INTRODUCTION ABSTRACT. beneficial effects of hypothermia therapy, the result of meta analyses has shown that therapeutic hypothermia
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1 Original Article Multicenter Randomized Controlled Trial of Therapeutic Hypothermia Plus Magnesium Sulfate Versus Therapeutic Hypothermia Plus Placebo in the Management of Term and Near term Infants with Hypoxic Ischemic Encephalopathy (The Mag Cool Study): A Pilot Study Sajjad Ur Rahman, Fuat Emre Canpolat 1, Mehmet Yekta Oncel 1, Abdurrahman Evli 1, Ugur Dilmen 1, Hussain Parappil, Jasim Anabrees 2, Khalid Hassan 2, Mohammed Khashaba 3, Islam Ayman Noor 3, Lucy Chai See Lum 4, Anis Siham 4, Melek Akar 5, Heybet Tuzun 5, Aiman Rahmani 6, Moghis Rahman 6, Lina Haboub, Mohammed Rijims, Rohana Jaafar 7, Lai Yin Key 7, Mohammad Tagin 8, on behalf of the Mag Cool Study Group* NICU Women s Hospital, Hamad Medical Corporation, Doha, Qatar, 1 Zekai Tahir Burak Maternity Teaching Hospital, Ankara, 5 Diyarbakir Children Hospital, Diyarbakir, Turkey, 2 Neonatal Care, Arrayan Hospital, Sulaiman Al Habib Medical Group, Riyadh, Saudi Arabia, 3 Mansoura University Children s Hospital, Mansoura, Egypt, 4 Universiti Malaya Medical Center, 7 Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia, 6 Tawam Hospital, Abu Dhabi, United Arab Emirates, 8 Women s Hospital, Winnipeg, MB, Canada ABSTRACT Background: Therapeutic hypothermia provides up to 30% neuroprotection in moderate to severe hypoxic ischemic encephalopathy (HIE). Additional neuroprotection may be achieved by using concomitant pharmacologic neuroprotective agents. Aim: The aim was to evaluate the safety of concomitant neuroprotective therapy of therapeutic hypothermia and magnesium sulfate ( ) in the management of moderate and severe HIE in term and near term infants. Study Design: Multicenter double blind randomized controlled trial. Methodology: Term and near term newborn infants ( 35 weeks) with a clinical diagnosis of moderate or severe HIE were randomized to either Arm A (therapeutic hypothermia plus ) or Arm B (therapeutic hypothermia plus placebo) using a net based randomization system. Both groups received, within 6 h of birth, standard hypothermia therapy (72 h of cooling to 33.5 C followed by slow rewarming over a period of 8 h) plus either (250 mg/kg/dose 3 doses) or placebo (normal saline). The groups were compared for short term predischarge adverse outcomes. Results: A total of 60 patients were randomized (29 in Arm A and 31 in Arm B). Both groups had similar baseline characteristics (P > 0.05) including severity of HIE. There were no differences in the short term adverse outcomes (death, seizures, thrombocytopenia, coagulopathy, renal failure, elevated liver function test s, hypotension, intracranial hemorrhage, necrotizing enterocolitis, pulmonary hemorrhage, persistent pulmonary hypertension, and pulmonary air leak syndromes) between the two groups (P > 0.05). Conclusions: The combined use of therapeutic hypothermia and appears to be safe particularly with respect to maintaining normal blood pressure and coagulopathy. Long term survival and neurodevelopmental outcomes remain to be evaluated. Key words: Hypoxic ischemic encephalopathy, magnesium sulfate, neuroprotection, newborn, therapeutic hypothermia INTRODUCTION There is convincing evidence that moderate therapeutic hypothermia (33 34 C for 72 h), when initiated within 6 h after birth among term and near term infants ( 35 weeks) with moderate to severe hypoxic ischemic encephalopathy (HIE) reduces the risk of death or major disability [1 4] and increases the rate of disability free survival at 6 7 years of age. [5,6] The National Institute of Clinical Excellence endorsed therapeutic hypothermia for routine clinical practice in United Kingdom in [7] Similar national guidelines have been issued in many other countries with the result that therapeutic hypothermia has now become a standard of care for moderate to severe HIE in term and near term infants in Neonatal Intensive Care Units (NICU s) worldwide. [8] Despite the remarkable beneficial effects of hypothermia therapy, the result of meta analyses has shown that therapeutic hypothermia Address for correspondence: Dr. Sajjad Ur Rahman, Women s Hospital, Hamad Medical Corporation, Associate Prof: Weill Cornell Medical College, PO Box 3050, Doha, Qatar. E mail: sajjadjan@hotmail.com Quick Response Code: Access this article online Website: DOI: / Journal of Clinical Neonatology Vol. 4 Issue 3 July-September 2015
