Original Article
Whole-Body Hypothermia for Neonates with Hypoxic–Ischemic Encephalopathy
N Engl J Med 2005; 353:1574-1584October 13, 2005
- Abstract
Background
Hypothermia is protective against brain injury after asphyxiation in animal models. However, the safety and effectiveness of hypothermia in term infants with encephalopathy is uncertain.
Methods
We conducted a randomized trial of hypothermia in infants with a gestational age of at least 36 weeks who were admitted to the hospital at or before six hours of age with either severe acidosis or perinatal complications and resuscitation at birth and who had moderate or severe encephalopathy. Infants were randomly assigned to usual care (control group) or whole-body cooling to an esophageal temperature of 33.5°C for 72 hours, followed by slow rewarming (hypothermia group). Neurodevelopmental outcome was assessed at 18 to 22 months of age. The primary outcome was a combined end point of death or moderate or severe disability.
Results
Of 239 eligible infants, 102 were assigned to the hypothermia group and 106 to the control group. Adverse events were similar in the two groups during the 72 hours of cooling. Primary outcome data were available for 205 infants. Death or moderate or severe disability occurred in 45 of 102 infants (44 percent) in the hypothermia group and 64 of 103 infants (62 percent) in the control group (risk ratio, 0.72; 95 percent confidence interval, 0.54 to 0.95; P=0.01). Twenty-four infants (24 percent) in the hypothermia group and 38 (37 percent) in the control group died (risk ratio, 0.68; 95 percent confidence interval, 0.44 to 1.05; P=0.08). There was no increase in major disability among survivors; the rate of cerebral palsy was 15 of 77 (19 percent) in the hypothermia group as compared with 19 of 64 (30 percent) in the control group (risk ratio, 0.68; 95 percent confidence interval, 0.38 to 1.22; P=0.20).
Conclusions
Whole-body hypothermia reduces the risk of death or disability in infants with moderate or severe hypoxic–ischemic encephalopathy.
Media in This Article
Figure 1
Mean Esophageal (Panel A) and Abdominal-Wall Skin (Panel B) Temperatures and Heart Rate (Panel C) during the 72-Hour Intervention Period.Figure 2
Kaplan–Meier Estimates of Survival.Article Activity
- Article
Among term infants, hypoxic–ischemic encephalopathy due to acute perinatal asphyxia remains an important cause of neurodevelopmental deficits in childhood. Infants with moderate encephalopathy have a 10 percent risk of death, and those who survive have a 30 percent risk of disabilities. Sixty percent of infants with severe encephalopathy die, and many, if not all, survivors are handicapped.1,2 Treatment is currently limited to supportive intensive care.
Reductions in brain temperature by 2°C to 5°C provide neuroprotection in newborn and adult animal models of brain ischemia.3-10 Brain cooling has a favorable effect on multiple pathways contributing to brain injury, including excitatory amino acids,11 the cerebral energy state,12 cerebral blood flow and metabolism,13 nitric oxide production,11 and apoptosis.14 Brain cooling is effective in reducing the extent of brain injury even when it is initiated up to 5.5 hours after brain ischemia in near-term sheep fetuses.10 We have previously demonstrated the feasibility of whole-body cooling in a pilot study of neonates with hypoxic–ischemic encephalopathy.15 Therefore, we conducted a randomized, controlled trial to evaluate whether whole-body cooling initiated before 6 hours of age and continued for 72 hours in term infants with encephalopathy would reduce death or disability at 18 to 22 months of age as compared with infants given usual care.
Methods
A committee of the principal investigators from participating sites developed a manual of operations that specified neurologic criteria for eligibility and details of the cooling and rewarming procedure. Each principal investigator certified additional neonatologists to perform the neurologic examination, and a training session for research personnel was held to standardize all study procedures. The protocol was approved by the institutional review board at each site.
Screening
Infants were screened for eligibility if they had a gestational age of at least 36 weeks and were admitted to the neonatal intensive care unit at six hours of age or less with either poor respiratory effort at birth and a need for resuscitation or a diagnosis of encephalopathy.
Inclusion Criteria
Infants were evaluated according to physiological criteria and subsequently by a neurologic examination.15 Eligibility criteria included a pH of 7.0 or less or a base deficit of 16 mmol per liter or more in a sample of umbilical-cord blood or any blood during the first hour after birth. If, during this interval, a pH was between 7.01 and 7.15, a base deficit was between 10 and 15.9 mmol per liter, or a blood gas was not available, additional criteria were required. These included an acute perinatal event (e.g., late or variable decelerations, cord prolapse, cord rupture, uterine rupture, maternal trauma, hemorrhage, or cardiorespiratory arrest) and either a 10-minute Apgar score of 5 or less or assisted ventilation initiated at birth and continued for at least 10 minutes.
