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A 16-Year Neonatal/Pediatric Extracorporeal Membrane Oxygenation Transport Experience

Bernard J. Wilson, Jr, MD^*, Howard S. Heiman, MD^*, Thomas J. Butler, MD, Kathryn A. Negaard, BSN^* and Robert DiGeronimo, MD^*

^* Department of Pediatrics, Section of Newborn Medicine, San Antonio Military Pediatric Center, San Antonio, Texas
Division of Neonatology, Children’s Hospital Medical Center of Akron, Akron, Ohio

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	ABSTRACT

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Objective. To characterize the population and survival of neonatal and pediatric patients transported by Wilford Hall Medical Center (WHMC) on extracorporeal membrane oxygenation (ECMO) since 1985.

Study Design. A retrospective chart, literature, and database review of pediatric and neonatal patients transported on ECMO by the WHMC ECMO transport team. In addition, a subpopulation analysis was performed comparing neonates with meconium aspiration syndrome (MAS) placed on ECMO at WHMC with those infants with MAS transported on ECMO. Characteristics of interest for this comparison included disease severity before ECMO, age at initiation of ECMO, survival, ECMO-related complications, and duration of ECMO support.

Results. Forty-two patients transported on ECMO were identified: 23 neonatal respiratory cases (survival 57%), 7 pediatric respiratory cases (survival 71%), 4 cardiac cases (survival 50%), and 8 extra-institutional ECMO transports (survival 63%). In the MAS subpopulation, there was significantly greater survival in the in-house group—97% (31/32)—than in the ECMO transport group—75% (9/12); there were no other significant differences between these groups. Overall, no ECMO-related complications leading to patient demise could be identified in the ECMO transport group.

Conclusions. ECMO transport, although demonstrating acceptable survival, is a risk-laden modality that should not replace early referral to an ECMO center.

Key Words: extracorporeal membrane oxygenation • respiratory insufficiency • congenital heart defects • infant • newborn • infant • child • transportation of patients

Abbreviations: ECMO, extracorporeal membrane oxygenation • WHMC, Wilford Hall Medical Center • ELSO, Extracorporeal Life Support Organization • EET, extra-institutional ECMO transport • PPHN, persistent pulmonary hypertension of the newborn • TAPVR, total anomalous pulmonary venous return • MAS, meconium aspiration syndrome • iNO, inhaled nitric oxide

	INTRODUCTION

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Extracorporeal membrane oxygenation (ECMO) is a method of heart-lung bypass that has been used in over 18 000 neonates and 4400 pediatric patients with life-threatening cardiac or respiratory failure.¹ Predicted mortality among the group of neonates with respiratory failure selected for this intervention is roughly 80%; cumulative mortality for this group is currently 22%. Because of the geographic diversity of the military population, and Wilford Hall Medical Center (WHMC) being 1 of only 2 ECMO centers west of the Mississippi at the time, WHMC began performing neonatal ECMO transports in November 1985. This system was designed to offer ECMO support to critically ill neonates who were too unstable for conventional transport to an ECMO center. Mobile ECMO capability allowed infants to be placed on ECMO at the referring institution, with subsequent transport to WHMC for completion of the ECMO course. In 1993, WHMC expanded its ECMO transport program to include pediatric patients. In addition, we identified the need for the transport of a small subset of patients already placed on ECMO but who required advanced therapies not available at the referral institution or WHMC (eg, cardiac surgery, heart-lung transplant). These patients were transported from the referral institution to a center capable of offering definitive therapy. The primary goal of this study was to characterize the patient population referred for ECMO transport and to determine survival to discharge or transfer in the various diagnostic groups of transported patients (neonatal respiratory, pediatric respiratory, cardiac).

	METHODS

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Existing data concerning WHMC ECMO transports before 1996 (compiled by Cornish² and Butler [unpublished data]) were available as a starting point for the project. WHMC Extracorporeal Life Support Organization (ELSO) data forms, local records, and the ELSO database were reviewed to compile a complete list of the ECMO transports performed between 1996–2001. Data available for all patients transported to WHMC on ECMO included diagnosis and survival to discharge. Survival data were also summarized for the extra-institutional ECMO transport (EET) group—those patients transported from one outside institution to another. Additional data were gathered for the largest diagnostic subgroup of patients transported on ECMO, those with meconium aspiration syndrome (MAS). This included age on ECMO, length of run, any significant complications that occurred while on bypass, and final PaO₂ before initiation of ECMO. As data were available for infants with MAS placed on ECMO at WHMC (in-house group), comparisons were made between this group and its peer ECMO transport group. Finally, survival data were compared for 2 epochs of WHMC neonatal ECMO transport—1985 to 1989 and 1990 to 2001. Continuous variables were analyzed by Student t test, and ² test was used to evaluate discrete data.

