a severe, rapidly progressive disease resulting from cardiac muscle inflammation: is an independent entity associated with an aggressive course and high risk for circulatory collapse. The most common causes are viral infections but it can be seen as a result of other infections, autoimmune diseases, and intoxications (1-3). Patients with FM typically have a short viral prodrome with distinct onset of symptoms (<14 days) and rapid deterioration requiring hemodynamic support. There is a wide spectrum of clinical manifestations at onset, from sub-clinical asymptomatic courses to refractory cardiogenic shock (4) that makes early diagnosis hard to depict. The prognosis depends mainly on the severity of clinical presentation. In all cases, treatment of the acute phase is supportive, because there are still no specific therapies. In cases of refractory cardiogenic shock, venoarterial (VA) extracorporeal membrane oxygenation (ECMO) is the most suitable mechanical support because it is easy to set up and quick insertion at bed-side is possible in case of emergency (5-7). The aim of the present paper is to report the results of VA ECMO for FM in infants, children and young adults at our Institution. We present this article in accordance with the STROBE reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-24-29/rc).

Methods

Study population and ECMO management

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was waived of ethical approval due to the retrospective nature and individual consent for this retrospective analysis was waived. The endpoints of the study are: survival, incidence of ECMO-related complications, rate of weaning from ECMO, recovery of cardiac function and the association between ECMO implantation during cardiopulmonary resuscitation (r-ECMO) and weaning failure/mortality.

This paper is designed as a single centre study, describing our experience with management of FM in our cardiac surgery centre in Verona. Starting from April 2009 to January 2021 we manage to collect 17 patients presenting with FM who were supported using VA ECMO. There were 8 male and 9 female patients with median age of 5.2 years [interquartile range (IQR), 2 months to 32 years] and median body weight of 16 kg (IQR, 3.8–56 kg). For the survival analysis we divided the population into three groups according to age: infants (0–2 months; n=5), children (2–6 years; n=5) and young adults (24–40 years; n=7). Patient demographics are summarized in Table 1. All data were collected by a meticulous research through clinical records and ambulatory documentation.