2 provides on the average up to 25% neuroprotection. [1 4] However, it is possible that pharmacologic neuroprotective therapies may add incrementally to the proven benefit of hypothermia. [9] This approach of adding a pharmacologic neuroprotective agent to supplement the neuroprotective role of therapeutic hypothermia has brought a new global era of neuroprotective research in neonatal practice called the hypothermia plus therapy. The potential neuroprotective pharmacologic agents include erythropoietin, melatonin, magnesium sulfate ( ), topiramate, xenon, and allopurinol. [9] Magnesium sulfate is a low cost readily available drug worldwide. The cochrane meta analysis 2009 [10] concluded that has a proven neuroprotective benefit in preterm newborn babies when given to their pregnant mothers antenatally. This conclusion is supported by the most recent review by Tataranno et al. [11] Although the postnatal neuroprotective use of in human infants with HIE, without concomitant hypothermia therapy, has confirmed safety as well as efficacy, [12 15] a recent preclinical study on animal models of term HIE, [16] has failed to find a consistent neuroprotective role of. Since a combination of therapeutic hypothermia and has never been tested for its therapeutic safety and neuroprotective efficacy in term human infants with HIE; we conducted this pilot study to compare and analyze the in hospital mortality and short term predischarge morbidity outcomes of this combined therapy as compared to hypothermia therapy alone. METHODOLOGY Study design The study was set up as a prospective, double blind (for ), placebo (0.9% saline) controlled multi center randomized controlled trial (MRCT) and multinational randomized controlled trial, which was conducted in the tertiary care NICU s in Qatar, Turkey, Saudi Arabia, Egypt, Malaysia, and Abu Dhabi between September 2012 and August The study population included all term and near term newborns ( 35 completed weeks) with moderate to severe HIE. The severity of HIE was determined using the Sarnat and Sarnat criteria. [17] Therapeutic hypothermia was started as a standard of care in all babies within 6 h after birth using either total body cooling method (Teicotherm Neo Insp Inc., UK) or head cooling (Olympic Cool Cal system) depending upon the individual unit policy. The babies were cooled to a core body temperature (rectal) of 33.5 C (range: C) for a period of 72 h followed by slow re warming over a period of 8 h at a rate not exceeding 0.5 C/h. Each newborn infant was provided standard intensive care as per individual unit protocol. Informed parental consent was obtained from the parents of eligible babies who met the inclusion and exclusion criteria given in Panel 1. Randomization to magnesium sulfate or placebo and study drug administration After parental consent, the babies were randomized using a net based randomization system provided by a London based independent clinical trials randomization company (sealed envelope). [18] Each recruitment center had its own unique password and PIN code for using the system. Each randomization was immediately notified by E mail directly from the randomization website to the data coordinating center in Doha, Qatar. Each Panel 1 Inclusion criteria The babies will be assessed sequentially for criteria A and B listed below A. Condition at birth: Infants 35 completed weeks gestation admitted to the NICU with at least one of the following Apgar score of <5 at 10 min after birth due to birth asphyxia/perinatal depression Continued need for resuscitation, including endotracheal or mask ventilation, at 10 min after birth Acidosis within 60 min of birth (defined as any occurrence of umbilical cord, arterial or capillary ph <7.00) Base deficit ( 16 mmol/l) in umbilical cord or any blood sample (arterial, venous or capillary) taken within 60 min of birth Infants that meet criteria A will be assessed by the attending neonatologist for criteria B B. Neurological assessment Evidence of moderate to severe encephalopathy, consisting of altered state of consciousness (lethargy, stupor or coma) and at least one of the following Hypotonia Abnormal reflexes including oculomotor or pupillary reflexes Absent or weak suck Clinical seizures Infants that meet criteria A and B and do not meet the exclusion criteria given below will be randomized for the study In case the unit has cerebral function monitoring facility and a trained