Cardiac arrest was the most frequent neurologic insult (23%), followed by traumatic brain injury (19%), status epilepticus (17%), and CNS infection/inflammation (Table 3).
All-cause mortality was 105 (12%). Children admitted after a cardiac arrest had the highest mortality (24%) and PIM (6.6 [2.4–20.6]), both p values less than 0.001 versus other neurologic insults (Table 3). Cause of death was provided in 49 subjects who died. The most common causes of death were withdrawal of support due to poor neurologic status (25%), brain death (11%), and cardiovascular failure (10%). Of subjects with a pre-ICU PCPC of 1 (no disability) with PCPC at hospital discharge or 3 months available, 211 of 475 (44%) remained PCPC of 1. The remainder of subjects with a pre-ICU PCPC of 1 had PCPC 2 (18%), PCPC 3 (11%), PCPC 4 (13%), PCPC 5 (4%), and PCPC 6 (9%) at the later time point. Subjects with traumatic brain injury had the highest rate of normal baseline PCPC (82%). Thirty-two percent of subjects had unfavorable outcome, which was most common in subjects with traumatic brain injury (49%) (p < 0.001).
Hospital and PICU length of stay were 22 (8–55) and 13 (4–33) days, respectively, and were longest in children with cardiac arrest (both p < 0.001). At the study’s endpoint, 58% of subjects were discharged home, and 17% were admitted to an inpatient rehabilitation center. Subjects with traumatic brain injury and spinal cord lesion had the highest frequency of rehabilitation disposition (28% and 37%, respectively).
The frequency of new morbidities differed by insult. Feeding tubes were most frequently placed in children with cardiac arrest (30%), and tracheostomy tubes were most frequently placed in children with spinal cord lesion (33%).
Subject and PICU characteristics varied by region, including age, type of insurance, number of PICU beds, and neurocritical care service (Tables 1, 2, and 4). Prevalence of acute neurologic insults was highest in North America (18.0 [16.7–19.3]) and Africa (15.8 [6.0–31.3]) and lowest in Asia (9.8 [6.1–14.7]) and Europe (12.7 [10.7–14.8]). The most common acute neurologic insult was cardiac arrest in North America, Europe, and Oceania, whereas CNS infection/inflammation was most prevalent in South America, Asia, and Africa (Supplemental Fig. 1, Supplemental Digital Content 2, http://links.lww.com/PCC/A391). PIM2 scores were highest in Oceania and lowest in South America and Asia. Length of stay was longest in Africa and shortest in Oceania and Asia. Mortality was 10–14% except at the single center in Africa, where no subjects died, but 50% had unfavorable outcome.
There are three chief findings of this study: 1) Acute neurologic insults are common among PICU patients, with global hypoxia-ischemia due to cardiac arrest being the most frequent insult; 2) The consequences of acute neurologic insults are serious: mortality was 4–6 times that of published PICU mortality rates (19), subjects had long length of stay, and survivors frequently acquired new morbidities; and 3) Many regional differences exist among center and subject characteristics with acute neurologic insults.
Our study population, and therefore our findings and implications, largely reflect critically ill children admitted to ICUs in academic pediatric hospitals in North America, Europe, and Oceania. The prevalence of acute neurologic insults is consistent with an analysis of 3 million pediatric hospital discharges in 11 U.S. states by Moreau et al (2) in which children with neurologic insults prompted 10% of pediatric hospital admissions but were responsible for 3 times the proportion of PICU admissions, longer length of stay, higher mortality, and higher cost versus children with nonneurologic diagnoses. Factors that may affect prevalence include the relatively long length of stay of children with acute neurologic insults (also seen in Moreau et al ), and occurrence of adverse events associated with long length of stay and severe illness (e.g., hospital-acquired infection) or additional organ insults/injuries (e.g., renal failure or acute respiratory distress syndrome); though these were not assessed in PANGEA (2, 22). The frequency of new morbidities including the need for new surgical technologic supports was high, especially in children with cardiac arrest.