Patients were diagnosed with FM on the basis of their clinical presentation which often reviled a history of viral prodrome with fever and flu-like symptoms that lead onto a rapid deterioration and development of severe cardiac dysfunction at echocardiography examination (8-11), without structural cardiac anomalies that could explain the degree of cardiac impairment. Where it was possible also a cardiac biopsy was performed, usually during ECMO or vent implant. Indications for ECMO initiation at our institution included: (I) development of severe hypotension (<80 mmHg for young adults, <60 mmHg for children and <50–40 mmHg for infants and neonates) refractory to maximal inotropic support; (II) generation and progressive increment of blood lactate (>2.5 mmol/L); (III) cardiac arrest requiring continuous cardiopulmonary resuscitation refractory to medical therapy; and (IV) uncontrolled arrhythmia (ventricular tachycardia and fibrillation) that generates a low cardiac output syndrome. All patients with the previous described criteria underwent VA ECMO using magnetic levitation centrifugal pumps. Mainly two types of magnetic levitation pumps and circuits were used: the PediVas Blood Pump (Levitronix LLC, Waltham, MA, USA) and Rotaflow pump (Maquet AG, Hirrlingen, Germany). The rest of the ECMO components were similar for both pumps and consisted of D 902 Lilliput II ECMO oxygenator (Sorin Group, Mirandola, Modena, Italy) or Quadrox oxygenator (Maquet AG, Hirrlingen, Germania) based on patient body surface area and biocompatible circuit (A.g.i.l.e. Eurosets, Medolla, Modena, Italy). The decision regarding the site of implant was mainly dependent upon the status of the patients, body weight, the setting of ECMO deployment and anatomical factors. In central deployment the arterial cannula was inserted directly in the ascending aorta and the venous cannula in the right atrium. In peripheral access ECMO, in all pediatric patients the arterial cannula was inserted in the right carotid artery and the venous cannula in the right atrium through the right internal jugular vein, both vessels were proximally ligated and, in case of left heart distension, a left ventricular vent was inserted through a left thoracotomy for decompression. In young adults, the preferred cannulation site was through the groin for both cannulas (right femoral vein for venous cannula and left femoral artery for the arterial cannula), and also when needed a left ventricular vent was inserted through a left thoracotomy. Correct positioning of the cannulae was assessed by transthoracic or transesophageal echocardiography. Pump flow was maintained between 125–150 mL/kg/min and anticoagulation was managed by intravenous (IV) heparin infusion with target activated coagulation time between 160–200 seconds. During mechanical support, minimal ventilation was maintained for pulmonary recruitment with rest settings [positive end expiratory pressure (PEEP) 3–4 cmH₂O; fraction inspired oxgen (FiO₂) 0.21–0.40 respiratory rate 6–15/min based on the patients age and weight; tidal volume 4–5 mL/kg]. When needed, a low-dose (0.01–0.04 mcg/kg/min) vasopressor, first choice was norepinephrine, support was utilized to maintain a mean arterial pressure of 40–50 mmHg in pediatric patients and 60–80 mmHg in young adults, while washing out from inotropic support was routinely performed. Broad spectrum antibiotics and blood products replacement therapy [hemoglobin (Hb) >10 g/dL, platelets (PLT) >50,000/mm³, antithormbyn 3 (ATTIII) >1 U/mL, fibrinogen >2 g/L] were utilized. Neurological assessment was performed every 48 hours utilizing transfontanellar ultrasound, when possible in neonates and children, and clinical assessment and computed tomography (CT) in remaining patients. Trans-esophageal or trans-thoracic echocardiography was performed every 24/48 hours to monitor ventricular recovery. Hemodynamic performance was assessed by bedside catheterization (arterial, right atrial, pulmonary artery/left atrial) monitoring manometry/oximetry during in full flow ECMO support. To establish weaning time, the same parameters were assessed at ECMO flow rates lower than 25% predicted with no more than moderate inotropic support (norepinephrine less than 0.05 mcg/kg/min), routinely using inhaled nitric oxide therapy for pulmonary recovery and to mitigate pulmonary hypertension. If the parameters remained stable at less than 25% flow rate ECMO support, decannulation was undertaken. In cases of failure to wean, ECMO support was resumed and bridge to heart transplant (HT) or ventricular assist device (VAD) was considered.

Statistical analysis

Descriptive statistical analysis was performed. Continuous variables are reported as median and IQR because, in the subgroup analysis, the distribution was not normal to the Shapiro-Wilk test. The between-group differences of the continuous variables were analyzed with non-parametric tests (Wilcoxon rank-sum test). Categorical variables are reported as frequencies and percentages and differences were assessed with the Fisher’s exact test, depending on the sample size.

A P value ≤0.05 was considered significant. Survival analysis was performed using Kaplan-Meier curves.

Results

Within 17 patients the etiology of FM was a viral infection in 8 patients (47.06%), bacterial in 1 (5.88%), 2 giant cellular myocarditis (11.76%) and in 6 patients the etiology was unknown (35.29%) and supposed to be viral (Table 2). To complete the diagnosis, a biopsy was performed in 9 out of 17 patients.

ECMO implantation approach was tailored to patients, in particular peripheral cannulation was used in 14 (82%) patients and central in 3 (18%) (Table 3). Left or systemic ventricle decompression via left atrial or left ventricular vent was adopted in 9/17 (53%) patients.

Median duration of support was 168 hours (range, 120–240 hours) (Table 3). Thirteen patients were weaned from support (weaning rate 76%), 2 (12%) underwent respectively cardiac transplantation and Bi-VAD Berlin Heart implantation while on ECMO support, while the other 2 (12%) succumbed during the ECMO support.

