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BACKGROUND: Children who undergo cardiac surgery may require post-cardiotomy extracorporeal membrane oxygenation (ECMO). Although morbidities are considerable, our understanding of outcome determinants is limited. We evaluated associations between patient and peri-operative factors with outcomes. METHODS: The STS Congenital Heart Surgery Database was queried for patients <18yo who underwent post-cardiotomy ECMO from 1/2016-6/2021. PRIMARY OUTCOME: survival to hospital discharge. SECONDARY OUTCOME: survival without neurologic injury. Logistic regression for binary outcomes and competing risk analysis for survival were used to identify the most important predictors. Variables were selected by stepwise procedure using entry level p=0.35. Those with p≤0.1 were kept in the final model. RESULTS: A total of 3,181 patients were supported with post-cardiotomy ECMO during the same hospitalization as cardiac surgery: (A) intra-operative initiation of ECMO, n=1206; (B) early post-operative (≤48 hours), n=936; (C) late post-operative (>48 hours), n=1039. Most common primary procedure of index operation was the Norwood procedure. 57% intra-op survived to discharge, versus 59% early post-op and 42% late post-op group (χ2 (2) = 64, p<0.0001, V = 0.14). In all groups, post-op septicemia, cardiac arrest, and new neurologic injury had the strongest association with mortality, while post-operative reintubation and unplanned non-cardiac reoperation were associated with higher survival. CONCLUSIONS: Multiple risk factors impact survival in children who undergo cardiac surgery and post-cardiotomy ECMO. ECMO initiated >48 hours after surgery is associated with the poorest outcomes. This is the first step in creating a predictive tool to educate clinicians and families regarding expectations in this high-risk population.
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OBJECTIVES: To describe epinephrine dosing distribution using time-stamped data and assess the impact of dosing strategy on survival after ECPR in children. METHODS: This was a retrospective study at five pediatric hospitals of children <18 years with an in-hospital ECPR event. Mean number of epinephrine doses was calculated for each 10-minute CPR interval and compared between survivors and non-survivors. Patients were also divided by dosing strategy into a frequent epinephrine group (dosing interval of ≤5 min/dose throughout the first 30 minutes of the event), and a limited epinephrine group (dosing interval of ≤5 min/dose for the first 10 minutes then >5 min/dose for the time between 10 and 30 minutes). RESULTS: A total of 191 patients were included. Epinephrine was not evenly distributed throughout ECPR, with 66% of doses being given during the first half of the event. Mean number of epinephrine doses was similar between survivors and non-survivors the first 10 minutes (2.7 doses). After 10 minutes, survivors received fewer doses than non-survivors during each subsequent 10-minute interval. Adjusted survival was not different between strategy groups [OR of survival for frequent epinephrine strategy: 0.78 (95% CI 0.36-1.69), p = 0.53]. CONCLUSIONS: Survivors received fewer doses than non-survivors after the first 10 minutes of CPR and although there was no statistical difference in survival based on dosing strategy, the findings of this study question the conventional approach to EPCR analysis that assumes dosing is evenly distributed.
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Reanimación Cardiopulmonar , Humanos , Niño , Estudios Retrospectivos , Tasa de Supervivencia , Epinefrina , Recolección de DatosRESUMEN
Background: Previous studies have reported racial disparities in extracorporeal membrane oxygenation (ECMO) utilization in pediatric cardiac patients. Objectives: The objective of this study was to determine if there was racial/ethnic variation in ECMO utilization and, if so, whether mortality was mediated by differences in ECMO utilization. Methods: This is a multicenter, retrospective cohort study of the Pediatric Cardiac Critical Care Consortium clinical registry. Analyses were stratified by hospitalization type (medical vs surgical). Logistic regression models were adjusted for confounders and evaluated the association between race/ethnicity with ECMO utilization and mortality. Secondary analyses explored interactions between race/ethnicity, insurance, and socioeconomic status with ECMO utilization and mortality. Results: A total of 50,552 hospitalizations from 34 hospitals were studied. Across all hospitalizations, 2.9% (N = 1,467) included ECMO. In medical and surgical hospitalizations, Black race and Hispanic ethnicity were associated with severity of illness proxies. In medical hospitalizations, race/ethnicity was not associated with the odds of ECMO utilization. Hospitalizations of other race had higher odds of mortality (adjusted odds ratio [aOR]: 1.61; 95% CI: 1.22-2.12; P = 0.001). For surgical hospitalizations, Black (aOR: 1.24; 95% CI: 1.02-1.50; P = 0.03) and other race (aOR: 1.50; 95% CI: 1.17-1.93; P = 0.001) were associated with higher odds of ECMO utilization. Hospitalizations of Hispanic patients had higher odds of mortality (aOR: 1.31; 95% CI: 1.03-1.68; P = 0.03). No significant interactions were demonstrated between race/ethnicity and socioeconomic status indicators with ECMO utilization or mortality. Conclusions: Black and other races were associated with increased ECMO utilization during surgical hospitalizations. There were racial/ethnic disparities in outcomes not explained by differences in ECMO utilization. Efforts to mitigate these important disparities should include other aspects of care.