Once these criteria were met, all infants underwent a standardized neurologic examination performed by a certified examiner. Infants were candidates for the study when encephalopathy or seizures were present. Encephalopathy was defined as the presence of one or more signs in at least three of the following six categories (Table 1Table 1
Criteria for Defining Moderate and Severe Encephalopathy.): level of consciousness, spontaneous activity, posture, tone, primitive reflexes (suck or Moro), and autonomic nervous system (pupils, heart rate, or respiration). The number of moderate or severe signs determined the extent of encephalopathy; if signs were equally distributed, the designation was based on the level of consciousness. Exclusion criteria were an inability to enroll by six hours of age, a major congenital abnormality, a severe growth restriction (birth weight of ≤1800 g), and refusal of consent by a parent or an attending neonatologist; moribund infants for whom no further aggressive treatment was planned also were excluded.Treatment Assignment
Written informed consent was obtained from the parents of 208 of 239 eligible infants. Consent was not requested from 16 mothers, parents refused consent for 10 infants, and physicians opposed the enrollment of 5 infants. After informed consent was obtained from a parent, the assignment to a treatment group was performed randomly by telephone by the data-coordinating center (RTI International). Assignments were stratified according to center and were generated by a random, permuted-block algorithm with block sizes of two and four.
Infants in the hypothermia group were placed on an infant-size blanket, 25 in. by 33 in. (64 cm by 84 cm), that was precooled to 5°C (Blanketrol II Hyper-Hypothermia System, Cincinnati Sub-Zero). Blankets and cooling systems were purchased by each site. An esophageal probe was inserted, and the esophageal temperature was lowered to 33.5°C by the blanket's servomechanism. A second blanket, 25 in. by 64 in. (64 cm by 163 cm), was attached to the cooling system. Water circulated simultaneously through both blankets to diminish the variability in the esophageal temperature.15 Neither an overhead warmer nor any other heat source was used during the cooling period. Abdominal-wall skin temperature was monitored with a skin probe by means of either the radiant warmer (with the heater turned off) or the temperature-monitoring unit (Mon-a-therm, Mallinckrodt Medical). Esophageal and skin temperatures were monitored continuously and recorded every 15 minutes for the first 4 hours, every hour for the next 8 hours, and every 4 hours during the remaining period of cooling.
After 72 hours of hypothermia, the set point of the automatic control on the cooling system was increased by 0.5°C per hour. After six hours, the esophageal probe was removed, and skin temperature was controlled by the radiant warmer's servomechanism. The temperature of the warmer was set 0.5°C higher than the skin temperature and was increased 0.5°C every hour until the set point of the warmer reached 36.5°C. Infants received routine clinical care, including the monitoring of vital signs and surveillance for organ dysfunction. Blood-gas measurements in the hypothermia group were corrected for body temperature.
Infants in the control group were cared for on overhead radiant warmers with abdominal-wall skin and esophageal temperatures recorded every four hours. Skin temperature was maintained by the servomechanism between 36.5°C and 37.0°C initially, and subsequent adjustments were made according to usual care at each center. Infants in the control group received the same monitoring of vital signs and surveillance for organ dysfunction as did the infants in the hypothermia group.
Adverse Events
During the 72-hour intervention period, infants in both groups were monitored for cardiac arrhythmia, persistent acidosis, major-vessel thrombosis or bleeding, skin changes, and death. Any equipment malfunction also was noted. All adverse events were reported within 72 hours to the institutional review board at the site and to the data center.
Follow-up
The primary outcome was death or disability (moderate or severe). All surviving infants were evaluated at 18 to 22 months of age; the families of those who did not return for follow-up were contacted by telephone to obtain information about the primary outcome. Data on growth, vision, and audiometric characteristics were obtained, and neurologic and developmental testing were performed by trained examiners who were blinded to intervention status. An assessment of neuromotor disability was based on the presence of cerebral palsy, and functional disability was graded according to the Gross Motor Function Classification System (GMFCS)16 (level 1 includes children who walk independently with some gait abnormalities; level 2 includes those who are unable to walk but who can sit, pull to standing, and cruise [take steps holding on to furniture]; level 3 includes those who are unable to walk or crawl, use hands for sitting support; level 4 includes those for whom support is needed for sitting; and level 5 includes those who require adult assistance to move). Cognitive outcome was assessed with the use of the Bayley Scales of Infant Development II,17 where a mean (±SD) score of 100±15 was normal on the Mental Development Index and Psychomotor Developmental Index. Severe disability was defined as any of the following: a Bayley Mental Development Index score more than 2 SD below the mean score (i.e., below 70), a GMFCS grade of level 3 to 5, hearing impairment requiring hearing aids, or blindness. Moderate disability was defined as a Mental Development Index score 1 to 2 SD below the mean score (i.e., 70 to 84) in addition to one or more of the following: a GMFCS grade of level 2, hearing impairment with no amplification, or a persistent seizure disorder.