Bleeding occurred in 6 (35%) patients, with the need for multiple transfusions of blood components; eight patients (47%) suffered from infection with increased blood inflammation markers and the need for intravenous antibiotic therapy and 5 patients (29%), all of them infant patients, required peritoneal dialysis for acute kidney injury (Table 3). There were no cases of thrombosis or thromboembolic complications. Mortality was 35% (n=6): all deaths were intra-hospital. Three patients, both with anatomically normal hearts, died after ECMO weaning. The first patient was a 17 days old, 3.4 kg affected from viral myocarditis and was assisted with VA ECMO through the neck. The neonate had a long clinical history which included several circuit’s change, pump change and a down grading form VA ECMO to veno-venous (VV)-ECMO/right-VAD in median sternotomy. After successful weaning the patient did well for 6 weeks and the heart recovered its function, but in proximity to hospital discharge she experienced fever, vomiting, diarrhea and a new episode of cardiac failure [ejection fraction (EF) <20%]. The child succumbed during the attempt to position another rescue ECMO device. The other patient was a 5 years old girl supported for 157 hours with peripheral VA ECMO from the neck for a FM caused by a bacterial infection (Staphylococcus aureus). After 41 days of good clinical status the child experienced signs and symptoms suggestive of reactivation of the disease. Cardiac echocardiography showed a severe bi-ventricular cardiac dysfunction (EF <20%) and the patients was assisted with a second central VA ECMO run. During support, several complications occurred such as bleeding, air embolism through the vent line and clot formation in the circuit which caused severe neurological complications. After 6 days of support the heart failed to recover, CT-scan showed severe neurological complications (absence of cerebral flow) which led to the stop of ECMO support and patient’s death. The other one was a 4-year-old boy who was assisted with VA ECMO for FM due to a Parvovirus B19 infection who was weaned and died in the pediatric intensive care unit (ICU) due to severe respiratory complications.

Three patients died during mechanical support. The first, was a 1-month-old neonate with an anatomically normal heart, suffering from giant cell FM. After 220 hours of support with VA ECMO, a Bi-VAD was implanted due to failure to recover ventricular function with an intent to bridge the patient to HT. The clinical condition worsened with the onset of multi-organ-failure (MOF) and subsequent death. The second was a 13-day-old neonate with a normal heart, who suffered from adenovirus myocarditis and died during ECMO support due to failure to recover ventricular function and a recurrent fatal arrhythmia. The last was a 1-month-old neonate who underwent an arterial switch operation for transposition of the great arteries (TGA) and subsequently suffered from giant cell myocarditis in the post-operative period: she died after 12 days of ECMO assistance due to failure to recover ventricular function and ECMO related uncontrolled bleeding. The overall survival at follow-up was 65% (Figure 1), with a statistically significant difference (P=0.050) between age groups: survival in the infant group was 20% (1/5) in the children group 60% (3/5) and in the adult group 100% (7/7) (Figure 2). In our case series, more than half of the patients (9/17) underwent ECMO set up during cardiopulmonary resuscitation (r-ECMO): there was no association between r-ECMO and weaning failure (33.3% vs. 12.5%; P=0.58) or hospital mortality (33.3% vs. 37.5%; P=0.99) (Table 4). Excluding the 6 patients deceased in early phase, the others 11 continued a median follow-up of 76 months (IQR, 52–99 months) in which there were no late deaths and, considering that 1/11 patient (9%) received a HT, the remaining 10/11 (91%) of surviving patients had a complete recovery of ventricular function. Only one patient of the late survivors has minor neurological sequelae.

Figure 1 Kaplan-Meier curve depicting survival in all patients.

Figure 2 Kaplan-Meier curve showing survival in patients stratified by groups.

Discussion

Myocarditis is a rare inflammatory disease of the heart and deserves special attention because it is the cause of approximately 10% of sudden cardiac death in the young population (8). An accurate and early diagnosis is crucial for the management of the disease but it could be difficult due to the broad spectrum of generic symptoms at presentation (9,10). Treatment of FM in the acute phase is mainly supportive as there are no targeted pharmacological treatments. There are protocols on the use of nonsteroidal anti-inflammatory drugs, immunoglobulins and immunosuppressive drugs but, in the case of FM refractory to maximum medical therapy, mechanical support is necessary (5,12-14).

