Pediatric Anesthesia ISSN 1155-5645
REVIEW ARTICLE
Update on pediatric neurocritical care Robert C. Tasker Departments of Neurology and Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children’s Hospital and Harvard Medical School, Boston, MA, USA
Keywords critical care; neurological disease; neurosurgery Correspondence Robert C. Tasker, Departments of Neurology and Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children’s Hospital and Harvard Medical School, 300 Longwood Avenue, Bader 627, Boston, MA 02115, USA Email: [email protected] Section Editor: Sulpicio Soriano
Summary Paralytic poliomyelitis, Reye syndrome, Hemophilus Influenzae type B epiglottitis, bacterial meningitis, and meningococcal septic shock are catastrophic illnesses that in the last 60 years have shaped the development of pediatric intensive care. Neurocritical care has been at the forefront of our thinking and, more latterly, as a specialty we have had the technology and means to develop this focus, educate the next generation and show that outcomes can be improved—first in adult critical care and now the task is to translate these benefits to critically ill children. In our future we will need to advance interventions in patient care with clinical trials. MeSH terms: Neurocritical care; child; traumatic brain injury; status epilepticus; cerebrovascular
Accepted 5 March 2014 doi:10.1111/pan.12398
Background In England and Wales, the approximate number of children requiring admission to a Pediatric Intensive Care Unit (PICU) is 10 000 per year (1). This number translates to ~100 per 100 000 child population per year. We can double this figure to ~200 per 100 000 child population per year if we also include those children requiring what is commonly called high-dependency care, which approximates the population statistic for admission to a PICU in the United States (US). Critically ill children with cardiac disease account for 50% of this population. Children with acute neurologic illness account for 17% of all critical care in children: the four separate categories of patients include neurosurgery, neurotrauma, and neurovascular (7% of the entire population); general critical care for children with chronic encephalopathy or neurogenetic, neurologic, or peripheral nervous system disease (3% of population); acute neurology of critical illness (4% of population); and, seizures or status epilepticus (3% of population). Given the volume of practice, it is no surprise that the medical and perioperative specialty of cardiac intensive care has developed, and in many large institutions © 2014 John Wiley & Sons Ltd
separated from PICU into an interdisciplinary service involving cardiology, cardiothoracic surgery, anesthesia, and intensive care. In contrast, the field of pediatric Neurocritical Care (NCC) has not, as yet, become a specialized practice or subspecialty of pediatric critical care. This narrative review will consider the history of NCC, the evolution and scope of current pediatric NCC practice, and future issues in development of the specialty. An historical perspective Modern day NCC had its origins both sides of the Atlantic. The history follows a trajectory that is worth reflection as we can see why and how the field has developed in adult practice (2). Ingenuity and innovation In 1926, Philip Drinker—a specialist in studies of industrial environments, air and dust analysis, ventilation, and illumination—worked on mechanical life-support in the event of industrial asphyxial accidents, such as gas poisoning and electric shock (3). By 1928, he and Louis Shaw, a physiologist, had built and tested on themselves 1
Neurocritical care
a new type of respirator device. In their metal tank device, a subject could be placed with their head protruding through a rubber collar attached to the open end and have breathing supported by vacuum-cleaner blowers that induced time-cycled changes in pressure. These experiments were carried out within yards of Boston Children’s Hospital. Notables such as Harvey Cushing had attended demonstrations of the device in action. On the afternoon of 13 October 1928, the tank respirator that Drinker and Shaw had tested on themselves was used on an 8-year-old girl with intercostal and pectoral muscle paralysis secondary to poliomyelitis (4). The child was under the care of Charles McKhann (5). At first, she did not need support from the device, but by the following morning her diaphragm was paralyzed and she was comatose and cyanosed. She regained consciousness within minutes of starting full supportive ventilation. The effect was so dramatic that those who witnessed it were brought to tears (3). Apparently, the child even asked for ice cream later in the day. Sadly, she died a few days later, but the principle of external assisted ventilation was established and news of the ‘mechanical respirator’ spread across the Atlantic. In 1938, most countries in Europe had a number of ‘iron lungs’ and in England Lord Nuffield supplied every hospital with a basic ‘Both’ device (6). Education and the prepared mind Bjørn Ibsen, a graduate of Copenhagen University, traveled to Boston for fellowship education in anesthesiology at Massachusetts General Hospital in 1949. During the voyage back to Copenhagen in 1950, his wife met Mogens Bjørneboe, who was deputy to Henry Lassen, the Chief Physician of Blegdams Fever Hospital (7). Two years later, the Blegdams Hospital was to become the center for one of the world’s largest local polio epidemics and the earlier meeting between Ibsen and Bjørneboe proved to be highly significant. At the Blegdams Hospital between 24 July and 25 August 1952, 31 patients with bulbar polio had been treated with the tank and cuirass respirators, but 27 (87%) had died (7,8). On 25 August, there was a hospital conference, at which the hospital’s leading physicians met to discuss why patients were dying and the impending disaster in public health. Lassen, Poul Astrup, head of the hospital laboratory, and Bjørneboe attended the meeting. Ibsen was also invited, though reluctantly: he did not work at the hospital and his operating room expertise was only just emerging as a clinical specialty and so still held in low regard. One of the observations considered at the meeting was that polio patients died with high total carbon dioxide (CO2) in their blood, as 2
R.C. Tasker