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OBJECTIVES: This systematic review aims to summarize the body of available literature on pediatric extracorporeal cardiopulmonary resuscitation in order to delineate current utilization, practices, and outcomes, while highlighting gaps in current knowledge. DATA SOURCES: PubMed, Embase, Scopus, Cochrane Library, and ClinicalTrials.gov databases. STUDY SELECTION: We searched for peer-reviewed original research publications on pediatric extracorporeal cardiopulmonary resuscitation (patients < 18 yr old) and were inclusive of all publication years. DATA EXTRACTION: Our systematic review used the structured Preferred Reporting Items for Systematic Reviews and Meta-Analyses methodology. Our initial literature search was performed on February 11, 2019, with an updated search performed on August 28, 2019. Three physician reviewers independently assessed the retrieved studies to determine inclusion in the systematic review synthesis. Using selected search terms, a total of 4,095 publications were retrieved, of which 96 were included in the final synthesis. Risk of bias in included studies was assessed using the Risk of Bias in Non-Randomized Studies of Interventions-I tool. DATA SYNTHESIS: There were no randomized controlled trials of extracorporeal cardiopulmonary resuscitation use in pediatrics. A vast majority of pediatric extracorporeal cardiopulmonary resuscitation publications were single-center retrospective studies reporting outcomes after in-hospital cardiac arrest. Most pediatric extracorporeal cardiopulmonary resuscitation use in published literature is in cardiac patients. Survival to hospital discharge after extracorporeal cardiopulmonary resuscitation for pediatric in-hospital cardiac arrest ranged from 8% to 80% in included studies, and there was an association with improved outcomes in cardiac patients. Thirty-one studies reported neurologic outcomes after extracorporeal cardiopulmonary resuscitation, of which only six were prospective follow-up studies. We summarize the available literature on: determination of candidacy, timing of activation of extracorporeal cardiopulmonary resuscitation, staffing/logistics, cannulation strategies, outcomes, and the use of simulation for training. CONCLUSIONS: This review highlights gaps in our understanding of best practices for pediatric extracorporeal cardiopulmonary resuscitation. We summarize current studies available and provide a framework for the development of future studies.
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Reanimación Cardiopulmonar , Oxigenación por Membrana Extracorpórea , Pediatría , Niño , Humanos , Estudios Prospectivos , Estudios RetrospectivosRESUMEN
OBJECTIVES: To describe the U.S. experience with interhospital transport of children in cardiac arrest undergoing cardiopulmonary resuscitation. DESIGN: Self-administered electronic survey. SETTING: Pediatric transport teams listed with the American Academy of Pediatrics Section on Transport Medicine. SUBJECTS: Leaders of U.S. pediatric transport teams. INTERVENTIONS: None. MEASUREMENTS AND MAIN RESULTS: Sixty of the 88 teams surveyed (68%) responded. Nineteen teams (32%) from 13 states transport children undergoing cardiopulmonary resuscitation between hospitals. The most common reasons for transfer of children in cardiac arrest are higher level-of-care (70%), extracorporeal life support (60%), and advanced trauma resuscitation (35%). Eligibility is typically decided on a case-by-case basis (85%) and sometimes involves a short interhospital distance (35%), or prompt institution of high-quality cardiopulmonary resuscitation (20%). Of the 19 teams that transport with ongoing cardiopulmonary resuscitation, 42% report no special staff safety features, 42% have guidelines or protocols, 37% train staff on resuscitation during transport, 11% brace with another provider, and 5% use mechanical cardiopulmonary resuscitation devices for patients less than 18 years. In the past 5 years, 18 teams report having done such cardiopulmonary resuscitation transports: 22% did greater than five transports, 44% did two to five transports, 6% did one transport, and the remaining 28% did not recall the number of transports. Seventy-eight percent recall having transported by ambulance, 44% by helicopter, and 22% by fixed-wing. Although patient outcomes were varied, eight teams (44%) reported survivors to ICU and/or hospital discharge. CONCLUSIONS: A minority of U.S. teams perform interhospital transport of children in cardiac arrest undergoing cardiopulmonary resuscitation. Eligibility criteria, transport logistics, and patient outcomes are heterogeneous. Importantly, there is a paucity of established safety protocols for the staff performing cardiopulmonary resuscitation in transport.