neonatologist/neurologist to apply and interpret the aeeg, the below given criteria C will be used as an additional help to recruit the babies into the study C. aeeg: At least 30 min duration of aeeg recording that shows abnormal background aeeg activity or seizures. There must be one of the following Normal background with some seizure activity Moderately abnormal activity Suppressed activity Seizure activity Note: Criteria C is optional and will be used as an additional help. The study recruitment will essentially be based on criteria A and B Exclusion criteria Infants expected to be >6 h of age at the time of randomization Major congenital abnormalities, such as diaphragmatic hernia requiring ventilation or congenital abnormalities suggestive of chromosomal anomaly or other syndromes that include brain dysgenesis Very severe HIE where the elective withdrawal is justified by the attending clinician NICU Neonatal Intensive Care Unit; aeeg Amplitude integrated electroencephalogram; HIE Hypoxic ischemic encephalopathy Journal of Clinical Neonatology Vol. 4 Issue 3 July-September
3 randomized baby received a unique randomization code with two letters and one number. The code was prescribed by the physician at a dose of 2.5 ml/kg/day q 24 h for three doses which would be equivalent to 250 mg/kg/dose of 10% or 2.5 ml/kg/dose of normal saline. Once the coded prescription was received by the pharmacist, he/ she un coded the prescription and dispensed the study medication in a sealed syringe labeled with the code and study number. The study medicine was administered as slow intravenous (IV) infusion over a period of 30 min within 6 h of birth. Data collection Data were collected on standard printed daily log books approved by the Institutional Review Board. The baseline characteristics and short term outcome variables were ascertained as per approved study protocol [Tables 1 and 2]. Table 1: Baseline characteristics Variables Total patients analyzed: 60 P Arm A (intervention) n=29 (%) Arm B (control) n=31 (%) Stages of HIE Moderate 14 (48.3) 19 (61.3) Severe 15 (51.7) 12 (38.7) Seizures 18 (62.1) 17 (54.8) Meconium aspiration 3 (10.3) 5 (16.1) Culture proven sepsis 3 (10.3) 1 (3.2) HIE Hypoxic ischemic encephalopathy Definitions Moderate hypotension was defined as the need for volume therapy and/or one inotrope. Severe hypotension was defined as the need for two or more inotropes or antihypotensive medication, e.g. hydrocortisone. Statistical analysis The decoding of individual patients was done by the study statistician keeping the investigators blinded. For statistical analysis, the patients were grouped into Arm A (therapeutic hypothermia plus ) or Arm B (therapeutic hypothermia plus placebo). The Chi square test of significance or Fisher exact test (for expected count <5 in at least one cell) were used to compare short term predischarge adverse outcomes between the two groups. The level of significance was set at P < RESULTS A total of 60 infants were randomized (29 in Arm A and 31 in Arm B). Both groups had similar baseline characteristics (P > 0.05) including severity of HIE, incidence of fetal sepsis and seizures as well as evidence of fetal distress (meconium aspiration) as shown in Table 1. All babies were treated with standard therapeutic hypothermia for 72 h followed by 8 h of re warming. Therapeutic hypothermia had to be terminated in one baby due to severe sinus bradycardia. Overall 55% (n = 33) had moderate HIE and 45% (n = 27) Table 2: Adverse outcomes at discharge from the hospital Variables Total patients analyzed: 60 P RR (95% CI) Arm A (intervention) n=29 (48.33%) Arm B (control) n=31 (51.67%) Deaths 2 (6.9) 5 (16.1) ( ) Seizure 18 (62.1) 17 (54.8) ( ) Prolonged coagulation 25 (86.2) 27 (87.1) ( ) Thrombocytopenia 22 (75.9) 19 (61.3) ( ) Renal failure 13 (44.8) 14 (45.2) ( Raised LFTs 19 (65.5) 19 (61.3) ( ) Hypotension Severe 12 (41.4) 15 (48.4) 0.86 ( ) Mild to moderate 12 (41.4) 12 (38.7) ( ) Total 24 (42.8) 27 (87.1) 0.95 ( ) Meconium aspiration 3 (10.3) 5 (16.1) ( ) Intracranial hemorrhage <grade 3 28 (96.6) 31 (100) ( ) grade 3 1 (3.4) 0 Total 29 (100%) 31 (100%) 1 ( ) Pulmonary air leak syndrome 0 (0) 2 (6.5) (0 1.96) Necrotizing enterocolitis 0 (0) 2 (6.5) (0 1.96) Pulmonary hemorrhage 1 (3.4) 1 (3.2) ( ) Pulmonary hypertension 2 (6.9) 1 (3.2) ( ) Major venous thrombosis 0 (0) 0 (0) NS Subcutaneous fat necrosis 0 (0) 0 (0) NS LFTs Liver function test s; CI Confidence interval; RR Risk ratio 160 Journal of Clinical Neonatology Vol. 4 Issue 3 July-September 2015