measured by the Van Slyke manometric method (9). At the time, this finding was interpreted as meaning metabolic alkalosis. Ibsen commented that the blood finding could equally reflect retention of CO2. After the meeting, Ibsen examined some patients and looked at specimens from four autopsies. He was convinced that the patients had died from lack of ventilation. Such a conclusion was significant, as the physicians had used the presence of cyanosis as a guide to assist patients’ breathing and give oxygen. If Ibsen was correct, they had overlooked the accumulation of CO2 from inadequate gas exchange. Ibsen proposed that patients be given a tracheostomy with an airtight seal to protect the airway and enable pulmonary toilet. He also suggested adding a CO2-absorber and using a gas mixture of equal parts of oxygen and nitrogen during manual ventilation. In essence, he applied operating room techniques to patients who were behaving as though they had been paralyzed with curare for an operation (10). On 26 August 1952, this technique was tested in a 12-year-old girl thought to be dying of quadriparetic polio. Ibsen’s hypothesis was correct; total CO2 content in her serum halved during manual positive pressure ventilation and her exhaled CO2 level gradually rose again during negative pressure ventilation. The next day, Astrup confirmed Ibsen’s prediction that patients with terminal stage bulbar polio were acidotic, not alkalotic, by using a newly developed pH electrode to measure pH in blood directly (9). This new intervention led Lassen to conclude, ‘this method has reduced the mortality-rate from above 80 to about 40%’ (8,11). Tracheostomy and manual bag ventilation became known as intermittent positive pressure ventilation. News of the work in Copenhagen spread, just as Drinker and McKhann’s experience had done some 25 years earlier. In Oxford, Lassen’s report led to an important collaboration between the departments of Neurology and Anesthetics. The two professors, W. Ritchie Russell (Neurology) and Robert Macintosh (Anesthetics), each provided a specialist to manage the newly formed ‘Respiration Unit’, namely John Spalding and Alex Crampton Smith, respectively. Within 10 years, a new field was defined by this neurology and anesthesia collaboration with one of the earliest books on the ‘Clinical Practice and Physiology of Artificial Respiration’ (12). New practices and a viable organization The development of Adult NCC practice in the modern era did not happen in a void. A critical illness—paralytic poliomyelitis—necessitated a healthcare response. To some extent, serendipity played its part. Also, there was the influence of having the right person, with the right © 2014 John Wiley & Sons Ltd
R.C. Tasker
education and knowledge, available to provide a unique perspective—a product of world-class fellowship education. Last, there was the foresight and good sense in applying a collaborative academic strategy to a new paradigm of clinical care. The next phase in the development of NCC in adult medicine was coordination of practices, demonstration of ‘benefit’ and the undertaking of randomized clinical trials (RCTs) to improve patient care. By 2013, in the US, there were 115 adult NCC units (NCCU) run by fellowship-educated neurointensivists (13), and 1-in-3 American adults were within 90 min of one of these units by ground transportation (14). The who, when, and why of admission for adult NCC is now well documented and understood (15), and the approach to investigating and managing common neurological conditions needing critical care is taught in recognized fellowshipeducation programs (13–16). It is also clear that in adults there is sufficient burden of disease to warrant cohorting such patients in NCCUs where the primary role is to manage acute neurological emergencies in the most effective way. As confirmation of the standard required for delivering NCC, the Leapfrog Group in the US announced in 2008 its recognition of practitioners in this field—that is, neurointensivists as being ‘specialists classified as neurologists and neurological surgeons who are board certified in their primary specialty and who have completed a United Council for Neurologic Subspecialties certified fellowship training program in NCC, or a physician who is board certified in NCC’ (17). The caseload in adult NCC practice includes patients who have compromise in control of airway, respiratory, bulbar, and hemodynamic systems, all in the context of acute neurological illness.
Neurocritical care
developed in different tertiary care hospitals for providing specialist NCC for such children (2). First, the adult model of a neurointensivist-led distinct NCCU (26,27) may be reproduced in centers with a large neurosurgical practice. Second, a special interest group led by critical care medicine faculty may be developed in centers with significant neurotrauma practice (23,28). Third, a combination of the above models into an operational policy that suits the resources, service, and educational needs of local PICU and hospital practice (2,25) may be used. Each model, however, has to overcome the problems of patient volume, need for multiple organ-system support, and a critical mass of clinical expertise. In the pediatric model described by Bell et al. (23), the institution developed a multidisciplinary group consisting of a critical care medicine attending, a neurologist, and a neurosurgeon to provide NCC in the PICU. In contrast, in the model described by LaRovere et al. (25), the institution developed a separate neurology consulting team for the hospital’s five intensive care units. Unlike adult NCC practice, which has evolved into a distinct discipline as a subspecialty of critical care medicine, these two pediatric models function as a multidisciplinary, cohesive group of specialists. That is, the critical care medicine physicians coordinate care and assume full responsibility for cardiorespiratory support, cerebral resuscitation, and neuroprotection, and pediatric subspecialists provide consultative services (29). To this end, these models also recognize that continuity of care is required following PICU and hospital discharge, and planning for long-term care is required in a significant proportion of cases. From the family’s perspective, to have professionals who have been with their child throughout the hospital stay advocating for them can only be beneficial.