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Reanimación Cardiopulmonar/métodos , Paro Cardíaco/terapia , Transferencia de Pacientes/organización & administración , Transferencia de Pacientes/estadística & datos numéricos , Protocolos Clínicos , Oxigenación por Membrana Extracorpórea/métodos , Femenino , Objetivos , Hospitales de Alto Volumen , Humanos , Capacitación en Servicio/organización & administración , Masculino , Grupo de Atención al Paciente/organización & administración , Seguridad del Paciente , Transferencia de Pacientes/normas , Estados UnidosRESUMEN
OBJECTIVES: To identify modifiable factors leading to unplanned readmission and characterize differences in adjusted unplanned readmission rates across hospitals. DESIGN: Retrospective cohort study using prospectively collected clinical registry data SETTING:: Pediatric Cardiac Critical Care Consortium clinical registry. PATIENTS: Patients admitted to a pediatric cardiac ICU at Pediatric Cardiac Critical Care Consortium hospitals. INTERVENTIONS: None. MEASUREMENTS AND MAIN RESULTS: We examined pediatric cardiac ICU encounters in the Pediatric Cardiac Critical Care Consortium registry from October 2013 to March 2016. The primary outcomes were early (< 48 hr from pediatric cardiac ICU transfer) and late (2-7 d) unplanned readmission. Generalized logit models identified independent predictors of unplanned readmission. We then calculated observed-to-expected ratios of unplanned readmission and identified higher-than or lower-than-expected unplanned readmission rates for those with an observed-to-expected ratios greater than or less than 1, respectively, and a 95% CI that did not cross 1. Of 11,301 pediatric cardiac ICU encounters (16 hospitals), 62% were surgical, and 18% were neonates. There were 175 (1.6%) early unplanned readmission, and 300 (2.7%) late unplanned readmission, most commonly for respiratory (31%), or cardiac (28%) indications. In multivariable analysis, unique modifiable factors were associated with unplanned readmission. Although shorter time between discontinuation of vasoactive infusions and pediatric cardiac ICU transfer was associated with early unplanned readmission, nighttime discharge was independently associated with a greater likelihood of late unplanned readmission. Two hospitals had lower-than-expected unplanned readmission in both the early and late categories, whereas two other hospitals were higher-than-expected in both. CONCLUSIONS: This analysis demonstrated time from discontinuation of critical care therapies to pediatric cardiac ICU transfer as a significant, modifiable predictor of unplanned readmission. We identified two hospitals with lower-than-expected adjusted rates of both early and late unplanned readmission, suggesting that their systems are well designed to prevent unplanned readmission. This offers the possibility of disseminating best practices to other hospitals through collaborative learning.
