Abstract
Background:
Limited data exist regarding neurobehavioral outcomes of children treated with open-chest cardiopulmonary resuscitation (CPR). Our objective was to describe neurobehavioral outcomes one year post-arrest among children who received open-chest CPR during in-hospital cardiac arrest; and explore factors associated with one-year survival and survival with good neurobehavioral outcome.
Methods:
The study is a secondary analysis of the Therapeutic Hypothermia after Pediatric Cardiac Arrest In-Hospital Trial. Fifty-six children who received open-chest CPR for in-hospital cardiac arrest were included. Neurobehavioral status was assessed using the Vineland Adaptive Behavior Scales, Second Edition (VABS-II) at pre-arrest baseline and 12-months post-arrest. Norms for VABS-II are 100 (mean) ±15 (SD). Outcomes included 12-month survival, 12-month survival with VABS-II decreased by ≤15 points from baseline, and 12-month survival with VABS-II ≥70.
Results
Of 56 children receiving open-chest CPR, 49 (88%) were post-cardiac surgery and 43 (77%) were <1 year old. Forty-four (79%) were cannulated for ECMO during CPR or within 6 hours of return of spontaneous circulation. Thirty-three (59%) survived to 12 months, 22 (41%) survived to 12 months with VABS-II decreased by ≤15 points from baseline, and of those with baseline VABS-II ≥70, 23 (51%) survived to 12 months with VABS-II ≥70. On multivariable analyses, use of ECMO, renal replacement therapy and higher maximum international normalized ratio were independently associated with lower 12-month survival with VABS-II ≥70.
Conclusions:
Approximately half of children survived with good neurobehavioral outcome one year after open-chest CPR for in-hospital cardiac arrest. Use of ECMO and post-arrest renal or hepatic dysfunction may be associated with worse neurobehavioral outcomes.
The Society of Thoracic Surgeons (STS) Task Force on Resuscitation after Cardiac Surgery recommends early emergency resternotomy for children and adults who arrest after cardiac surgery and fail to achieve return of spontaneous circulation after immediate correction of readily reversible causes [1]. Specifically, STS experts recommend resternotomy within 5 minutes for ventricular fibrillation or pulseless ventricular tachycardia unresponsive to three sequential defibrillation attempts, asystole or severe bradycardia unresponsive to pacing, and pulseless electrical activity without a quickly reversible cause. Emergency resternotomy allows for the treatment of tamponade or hypovolemia caused by intrathoracic bleeding, both common causes of arrest after cardiac surgery. Emergency resternotomy also allows for the provision of direct cardiac compressions via the open chest. Animal studies suggest that open-chest cardiac compressions result in greater cardiac index and coronary perfusion pressure than closed-chest compressions although human data are sparse [2]. Additionally, use of open-chest cardiac compressions can potentially prevent complications observed with closed-chest compressions such as rupture of cardiac chambers, prosthetic valve dehiscence and vascular dissection [3]. Open-chest cardiopulmonary resuscitation (CPR) has also been used for traumatic cardiac arrest; however, recent studies found no significant improvement in outcomes compared to closed-chest CPR in the setting of blunt or penetrating trauma [4,5].
Limited data exist regarding long-term survival and neurological outcomes of patients, especially children, treated with open-chest CPR. The Therapeutic Hypothermia after Pediatric Cardiac Arrest In-Hospital (THAPCA-IH) trial was a randomized trial comparing the efficacy of therapeutic hypothermia with that of therapeutic normothermia on survival with good neurobehavioral outcome in children one year after in-hospital cardiac arrest [6]. Although no significant benefit on survival with good neurobehavioral outcome was observed with either temperature management intervention, the THAPCA-IH database can be used to explore outcomes of children exposed to other aspects of resuscitation or post-arrest care. Children recruited to the THAPCA-IH trial were comatose post-arrest and at high risk of neurologic disability. Neurobehavioral function was evaluated in the THAPCA-IH trial using the Vineland Adaptive Behavior Scales, Second Edition (VABS-II) at baseline (reflecting pre-arrest status) and one year post-arrest [7]. The objective of this study was to describe neurobehavioral outcomes one year post-arrest among children who received open-chest CPR and were recruited to the THAPCA-IH trial; and to explore factors associated with one-year survival and survival with good neurobehavioral outcome.