The evolution of pediatric NCC practice Acute, severe neurological and neurosurgical diseases are significant causes of death in the PICU (18–20). The type of critical condition encountered in this population includes brain tissue herniation, hypoxic-ischemic injury, hemorrhage, trauma, tumor, epilepsy, and peripheral neuromuscular disorders (18–25). The specific conditions that have been formative in our development and engaged our research in the past include Reye syndrome, traumatic brain injury (TBI), drowning, postresuscitation neurologic disease and cardiac arrest, and meningitis. Models of pediatric NCC practice Over recent years, most of our focus has been on better care for severe TBI and three potential models have © 2014 John Wiley & Sons Ltd
Present day scope of pediatric NCC practice In general, pediatric NCC practice is now a collective expertise of multiple disciplines (e.g., critical care, neuroanesthesia, neurology, neurosurgery, neuroradiology, and neurorehabilitation) and the issue that we deal with each day is how best to coordinate patient care throughout the child’s hospital admission. Whether the local caseload and referral pattern warrant specialization and management of patients in a cohort or a separate unit is a local decision, and to date there are no stand-alone pediatric NCCUs. Rather, around the US, some PICUs have developed a subsidiary team within their faculty focused on the care of patients suffering TBI, other PICUs have a team focused on monitoring and developing designated beds for seizure care and continuous electroencephalography (cEEG), and others have a team 3
Neurocritical care
focused on postoperative neurosurgery and cerebrovascular care. Traumatic brain injury Tasker et al. (30) examined the healthcare system in England and Wales from 2004 to 2008 for 2575 critically ill children with severe TBI admitted to any of 27 PICUs. The authors found that the lowest-volume sector, with little or no pediatric neurosurgical activity on the unit, exhibited worse than expected outcome, particularly in those patients undergoing intracranial pressure (ICP) monitoring. The best outcomes were seen in PICUs in the mid-volume sector (i.e., 20–40 cases per year) rather than the highest-volume sector. It was not clear what accounted for this hierarchy in performance. The major difference in outcomes was seen in those undergoing ICP monitoring, yet there was no difference in the surrogate markers of this practice such as use of inotropes or duration of stay. The authors were not able to address system factors such as co-location with an adult neurotrauma center, the nature of neurosurgical involvement and supervision of intensive care, staffing levels, or standardized medical management. Recently, Pineda et al. (28) reported the results of their pediatric NCC program within the PICU focused on patients with severe TBI. The program was implemented in 2005, and involved ‘a coordinated communication and activity of PICU staff and physician faculty and trainees in several disciplines (critical care, neurosurgery, surgery, anesthesia, and radiology) and was implemented through a detailed training program, an explicit process for maintenance of pathway fidelity, and continuous quality improvement.’ The supplementary appendix to the paper describes the details of the pathway and the approach taken by the team at St Louis Children’s Hospital. The center cares for 20–40 patients with severe TBI each year, and the report focused on a before-and-after analysis using data from 123 patients (~10 per year after excluding those with abusive head trauma, Glasgow Coma Scale score 3 and fixed and dilated pupils at presentation, preadmission cardiac arrest, and gunshot wounds to the head). By using an ordered probit statistical model to assess adjusted outcome as a function of initial severity, the authors came to the conclusion that outcomes for children with TBI can be improved by altering the system of care. Monitoring and treatment of seizures and status epilepticus Continuous EEG monitoring is being used in adult NCC practice with increasing frequency, and up to 48% 4
R.C. Tasker
of critically ill patients have nonconvulsive seizures (31,32). In recent overviews of pediatric NCC practice, EEG was needed in 35% and 50% of cases, as reported by Bell et al.(23) and LaRovere et al.(25), respectively. LaRovere et al. (25) also reported that cEEG was used in one-quarter of their EEG studies. Seizures may be difficult to detect in comatose critically ill children, especially if the episode is subtle or when neuromuscular blocking agents are used during mechanical ventilation. In these and similar situations, brief EEG seizure (ES) activity or more prolonged episodes of EEG status epilepticus (ESE) may occur. However, to date, the clinical significance of ES and ESE remains largely unknown, including, for example, whether the relationship of such activity to outcome is independent of the underlying cause or even whether treatment is advisable. There is a wide range in prevalence of ES and ESE in the recent PICU literature, which likely reflects the case-mix in different series (33–44). Groups at high risk for ES are patients with epilepsy, central nervous system infection, structural brain lesions, encephalopathy after cardiac arrest, and TBI. Recently, Topjian et al. (44) reported a PICU series of 200 patients undergoing cEEG monitoring during acute encephalopathy (in the setting of primary brain disorder), ESE was observed in 21.5% and ES alone was found in 20.5% of cases. Prevalence of ESE and ES also depended on diagnosis (56% in epilepsy, 45% in encephalitis, 36% in hypoxic-ischemic encephalopathy after cardiac arrest, and 31% in TBI), and in the whole series, ESE rather than ES alone was associated with worsened outcome. The implication was that controlling or treating these events by first identifying them and then administering medications would lead to better outcomes. At present, however, this logic and the need for such monitoring is undertaken only to some and not all of us in the field (45). Imagine the consequences of deciding that all comatose and deeply sedated patients on the PICU necessitated cEEG monitoring. Instituting such a service would require significant resources, and if we think it is really necessary, then it ought to be available nights and weekends. Also, as it is not cEEG monitoring per se that improves outcome, but possibly our interventions guided by this technology, we would also need to focus on the value of ES/ESE goal-directed therapy. Who is going to provide the technical and diagnostic support? In some PICUs this support is provided by the extended NCC consult service, but not all units have this resource. Alternatively, is it time that some epileptologists in training develop an interest in cEEG monitoring in the PICU? © 2014 John Wiley & Sons Ltd