WHMC selection criteria for neonates in respiratory failure being considered for transport ECMO are fairly standard, and include gestational age of at least 34 weeks, birth weight of greater than 2 kg, absence of severe, underlying nonpulmonary disease, no evidence of intracranial hemorrhage on cranial ultrasound (germinal matrix hemorrhage excluded), and no uncontrolled bleeding or known bleeding diathesis. In addition, the infant must demonstrate severe, reversible respiratory failure, defined by standard oxygenation index criteria, which is not responsive to conventional medical management. Duration of mechanical ventilation greater than 10 days is considered a relative contraindication. Pediatric or cardiac candidates for transport ECMO are considered on a case-by-case basis, with input from a pediatric intensivist or cardiologist as warranted.

The WHMC ECMO transport cart has changed significantly since its original description by Cornish et al in 1991.² The cart, originally designed to accommodate only neonates, is now large enough for an adult-sized patient. Its dimensions are 84-inches long by 20-inches wide by 52.5-inches high, and its weight is 740 lbs. In its neonatal configuration, it has a bassinette tray bolted to the top. This can be removed and a pad can be placed to carry a larger pediatric patient. The cart is designed so that all of the necessary ECMO equipment is secured on the shelf space below the patient. This equipment includes a Stöckert roller pump (Cobe Cardiovascular, Arvada, CO), Seabrook water heater (Cincinnati Sub-Zero, Cincinnati, OH), bladder box, cardiorespiratory monitor, MVP-10 ventilator (Bio-Med Inc, Guilford, CT), 3 uninterruptible power sources, and a CDI 400 (Terumo/Sarns/CDI, Ann Arbor, MI). The latter provides continuous arterial and venous blood gases from the ECMO circuit, as well as venous saturation. Also housed on the transport cart are 3 "Q" tanks—1 containing medical air, 1 containing oxygen, and 1 containing carbogen. All of the above equipment has been tested by the Air Force Research Laboratory at Brooks Air Force Base, San Antonio, Texas, and meets or exceeds all Air Force airworthiness standards for aeromedical equipment. Standard manometers are used to monitor premembrane and postmembrane pressures. Other essential equipment is taken in 3 large rolling containers; the total weight of equipment, including the cart, is 1670 lbs.

Vehicles required for a ground ECMO transport include an ambulance and 2 large vans to carry transport personnel and equipment. Air transports are performed using a variety of Air Force fixed-wing aircraft with aeromedical capability. The aircraft chosen depends on availability and distance of the transport.

The WHMC ECMO transport team is individually tailored for specific missions. For long-distance air transports, essential personnel includes 2 staff ECMO physicians, 2 neonatal fellows, 1 staff surgeon, 1 surgical resident, 2 patient nurses, 2 ECMO coordinators, and 2 respiratory therapists.

	RESULTS

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The WHMC ECMO transport team, between November 1985 and September 2001, performed a total of 42 ECMO transports. Thirteen of these were ground transports and 29 were fixed wing. The shortest transport was a distance of 10 miles on bypass and the longest was 6700 miles. A summary of neonatal respiratory, pediatric respiratory, and pediatric/neonatal cardiac ECMO transport survival is shown in Table 1. In addition, 8 EET runs were performed during this time period. Five of these patients survived (1/1 MAS/persistent pulmonary hypertension of the newborn [PPHN], 2/3 myocarditis—bridge to transplant, 1/1 total anomalous pulmonary venous return [TAPVR]—bridge to reparative surgery, 1/1 TAPVR status postrepair). The deaths in the EET group were an infant with alveolar capillary dysplasia, and a 2-year-old and 7-year-old with cardiac failure, from viral myocarditis and status postaortic valve repair, respectively, who died awaiting organ transplantation. Survival for transported, pediatric respiratory cases is 71% (5/7), compared with a 66% (4/6) in-house survival rate for this same group and an overall ELSO Registry survival of 55%.