Statistical Analysis
A requirement for a sample size of 104 infants in each group was based on a two-tailed type 1 error rate of 0.05, a statistical power of 80 percent, a 10 percent loss to follow-up, and an incidence of death or disability in the control group of 50 percent and a reduction to 30 percent in the intervention group. All data analyses were performed according to the intention-to-treat principle. The data were analyzed for treatment group differences with chi-square or Fisher's exact tests for the categorical variables and with t-tests for the continuous variables. The data for the primary and secondary outcomes were analyzed by the Mantel–Haenszel test, with adjustment according to center. An external data and safety monitoring committee monitored safety and efficacy during three interim analyses. All reported P values are two-sided and not adjusted for multiple comparisons.
Results
The 15 participating centers of the National Institute of Child Health and Human Development Neonatal Research Network recruited subjects between July 2000 and May 2003. Of 798 infants who were screened, 239 were eligible and 208 were enrolled (102 in the hypothermia group and 106 in the control group). Baseline characteristics were similar in the two groups (Table 2Table 2
Maternal and Neonatal Characteristics.). Cooling was initiated in the hypothermia group at a median of 35.5 minutes after randomization and at an average of 302 minutes after birth.Monitoring of Infants
The mean esophageal temperature at baseline was 36.6±1.0°C among the infants in the hypothermia group (Figure 1AFigure 1
Mean Esophageal (Panel A) and Abdominal-Wall Skin (Panel B) Temperatures and Heart Rate (Panel C) during the 72-Hour Intervention Period.). After an initial overshoot to a mean of 32.7°C, the target temperature of 33.5°C was achieved within 90 minutes and remained constant throughout the intervention period (mean, 33.4±0.9°C; 25th and 75th percentiles, 33.2°C and 33.5°C). In the control group, the mean esophageal temperature was 37.2±0.6°C during the same interval (25th and 75th percentiles, 36.9°C and 37.5°C). Esophageal temperatures in the control group exceeded 38°C on at least one measurement in 41 infants. The mean skin temperature was 31.9±1.4°C in the hypothermia group and 36.5±0.8°C in the control group during the intervention period (Figure 1B). The mean heart rate was similar in the two groups before the intervention. It decreased in the hypothermia group during cooling to a mean of 109 beats per minute but remained greater than 140 beats per minute in the control group (Figure 1C). Blood pressure was similar in the two groups (data not shown).Adverse Events and Follow-up
The incidence of serious adverse events was similar in the hypothermia and control groups (Table 3Table 3
Hospital Course and Status at Discharge.). The median age at follow-up was 19.8 months in the hypothermia group (follow-up rate, 100.0 percent) and 20.2 months in the control group (follow-up rate, 95.6 percent). The follow-up visits for the study ended in December 2004.Primary Outcome
Primary outcome data were available for 205 of the 208 enrolled infants. Three infants in the control group were lost to follow-up. Death or moderate or severe disability occurred in 45 of 102 infants (44 percent) in the hypothermia group and 64 of 103 infants (62 percent) in the control group (relative risk after adjustment according to center, 0.72; 95 percent confidence interval, 0.54 to 0.95; number needed to treat, 6) (Table 4Table 4
Outcome at 18 to 22 Months of Age.). The protective effect of hypothermia persisted after adjustment according to center and the severity of encephalopathy at randomization (relative risk, 0.76; 95 percent confidence interval, 0.60 to 0.97). A test of homogeneity of risk ratios across the centers revealed no significant interaction among treatments according to center (P=0.25). There was also no significant interaction between treatment and the severity of encephalopathy at enrollment (P=0.36). Results stratified according to the initial severity of encephalopathy (moderate or severe) are shown in Table 4.There were 24 deaths in the hypothermia group and 38 deaths in the control group (relative risk, 0.68; 95 percent confidence interval, 0.44 to 1.05) (Table 4). In the hypothermia and control groups, respectively, the rates of disabling cerebral palsy were 19 and 30 percent, the rates of blindness were 7 and 14 percent, and the rates of hearing impairment requiring aids were 4 and 6 percent (the P values for all comparisons were not significant). The proportion of infants with scores of 85 or more, 70 to 84, or below 70 on either the Mental Development Index or the Psychomotor Developmental Index also did not differ significantly between the groups.