R.C. Tasker
Other special interest populations and practices The other specialist practices that are developing in some centers of pediatric NCC include neurooncology, perioperative neurosurgery, and neurovascular. These developments depend on referral practice. For example, 30% of cases described by LaRovere et al. (25) were perioperative neurosurgical patients. The future of pediatric NCC as a discipline The brain is the vital organ and, unfortunately, all too vulnerable during critical illness (46). Hence, the future of pediatric critical care medicine is intricately linked to the future of pediatric NCC—the brain is our final frontier. However, the mere presence of a neurointensivist will not of itself lead to improvements in outcomes. Rather, if we think about this field as a development in the PICU, then a significant volume of practice is needed to justify this focus; that is, developing a pathway of care, improving communications, auditing practice, and championing innovations in practice. Training a specialist for pediatric NCC Each of the models and scope of practice in so-called pediatric NCC described in the previous section has to be applicable to the educational needs of specialists in training and their likely future practice. Certain clinical realities need to be addressed at each institution. Higher professional training in pediatric critical care medicine, neurology, neuroanesthesia, or neurosurgery is not sufficient for the needs of ‘neurocritical care’ patients as they follow a clinical pathway from admission to hospital discharge. For example, these patients have high-acuity illness that is not usually managed by pediatric neurology trainees: 57% of patients are supported by mechanical ventilation, 45% have coexisting general medical or surgical diagnoses, and 7% die, which is four times the rate of death observed in the general pediatric intensive care unit population (25). A significant proportion of these patients remain in the hospital for a prolonged period, have poor outcome, and require neurology and rehabilitative inpatient support not usually managed by trainees in pediatric critical care or neuroanesthesia. These realities have significant implications for education and training for the main stakeholders in the fields of NCC, critical care, neurology, neuroanesthesia and neurosurgery. Training programs in pediatric critical care medicine, neurology, neuroanesthesia, neurosurgery, and other interested disciplines may consider devising curriculum and practice tracks/pathways. For example, the © 2014 John Wiley & Sons Ltd
Neurocritical care
principles, fundamental practices and skills needed to create a multidisciplinary group of healthcare providers with a common understanding of each other’s perspective and language. How each subspecialty ultimately dovetails with critical care will likely depend on local resources and needs. Creating a group of providers who can ensure high-quality care for critically ill children and their families from admission through followup in the outpatient setting should be one overarching goal for the delivery of pediatric NCC. In essence, borrowing a framework from the cardiac intensive care model. Addressing the question of benefit of NCC practices Does care differ for neurological patients admitted to a PICU that has a neurointensivist vs one that does not? What is the impact of a specialized NCC team on the outcome of critically ill patients? Does the NCC team improve resource utilization and fiscal benefits? These questions are impossible to answer in the pediatric field as we have no data. However, there are data in adults. Kramer and Zygun systematically searched the literature and identified 12 studies, involving almost 25 000 patients, which presented original data comparing models of care for adult NCC patients (47). The results showed that in specialized NCCUs mortality was lower and neurologic outcomes were improved. Elsewhere, others have described additional benefits to having a neurointensivist-led team for NCC patients; these include reduced length of stay, cost savings, less need for ventriculoperitoneal shunts in subarachnoid patients, improved documentation, and increased organ and tissue donation rates. Pediatric ‘neurointensivists’ now need to demonstrate the same. Developing a patient-centered pediatric NCC research agenda Undertaking RCTs helped adult NCC practice thrive, and resulted in better care for patients. For example, current clinical projects involve patients with stroke, status epilepticus, neuromuscular respiratory failure, intracerebral hemorrhage, intraventricular hemorrhage, hydrocephalus, subarachnoid hemorrhage, TBI, and spinal cord injury (13). In contrast to adult practice, even though pediatric critical care specialists have undertaken RCTs (236 in the period 1986–2012) (48), there are too few in pediatric NCC. For example, in the best-studied area—pediatric TBI—there have been five RCTs of hypothermia therapy (49) involving, in total, only 400 patients (which is grossly underpowered (50)). Taking these studies 5
Neurocritical care
R.C. Tasker
together, the risk ratio of death in the hypothermia group compared with the normothermia group was not statistically significant, and there was a suggestion of increased risk of death with hypothermia therapy. Therefore hypothermia for severe TBI is not recommended. So where does that leave us for the future? Recently, the US National Institutes of Health has started a comparative effectiveness research (CER) study (UO1NS081041) in severe TBI that aims to recruit 1000 children managed in the US and Europe over the next three years. CER measures difference in outcome and relates it to the package of care and its constituent components. The idea is to capture what actually happens in patients and identify future best practices and hypotheses for research.