PATIENTS AND METHODS
Design and Setting
This study is a secondary analysis of the THAPCA-IH trial [6]. Thirty-seven children’s hospitals in the United States, Canada, and the United Kingdom recruited children between September 1, 2009 and February 27, 2015. Details of the THAPCA-IH trial were previously published [6,8]. Institutional Review Boards at each study site, the Kennedy Krieger Institute Outcome Assessment Center and the University of Utah Data Coordinating Center approved the study. Caregiver permission was obtained for all participants.
Participants
Inclusion criteria for the THAPCA-IH trial were age >48 hours and <18 years, occurrence of an in-hospital cardiac arrest with chest compressions for ≥2 minutes, need for mechanical ventilation after return of circulation, and a Glasgow Coma Scale motor score <5 [9]. A Glasgow Coma Scale motor score of 5 represents localizing pain or (if less than 2 years of age) withdrawing to touch. Additional inclusion criteria for this secondary analysis included receipt of open-chest CPR. Exclusion criteria for the THAPCA-IH trial included inability to be randomized within 6 hours of return of circulation, cardiac arrest due to trauma, and a decision to withhold aggressive treatment. A full list of exclusion criteria were previously published [6, 8]. Of 329 children randomized in the THAPCA-IH trial, 56 received open-chest CPR.
Independent Variables
Trained research coordinators collected data at the time of study entry by medical record review and direct interaction with caregivers and clinicians. Child characteristics included age, sex, body habitus, technology dependence, post-operative from cardiac surgery at the time of arrest, previous intensive care unit (ICU) admissions during the hospitalization, and pre-existing conditions. Body habitus was evaluated using body mass index-for-age (BMI-for-age) percentiles for children ≥2 years of age, and weight-for-length percentiles for children <2 years of age [10]. Children were considered obese if their BMI-for-age or weight-for-length was ≥95th percentile, and underweight if <5th percentile as recommended by the U.S. Centers for Disease Control and Prevention [10]. Technology dependence was defined as presence of a tracheostomy or percutaneous feeding tube prior to the cardiac arrest. Children categorized as post-operative cardiac surgery had a cardiac surgical procedure during the hospitalization in which the arrest occurred. Pre-existing conditions included cardiac, respiratory, neurologic, gastrointestinal, prenatal, pulmonary hypertension, renal, and other conditions. Pre-existing cardiac conditions were categorized as single ventricle or not.
Cardiac arrest characteristics included primary etiology of arrest, initial cardiac rhythm at the time chest compressions were started, duration of chest compressions, number of epinephrine doses administered during the arrest, epinephrine-dosing interval, whether cardiac defibrillation was attempted, location of arrest within the hospital, and presence of an intravenous catheter or endotracheal tube at the time of arrest. Primary etiology of arrest was categorized as cardiovascular or respiratory. Initial cardiac rhythm was categorized as asystole, bradycardia, pulseless electrical activity, ventricular tachycardia/fibrillation, or unknown. Epinephrine-dosing interval was defined as the duration of chest compressions divided by the total number of epinephrine doses administered during chest compressions. Location of arrest was categorized as ICU (including intermediate care), operating room, non-ICU inpatient ward, or other clinical area.
Post-arrest characteristics included the THAPCA-IH trial intervention (i.e., therapeutic hypothermia versus therapeutic normothermia), and use of extracorporeal membrane oxygenation (ECMO) at the time of initiation of the temperature management intervention (i.e., ECMO cannulation either during CPR or within 6 hours of return of spontaneous circulation). Post-arrest characteristics also included the presence of clinical or electrographic seizures and the use of renal replacement therapy from the time of randomization in the THAPCA-IH trial through day 5 of the trial, and the presence of serious arrhythmias, culture-positive infection, and the use of blood products from the time of randomization through day 7. Laboratory data included post-arrest arterial blood pH and lactate, and international normalized ratio (INR), total bilirubin and alanine aminotransferase (ALT). The minimum and maximum values for each of these in the time interval from 2 hours before to 48 hours after the start of the temperature management intervention were recorded.