The distribution of age at death according to treatment group is shown in Figure 2Figure 2
Kaplan–Meier Estimates of Survival.. Support was withdrawn from 12 infants in the hypothermia group (9 during the 72-hour intervention and 3 later during hospitalization) and 27 in the control group (10 during the intervention period, 15 later during hospitalization, and 2 after the initial hospitalization). The most frequent diagnosis for which support was withdrawn was asphyxial brain injury (8 of 12 infants in the hypothermia group and 18 of 27 in the control group).Discussion
As compared with usual care, whole-body cooling to an esophageal temperature of 33.5°C initiated within the first 6 hours after birth and continued for 72 hours reduced the rate of death or moderate or severe disability in term newborns with encephalopathy in this study. Hypothermia has been widely studied as a neuroprotective strategy in newborn and adult animals after ischemia and hypoxia–ischemia. In perinatal animals (sheep, rats, and piglets7-10,18,19), hypothermia has been beneficial when implemented up to 5.5 hours after brain ischemia.10
The eligibility criteria for this trial were designed to include infants with acute hypoxic–ischemic encephalopathy as indicated by profound fetal acidemia or infants with the need for resuscitation after acute hypoxic events. The trial was also designed to select infants who had a high probability of a poor outcome (i.e., death or disability). In the control group, the incidence of death or disability was 48 percent in the subgroup of infants with moderate encephalopathy at enrollment and 85 percent in the subgroup of infants with severe encephalopathy. In this study, the classification of encephalopathy as moderate or severe during the first hours after birth predicted outcome as readily as assessments later in the first week.1,2
The brain can be cooled by cooling the body, cooling the head selectively, or cooling the head and body together. The majority of studies in animals have used whole-body cooling,3-8,11-14,18,19 but some have used selective head cooling.9,10,20-24 Whole-body cooling provides homogeneous cooling to all brain structures, including peripheral and central brain regions.25 Selective head cooling provides greater cooling to the periphery of the brain than to the central brain structures25; head cooling combined with some body cooling minimizes temperature gradients across the brain and facilitates the cooling of central regions.24 Given the propensity for hypoxic–ischemic injury to affect deep-brain structures such as the thalamus, internal capsule, and basal ganglia in the human neonate,26-28 we chose whole-body cooling to achieve a consistent reduction in brain temperature in such structures. The target temperature of 33.5°C was selected on the basis of studies in animals3 that showed attenuation of brain injury at this temperature without the adverse effects (e.g., myocardial injury) that occur at lower temperatures.29
The cooling system used in this study was easily initiated, achieved the target temperature rapidly, and required minimal effort by providers to monitor the temperature. These features are important, given that the intervention was initiated within a defined time interval and maintained for 72 hours. Cooling was well tolerated and not associated with an increase in death or serious adverse events.
If esophageal temperature is a proxy for the core temperature of the brain, the observation that more than one third of the infants in the control group had an elevated esophageal temperature on at least one occasion suggests that brain temperatures may have risen intermittently in these infants. This study cannot establish a causal relationship between an elevated esophageal temperature and brain injury. An elevated brain temperature may result from brain injury, and conversely, a moderate increase in brain temperature can exacerbate hypoxic–ischemic brain injury.30,31
A concern with any therapy that reduces mortality among infants at high risk of death and disability is the possibility of an increase in the number of infants who survive with disabilities. In our study, there was no evidence of increased rates of moderate or severe disability at 18 to 22 months of age among infants treated with hypothermia. The rates of disabling cerebral palsy were 19 percent in the hypothermia group and 30 percent in the control group, and the rates of a Mental Development Index below 70 were 25 percent and 39 percent, respectively.
Recently, the results of a large, randomized, controlled trial of selective head cooling with systemic hypothermia (rectal temperature, 34°C to 35°C for 72 hours) (the Cool-Cap Trial)32 and a pilot trial of body cooling (rectal temperature, 33°C for 48 hours)33 have been published. The Cool-Cap Trial demonstrated a benefit associated with selective head cooling among infants with moderate abnormalities on an amplitude-integrated electroencephalogram (aEEG) at enrollment,32 whereas the pilot trial of body cooling showed protection among all infants studied.33 The eligibility criteria in our study did not make use of the aEEG, although data are accumulating to support the possibility that aEEG results predict outcomes after perinatal hypoxia–ischemia.34,35 The criteria we used for eligibility are assessed easily by clinicians and do not require the availability of aEEG equipment.
In summary, our findings demonstrate the safety and effectiveness of whole-body cooling in reducing the risk of death or disability among infants with moderate or severe encephalopathy. Rigorous criteria were used to define moderate and severe encephalopathy, and we used certified examiners and trained personnel to implement and monitor the study interventions and outcome.
Supported by grants from the National Institute of Child Health and Human Development and the Department of Health and Human Services (U10 HD21385, U10 HD40689, U10 HD27871, U10 HD21373, U01 HD36790, U10 HD40498, U10 HD40461, U10 HD34216, U10 HD21397, U10 HD27904, U10 HD40492, U10 HD27856, U10 HD40521, U10 HD27853, U10 HD27880, and U10 HD27851) and from the National Institutes of Health (GCRC M01 RR 08084, M01 RR 00125, M01 RR 00750, M01 RR 00070, M01 RR 0039-43, M01 RR 00039, and 5 M01 RR00044).
Dr. Cotten reports having served on the data and safety monitoring board for the Inhibitex phase 3 study of Vernonate for the prevention of infections in preterm infants. Dr. Donovan reports having received support from the Environmental Protection Agency (Lanphear) and the Gerber Foundation. Dr. Carlo reports having served on the advisory board of Pediatrix Medical Group and ParadigmHealth and holding stock options at the Pediatrix Medical Group. Dr. Stevenson reports having received research support from Pfizer. Dr. Seetha Shankaran reports having served on the advisory board of ParadigmHealth.