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Enfermedades Cardiovasculares/epidemiología , Enfermedad Crítica/epidemiología , Unidades de Cuidado Intensivo Pediátrico/estadística & datos numéricos , Readmisión del Paciente/estadística & datos numéricos , Adolescente , Peso Corporal , Niño , Preescolar , Grupos Diagnósticos Relacionados , Femenino , Humanos , Lactante , Recién Nacido , Modelos Logísticos , Masculino , Transferencia de Pacientes , Respiración Artificial , Estudios Retrospectivos , Factores de Riesgo , Factores Socioeconómicos , Factores de Tiempo , Vasoconstrictores , Adulto JovenRESUMEN
OBJECTIVES: Cardiopulmonary failure in children with cardiac disease differs from the general pediatric critical care population, yet the epidemiology of extracorporeal membrane oxygenation support in cardiac ICUs has not been described. We aimed to characterize extracorporeal membrane oxygenation utilization and outcomes across surgical and medical patients in pediatric cardiac ICUs. DESIGN: Retrospective analysis of the Pediatric Cardiac Critical Care Consortium registry to describe extracorporeal membrane oxygenation frequency and outcomes. Within strata of medical and surgical hospitalizations, we identified risk factors associated with extracorporeal membrane oxygenation use through multivariate logistic regression. SETTING: Tertiary-care children's hospitals. PATIENTS: Neonates through adults with cardiac disease. INTERVENTIONS: None. MEASUREMENTS AND MAIN RESULTS: There were 14,526 eligible hospitalizations from August 1, 2014, to June 30, 2016; 449 (3.1%) included at least one extracorporeal membrane oxygenation run. Extracorporeal membrane oxygenation was used in 329 surgical (3.5%) and 120 medical (2.4%) hospitalizations. Systemic circulatory failure and extracorporeal cardiopulmonary resuscitation were the most common extracorporeal membrane oxygenation indications. In the surgical group, risk factors associated with postoperative extracorporeal membrane oxygenation use included younger age, extracardiac anomalies, preoperative comorbidity, higher Society of Thoracic Surgeons-European Association for Cardiothoracic Surgery category, bypass time, postoperative mechanical ventilation, and arrhythmias (all p < 0.05). Bleeding requiring reoperation (25%) was the most common extracorporeal membrane oxygenation complication in the surgical group. In the medical group, risk factors associated with extracorporeal membrane oxygenation use included acute heart failure and higher Vasoactive Inotropic Score at cardiac ICU admission (both p < 0.0001). Stroke (15%) and renal failure (15%) were the most common extracorporeal membrane oxygenation complications in the medical group. Hospital mortality was 49% in the surgical group and 63% in the medical group; mortality rates for hospitalizations including extracorporeal cardiopulmonary resuscitation were 50% and 83%, respectively. CONCLUSIONS: This is the first multicenter study describing extracorporeal membrane oxygenation use and outcomes specific to the cardiac ICU and inclusive of surgical and medical cardiac disease. Mortality remains high, highlighting the importance of identifying levers to improve care. These data provide benchmarks for hospitals to assess their outcomes in extracorporeal membrane oxygenation patients and identify unique high-risk subgroups to target for quality initiatives.
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Oxigenación por Membrana Extracorpórea/estadística & datos numéricos , Cardiopatías/terapia , Unidades de Cuidado Intensivo Pediátrico/estadística & datos numéricos , Aceptación de la Atención de Salud/estadística & datos numéricos , Adolescente , Adulto , Niño , Preescolar , Oxigenación por Membrana Extracorpórea/efectos adversos , Femenino , Cardiopatías/mortalidad , Mortalidad Hospitalaria , Hospitalización/estadística & datos numéricos , Humanos , Lactante , Recién Nacido , Masculino , Sistema de Registros , Estudios Retrospectivos , Factores de Riesgo , Adulto JovenRESUMEN
BACKGROUND: Factors leading to cardiac intensive care unit (CICU) readmission and the impact on mortality have yet to be well delineated. We sought to define the prevalence and outcome for unscheduled CICU readmission. Secondary objectives were to identify indications and risk factors for unscheduled CICU readmission. METHODS: Retrospective analysis of prospectively collected registry data at a tertiary care children's hospital. Pediatric and adult patients with congenital and acquired heart disease who survived to initial CICU discharge were included. Patients with unexpected return to the CICU for acute change in clinical status were defined as unscheduled readmissions. RESULTS: Of the 645 discharges that met inclusion criteria, 37 resulted in unplanned readmission to the CICU. Patients requiring unscheduled readmission had higher mortality rates (16.2% vs 0.5%, P < .0001). Cardiac symptoms were the most common reason for readmission. On multivariate analysis, genetic anomaly (P = .001) and longer length of stay (LOS) during the index CICU admission (P = .01) were independently associated with readmission. For surgical patients, genetic anomaly (P = .001), single-ventricle anatomy (P = .05), and longer surgical support time (P < .001) were independently associated with readmission. CONCLUSION: Unscheduled readmission to the CICU within the same hospitalization was uncommon but associated with a higher mortality rate. Genetic anomaly and longer initial LOS were important risk factors for the entire cohort. Single-ventricle anatomy and longer intraoperative course were risk factors for surgical readmissions.