4 severe HIE. Totally, 55 babies (91.7%) were cooled by total body cooling (Teicotherm Neo Insp Inc., UK) and five babies (8.3%) by head cooling (Olympic Cool Cal System). There were no differences in the short term adverse outcomes (death, seizures, thrombocytopenia, coagulopathy, renal failure, raised liver function test, hypotension, intracranial hemorrhage, necrotizing enterocolitis, pulmonary hemorrhage, pulmonary hypertension, and pulmonary air leak syndromes) between the two groups (P > 0.05) as shown in Table 2. DISCUSSION Perinatal asphyxia remains a major cause of neonatal mortality [19] as well as long term sensorineural impairments and disabilities. [20 22] The incidence has been almost static; 1 2/1000 births in developed countries and up to 5/1000 birth and even higher in some developing countries. [20,23,24] There was no specific neuroprotective treatment available for affected infants till the recent discovery of therapeutic hypothermia which has been proven to reduce death and major disabilities; both at months [1 4] and in middle childhood. [6] However, the neuroprotective achievement remains far from perfect. Despite effective therapeutic hypothermia delivered according to the standard research protocols, 50% of newborn infants with moderate to severe HIE will still continue to die or survive with major disabilities including cerebral palsy (CP) and major neurodevelopmental delay; [1] hence, the search to discover additional neuroprotective therapies continues. [25] The term hypothermia plus therapy has been used for adding a pharmacologic agent with potential neuroprotective action to the standard hypothermia therapy. [25,26] The pharmacologic agents with potential additive neuroprotective role in neonatal HIE include, [27] xenon, [28] topiramate, [29] allopurinol, [30] and erythropoietin. [31] Antenatal administered to pregnant women with preterm labor has an established role in preterm neonatal neuroprotection. given to women at risk of premature birth significantly reduced the risk of CP without increasing the risk of perinatal or infant death. [10,11,32] According to the cochrane meta analysis 2009, the neuroprotective role for antenatal therapy given to women at risk of preterm birth for the preterm fetus is now established. [10] Another recent meta analysis also found persuasive evidence that administered to women at high risk of delivery before 34 weeks of gestation reduces the risk of CP in their children. [33] The National Institute of Child Health and Human Development meta analysis of 2009 also concluded that fetal exposure to in women at risk of preterm delivery significantly reduces the risk of CP without increasing the risk of death. [34] The most recent review article by Tataranno et al. [11] states that recent evidences demonstrate that fetal exposure to in women at risk for preterm delivery significantly reduces the risk of CP without increasing the risk of death. However, there are views contrary to this as well. The preclinical study by Galinsky et al. [16] using term HIE animal models suggests that magnesium is not consistently neuroprotective for perinatal hypoxia ischemia in term equivalent animal HIE models. The postnatal neuroprotective use of in human infants, without concomitant hypothermia therapy, has confirmed safety as well as efficacy. [12 15] The results from the recent systematic review and meta analysis by Tagin et al. [27] on the use of in newborns with HIE indicates an improvement in the short term composite outcome of survival without abnormalities in any of the following: Neurodevelopmental examination, neuroimaging or neurophysiologic studies. It is plausible that a concomitant use of may add to the established neuroprotective efficacy of therapeutic hypothermia therapy. However, the neuroprotective efficacy of a combination of hypothermia and has been tested only in animals. Campbell et al., in their study on rat models, have shown that combined and hypothermia treatment reduced infarct volumes by 54% at 2 h (P = 0.048) and by 39% at 4 h (P = 0.012), but there was no treatment effect detected at 6 h or in the hypothermia alone or alone groups. [35] Similarly Zhu et al., [36] from their study of global cerebral ischemia in rats, have shown that postischemic modest hypothermia (35 C) combined with IV magnesium is more effective at reducing neuronal death than either treatment used alone. Since is a