Source Information
From the Division of Neonatal–Perinatal Medicine, Wayne State University, Detroit (S.S.); Women's and Infant's Hospital, Providence, R.I. (A.R.L., W.O.); Yale University School of Medicine, New Haven, Conn. (R.A.E.); University of Texas at Houston, Houston (J.E.T.); Research Triangle Institute, Research Triangle Park, N.C. (S.A.M., W.K.P.); College of Medicine, University of Cincinnati, Cincinnati (E.F.D., A.H.J.); Rainbow Babies and Children's Hospital, Case Western University, Cleveland (A.A.F.); National Institute of Child Health and Human Development, Bethesda, Md. (L.L.W., R.D.H.); University of California at San Diego, San Diego (N.N.F.); University of Alabama, Birmingham (W.A.C.); Department of Pediatrics, University of Miami, Miami (S.D.); Duke University Medical Center, Durham, N.C. (C.M.C.); Stanford University School of Medicine, Palo Alto, Calif. (D.K.S.); Emory University School of Medicine, Atlanta (B.J.S.); Indiana University School of Medicine, Indianapolis (J.A.L.); and the University of Rochester, Rochester, N.Y. (R.G.).
Address reprint requests to Dr. Shankaran at the Division of Neonatal–Perinatal Medicine, Wayne State University, Children's Hospital of Michigan, 3901 Beaubien Blvd., Rm. 4H46, Detroit, MI 48201, or at sshankar@med.wayne.edu.
Members of the National Institute of Child Health and Human Development (NICHD) Neonatal Research Network are listed in the Appendix.
Appendix
Members of the National Institute of Child Health and Human Development (NICHD) Neonatal Research Network are as follows: The Hypothermia Study Group — Case Western Reserve University, Rainbow Children's Hospital: A.A. Fanaroff, M.C. Walsh, N. Newman, D. Wilson-Costello, B. Siner; Brown University, Women & Infant's Hospital: W. Oh, A. Hensman, B. Vohr, L. Noel; Duke University: C.M. Cotten, K. Auten, R. Goldstein, M. Lohmeyer; Emory University, Grady Memorial Hospital, and Crawford Long Hospital:B.J. Stoll, L. Jain, E. Hale; Indiana University, Riley Hospital for Children, and Methodist Hospital: J.A. Lemons, D.D. Appel, L. Miller, A. Dusick, L. Richard; Stanford University: D.K. Stevenson, K. Van Meurs, M.B. Ball, S.R. Hintz; University of Alabama at Birmingham, University Hospital: W.A. Carlo, M. Collins, S. Cosby, M. Peralta-Carcelen, V. Phillips; University of Cincinnati, The University Hospital, and Cincinnati Children's Hospital Medical Center: E.F. Donovan, C. Grisby, B. Alexander, J. Shively, H. Mincey, J. Steichen, T. Gratton; University of California–San Diego, UCSD Medical Center, and Sharp Mary Birch Hospital for Women: N.N. Finer, D. Kaegi, C. Henderson, W. Rich, K. Arnell, Y.E. Vaucher, M. Fuller; University of Miami: S. Duara, R. Everett, C.R. Bauer; University of Rochester, Golisano Children's Hospital at Strong: R. Guillet, L. Reubens, G. Myers, D. Hust; University of Texas Southwestern Medical Center at Dallas, Parkland Hospital: A.R. Laptook, S. Madison, G. Hensley, N. Miller, R. Heyne, S. Broyles, J. Hickman; University of Texas–Houston, Memorial Hermann Children's Hospital: J.E. Tyson, G. McDavid, E.G. Akpa, C.Y. Franco, P.A. Cluff, A.E. Lis, B.H. Morris, P.J. Bradt; Wayne State University, Hutzel Women's Hospital, and Children's Hospital of Michigan: S. Shankaran, R. Bara, G. Muran, Y. Johnson, D. Kennedy; Yale University, New Haven Children's Hospital: R.A. Ehrenkranz, P. Gettner, E. Romano; NICHD Neonatal Research Steering Committee — Brown University: W. Oh; Case Western University: A.A. Fanaroff; Duke University: R.N. Goldberg; Emory University: B.J. Stoll; Indiana University: J.A. Lemons; Stanford University: D.K. Stevenson; University of Alabama at Birmingham: W.A. Carlo; University of Cincinnati: E.F. Donovan; University of California–San Diego: N.N. Finer; University of Miami: S. Duara; University of Rochester: D.L. Phelps; University of Texas–Dallas: A.R. Laptook; University of Texas–Houston: J.E. Tyson; Wake Forest University: T.M. O'Shea; Wayne State University: S. Shankaran; Yale University: R.A. Ehrenkranz; University of Cincinnati: A. Jobe, Chair; Data Coordinating Center — RTI International: W.K. Poole, B. Hastings, C.M. Petrie; NICHD — R.D. Higgins, L.L. Wright, E. McClure; Data and Safety Monitoring Committee — Children's National Medical Center: G. Avery; Columbia University: M. D'Alton; RTI International: W.K. Poole (ex officio); University of Virginia: J.C. Fletcher (deceased); University of Washington: C.A. Gleason; University of Pittsburgh: C. Redmond.