Cardiac arrest, the neurologic insult with the highest mortality rate, was also the most common insult overall. Cardiac arrest causes global hypoxia-ischemia, which can lead to varying degrees of postresuscitation syndrome in which brain injury is often the most significant organ affected long term (23). Notably, other neurologic insults are associated with organ injury outside the CNS, which can affect outcome (24–26). Traumatic brain injury was the second most common insult overall in PANGEA, and unintentional injury is the leading cause of death for children of 10–19 years old worldwide (27). Although traumatic brain injury subjects had the highest frequency of unfavorable outcome, children with neurologic insults often have great potential for rehabilitation, and assessment of longer term outcomes is needed (28).
The growth of pediatric neurocritical care services in PICUs and development of a pediatric neurocritical care research network reflect the specialty’s acknowledgement and commitment to improve outcomes for children with acute neurologic insults (29–31). In PANGEA, nearly half of centers reported having a neurocritical care service (of variable make-up), more than double that of a recent survey (32). Data are needed to elucidate the optimal configuration and integration of neurocritical care services that affect outcomes (29, 30, 33, 34). Few centers reported having ICU follow-up clinics, an innovative multidisciplinary effort to address recovery from critical illness (35).
Although exploratory in this study, regional epidemiologic and center differences are important to investigate before planning prospective research studies, allocating healthcare resources, and developing advocacy programs (36–39). For example, CNS infection/inflammation was the most frequent neurologic insult in South America, Asia, and the single African site compared with cardiac arrest in the remaining regions. Overall prevalence of acute neurologic insult was highest in North America, nearly double that found in Asian centers, but not the highest length of stay. Centers in Oceania had the highest median risk of mortality scores but not the highest unadjusted mortality rate. Regions showed differences in patient age, sex, and health insurance status, variables associated with outcome (40–42). Additionally, regions differed in terms of monitoring and testing capabilities and numbers of personnel providing care in the ICU and in a neurocritical care service and hospital beds. These findings speak to the idea that the optimal delivery of healthcare for neurocritical care patients may differ regionally.
These findings, taken together with a dearth of efficacious neuroprotective therapies and overall lack of high-quality evidence to support care, represent a compelling case for the need for increased research and healthcare resources to assist in improving outcomes for children with acute neurologic insults. Transformational ideas to address these issues are critically needed (43, 44).
The strengths and limitations of the point prevalence/cross-sectional method of study have been reviewed, and limitations include: 1) findings lack cause and effect conclusiveness; rather serving as more descriptive purposes and 2) potential underestimation of rapidly fatal disease processes and infrequently used medications and interventions (15). Centers participating in PANGEA are from middle- and high-income regions. Therefore, our results are not fully representative of the global health problem of children with neurologic insult in need of pediatric critical care in resource-limited settings, where most child mortality occurs. PANGEA is also conducting research into the epidemiology and outcomes of acute neurologic insult in these settings (45, 46). Children who died prior to reaching medical care and children with milder injuries who did not require ICU resources were not included in this study. Most participating ICUs were academic, reflecting regionalization typical of pediatric critical care but may limit the generalization of findings. Unfavorable outcome was based on change in PCPC score, which may be less informative in infants than in older children. The wide range of regions and centers collecting PCPC data using the medical chart may have limited its reliability. The deliberate avoidance of choosing study dates on weekends and major holidays may increase the chance of sampling bias. This study focused on primary neurologic insults; inclusion of subjects with secondary neurologic insults, a common cause of mortality and morbidity in critically ill children, would also be valuable to inform our long-term objective of improving outcomes for these children.
Children with acute neurologic insults are common in ICUs and are associated with high morbidity and mortality rates and prolonged ICU stays, posing significant challenges to public, family, and individual health. These data suggest a vital need for resources to assist in the challenge of improving outcomes for these children throughout the span of the periods of emergency care through to rehabilitation.
We thank the nonfinancial support of the following groups committed to the provision of excellent clinical care and research: Pediatric Acute Lung Injury and Sepsis Investigators (PALISI), Australian and New Zealand Intensive Care Society (ANZICS), European Society of Paediatric Neonatal Intensive Care (ESPNIC), Canadian Critical Care Trials Group (CCCTG), World Federation of Pediatric Intensive and Critical Care (WFPICCS), and Pediatric Neurocritical Care Research Group (PNCRG). In addition, we thank Carrie Pidro (PANGEA study coordinator) and Kyle Landis (PANGEA data management). We are grateful to the staff, nurses, and physicians of all ICUs in this study for their generous efforts to help improve the outcomes of children with critical illness.