As recent literature has shown, we too have concluded that VA ECMO is the most suitable mechanical support for FM. Its results are comparable to those of a left ventricular assist device (LVAD) and there are also decisive technical advantages: ECMO is easier and quicker to implant even at the patient’s bedside or during cardiopulmonary resuscitation and it also provides bi-ventricular assistance (15-18). Moreover, the use of ECMO is especially indicated in patients presenting with recurrent arrhythmias, who would not benefit from the use of vasopressors or LVADs (5,18). As a policy in our institution we prefer assisting the patients with peripheral VA-ECMO (14/17; 82.35%) over central ECMO for a number of reasons including lower risk of bleeding, effective cardiac massage during ECMO implant, lower risk of infections, possibility of percutaneous implant in bigger patients and feasibility and rapidity of the implant per se. Escalation to LVAD after ECMO in our cohort was not necessary and thus not considered by us, even though it is preferred by some authors in literature (18,19). We managed to wean patients as early as possible and in 2 patents who succumbed while in ECMO, escalation to LVAD was not possible due to right heart failure and pulmonary inflammation. To accelerate recovery, a left ventricular venting strategy was adopted in 9/17 (52.9%) patients and included position in the apex through minithoracotomy in 3 patients, 2 via the right superior pulmonary vein, 2 via atrioseptostomy and 2 Impella device (Abiomed, Europe, GMBH).

In our centre, we use the latest generation of magnetic levitation centrifugal pumps which, in a previous paper we published, were shown to have comparable results to data registry using mainly roller pumps and also further improve end-organ recovery (20).

In our experience, using latest generation centrifugal pumps (20) has contributed to achieving better results in terms of survival and recovery of ventricular function in the whole population, even though they differ significantly when stratified by age groups. The adult and paediatric population showed excellent results, comparable to the best results reported in the literature.

Two previous meta-analyses by Pozzi et al. (4) and Chen et al. (5) respectively identified a survival of 55% to 78% and 58% to 88% in the population of adults with FM who needed support with VA ECMO for cardiogenic shock. In our experience, survival in the adult group was 100% and complete recovery of ventricular function occurred in 86% of patients (one patient underwent HT).

In the pediatric population, the survival rate reported in previous studies is between 53% and 80% (14,21-24). A meta-analysis by Xiong et al. noted that in cases of cardiac failure unresponsive to conventional therapies, ECMO should be considered because nearly 62.9% of children survive to discharge (25). In our experience, survival was 60% with complete recovery of ventricular contractility at follow-up in all discharged patients. One of the deaths that occurred in this group was for respiratory complications and non-cardiac related which had fully recovered, thus the child succumbed due to re-intubation failure for severe pulmonary and airway obstruction. Interestingly, the other patient who died in this group corresponds to the only patient in the series with bacterial myocarditis (S. aureus) which has a high morbidity and mortality and very poor prognosis as shown in a recent report and data derived from a pooled analysis by Ferrero et al. (26).

On the other hand, in the infant group, the survival rate was much lower but not significantly different from that reported in previous studies.

In a 2018 paper, Cortina et al. observed a survival of 43% in their 7 cases of neonates with FM supported with VA ECMO, but with full recovery of ventricular function in all surviving patients, without neurological damage. Adding their 7 cases to the 35 previously described in the literature, the calculated survival rate is 36% (27). A high mortality in the neonatal population, between 50% and 75% has also been reported in other smallest studies (28,29). One of the best-known single-center study, published by Madden et al. in 2011, reported a survival rate of 33%. The results in infants with FM requiring VA ECMO support for cardiogenic shock are certainly sub-optimal, but still acceptable considering that the mortality rate without mechanical support would be around 100% (30). Moreover, infants supported with ECMO often demonstrated a complete recovery of cardiac function at follow-up without neurological sequelae (31). In contrast, a report that analyzed the prognosis of infants with FM with heart failure without the need for ECMO support showed a better survival (mortality 33%) but a worse long-term prognosis: only 23% of patients had a complete recovery, while the remainder had severe cardiological sequelae such as aneurysms of the left ventricle and severe ventricular dysfunction (32). As in our experience, many previous studies have shown a significantly better prognosis in the pediatric population than in infants. The most widely accepted explanation is that the immune system of newborns is still immature, the inadequate transmission of antibodies during pregnancy and sometimes perinatal virus transmission, such as nonpolio enteroviruses, leads to severe illness and worse outcomes (27,30,33).