Outcomes
Outcomes included 12-month survival, 12-month survival with VABS-II decreased by ≤15 points from baseline, and 12-month survival with VABS-II ≥70 [7]. The VABS-II is a caregiver report measure of adaptive behavior from birth to adulthood. Adaptive behavior is defined as performance on daily life activities necessary for personal and social independence. VABS-II domains include communication, daily living, socialization and motor skills. The number of tasks that can be performed in each domain is standardized for the child’s age. In normative U.S. populations, the mean VABS-II is 100, and the standard deviation is 15. Higher scores indicate better functioning. Caregivers completed baseline VABS-II assessments (reflecting pre-arrest status) at the local sites within 24 hours of randomization into the THAPCA-IH trial, and 12-month assessments by telephone with interviewers from the Kennedy Krieger Institute who were blinded to treatment group assignment. For the outcome of survival with VABS-II ≥70, only children with baseline VABS-II ≥70 (n=47) were considered.
Statistical Analyses
Cardiac arrest and post-arrest characteristics were summarized using frequencies and percentages. Univariate associations between these characteristics and the outcomes were examined using Fisher’s exact test or the Cochran-Armitage exact test for trend. Laboratory values were summarized as medians and quartiles. Univariate associations between laboratory values and outcomes were examined using Wilcoxon rank-sum tests. Logistic regression models were run for each outcome to estimate odds ratios and 95% confidence intervals. Two sets of models were generated. For the first set of models, only early variables (i.e., variables available up to the time of initiation of the THAPCA-IH temperature management intervention) were considered. For the second set of models, both early and late variables (i.e., variables available through day 7) were considered. Variables that had a univariate p-value <0.1 were entered into each model using a stepwise selection approach and only those with a p-value <0.05 were retained in the final models. All analyses were completed using SAS software v9.4 (Cary, NC).
RESULTS
Of 56 children receiving open-chest CPR, 34 (61%) were male, and 43 (77%) were <1 year old (Supplemental Table 1). Nine (16%) children were underweight and 7 (13%) were obese. Seven (13%) had pre-arrest technology dependence and 8 (14%) had a previous ICU admission during the hospitalization. Fifty-five (98%) had at least one pre-existing condition. Fifty-three (95%) had a pre-existing cardiac condition (17 with single ventricle), 18 (32%) prenatal condition, 12 (21%) gastrointestinal condition, 11 (20%) respiratory condition, 10 (18%) renal condition, 8 (14%) neurologic condition, 2 (4%) pulmonary hypertension, and 16 (29%) other condition.
Forty-nine (88%) children were post-operative from cardiac surgery at the time of open-chest CPR (Supplemental Table 2). Of the 7 (13%) who were not post-operative from cardiac surgery, three underwent primary sternotomy for central cannulation for ECMO. One received open-chest compressions during a cardiac operation, one during an operation for excision of an extra lobar sequestration, and one after an operation for congenital chylothorax complicated by severe bleeding. One additional child received open-chest CPR through a resternotomy after remote cardiac surgery (i.e., cardiac surgery during a prior hospitalization) and pacemaker placement.
Primary etiology of arrest was deemed a cardiovascular event for 49 (88%) children and a respiratory event for 7 (13%) (Supplemental Table 2). Initial cardiac rhythm at the time chest compressions were started was bradycardia for 30 (54%), pulseless electrical activity for 16 (29%), ventricular tachycardia/fibrillation for 6 (11%) and asystole for 3 (5%). Sixteen (29%) had at least one defibrillation attempt. Thirty-one (55%) received chest compressions for >30 minutes; for all children, the median duration of chest compressions was 32.5 minutes (IQR 16.8, 46.0 minutes). The number of epinephrine doses was >8 for 16 (29%) and the epinephrine dosing interval was ≥5 minutes for 32 (57%). Fifty-five (98%) had intravenous access at the time of arrest, and 45 (80%) were intubated. Cardiac arrest occurred in the ICU for 43 (77%), the operating room for 10 (18%) and a non-ICU inpatient ward for 3 (5%).