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Cardiopatías/terapia , Unidades de Cuidado Intensivo Pediátrico/estadística & datos numéricos , Readmisión del Paciente/estadística & datos numéricos , Sistema de Registros , Niño , Preescolar , Femenino , Cardiopatías/epidemiología , Humanos , Lactante , Tiempo de Internación/tendencias , Masculino , Alta del Paciente/tendencias , Prevalencia , Estudios Retrospectivos , Factores de Riesgo , Estados Unidos/epidemiologíaRESUMEN
Newborns with hypoplastic left heart syndrome and other single right ventricular variants require substantial health care resources. Weekend acute care has been associated with worse outcomes and increased resource use in other populations but has not been studied in patients with single ventricle. Subjects of the Single Ventricle Reconstruction trial were classified by whether they had a weekend admission and by day of the week of Norwood procedure. The primary outcome was hospital length of stay (LOS); secondary outcomes included transplant-free survival, intensive care unit (ICU) LOS, and days of mechanical ventilation. The Student's t test with log transformation and the Wilcoxon rank-sum test were used to analyze associations. Admission day was categorized for 533 of 549 subjects (13% weekend). The day of the Norwood was Thursday/Friday in 39%. There was no difference in median hospital LOS, transplant-free survival, ICU LOS, or days ventilated for weekend versus non-weekend admissions. Day of the Norwood procedure was not associated with a difference in hospital LOS, transplant-free survival, ICU LOS, or days ventilated. Prenatally diagnosed infants born on the weekend had lower mean birth weight, younger gestational age, and were more likely to be intubated but did not have a difference in measured outcomes. In conclusion, in this cohort of patients with single right ventricle, neither weekend admission nor end-of-the-week Norwood procedure was associated with increased use of hospital resources or poorer outcomes. We speculate that the complex postoperative course following the Norwood procedure outweighs any impact that day of admission or operation may have on these outcomes.
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Recursos en Salud/estadística & datos numéricos , Hospitalización , Síndrome del Corazón Izquierdo Hipoplásico/cirugía , Procedimientos de Norwood , Cuidados Paliativos , Estudios de Cohortes , Cuidados Críticos , Femenino , Trasplante de Corazón , Humanos , Síndrome del Corazón Izquierdo Hipoplásico/complicaciones , Síndrome del Corazón Izquierdo Hipoplásico/mortalidad , Lactante , Recién Nacido , Masculino , Respiración Artificial , Tasa de Supervivencia , Factores de Tiempo , Tiempo de Tratamiento , Resultado del TratamientoRESUMEN
OBJECTIVE: To determine whether blood levels of the brain-specific biomarker glial fibrillary acidic protein rise during cardiopulmonary bypass for repair of congenital heart disease. METHODS: This is a prospective observational pilot study to characterise the blood levels of glial fibrillary acidic protein during bypass. Children <21 years of age undergoing bypass for congenital heart disease at Johns Hopkins Hospital and Texas Children's Hospital were enrolled. Blood samples were collected during four phases: pre-bypass, cooling, re-warming, and post-bypass. RESULTS: A total of 85 patients were enrolled between October, 2010 and May, 2011. The median age was 0.73 years (range 0.01-17). The median weight was 7.14 kilograms (range 2.2-86.5). Single ventricle anatomy was present in 18 patients (22%). Median glial fibrillary acidic protein values by phase were: pre-bypass: 0 ng/ml (range 0-0.35); cooling: 0.039 (0-0.68); re-warming: 0.165 (0-2.29); and post-bypass: 0.112 (0-0.97). There were significant elevations from pre-bypass to all subsequent stages, with the greatest increase during re-warming (p = 0.0001). Maximal levels were significantly related to younger age (p = 0.03), bypass time (p = 0.03), cross-clamp time (p = 0.047), and temperature nadir (0.04). Peak levels did not vary significantly in those with single ventricle anatomy versus two ventricle repairs. CONCLUSION: There are significant increases in glial fibrillary acidic protein levels in children undergoing cardiopulmonary bypass for repair of congenital heart disease. The highest values were seen during the re-warming phase. Elevations are significantly associated with younger age, bypass and cross-clamp times, and temperature nadir. Owing to the fact that glial fibrillary acidic protein is the most brain-specific biomarker identified to date, it may act as a rapid diagnostic marker of brain injury during cardiac surgery.