- References
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Emily W.Y. Tam, Laurel A. Haeusslein, Sonia L. Bonifacio, Hannah C. Glass, Elizabeth E. Rogers, Rita J. Jeremy, A. James Barkovich, Donna M. Ferriero. (2012) Hypoglycemia is Associated with Increased Risk for Brain Injury and Adverse Neurodevelopmental Outcome in Neonates at Risk for Encephalopathy. The Journal of Pediatrics
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Robert D. Christensen, Mark J. Sheffield, Diane K. Lambert, Vickie L. Baer. (2012) Effect of Therapeutic Hypothermia in Neonates with Hypoxic-Ischemic Encephalopathy on Platelet Function. Neonatology 101:2, 91-94
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George A. Woodward, Roxanne Kirsch, Michael Stone Trautman, Monica E. Kleinman, Gil Wernovsky, Bradley S. Marino. 2012. Stabilization and Transport of the High-Risk Infant. , 341-356.
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Cédric Delhaye, Michael Mahmoudi, Ron Waksman. (2012) Hypothermia Therapy. Journal of the American College of Cardiology 59:3, 197-210
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James E. Cottrell, John Hartung. (2012) Developmental Disability in the Young and Postoperative Cognitive Dysfunction in the Elderly After Anesthesia and Surgery: Do Data Justify Changing Clinical Practice?. Mount Sinai Journal of Medicine: A Journal of Translational and Personalized Medicine 79:1, 75-94
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Hilary P. Grocott, Adam Andreiw. (2012) Con: Topical Head Cooling Should Not Be Used During Deep Hypothermic Circulatory Arrest. Journal of Cardiothoracic and Vascular Anesthesia
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Alexander B. Kowski, Hassan Kanaan, Friedhelm C. Schmitt, Martin Holtkamp. (2012) Deep hypothermia terminates status epilepticus – an experimental study. Brain Research
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Daniel E. Warren, Philip E. Bickler, John P. Clark, Maren Gregersen, Heather Brosnan, Will McKleroy, Pablo Gabatto. (2012) Hypothermia and rewarming injury in hippocampal neurons involves intracellular Ca 2+ and glutamate excitotoxicity. Neuroscience
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Niranjan Thomas, Sridhar Santhanam, Manish Kumar, Kurien Anil Kuruvilla, Atanu Kumar Jana. (2012) Hypothermia for neonatal encephalopathy in resource-poor environments. The Journal of Pediatrics
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Lucia Rivera-Lara, Jiaying Zhang, Susanne Muehlschlegel. (2011) Therapeutic Hypothermia for Acute Neurological Injuries. Neurotherapeutics
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Elavazhagan Chakkarapani, Marianne Thoresen, Xun Liu, Lars Walloe, John Dingley. (2011) Xenon offers stable haemodynamics independent of induced hypothermia after hypoxia–ischaemia in newborn pigs. Intensive Care Medicine
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Siri St. Llaurent Kowalski. (2011) The effects of therapeutic hypothermia on term infants with neonatal asphyxial encephalopathy. Journal of Neonatal Nursing 17:6, 197-202
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Oliver Bandschapp, Matthew T. Sweney, Judy A. Miller, Samira Tahvildari, Daniel C. Sigg, Paul A. Iaizzo. (2011) Induction of Mild Hypothermia by Noninvasive Body Cooling in Healthy, Unanesthetized Subjects. Therapeutic Hypothermia and Temperature Management 1:4, 193-198
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Sarah B. Mulkey, Eudice E. Fontenot, Michiaki Imamura, Vivien L. Yap. (2011) Therapeutic Hypothermia in a Neonate with Perinatal Asphyxia and Transposition of the Great Arteries. Therapeutic Hypothermia and Temperature Management 1:4, 205-208
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Osuke Iwata, Makoto Nabetani, Toshiki Takenouchi, Takayuki Iwaibara, Sachiko Iwata, Masanori Tamura, . (2011) Hypothermia for Neonatal Encephalopathy: Nationwide Survey of Clinical Practice in Japan as of August 2010. Acta Paediatricano-no
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Amade Bregy, Ryan Nixon, George Lotocki, Ofelia F. Alonso, Coleen M. Atkins, Pantelis Tsoulfas, Helen M. Bramlett, W. Dalton Dietrich. (2011) Posttraumatic hypothermia increases doublecortin expressing neurons in the dentate gyrus after traumatic brain injury in the rat. Experimental Neurology
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Barnaby Scholefield, Kevin Morris, Heather Duncan, Paul Davies, Fang Gao Smith, Khalid Khan, Barnaby Scholefield. 2011. Hypothermia for neuroprotection in children after cardiopulmonary arrest. .