Acknowledgments RC Tasker receives support from the NIH (UO1N S081041). Funding This research was carried out without funding. Conflicts of interest RC Tasker has no conflicts of interest.
References 1 Paediatric Intensive Care Audit Network. PICANet 2013 summary report. Available at: http://www.picanet.org.uk. Accessed 5 March, 2014. 2 Tasker RC. Pediatric neurocritical care: is it time to come of age? Curr Opin Pediatr 2009; 21: 724–730. 3 Drinker PA, McKhann CF. The iron lung: first practical means of respiratory support. JAMA 1986; 255: 1476–1480. 4 Drinker P, Shaw LA. An apparatus for the prolonged administration of artificial respiration: I. A design for adults and children. J Clin Invest 1929; 7: 229–247. 5 Drinker P, McKhann CF. The use of a new apparatus for prolonged administration of artificial respiration: I. A fatal case of poliomyelitis. JAMA 1929; 92: 1658–1660. 6 Dr John Spalding in Conversation. Oxford Medicine, 2005: 4–6. Available at: http:// www.medsci.ox.ac.uk/oma/oxmed/oxmedjul2005. Accessed 19 March, 2014. 7 Richmond C. Obituaries: Bjørn Ibsen. BMJ 2007; 335: 674. 8 Lassen HCA. A preliminary report on the 1952 epidemic of poliomyelitis in Copenhagen with special reference to the treatment of acute respiratory failure. Lancet 1953; 1: 37– 41. 9 Severinghaus JW, Astrup P, Murray JF. Blood gas analysis and critical care medicine. Am J Respir Crit Care Med 1998; 157: S114– S122. 10 West JB. The physiological challenges of the 1952 Copenhagen poliomyelitis epidemic and a renaissance in clinical respiratory physiology. J Appl Physiol 2005; 99: 424–432. 11 Trubuhovich RV. In the beginning: the 1952–1953 Danish epidemic of poliomyelitis and Bjørn Ibsen. Crit Care Resusc 2003; 5: 227–230.
6
12 Spalding JMK, Crampton Smith A. Clinical Practice and Physiology of Artificial Respiration. Oxford: Blackwell Scientific Publications, 1963. 13 Neurocritical Care Society. Available at: http://maps.google.com/maps/ms? ie=UTF8&hl=en&msa=0&msid=108542175118493601623. 00047fcc91780cd976daf&ll=33.000884,-111. 965918&spn=29.210936,91.784334&source=embed. Accessed 5 March, 2014. 14 Ward MJ, Shutter LA, Branas CC et al. Geographical access to US neurocritical care units registered with the Neurocritical Care Society. Neurocrit Care 2012; 16: 232–240. 15 Howard RS, Kullmann DM, Hirsch NP. Admission to neurological intensive care: who, when, and why? J Neurol Neurosurg Psychiatry 2003; 74: 2–9. 16 Howard RC. Neurological problems on the ICU. Clin Med 2007; 7: 148–153. 17 Mirski MA. Leapfrog jumps on board with neuro-intensivists. Currents 2008; 3: 1–9. 18 Sands R, Manning JC, Vyas H et al. Characteristics of deaths in paediatric intensive care: a 10-year study. Nurs Crit Care 2009; 14: 235–240. 19 Au AK, Carcillo JA, Clark RS et al. Brain injuries and neurological system failure are the most common proximate causes of death in children admitted to a pediatric intensive care unit. Pediatr Crit Care Med 2011; 12: 566–571. 20 Namachivayam P, Shann F, Shekerdemian L et al. Three decades of pediatric intensive care: who was admitted, what happened in intensive care, and what happened afterward. Pediatr Crit Care Med 2010; 11: 549–555. 21 Michaud LJ, Rivara FP, Grady MS et al. Predictors of survival and severity of disability after severe brain injury in children. Neurosurgery 1992; 31: 254–264.