	DISCUSSION

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We have reported on a series of 42 neonatal and pediatric patients transported on ECMO over the past 16 years by the WHMC ECMO transport team. This represents the cumulative experience of the only facility capable of performing worldwide ECMO transport, and the largest ECMO transport experience reported to date. Despite an increase in the number of ECMO centers since 1985, WHMC remains the only military hospital that provides ECMO and 1 of only 3 US ECMO centers known to us that transport patients routinely on ECMO (the others being the University of Michigan and Arkansas Children’s Hospital). The early WHMC experience was published by Cornish et al in 1991² and consisted of 13 neonatal patients transported on ECMO between November 1985 and October 1989. The survival (until discharge or 30 days of life) for this group was 31%. This report also addressed transport complications specific to ECMO and found that although such complications did occur in transport, they did not contribute to the overall mortality of this group. They postulated that the decreased survival in the transport group when compared with their ECMO population as a whole (79%) might have resulted from delays in the referral of these infants. Supporting this was an average time between the first blood gas qualifying an infant for ECMO and the institution of bypass in the transport group of 28 hours compared with 12.8 hours in all other ECMO patients in their series. The 3 deaths in our MAS ECMO transport group were from this original 1985 to 1989 series, and when one considers only those infants with MAS transported between 1990 and 2001 to our in house MAS ECMO group, the difference in survival is no longer significant. Cornish’s hypothesis regarding delays in referral of these infants may by itself explain the difference in survival; however, data are unavailable to examine whether improved survival in the ECMO transport group post-1990 is related to more expeditious referral. Roy et al³ examined the changing demographics of the neonatal ECMO population between 1988 and 1997 and found that pre-ECMO use of surfactant, high frequency ventilation, and inhaled nitric oxide (iNO) had, in that time period, increased from 0% to 36%, 46% and 24%, respectively. They also noted that the 1997 group was "healthier" before ECMO based on improved indices of gas exchange and decreased peak inspiratory pressure required just before ECMO. These factors may have contributed to the difference in survival between our 1985 to 1989 group and 1990 to 2001 group, as well as the difference between the MAS groups.

The University of Arkansas’ ECMO transport experience for the years 1990 to 1994 was published in a 1995 article by Heulitt et al.⁴ Survival was 9/13 (70%) for their series of neonatal patients, and 8/9 patients had normal brain magnetic resonance imaging post-ECMO. They described no major complications during their "mobile-ECMO" runs but did note multiple minor equipment and communication complications specific to transport ECMO. The Arkansas experience differs from that of WHMC in that Arkansas performs regional ECMO transport only, whereas nearly half of the ECMO transports performed by WHMC have been of distances greater than 1000 miles. These distances necessitate occasionally performing ECMO on a transport aircraft for time periods exceeding 12 hours.

Boedy et al⁵ in 1990 described a "hidden" mortality associated with delayed referral of critically ill infants to an ECMO center for evaluation for ECMO. Twelve percent of their population of 158 outborn ECMO referrals died either before or during conventional transport, yet these deaths are not reported to ELSO, which maintains a database of all ECMO runs reported by its members. Boedy et al⁵ postulated that earlier, expedited transfer of these infants to a regional ECMO center would curtail their mortality. This "hidden" mortality may be an even larger issue in the milieu that exists in neonatal intensive care today.

Concomitant with the advent of iNO therapy for use in near-term neonates with pulmonary hypertension, the use of surfactant in term infants with respiratory failure, and the proliferation of high frequency ventilation, the number of annual ECMO cases for neonatal respiratory failure has been decreasing.¹ This is not surprising given the results of recent, randomized, controlled trials of each of these therapies.^6–8 The decline in neonatal ECMO cases over the past decade has paralleled a modest decline in the number of active ECMO centers. As expected, those centers that still offer neonatal ECMO are doing fewer cases per year.³

Although novel therapies have contributed to the decline in neonatal ECMO, they do not obviate the need for ECMO.^6–8 Many centers that routinely use these therapies do not have ECMO capability, and failure criteria for iNO and high-frequency ventilation are ill-defined. Wilson et al⁹ in 1996 reported on the changing demographics of the ECMO population at the Children’s Hospital of Boston. They compared 4 consecutive 3-year periods and found that survival post-ECMO decreased over time, whereas duration of ECMO runs and complications of ECMO significantly increased. In addition, they noted that at least 6 neonatal patients referred for ECMO over the last 3-year period were unable to be converted from high-frequency ventilation to conventional mechanical ventilation for transport and subsequently died.⁹ The WHMC ECMO transport experience supports Wilson’s findings. In our neonatal respiratory population between 1990 and 2001, the rationale for request for ECMO transport in every case was instability off of high-frequency ventilation and thus inability to be transported conventionally. As can be inferred from the above examples, there is presently no high-frequency transport ventilator for neonates that is in widespread use. Recent recommendations regarding the use of iNO state that its initiation should "generally" be limited to centers with ECMO capability.¹⁰ If used in non-ECMO centers, these guidelines call for predetermined failure criteria for iNO therapy and a means of uninterrupted delivery of nitric oxide if transport to an ECMO center is necessary. The latter is necessary because of the possibility of severe deterioration on discontinuation of iNO therapy even in infants who are considered nonresponders.¹¹