Duncan et al. (21) and Wilmot et al. (19) reported their results with mechanical circulatory support (MCS) (ECMO and VAD) for FM and found that when MCS is used as a bridge to transplant or to recovery, survival rates approach 80% and 75% respectively. In those studies, 40% (6/15) (21) and 37.5% (6/16) (19) of the patients underwent HT after initial MCS and the mean time from MCS to HT was relatively short, in median 5 to 6 days (21). It is not clear and specified the number of neonates supported for FM in these two studies and appears that patients who had VAD support and HT had a bigger age and body weight (21).

In our study, there were in the infant group 5 patients, 4 were neonates (median age 12 days; median weight 3.4 kg) which experienced neonatal deaths. Two neonates suffered from giant cell myocarditis (one of the worst forms of autoimmune myocarditis, with a 1-year mortality of 70%) (34), one patient had just undergone arterial switch operation at 1 month of age, thus with a partially deconditioned left ventricle. In this series, one neonate which failed ECMO weaning was bridge to Bi-VAD implant with the intent to further bridge the patient to HT. Unfortunately, the patient died due to VAD complications, after 24 days of support, while waiting for a HT. HT for this group of patients is an option to consider but unfortunately is exceedingly rare in the neonatal population. Thus, for a pediatric HT in Italy, the waiting list is long and usually falls between 3 to 6 months (mean time considering all listing is around 4.7 months and 35.6 days in national urgency criteria) (35).

Some studies have found that in the case of r-ECMO the survival at discharge is lower than normal (between 46% and 58%) (5). In our experience, we found no significant differences in weaning rate or mortality if ECMO was implanted during cardiopulmonary resuscitation: survival in the r-ECMO group was 67% and was comparable with the survival in the non r-ECMO group (62.5%).

There are conflicting opinions on the outcome of FM: some reports suggested that despite their catastrophic onset, patients with FM might have better outcome than those with acute non-FM (36). This result would be the consequence of the absence of specific symptoms at the onset of the disease, which can lead to a missed diagnosis, resulting in the progression of ventricular remodeling to dilated cardiomyopathy (3,4,11,37). In contrast, another report published by Ammirati et al. in 2017 (38), observed that patients with FM have an increased mortality and need for cardiac transplantation than patients with non-FM: patients with FM have a more impaired left ventricular function at onset of the disease which, despite improvements achieved with therapy, remains lower than that in patients with non-FM patients at long-term follow-up.

Based on our results regarding FM, we believe that young adult and children supported with VA ECMO have excellent survival with complete recovery of ventricular function at follow-up. In infants, we did not observe equally favorable results and, we can speculate that this may be due to the inherent fragility of this particular subset of patients.

Limitations of the study

Limitations of the present study are inherent with the retrospective nature of the study, small number of patients and heterogeneity of the population. It was not possible to identify the etiology agent of the FM in all patients and to perform a cardiac biopsy.

Moreover, as previously listed, different body weight and anatomical factors had a critical impact over the decision regarding the site of ECMO implant and subsequent management of mechanical support. Different surgical possibilities and options represent obviously a limitation when comparing a group of different patients.

Conclusions

Acute FM with refractory cardiogenic shock still carries a high mortality despite medical therapy. VA ECMO should always be considered in adult and child patients with FM and cardiogenic shock refractory to conventional therapies, because despite critical clinical conditions, in more than 65% of patients it leads to survival to discharge and complete recovery of ventricular function at follow-up. In infants and neonates which carry the highest mortality and morbidity for FM, results are still suboptimal, but VA ECMO should still be considered because it is the only current possibility for survival.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Antonio F. Corno & Ali Dodge-Khatami) for the column “Pediatric Heart” published in Translational Pediatrics. The article has undergone external peer review.

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-24-29/rc

Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-24-29/dss

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-24-29/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-24-29/coif). The column “Pediatric Heart” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was waived of ethical approval due to the retrospective nature and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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