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APPENDIX 1. THE PANGEA INVESTIGATORS
North America—United States: Craig Smith, MD and Claire Ryan (Ann & Robert H. Lurie Children’s Hospital of Chicago); Josh Koch, MD (Children’s Medical Center of Dallas/University of Texas Southwestern Medical Center); Karen Walson, MD (Children’s Healthcare of Atlanta); Edward Truemper, MD (Children’s Hospital and Medical Center, Omaha); Heidi Flori, MD and Julie Simon, (Children’s Hospital and Research Center Oakland); Jennifer Exo, DO (Children’s Hospital Colorado); Barry Markovitz, MD, MPH and Rica Morzov, RN, BSN, CPN (Children’s Hospital Los Angeles); Kerri LaRovere, MD (Boston Children’s Hospital); Akira Nishisaki, Judy Verger, RN, PhD, FCCM, Janice Prodell, RN, CCRC, Martha Sisko, BSN, RN, MS, CCRC Sheila McGowan, BSN, RN, Tesa Idell, Carolann Twelves, RN, BSN, William Kamens, Brooke Park, BSN, RN, and Mary Ann Diliberto, BS, RN, CCRC (Children’s Hospital of Philadelphia); Ericka Fink, MD, MS and Alan Abraham (Children’s Hospital of Pittsburgh); Sheila Hanson, MD and Kathy Murkowski, RRT, CCRC (Children’s Hospital of Wisconsin); Jeffrey Nowak, MD, Erin Zielinski, and Alison Overman (Children’s Hospitals and Clinics of Minnesota); Kelly Tieves, DO, MS, Trisha Williams, RN, BSN, CPN, and Amber Hughes-Schalk (Children’s Mercy Hospital); Nathan Dean, MD, Aparna Bala, and Anne Watson (Children’s National Medical Center); Derek Wheeler, MD, MMM, Sharon Banschbach, Eileen Beckman, and Erin Frank (Cincinnati Children’s Hospital Medical Center); Sholeen Nett, MD, PhD and J. Dean Jarvis, BSN, MBA, CCRP (Dartmouth-Hitchcock Medical Center); Renee Higgerson, MD, LeeAnn Christie, MSN, RN, and Jodie Reed, FNP, ACNP (Dell Children’s Medical Center of Central Texas); Ira Cheifetz, MD, Samantha Tate, Tammy Uhl, and Karin Reuter-Rice, PhD, NP, FCCM (Duke University Medical Center); Catherine Haskins-Kiefer, MSN, RN, NE-BC, Pamela Hendricks, MSN, RN, CCRN, Jeanette Green, and Robin Barron-Nelson, MSN, RN (Florida Hospital for Children); Steven Baisch, MD, Jody Evenson, and Heather Wendorf, MPH, CCRC (Gillette Children’s Hospital); David McKinley, MD and Jennifer Sankey, RN (Janet Weis Children’s Hospital Geisinger Medical Center); Melania Bembea, MD, MPH, Corina Noje, MD, and Elizabeth White (Johns Hopkins University); Nicole O’Brien, MD and Tensing Maa, MD (Nationwide Children’s Hospital); Edward Truemper, MD, Machelle Zink, MEd, and Brenda Weidner, MD (Nebraska Medical Center); Katherine Biagas, MD and Monique Superville (New York Presbyterian Hospital/Columbia University); Chani Traube, MD and Charlene Carlo (NY Presbyterian Hospital-Weill Cornell Medical College); Neal Thomas, MD, MSc and Debbie Spear, RN, CCRN (Penn State Hershey Children’s Hospital); Sandra Buttram, MD and Aimee Franken, CPNP-AC (Phoenix Children’s Hospital); Tell Bennett, MD and Eun Hea Kim (Primary Children’s Hospital/University of Utah); Mara Nitu, MD and Christi Rider, LPN (Riley Hospital for Children); Monica S. Vavilala, MD and Dawn Lum (Seattle Children’s Hospital & Harborview Medical Center, University of Washington); Margaret