low cost medicine and is readily available in resource restricted countries which bear the highest share of the global burden of perinatal asphyxia, we decided to test for hypothermia plus therapy. To our knowledge, Mag Cool study is the first MRCT of combined hypothermia plus therapy in human infants with moderate to severe HIE. Hence, the current pilot study was essential to establish the safety of combined use of and therapeutic hypothermia in human infants with HIE before proceeding any further with the full trial which would test the neuroprotective efficacy at months. Tagin et al., in their meta analysis, have reported a statistically insignificant higher trend in mortality in the group. [27] On the other hand, in our study, the trend of mortality was higher in the placebo group which was also statistically nonsignificant. The use of also carries the potential transient risk of systemic hypotension and respiratory depression. [37,38] The likelihood of hypotension is high in the clinical scenario of a baby with moderate to severe HIE and concomitant use of hypothermia therapy. Journal of Clinical Neonatology Vol. 4 Issue 3 July-September
5 Inadvertent overcooling and inappropriate rapid rewarming during hypothermia therapy can produce hypotension. [39] The study by Levene et al. [37] has shown that given to term babies with HIE, as slow IV infusion in a dose of 250 mg/kg/dose once a day for 3 days (low dose) is less likely to produce hypotension as compared to a dose of 400 mg/ kg/dose once a day for 3 days (high dose). The studies of Bhat et al. [12] and Khashaba et al. [13] have also shown no difference in the incidence of hypotension between the and the control groups. Both studies used low dose (250 mg/kg/dose once a day). None of these studies used a concomitant hypothermia therapy. We also used low dose (250 mg/kg/dose once a day) as IV infusion and despite the concomitant use of standard therapeutic hypothermia therapy, there was no difference in the incidence of moderate to severe hypotension between the group and placebo group. The sedative effect of was neither estimated nor considered a problem because all babies were on respiratory support during the first 72 h of life. The difference between other short term, in the hospital, predischarge adverse outcomes was also nonsignificant between the and placebo groups in our study. The results of our pilot data show that combined use of therapeutic hypothermia and in the management of moderate to severe HIE in term and near term infants is safe; both in terms of mortality as well as predischarge in hospital morbidity. Hence, it is reasonable to conduct a well designed, large MRCT to evaluate the long term safety, as well as neuroprotective efficacy of hypothermia plus as compared to hypothermia therapy alone. SUMMARY The on going research on hypothermia plus therapies carries a potential promise of additional neuroprotection in term and near term babies with moderate to severe HIE. The combined use of therapeutic hypothermia and is one such therapy which appears to be safe particularly with respect to the risk of mortality and short term adverse outcomes. Long term survival and neurodevelopmental outcomes remain to be evaluated. ACKNOWLEDGMENTS We are indebted to the Mag Cool Study group and the staff in all participating hospitals for their hard work and contribution to the study. We specially thank our patients and their families for consenting to be included in the study. Our particular gratitude goes for Sarah Al Tinaye, Anila Tabassum, Sameera Ameer, Monisha Mohen, and Anette Jacobs for assembling and cleaning the data; Mohammad Tahir Yousafzai and Dr. Shafiw Rehamn for data organization and analysis,, cleaning and statistical analysis and Dr. Fares Chedid for analyzing, organizing, and reshaping the tables. REFERENCES 1. Tagin MA, Woolcott CG, Vincer MJ, Whyte RK, Stinson DA. Hypothermia for neonatal hypoxic ischemic encephalopathy: An updated systematic review and meta analysis. Arch Pediatr Adolesc Med 2012;166: Edwards AD, Brocklehurst P, Gunn AJ, Halliday H, Juszczak E, Levene M, et al. Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: Synthesis and meta analysis of trial data. BMJ 2010;340:c Jacobs SE, Berg M, Hunt R, Tarnow Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2013;1:CD Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cochrane review update. Cooling for Newborns with hypoxic ischemic encephalopathy. Neonatology 2013;104: Shankaran S, Pappas A, McDonald SA, Vohr BR, Hintz SR, Yolton K, et al. Childhood outcomes after hypothermia for neonatal encephalopathy. N Engl J Med 2012;366: Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O, et al. 