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Seetha Shankaran, Abbot R. Laptook, Jon E. Tyson, Richard A. Ehrenkranz, Carla M. Bann, Abhik Das, Rosemary D. Higgins, Rebecca Bara, Athina Pappas, Scott A. McDonald, Ronald N. Goldberg, Michele C. Walsh. (2011) Evolution of Encephalopathy during Whole Body Hypothermia for Neonatal Hypoxic-Ischemic Encephalopathy. The Journal of Pediatrics
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Rosemary D. Higgins, Tonse Raju, A. David Edwards, Denis V. Azzopardi, Carl L. Bose, Reese H. Clark, Donna M. Ferriero, Ronnie Guillet, Alistair J. Gunn, Henrik Hagberg, Deborah Hirtz, Terrie E. Inder, Susan E. Jacobs, Dorothea Jenkins, Sandra Juul, Abbot R. Laptook, Jerold F. Lucey, Mervyn Maze, Charles Palmer, LuAnn Papile, Robert H. Pfister, Nicola J. Robertson, Mary Rutherford, Seetha Shankaran, Faye S. Silverstein, Roger F. Soll, Marianne Thoresen, William F. Walsh. (2011) Hypothermia and Other Treatment Options for Neonatal Encephalopathy: An Executive Summary of the Eunice Kennedy Shriver NICHD Workshop. The Journal of Pediatrics 159:5, 851-858.e1
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HANNAH C. GLASS, KAREN J. HONG, ELIZABETH E. ROGERS, RITA J. JEREMY, SONIA L. BONIFACIO, JOSEPH E. SULLIVAN, A. JAMES BARKOVICH, DONNA M. FERRIERO. (2011) Risk Factors for Epilepsy in Children With Neonatal Encephalopathy. Pediatric Research 70:5, 535-540
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Subrata Sarkar, Steven M. Donn, Jayapalli R. Bapuraj, Indira Bhagat, Ronald E. Dechert, John D. Barks. (2011) The Relationship between Clinically Identifiable Intrapartum Sentinel Events and Short-Term Outcome after Therapeutic Hypothermia. The Journal of Pediatrics 159:5, 726-730
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D. Blanco, A. García-Alix, E. Valverde, V. Tenorio, M. Vento, F. Cabañas. (2011) Neuroprotección con hipotermia en el recién nacido con encefalopatía hipóxico-isquémica. Guía de estándares para su aplicación clínica. Anales de Pediatría 75:5, 341.e1-341.e20
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Hannah C. Glass, Kendall B. Nash, Sonia L. Bonifacio, A. James Barkovich, Donna M. Ferriero, Joseph E. Sullivan, Maria Roberta Cilio. (2011) Seizures and Magnetic Resonance Imaging–Detected Brain Injury in Newborns Cooled for Hypoxic-Ischemic Encephalopathy. The Journal of Pediatrics 159:5, 731-735.e1
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Denise M. Casey, Nancy Tella, Rachel Turesky, Michelle Labrecque. (2011) Therapeutic Hypothermia: Treatment for Hypoxic-Ischemic Encephalopathy in the NICU. Neonatal Network: The Journal of Neonatal Nursing 30:6, 370-380
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E. Lopez. (2011) Prise en charge pédiatrique du nouveau-né post-terme. Journal de Gynécologie Obstétrique et Biologie de la Reproduction
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P. Wintermark, A. Hansen, M. C. Gregas, J. Soul, M. Labrecque, R. L. Robertson, S. K. Warfield. (2011) Brain Perfusion in Asphyxiated Newborns Treated with Therapeutic Hypothermia. American Journal of Neuroradiology
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Pablo Galeano, Eduardo Blanco Calvo, Diêgo Madureira de Oliveira, Lucas Cuenya, Giselle Vanesa Kamenetzky, Alba Elisabeth Mustaca, George Emilio Barreto, Lisandro Diego Giraldez-Alvarez, José Milei, Francisco Capani. (2011) Long-lasting effects of perinatal asphyxia on exploration, memory and incentive downshift. International Journal of Developmental Neuroscience 29:6, 609-619
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Luc Mertens, Istvan Seri, Jan Marek, Romaine Arlettaz, Piers Barker, Patrick McNamara, Anita J. Moon-Grady, Patrick D. Coon, Shahab Noori, John Simpson, Wyman W. Lai. (2011) Targeted Neonatal Echocardiography in the Neonatal Intensive Care Unit: Practice Guidelines and Recommendations for Training. Journal of the American Society of Echocardiography 24:10, 1057-1078
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Dieter Hüseman, Boris Metze, Elisabeth Walch, Christoph Bührer. (2011) Laboratory markers of perinatal acidosis are poor predictors of neurodevelopmental impairment in very low birth weight infants. Early Human Development 87:10, 677-681
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Lina F. Chalak, Nancy Rollins, Michael C. Morriss, Luc P. Brion, Roy Heyne, Pablo J. Sánchez. (2011) Perinatal Acidosis and Hypoxic-Ischemic Encephalopathy in Preterm Infants of 33 to 35 Weeks’ Gestation. The Journal of Pediatrics