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Puente Cardiopulmonar , Proteína Ácida Fibrilar de la Glía/sangre , Cardiopatías Congénitas/cirugía , Hipotermia Inducida , Recalentamiento , Adolescente , Biomarcadores/sangre , Procedimientos Quirúrgicos Cardíacos , Niño , Preescolar , Femenino , Cardiopatías Congénitas/sangre , Humanos , Lactante , Recién Nacido , Masculino , Tempo Operativo , Proyectos Piloto , Estudios ProspectivosRESUMEN
BACKGROUND: The amount of imaging studies performed for disease diagnosis has been rapidly increasing. We examined the amount of radiation exposure that pediatric trauma patients receive because they are an at-risk population. Our hypothesis was that pediatric trauma patients are exposed to high levels of radiation during a single hospital visit. METHODS: Retrospective review of children who presented to Johns Hopkins Pediatric Trauma Center from July 1, 2004, to June 30, 2005. Radiographic studies were recorded for each patient and doses were calculated to give a total effective dose of radiation. All radiographic studies that each child received during evaluation, including any associated hospital admission, were included. RESULTS: A total of 945 children were evaluated during the study year. A total of 719 children were included in the analysis. Mean age was 7.8 (±4.6) years. Four thousand six hundred three radiographic studies were performed; 1,457 were computed tomography (CT) studies (31.7%). Average radiation dose was 12.8 (±12) mSv. We found that while CT accounted for only 31.7% of the radiologic studies performed, it accounted for 91% of the total radiation dose. Mean dose for admitted children was 17.9 (±13.8) mSv. Mean dose for discharged children was 8.4 (±7.8) mSv (p<0.0001). Burn injuries had the lowest radiation dose [1.2 (±2.6) mSv], whereas motor vehicle collision victims had the highest dose [18.8 (±14.7) mSv]. CONCLUSION: When the use of radiologic imaging is considered essential, cumulative radiation exposure can be high. In young children with relatively long life spans, the benefit of each imaging study and the cumulative radiation dose should be weighed against the long-term risks of increased exposure.
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Dosis de Radiación , Heridas y Lesiones/diagnóstico por imagen , Accidentes de Tránsito/estadística & datos numéricos , Niño , Femenino , Humanos , Masculino , Admisión del Paciente , Alta del Paciente , Estudios Retrospectivos , Tomografía Computarizada por Rayos X , Centros Traumatológicos/estadística & datos numéricosRESUMEN
BACKGROUND: There are no guidelines and multiple devices available now for closure of PDA. OBJECTIVE: We sought to determine which devices are used and their outcomes. METHODS: Prospectively collected data on closure of PDA at 12 US catheterization labs was entered into the MAGIC data registry between November 2005 and September 2008. RESULTS: PDA closure was accomplished in 357 of 359 attempted closures during the study period. Mean age, weight, and minimum ductal diameter were 4.3 ± 6.8 years, 18.7 ± 18.4 kg, and 2.1 ± 1.4 mm, respectively. Devices used were Gianturco coils (161/359), Amplatzer Duct Occluder (ADO, 174/359), Flipper coils (18/359), and other devices (6/359). Gianturco coils had the least fluoroscopy and contrast exposure (8.7 ± 7.5 min, P = 0.00001, 2.6 ± 1.4 cm(3) kg(-1), P = 0.00001). Immediate angiographic success rates were 96.9% (156/161) for Gianturco coils, 89.7% (156/174) for the ADO, 100% (18/18) for Flipper coils, and 66.7% (4/6) for other devices. Major complication rates were 0.6% for Gianturco coils (1/161), 1.7% for ADO (3/174), and 83.3% for other devices (4/6). Minor complication rates by device were 1.9% for Gianturco coils (3/161), 2.3% for ADO (4/174), and 16.7% (1/6) for other devices. CONCLUSIONS: Gianturco coils, the ADO and Flipper coils were immediately successful with low complication profiles. The ADO and Gianturco coils were the predominate devices. The ADO was the device of choice for PDA > 3 mm with good success. In PDA < 3 mm, the Gianturco coil is as effective and safe as the ADO with less cost, less radiation, and less contrast exposure. © 2010 Wiley-Liss, Inc.