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6 20. Gonzalez FF, Miller SP. Does perinatal asphyxia impair cognitive function without cerebral palsy? Arch Dis Child Fetal Neonatal Ed 2006;91:F Marlow N, Rose AS, Rands CE, Draper ES. Neuropsychological and educational problems at school age associated with neonatal encephalopathy. Arch Dis Child Fetal Neonatal Ed 2005;90:F Van Handel M, Swaab H, de Vries LS, Jongmans MJ. Long term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: A review. Eur J Pediatr 2007;166: Lawn JE, Cousens S, Zupan J, Lancet Neonatal Survival Steering Team 4 million neonatal deaths: When? Where? Why? Lancet 2005;365: Paul VK. Neonatal morbidity and mortality: Report of the national neonatal and perinatal database. Indian Pediatr 1999;36: Edwards AD, Azzopardi DV. Hypothermic neural rescue: Work continues. J Pediatr 2010;157: Marro PJ, Delivoria Papadopoulos M. Pharmacology review: Neuroprotective treatments for hypoxic ischemic injury. Neoreviews 2010;11:e Tagin M, Shah PS, Lee KS. Magnesium for newborns with hypoxic ischemic encephalopathy: A systematic review and meta analysis. J Perinatol 2013;33: Hobbs C, Thoresen M, Tucker A, Aquilina K, Chakkarapani E, Dingley J. Xenon and hypothermia combine additively, offering long term functional and histopathologic neuroprotection after neonatal hypoxia/ischemia. Stroke 2008;39: Filippi L, Poggi C, la Marca G, Furlanetto S, Fiorini P, Cavallaro G, et al. Oral topiramate in neonates with hypoxic ischemic encephalopathy treated with hypothermia: A safety study. J Pediatr 2010;157: Kaandorp JJ, van Bel F, Veen S, Derks JB, Groenendaal F, Rijken M, et al. Long term neuroprotective effects of allopurinol after moderate perinatal asphyxia: Follow up of two randomised controlled trials. Arch Dis Child Fetal Neonatal Ed 2012;97:F Zhu C, Kang W, Xu F, Cheng X, Zhang Z, Jia L, et al. Erythropoietin improved neurologic outcomes in newborns with hypoxic ischemic encephalopathy. Pediatrics 2009;124:e Heyborne K, Bowes WA. The use of antenatal magnesium sulfate for neuroprotection for infants born prematurely. F1000 Med Rep 2010;2: Conde Agudelo A, Romero R. Antenatal magnesium sulfate for the prevention of cerebral palsy in preterm infants less than 34 weeks gestation: A systematic review and metaanalysis. Am J Obstet Gynecol 2009;200: Costantine MM, Weiner SJ, Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal Fetal Medicine Units Network. Effects of antenatal exposure to magnesium sulfate on neuroprotection and mortality in preterm infants: A meta analysis. Obstet Gynecol 2009;114: Campbell K, Meloni BP, Knuckey NW. Combined magnesium and mild hypothermia (35 degrees C) treatment reduces infarct volumes after permanent middle cerebral artery occlusion in the rat at 2 and 4, but not 6 h. Brain Res 2008;1230: Zhu H, Meloni BP, Bojarski C, Knuckey MW, Knuckey NW. Post ischemic modest hypothermia (35 degrees C) combined with intravenous magnesium is more effective at reducing CA1 neuronal death than either treatment used alone following global cerebral ischemia in rats. Exp Neurol 2005;193: Levene M, Blennow M, Whitelaw A, Hankø E, Fellman V, Hartley R. Acute effects of two different doses of magnesium sulphate in infants with birth asphyxia. Arch Dis Child Fetal Neonatal Ed 1995;73:F Greenberg MB, Penn AA, Whitaker KR, Kogut EA, El Sayed YY, Caughey AB, et al. Effect of magnesium sulfate exposure on term neonates. J Perinatol 2013;33: Thoresen M, Whitelaw A. Cardiovascular changes during mild therapeutic hypothermia and rewarming in infants with hypoxic ischemic encephalopathy. Pediatrics 2000;106:92 9. How to cite this article: Rahman SU, Canpolat FE, Oncel MY, Evli A, Dilmen U, Parappil H, et al. Multicenter randomized controlled trial of therapeutic hypothermia plus magnesium sulfate versus therapeutic hypothermia plus placebo in the management of term and near-term infants with hypoxic ischemic encephalopathy (The Mag Cool study): A pilot study. J Clin Neonatol 2015;4: Source of Support: The study was funded by the Hamad Medical Corporation Internal Grants Competition (IG 1028). Conflict of Interest: None declared. Journal of Clinical Neonatology Vol. 4 Issue 3 July-September
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