Twenty-five (45%) children were managed post-arrest with therapeutic hypothermia and 31 (55%) with therapeutic normothermia (Supplemental Table 2). Forty-four (79%) were receiving ECMO at the time of initiation of the temperature management intervention (i.e., ECMO cannulation either during CPR or within 6 hours of return of spontaneous circulation). Renal replacement therapy was used in 17 (30%) children and clinical or electrographic seizures were documented in 7 (13%) between the time of randomization in the THAPCA-IH trial through day 5. Fifty-four (96%) received blood products between the time of randomization through day 7. Of these, 52 (96%) received red blood cells, 49 (91%) platelets, 35 (65%) fresh frozen plasma and 29 (54%) cryoprecipitate. Fourteen (25%) had a culture-positive infection. Of these 9 (64%) had respiratory infection, 4 (29%) urinary tract infection, and one (7%) bloodstream infection. Nine (16%) had a serious arrhythmia. Lactate declined to <2 mmol/L in 42 (75%) within 48 hours of the start of the temperature management intervention. Thirty-three (59%) children survived to 12 months, 22 (41%) survived to 12 months with VABS-II decreased by ≤15 points from baseline, and of those with baseline VABS-II ≥70, 23 (51%) survived to 12 months with VABS-II ≥70. A Kaplan-Meier survival graph for all 56 children is shown in Figure 1.
Figure 1.
Kaplan-Meier Estimates of Survival to One Year after Cardiac Arrest.
Univariate Associations
Presence of a pre-existing renal condition was associated with lower 12-month survival (Supplemental Table 1). Epinephrine dosing interval of 3 to 5 minutes was associated with greater 12-month survival and failure of lactate to decline to <2 mmol/L within 48 hours of the start of the temperature management intervention was associated with lower 12-month survival (Supplemental Table 2). Use of ECMO and the presence of clinical or electrographic seizures were associated with lower 12-month survival with VABS-II ≥70. Use of renal replacement therapy was associated with lower 12-month survival, lower 12-month survival with VABS-II decreased ≤15 points from baseline, and lower 12-month survival with VABS-II ≥70. Univariate associations between laboratory values and outcomes are shown in Supplemental Table 3.
Logistic Regression Models
Logistic regression models including early variables (i.e., variables available up to the time of initiation of the temperature management intervention) are shown in Supplemental Table 4. Presence of a pre-existing renal condition was independently associated with lower 12-month survival. Use of ECMO was independently associated with lower 12-month survival with VABS-II ≥70.
Logistic regression models including early and late variables (i.e., variables available through day 7) are shown in Supplemental Table 5. Higher minimum bilirubin was independently associated with lower 12-month survival. When bilirubin was excluded from the model of 12-month survival, higher minimum INR was independently associated with lower 12-month survival. Higher minimum INR was independently associated with lower 12-month survival with VABS-II decreased by ≤15 points from baseline. Higher maximum INR and use of renal replacement therapy were independently associated with lower 12-month survival with VABS-II ≥70.
COMMENT
To our knowledge, this is the first report of one-year neurobehavioral outcomes in a cohort of children who received open-chest CPR during in-hospital cardiac arrest. Our findings demonstrate that about half of children who received open-chest CPR survived with good neurobehavioral outcome at one year. Most of the children in our study were post-operative from cardiac surgery at the time of open-chest CPR and cannulated for ECMO either during CPR or within 6 hours of return of spontaneous circulation. It is important to acknowledge that the children included in our study were recruited to the THAPCA-IH trial and as such were comatose post-arrest. Therefore, children included in our study were likely at greater risk of neurologic disability compared to other children experiencing in-hospital arrest and open-chest CPR. Children participating in randomized controlled trials may also differ from children whose caregivers refuse participation in ways that are unknown.