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Matthew D. Smyth, Steven M. Rothman. (2011) Focal Cooling Devices for the Surgical Treatment of Epilepsy. Neurosurgery Clinics of North America 22:4, 533-546
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L. Mertens, I. Seri, J. Marek, R. Arlettaz, P. Barker, P. McNamara, A. J. Moon-Grady, P. D. Coon, S. Noori, J. Simpson, W. W. Lai, . (2011) Targeted Neonatal Echocardiography in the Neonatal Intensive Care Unit: Practice Guidelines and Recommendations for Training: Writing group of the American Society of Echocardiography (ASE) in collaboration with the European Association of Echocardiography (EAE) and the Association for European Pediatric Cardiologists (AEPC). European Journal of Echocardiography 12:10, 715-736
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Javier Vaquero. (2011) Therapeutic hypothermia in the management of acute liver failure. Neurochemistry International
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Jessie S Truettner, Ofelia F Alonso, Helen M Bramlett, W Dalton Dietrich. (2011) Therapeutic hypothermia alters microRNA responses to traumatic brain injury in rats. Journal of Cerebral Blood Flow & Metabolism 31:9, 1897-1907
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Javier F. Cárdenas, Jong M. Rho, Adam Kirton. (2011) Pediatric stroke. Child's Nervous System 27:9, 1375-1390
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Katherine M. Newnam, Donna L. DeLoach. (2011) Neonatal Hypothermia: A Method to Provide Neuroprotection After Hypoxic Ischemic Encephalopathy. Newborn and Infant Nursing Reviews 11:3, 113-124
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Christopher S. Ennen, Thierry A.G.M. Huisman, William J. Savage, Frances J. Northington, Jacky M. Jennings, Allen D. Everett, Ernest M. Graham. (2011) Glial fibrillary acidic protein as a biomarker for neonatal hypoxic-ischemic encephalopathy treated with whole-body cooling. American Journal of Obstetrics and Gynecology 205:3, 251.e1-251.e7
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Marcia Hogeling, Katharine Meddles, David R. Berk, Anna L. Bruckner, Thomas K. Shimotake, Ronald S. Cohen, Ilona J. Frieden. (2011) Extensive Subcutaneous Fat Necrosis of the Newborn Associated with Therapeutic Hypothermia. Pediatric Dermatologyno-no
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Sindhu Sivanandan, Yacov Rabi, Majeeda Kamaluddeen, Albert Akierman, Abhay Lodha. (2011) Subcutaneous Fat Necrosis as a Complication of Therapeutic Hypothermia in a Term Neonate. The Indian Journal of Pediatrics
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Dianne L. Atkins, Stuart Berger. (2011) Improving Outcomes from Out-of-Hospital Cardiac Arrest in Young Children and Adolescents. Pediatric Cardiology
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Toshiki Takenouchi, Elayna O. Rubens, Vivien L. Yap, Gail Ross, Murray Engel, Jeffrey M. Perlman. (2011) Delayed Onset of Sleep-Wake Cycling with Favorable Outcome in Hypothermic-Treated Neonates with Encephalopathy. The Journal of Pediatrics 159:2, 232-237
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Gergely Silasi, Frederick Colbourne. (2011) Therapeutic hypothermia influences cell genesis and survival in the rat hippocampus following global ischemia. Journal of Cerebral Blood Flow & Metabolism 31:8, 1725-1735
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(2011) Introduction to Resuscitation of the Newborn Infant. ARC and NZRC Guideline 2010. Emergency Medicine Australasia 23:4, 419-423
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Stuart Faulkner, Alan Bainbridge, Takenori Kato, Manigandan Chandrasekaran, Andrew B. Kapetanakis, Mariya Hristova, Mengyan Liu, Samantha Evans, Enrico De Vita, Dorottya Kelen, Robert D. Sanders, A. David Edwards, Mervyn Maze, Ernest B. Cady, Gennadij Raivich, Nicola J. Robertson. (2011) Xenon augmented hypothermia reduces early lactate/N-acetylaspartate and cell death in perinatal asphyxia. Annals of Neurology 70:1, 133-150
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Alexis Topjian, Michael Hamid, Larissa Hutchins, Vinay Nadkarni. (2011) Can a Cold (4°C) IV Fluid Bolus to Induce Therapeutic Hypothermia Really Deliver 4°C to Children?. Therapeutic Hypothermia and Temperature Management 1:2, 95-98
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