Parker, MD, MCCM and Kathleen Culver, DNP, RN, CPNP-AC (Stony Brook University); Laura Loftis, MD and Nancy Jaimon, MSN, BSN (Texas Children’s Hospital); David Shellington, MD and Jennifer Foley (University of California, San Diego/Rady Children’s Hospital of San Diego); Jose Irazuzta, MD and Tricia Alleyne, MD (University of Florida College of Medicine); Scot Bateman, MD and Michael Sylvia, MD (University of Massachusetts Memorial Children’s Medical Center); Jill M. Cholette, MD (University of Rochester Medical Center); Douglas Willson, MD and Robin Kelly (University of Virginia Children’s Hospital); Jose Pineda, MD, Tina Hicks, Dana Middleton, and Tina Day, CCRC (Washington University School of Medicine); Simon Li, MD (Westchester Medical Center); Sarah Kandil, MD and John Giuliano, MD (Yale University). Canada: Peter Skippen, MD, David Wensley, and Gordon Krahn (BC Children’s Hospital); Macha Bourdages, MD, Marc-Andre Dugas, and Louise Gosselin (Centre Hospitalier Universitaire de Québec); Miriam Santschi, MD (Centre Hospitalier Universitaire de Sherbrooke); Douglas Fraser, MD and Chris Blom (Children’s Hospital, London Health Sciences Centre); Philippe Jouvet, MD, PhD, Nicole Poitras, Laurence Bertout, and Mariana Dumitrascu (Hôpital Ste-Justine, Montreal); Ronald Gottesman, MD and Karen Trudel, MDCM (McGill University Health Center, Montreal); Jamie Hutchison, MD, Sathishkumar Kandath, MD, Judith Van Huyse, RN, CCRP, and Kelly Fusco (The Hospital for Sick Children, Toronto). South America—Argentina: Pablo Niera, MD (Hospital de Ninos Ricardo Gutierrez); Thomas Iolster, MD (Hospital Universitario Austral). Brazil: Maria Barbosa, MD, Vanessa Soares, MD, MSc, and Fernanda Lima, MD (Rede D’Or). Chile: Raul Bustos Betanzo, MD (Hospital Guillermo Grant Benavente). Columbia: Mauricio Fernández Laverde, MD (CES Universidad). Peru: Rosario Becerra, MD (Instituto Nacional de Salud de Nino). Europe—France: Julia Guilbert, MD and Pierre-Louis Léger (Armand-Trousseau Children’s Hospital); Benedicte Ringuier, MD (Centre Hospitalier Universitaire D’Angers); Olivier Brissaud, MD (CHU de Bordeaux); Valerie Payen, MD (CHU de Grenoble); Christopher Milesi, MD (CHU de Montepellier); Jean-Michel Liet, MD, PhD and Arnaud Legrand (CHU Nantes); Audrey Breining, MD and Julie Bienz (Hôpital de Hautepierre/CHRU Strasbourg); Etienne Javouhey, MD, PhD, Tiphanie Ginhoux, PhD, and Sonia Courtil-Teyssedre, MD (EPICIME-CIC 1407 de Lyon, Inserm, Service de Pharmacotoxicologie, CHU-Lyon, F-69677, Bron, France); Jean Bergounioux, MD (Hôpital Necker Enfants Malade); Philippe Sachs, MD (Hôpital Robert Debré); Francis Leclerc, MD, PhD and Marie-Emilie Lampin, MD (University Hospital of Lille). Italy: Angela Amigoni, MD and Antonio Marzollo, MD (University of Padua). Latvia: Arta Barzdina, MD (University Children’s Hospital Riga). Netherlands: Dick Tibboel, MD and Karin Geleijns, MD, PhD (Erasmus Medical Center); Sjef van Gestel, MD (University Medical Center Utrecht). Portugal: Alexandra Dinis, MD (Hospital Pediátrico de Coimbra). Spain: Juan García-Iñiguez, MD, PhD and Paula Madurga-Revilla, MD (Children’s