22 Lopez Pison J, Galvan Manso M, Rubio Morales L et al. Descriptive analysis of neurological disorders in the pediatric intensive care unit of a regional reference hospital. An Esp Pediatr 2000; 53: 119–124. 23 Bell MJ, Carpenter J, Au AK et al. Development of a pediatric neurocritical care service. Neurocrit Care 2009; 10: 4–10. 24 Spentzas T, Escue JE, Patters AB et al. Brain tumor resection in children: neurointensive care unit course and resource utilization. Pediatr Crit Care Med 2010; 11: 718–722. 25 LaRovere KL, Graham RJ, Tasker RC; Pediatric Central Nervous System program (pCNSp). Pediatric neurocritical care: a neurology consultation model and implication for education and training. Pediatr Neurol 2013; 48: 206–211. 26 Suarez JI, Zaidat OO, Suri MF et al. Length of stay and mortality in neurocritically ill patients: impact of a specialized neurocritical care team. Crit Care Med 2004; 32: 2311– 2317. 27 Varelas PN, Conti MM, Spanaki MV et al. The impact of a neurointensivist-led team on a semiclosed neurosciences intensive care unit. Crit Care Med 2004; 32: 2191–2198. 28 Pineda JA, Leonard JR, Mazotas IG et al. Effect of implementation of a paediatric neurocritical care programme on outcomes after severe traumatic brain injury: a retrospective cohort study. Lancet Neurol 2013; 12: 45–52. 29 Scher M. Proposed cross-disciplinary training in pediatric neurointensive care. Pediatr Neurol 2008; 39: 1–5. 30 Tasker RC, Fleming TJ, Young AE et al. Severe head injury in children: intensive care unit activity and mortality in England and Wales. Br J Neurosurg 2011; 25: 68–77. 31 Claassen J, Mayer SA, Kowalski RG et al. Detection of electrographic seizures with © 2014 John Wiley & Sons Ltd
Neurocritical care
R.C. Tasker
32
33
34
35
36
37
continuous EEG monitoring in critically ill patients. Neurology 2004; 62: 1743–1748. Friedman D, Claassen J, Hirsch LJ. Continuous electroencephalogram monitoring in the intensive care unit. Anesth Analg 2009; 109: 506–523. Hosain SA, Solomon GE, Kobylarz EJ. Electroencephalographic patterns in unresponsive pediatric patients. Pediatr Neurol 2005; 32: 162–165. Jette N, Claassen J, Emerson RG et al. Frequency and predictors of nonconvulsive seizures during continuous electroencephalographic monitoring in critically ill children. Arch Neurol 2006; 63: 1750– 1755. Saengpattrachai M, Sharma R, Hunjan A et al. Nonconvulsive seizures in the pediatric intensive care unit: etiology, EEG, and brain imaging findings. Epilepsia 2006; 47: 1510– 1518. Hyllienmark L, Amark P. Continuous EEG monitoring in a paediatric intensive care unit. Eur J Paediatr Neurol 2007; 11: 70–75. Carrera E, Claassen J, Oddo M et al. Continuous electroencephalographic monitoring in critically ill patients with central nervous sys-
© 2014 John Wiley & Sons Ltd
38
39
40
41
42
43
44
tem infections. Arch Neurol 2008; 65: 1612– 1618. Shahwan A, Bailey C, Shekerdemian L et al. The prevalence of seizures in comatose children in the pediatric intensive care unit: a prospective video-EEG study. Epilepsia 2010; 51: 1198–1204. Abend NS, Gutierrez-Colina AM, Topjian AA et al. Nonconvulsive seizures are common in critically ill children. Neurology 2011; 76: 1071–1077. McCoy B, Sharma R, Ochi A et al. Predictors of nonconvulsive seizures among critically ill children. Epilepsia 2011; 52: 1973–1978. Greiner HM, Holland K, Leach JL et al. Nonconvulsive status epilepticus: the encephalopathic pediatric patient. Pediatrics 2012; 129: e748–e755. Kirkham FJ, Wade AM, McElduff F et al. Seizures in 204 comatose children: incidence and outcome. Intensive Care Med 2012; 38: 853–862. Schreiber JM, Zelleke T, Gaillard WD et al. Continuous video EEG for patients with acute encephalopathy in a pediatric intensive care unit. Neurocrit Care 2012; 17: 31–38. Topjian AA, Gutierrez-Colina AM, Sanchez SM et al. Electrographic status epilepticus is
45
46
47
48
49
50
associated with mortality and worse shortterm outcome in critically ill children. Crit Care Med 2013; 41: 215–223. Abend NS, Dlugos DJ, Hahn CD et al. Use of EEG monitoring and management of nonconvulsive seizures in critically ill patients: a survey of neurologists. Neurocrit Care 2010; 12: 382–389. Tasker RC. Pediatric critical care, glycemic control, and hypoglycemia: what is the real target? JAMA 2012; 308: 1687–1688. Kramer AH, Zygun DA. Do neurocritical care units save lives? Measuring the impact of specialized ICUs. Neurocrit Care 2011; 14: 329–333. Duffett M, Choong K, Hartling L et al. Randomized controlled trials in pediatric critical care: a scoping review. Crit Care 2013; 17: R256. Hutchison JS, Guerguerian AM. Cooling of children with severe traumatic brain injury. Lancet Neurol 2013; 12: 527–529. Forsyth RJ, Parslow RC, Tasker RC et al. Prediction of raised intracranial pressure complicating severe traumatic brain injury in children: implications for trial design. Pediatr Crit Care Med 2008; 9: 8–14.