We believe that as the number of local or regional ECMO centers decline, and the use of adjunctive therapies in non-ECMO centers to treat respiratory failure in term and near-term infants increases, there will continue to be a need for ECMO transport in a subpopulation of neonates with severe cardiorespiratory failure unable to be transported conventionally. In addition, there will remain a group of infants placed on ECMO for respiratory failure of unknown cause, whose ultimate diagnoses (surfactant protein B deficiency, alveolar capillary dysplasia, TAPVR) requires intervention (heart-lung transplant, cardiac surgery) not available at that institution. Discontinuation of ECMO for transport to a center capable of providing definitive care will likely not be feasible in most of these cases. Thus, ECMO transport will be the only option to safely transport these patients.

Pediatric ECMO has burgeoned since 1988, and the number of annual cases has not decreased as precipitously as neonatal ECMO cases. Indeed the number of annual pediatric respiratory ECMO cases has been fairly static at about 200.¹ Almost 2000 pediatric respiratory cases have been reported to ELSO as of July 2000, with 55% surviving to discharge or transfer. Over the past 5 years, our center has received an increasing number of pediatric ECMO referrals and an increasing number of requests for pediatric ECMO transport. Of the 18 referrals for pediatric ECMO in the last 3 years, 10 were accepted and placed on bypass for respiratory support, with 5 requiring transport ECMO. Patients referred for ECMO transport but not accepted were refused for a variety of reasons including: 1) failure to meet defined ECMO criteria, 2) the patient expired or alternatively stabilized allowing for conventional transport, and/or 3) inadequate logistic and personnel support available at the time to accomplish the transport. Overall, the WHMC ECMO transport team accepts and transports approximately 40% of ECMO transport referrals.

A review of the cases of the 3 children who ultimately did not survive after extra-institutional ECMO transport raises several important questions concerning the utility of ECMO transport in this subpopulation. All of these patients, including 1 neonate and 2 pediatric patients, were originally placed on ECMO at their referral institution but subsequently required transport to another center for transplantation. The neonatal patient was placed on ECMO within the first day of life for severe respiratory failure. He was subsequently diagnosed with alveolar capillary dysplasia via lung biopsy, and transported on ECMO to a transplant center after preliminary acceptance for lung transplantation. Unfortunately, head computed tomography done after transport revealed an infarct that disqualified the infant from transplant consideration, and the infant was taken off of bypass. Although the infarct was felt to most likely have existed before transport, cranial ultrasonography done at the referring institution had not demonstrated this pathology. In this case, had a previous head computed tomography or magnetic resonance imaging been performed and an infarct identified, ECMO transport could have been averted. The 2 pediatric patients in this subgroup that required ECMO transport to a transplant center originally presented in acute cardiac failure. The first patient was a 2-year-old female who had heart failure secondary to viral myocarditis, and the second a 7-year-old male unable to wean off cardiac bypass in the operating room after repair of severe aortic stenosis. Both patients were placed on ECMO but were subsequently unable to come off bypass, so they were referred to outside institutions to be listed for cardiac transplantation. They were successfully moved on ECMO to their accepting hospitals. However, although both patients were initially good candidates for heart transplantation, they eventually died from complications related to long-term bypass, still awaiting transplantation.

Concerning EETs, these 3 cases illustrate the need to identify as precisely as possible a patient’s condition and eligibility for ECMO before accepting any child for ECMO transport. Both the accepting and referral facility, in conjunction with the wishes of the family, must work closely together to determine whether ECMO transport is desirable in each individual case. In addition, although the utility of ECMO transport for neonatal and pediatric respiratory failure, as well as for reversible cardiac failure, seems justified in our experience, the use of this modality as a bridge to transplantation may not be. Better delineation of subpopulations of neonatal and pediatric patients appropriate for ECMO transport needs to be further investigated.