We performed exploratory logistic regression analyses using early variables to identify those most strongly associated with outcomes. These analyses demonstrated that pre-existing renal failure was independently associated with lower 12-month survival, and that the peri-resuscitation use of ECMO was independently associated with lower 12-month survival with VABS-II ≥70. Several studies have shown an association between pre-existing renal failure and mortality after in-hospital cardiac arrest [11–16]. A recent analysis of the Virtual Pediatric Systems (VPS, LLC) Database between 2009 and 2014 found that among children undergoing cardiac surgery (n=26,909), pre-existing renal failure was one of several factors associated with increased risk of post-operative cardiac arrest [12]. Among those with post-operative cardiac arrest, pre-existing renal failure and use of post-operative ECMO were associated with increased mortality at ICU discharge [12]. Acid-base and electrolyte abnormalities are common during and after cardiac arrest. Pre-existing renal failure may increase the severity of these derangements and make them difficult to treat potentially contributing to worse outcomes. The peri-resuscitation use of ECMO in our study represents ECMO cannulation during open-chest CPR or within 6 hours of return of spontaneous circulation. Children who require ECMO during or after CPR are likely to have persistent cardiogenic shock until the time of ECMO initiation; thus, those requiring ECMO may be more severely ill than children who do not require ECMO. Greater severity of illness may potentially explain the relationship between the use of peri-resuscitation ECMO and lower survival with good neurobehavioral outcome at one year.
We also performed exploratory logistic regression analyses using both early and late variables. Higher minimum bilirubin was independently associated with lower 12-month survival; when bilirubin was excluded from the analysis, higher minimum INR was associated with lower 12-month survival. Higher minimum INR was also independently associated with lower 12-month survival with VABS-II decreased by ≤15 points from baseline. Higher maximum INR and use of renal replacement therapy were independently associated with lower 12-month survival with VABS-II ≥70. These findings suggest that post-arrest hepatic or renal dysfunction may contribute to reduced one-year survival with good neurobehavioral outcome. These findings are consistent with prior reports demonstrating an association between end-organ injury after extracorporeal CPR (ECPR) and worse outcomes at hospital discharge [17–20].
Some important variables not associated with outcomes in our study include the presence of single ventricle lesions, duration of cardiac compressions, and occurrence of post-arrest infection. Although outcomes of children with single ventricle lesions receiving open-chest CPR have not been explicitly reported, studies of the use of ECPR (open- and closed-chest) have suggested higher mortality at hospital discharge for children with single ventricle compared to biventricular lesions [18, 21–23]. Significant late attrition following ECPR has also been reported for children with single ventricle lesions [24]. Longer duration of CPR is a known predictor of outcomes following in-hospital cardiac arrest [11,25,26]. However, conflicting findings exist in the setting of ECPR [20,22,24,27]. Similar to our findings, prior reports that failed to identify CPR duration as a predictor of outcome often had long median durations of CPR (e.g., >30 minutes). A recent study found post-arrest infection in 56% of children with in-hospital cardiac arrest and return of spontaneous circulation; 82% of infected children had a positive culture [28]. Similar to our findings, respiratory infections were most common and no association with mortality was identified. Difficulty interpreting the significance of positive respiratory cultures in intubated children may confound associations with outcomes [29]. Data regarding wound or mediastinal infections were not collected in the THAPCA-IH trial.
Strengths of our study include the multicenter design, prospective data collection and use of the VABS-II to measure neurobehavioral outcomes one year after open-chest CPR for in-hospital cardiac arrest. Limitations include the potential bias inherent in including children recruited to a randomized controlled trial; specifically, all children recruited to the THAPCA-IH trial were comatose post-arrest with high risk of neurologic disability. Of 56 children receiving open-chest CPR, only 33 survived 12 months limiting the number of neurobehavioral assessments performed. Other limitations include the large number of variables evaluated, as well as lack of data on some potentially important variables. For example, most children receiving open-chest CPR were post-operative from cardiac surgery and received peri-resuscitation ECMO; however, data regarding cardiac diagnoses, surgical complexity, and details of ECMO cannulation and management were not available in the THAPCA-IH database. Some children may have received closed-chest CPR prior to open-chest CPR during the cardiac arrest event; the proportion of time spent undergoing closed- and open-chest compressions for these children is unknown. The number of children whose sternum was open prior to arrest while waiting for delayed sternal closure is also unknown. Data regarding the occurrence of central nervous system stroke was not available. Importantly, although several associations were observed, causation cannot be inferred. Our findings can be useful to help guide clinical decision making and in counseling parents. For example, the finding that about half of children survived with good neurobehavioral outcome after open-chest CPR could be shared with parents when discussing prognosis. Similarly, clinicians and parents could consider the identified risk factors for worse outcomes when discussing options for care.
Supplementary Material
Footnotes
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