7
REVIEW ARTICLE
Update on pediatric neurocritical care Robert C. Tasker Departments of Neurology and Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children’s Hospital and Harvard Medical School, Boston, MA, USA
Keywords critical care; neurological disease; neurosurgery Correspondence Robert C. Tasker, Departments of Neurology and Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children’s Hospital and Harvard Medical School, 300 Longwood Avenue, Bader 627, Boston, MA 02115, USA Email: [email protected] Section Editor: Sulpicio Soriano
Summary Paralytic poliomyelitis, Reye syndrome, Hemophilus Influenzae type B epiglottitis, bacterial meningitis, and meningococcal septic shock are catastrophic illnesses that in the last 60 years have shaped the development of pediatric intensive care. Neurocritical care has been at the forefront of our thinking and, more latterly, as a specialty we have had the technology and means to develop this focus, educate the next generation and show that outcomes can be improved—first in adult critical care and now the task is to translate these benefits to critically ill children. In our future we will need to advance interventions in patient care with clinical trials. MeSH terms: Neurocritical care; child; traumatic brain injury; status epilepticus; cerebrovascular
Accepted 5 March 2014 doi:10.1111/pan.12398
Background In England and Wales, the approximate number of children requiring admission to a Pediatric Intensive Care Unit (PICU) is 10 000 per year (1). This number translates to ~100 per 100 000 child population per year. We can double this figure to ~200 per 100 000 child population per year if we also include those children requiring what is commonly called high-dependency care, which approximates the population statistic for admission to a PICU in the United States (US). Critically ill children with cardiac disease account for 50% of this population. Children with acute neurologic illness account for 17% of all critical care in children: the four separate categories of patients include neurosurgery, neurotrauma, and neurovascular (7% of the entire population); general critical care for children with chronic encephalopathy or neurogenetic, neurologic, or peripheral nervous system disease (3% of population); acute neurology of critical illness (4% of population); and, seizures or status epilepticus (3% of population). Given the volume of practice, it is no surprise that the medical and perioperative specialty of cardiac intensive care has developed, and in many large institutions © 2014 John Wiley & Sons Ltd
separated from PICU into an interdisciplinary service involving cardiology, cardiothoracic surgery, anesthesia, and intensive care. In contrast, the field of pediatric Neurocritical Care (NCC) has not, as yet, become a specialized practice or subspecialty of pediatric critical care. This narrative review will consider the history of NCC, the evolution and scope of current pediatric NCC practice, and future issues in development of the specialty. An historical perspective Modern day NCC had its origins both sides of the Atlantic. The history follows a trajectory that is worth reflection as we can see why and how the field has developed in adult practice (2). Ingenuity and innovation In 1926, Philip Drinker—a specialist in studies of industrial environments, air and dust analysis, ventilation, and illumination—worked on mechanical life-support in the event of industrial asphyxial accidents, such as gas poisoning and electric shock (3). By 1928, he and Louis Shaw, a physiologist, had built and tested on themselves 1
Neurocritical care
a new type of respirator device. In their metal tank device, a subject could be placed with their head protruding through a rubber collar attached to the open end and have breathing supported by vacuum-cleaner blowers that induced time-cycled changes in pressure. These experiments were carried out within yards of Boston Children’s Hospital. Notables such as Harvey Cushing had attended demonstrations of the device in action. On the afternoon of 13 October 1928, the tank respirator that Drinker and Shaw had tested on themselves was used on an 8-year-old girl with intercostal and pectoral muscle paralysis secondary to poliomyelitis (4). The child was under the care of Charles McKhann (5). At first, she did not need support from the device, but by the following morning her diaphragm was paralyzed and she was comatose and cyanosed. She regained consciousness within minutes of starting full supportive ventilation. The effect was so dramatic that those who witnessed it were brought to tears (3). Apparently, the child even asked for ice cream later in the day. Sadly, she died a few days later, but the principle of external assisted ventilation was established and news of the ‘mechanical respirator’ spread across the Atlantic. In 1938, most countries in Europe had a number of ‘iron lungs’ and in England Lord Nuffield supplied every hospital with a basic ‘Both’ device (6). Education and the prepared mind Bjørn Ibsen, a graduate of Copenhagen University, traveled to Boston for fellowship education in anesthesiology at Massachusetts General Hospital in 1949. During the voyage back to Copenhagen in 1950, his wife met Mogens Bjørneboe, who was deputy to Henry Lassen, the Chief Physician of Blegdams Fever Hospital (7). Two years later, the Blegdams Hospital was to become the center for one of the world’s largest local polio epidemics and the earlier meeting between Ibsen and Bjørneboe proved to be highly significant. At the Blegdams Hospital between 24 July and 25 August 1952, 31 patients with bulbar polio had been treated with the tank and cuirass respirators, but 27 (87%) had died (7,8). On 25 August, there was a hospital conference, at which the hospital’s leading physicians met to discuss why patients were dying and the impending disaster in public health. Lassen, Poul Astrup, head of the hospital laboratory, and Bjørneboe attended the meeting. Ibsen was also invited, though reluctantly: he did not work at the hospital and his operating room expertise was only just emerging as a clinical specialty and so still held in low regard. One of the observations considered at the meeting was that polio patients died with high total carbon dioxide (CO2) in their blood, as 2