	CONCLUSION

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Based on the summary of our transport ECMO data as detailed above, we believe that the WHMC ECMO transport experience demonstrates the feasibility, efficacy, and the safety of short- and long-range ECMO transport. We also believe that there will continue to be a subset of neonatal and pediatric patients in the near future whose clinical situation necessitates the use of this modality. However, despite the absence of significant complications and an acceptable survival in our experience, ECMO transport remains an extremely risk laden and expensive tool that should not replace early referral to an ECMO center of potential candidates who are not responding to conventional therapy.

	WHAT THE FANATICS CAN’T UNDERSTAND

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" ... The Islamic terrorists think our wealth and power is unrelated to anything in the soul of this country—that we are basically a godless nation, indeed the enemies of God. And if you are an enemy of God you deserve to die...Terrorists believe that wealth and power can be achieved only by giving up your values, because they look at places such as Saudi Arabia and see that many of the wealthy and powerful there lead lives disconnected from their faith.

Of course, what this view of America completely misses is that American power and wealth flow directly from a deep spiritual source—a spirit of respect for the individual, a spirit of tolerance for differences of faith or politics, a respect for freedom of thought as the necessary foundation for all creativity and a spirit of unity that encompasses all kinds of differences. Only a society with a deep spiritual energy, that welcomes immigrants and worships freedom, could constantly renew itself and its sources of power and wealth.

Which is why the terrorists can hijack Boeing planes, but in the spiritless, monolithic societies they want to build, they could never produce them. The terrorists can exploit the US-made Internet, but in their suffocated world of one God, one truth, one way, one leader, they could never invent it."

Friedman TL. New York Times. October 2, 2001

Noted by JFL, MD

	FOOTNOTES

 
Received for publication Jun 18, 2001; Accepted Oct 2, 2001.

Reprint requests to (R.D.) Wilford Hall Medical Center/MMNP, 2200 Bergquist Dr, Suite 1, Lackland Air Force Base, TX, 78236-5300. E-mail: robert.digeronimo{at}59mdw.whmc.af.mil

The opinions and assertions contained in this manuscript are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of Defense (and/or the Department of the Army).

	REFERENCES

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1. Extracorporeal Life Support Organization. ELSO Registry Report, International Summary. Ann Arbor, MI: ELSO; July2001
2. Cornish JD, Carter JM, Gerstmann DR, et al. Extracorporeal membrane oxygenation as a means of stabilizing and transporting high risk neonates. ASAIO Trans.1991; 37 :564 –568[Medline]
3. Roy BJ, Rycus P, Conrad SA, et al. The changing demographics of neonatal extracorporeal membrane oxygenation patients reported to the ELSO registry. Pediatrics.2000; 106 :1334 –1338[Abstract/Full Text]
4. Heulitt MJ, Taylor BJ, Faulkner SC, et al. Interhospital transport of neonatal patients on extracorporeal membrane oxygenation: mobile ECMO. Pediatrics.1995; 95 :562 –566[Abstract]
5. Boedy RF, Howell CG, Kanto WP. Hidden mortality rate associated with extracorporeal membrane oxygenation. J Pediatr.1990; 117 :462 –464[Medline]
6. Clark RH, Yoder BA, Sell MS. Prospective, randomized comparison of high frequency oscillation and conventional ventilation in candidates for extracorporeal membrane oxygenation. J Pediatr.1994; 124 :447 –454[Medline]
7. Lotze A, Mitchell BR, Bulas DI, et al. Multicenter study of surfactant (beractant) in treatment of term infants with severe respiratory failure. Survanta in Term Infants Study Group. J Pediatr.1998; 132 :40 –47[Medline]
8. The Neonatal Inhaled Nitric Oxide Study Group. Inhaled nitric oxide in full-term and nearly full-term infants with hypoxic respiratory failure. N Engl J Med.1997; 336 :597 –604[Abstract/Full Text]
9. Wilson JM, Bower LK, Thompson JE, et al. ECMO in evolution: the impact of changing patient demographics and alternative therapies on ECMO. J Pediatr Surg.1996; 31 :1116 –1123[Medline]
10. American Academy of Pediatrics, Committee on Fetus and Newborn. Use of inhaled nitric oxide. Pediatrics.2000; 106 :344 –345[Abstract/Full Text]
11. Davidson D, Barefield ES, Kattwinkel J, et al. Safety of withdrawing inhaled nitric oxide therapy in persistent pulmonary hypertension of the newborn. Pediatrics.1999; 104 :231 –236[Abstract/Full Text]

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