Hospital Miguel Servet of Zaragoza); Federico Martinon-Torres, MD, PhD and Maria José De Castro (Hospital Clínico Universitario de Santiago de Compostela); Jesus Lopez-Herce, MD and Javier Urbano (Hospital General Universitario Gregorio Marañón de Madrid and Red SAMID); Patricia García-Soler, MD (Hospital Regional Universitario Materno Infantil de Málaga); Francisco Fernandez-Carrion, MD (Hospital Universitario de Salamanca); Romy Rossich, MD (Hospital Vall Hebron); David Arjona, MD and Raul Borrego (Hospital Virgen de la Salud). Switzerland: Oliver Karam, MD, MSc (Geneva University Hospital). Turkey: Oguz Dursun, MD and Hakan Tekguc, MD (Akdeniz University School of Medicine); Tanil Kendirli, MD, Caglar Odek, MD, and Ayhan Yaman, MD (Ankara University School of Medicine); Ali Arslankoylu, MD (Mersin University Faculty of Medicine). United Kingdom: Lyvonne Tume, RN, PhD (Alder Hey Children’s NHS Foundation Trust); Barney Scholefield, MBBS, MRCPH, PhD and Helen Winmill (Birmingham Children’s Hospital); Sarah Morley, MD, Deborah White, and Bina Mukhtyar (Cambridge University Hospitals NHS Trust); Rachel Agbeko, MD, PhD, FRCPCH (Great North Children’s Hospital Newcastle upon Tyne); Mark Peters, MD and Amy Jones (Great Ormond Street Hospital); David Inwald, MB, FRCPCH, Amy Brewer, and Amina Abdulla (Imperial College Healthcare NHS Trust); Akash Deep, MD, FRCPCH and Eniola Nsirim (King’s College Hospital); Alison Shefler, MD and Rohit Joshi, MBBS (Oxford University Hospitals NHS Trust); Gnanalingham Muhuntha, FRCPCH, FFICM, PhD, Philip Hudnott, MD, and Maria MacDonald (Royal Manchester Children’s Hospital); John Pappachan, MA, MBBChir, FRCA (Southampton General Hospital); Martin Peter Gray, MRCP, FFICM (St. Georges Hospital); Kay Rushforth, MD (The General Infirmary at Leeds). Arabian Peninsula—Oman: Anas-Alwogud Abdelmogheth, MD, AL Futaisi Amna Mohamed, Naga Ram Dhande, Rana Ali Abdulrahim, Safiya Saleh, and Safia Al-Hasani (Sultan Qaboos University Hospital). Africa—South Africa: Andrew Argent, MD and Shamiel Salie (University of Cape Town, School of Child and Adolescent Health/Red Cross War Memorial Hospital). India: Suchitra Ranjit, MD and Indira Jayakumar, DCH, DNB (Apollo Children’s Hospital); Shrishu Kamath, MD and Anitha V. P., DCH (Mehta Children’s Hospital). China: Hon Ming Cheung, MD (Prince of Wales Hospital, Hong Kong); Ying Wang, MD (Shanghai Children’s Medical Center). Oceana—Australia: Marino Festa, MBBS, MRCP, MD(Res), FCICM, Karen Walker, RGN, RSCN, BAppSC, MN, PhD, and Nicola Watts, Bpsyc (Hons), PhD (Children’s Hospital at Westmead); Simon Erickson, MD, FFICANZCA, FCICM (Princess Margaret Hospital for Children); Anthony Slater, MB BS, FCICM and Debbie Long (Royal Children’s Hospital-Brisbane); Warwick Butt, MD and Carmel Delzoppo (Royal Children’s Hospital-Melbourne); Michael Yung, MD, Subodh Ganu, MBBS, MD, FCICM, MClinEpi, and Georgia Letton (Women and Children’s Hospital Adelaide). New Zealand: John Beca, MBChB, Claire Sherring, Miriam Rea, and Tracey Bushell (Starship Children’s Hospital).
child; epidemiology; international; neurocritical care; outcomes