R.C. Tasker
measured by the Van Slyke manometric method (9). At the time, this finding was interpreted as meaning metabolic alkalosis. Ibsen commented that the blood finding could equally reflect retention of CO2. After the meeting, Ibsen examined some patients and looked at specimens from four autopsies. He was convinced that the patients had died from lack of ventilation. Such a conclusion was significant, as the physicians had used the presence of cyanosis as a guide to assist patients’ breathing and give oxygen. If Ibsen was correct, they had overlooked the accumulation of CO2 from inadequate gas exchange. Ibsen proposed that patients be given a tracheostomy with an airtight seal to protect the airway and enable pulmonary toilet. He also suggested adding a CO2-absorber and using a gas mixture of equal parts of oxygen and nitrogen during manual ventilation. In essence, he applied operating room techniques to patients who were behaving as though they had been paralyzed with curare for an operation (10). On 26 August 1952, this technique was tested in a 12-year-old girl thought to be dying of quadriparetic polio. Ibsen’s hypothesis was correct; total CO2 content in her serum halved during manual positive pressure ventilation and her exhaled CO2 level gradually rose again during negative pressure ventilation. The next day, Astrup confirmed Ibsen’s prediction that patients with terminal stage bulbar polio were acidotic, not alkalotic, by using a newly developed pH electrode to measure pH in blood directly (9). This new intervention led Lassen to conclude, ‘this method has reduced the mortality-rate from above 80 to about 40%’ (8,11). Tracheostomy and manual bag ventilation became known as intermittent positive pressure ventilation. News of the work in Copenhagen spread, just as Drinker and McKhann’s experience had done some 25 years earlier. In Oxford, Lassen’s report led to an important collaboration between the departments of Neurology and Anesthetics. The two professors, W. Ritchie Russell (Neurology) and Robert Macintosh (Anesthetics), each provided a specialist to manage the newly formed ‘Respiration Unit’, namely John Spalding and Alex Crampton Smith, respectively. Within 10 years, a new field was defined by this neurology and anesthesia collaboration with one of the earliest books on the ‘Clinical Practice and Physiology of Artificial Respiration’ (12). New practices and a viable organization The development of Adult NCC practice in the modern era did not happen in a void. A critical illness—paralytic poliomyelitis—necessitated a healthcare response. To some extent, serendipity played its part. Also, there was the influence of having the right person, with the right © 2014 John Wiley & Sons Ltd
R.C. Tasker
education and knowledge, available to provide a unique perspective—a product of world-class fellowship education. Last, there was the foresight and good sense in applying a collaborative academic strategy to a new paradigm of clinical care. The next phase in the development of NCC in adult medicine was coordination of practices, demonstration of ‘benefit’ and the undertaking of randomized clinical trials (RCTs) to improve patient care. By 2013, in the US, there were 115 adult NCC units (NCCU) run by fellowship-educated neurointensivists (13), and 1-in-3 American adults were within 90 min of one of these units by ground transportation (14). The who, when, and why of admission for adult NCC is now well documented and understood (15), and the approach to investigating and managing common neurological conditions needing critical care is taught in recognized fellowshipeducation programs (13–16). It is also clear that in adults there is sufficient burden of disease to warrant cohorting such patients in NCCUs where the primary role is to manage acute neurological emergencies in the most effective way. As confirmation of the standard required for delivering NCC, the Leapfrog Group in the US announced in 2008 its recognition of practitioners in this field—that is, neurointensivists as being ‘specialists classified as neurologists and neurological surgeons who are board certified in their primary specialty and who have completed a United Council for Neurologic Subspecialties certified fellowship training program in NCC, or a physician who is board certified in NCC’ (17). The caseload in adult NCC practice includes patients who have compromise in control of airway, respiratory, bulbar, and hemodynamic systems, all in the context of acute neurological illness.
Neurocritical care
developed in different tertiary care hospitals for providing specialist NCC for such children (2). First, the adult model of a neurointensivist-led distinct NCCU (26,27) may be reproduced in centers with a large neurosurgical practice. Second, a special interest group led by critical care medicine faculty may be developed in centers with significant neurotrauma practice (23,28). Third, a combination of the above models into an operational policy that suits the resources, service, and educational needs of local PICU and hospital practice (2,25) may be used. Each model, however, has to overcome the problems of patient volume, need for multiple organ-system support, and a critical mass of clinical expertise. In the pediatric model described by Bell et al. (23), the institution developed a multidisciplinary group consisting of a critical care medicine attending, a neurologist, and a neurosurgeon to provide NCC in the PICU. In contrast, in the model described by LaRovere et al. (25), the institution developed a separate neurology consulting team for the hospital’s five intensive care units. Unlike adult NCC practice, which has evolved into a distinct discipline as a subspecialty of critical care medicine, these two pediatric models function as a multidisciplinary, cohesive group of specialists. That is, the critical care medicine physicians coordinate care and assume full responsibility for cardiorespiratory support, cerebral resuscitation, and neuroprotection, and pediatric subspecialists provide consultative services (29). To this end, these models also recognize that continuity of care is required following PICU and hospital discharge, and planning for long-term care is required in a significant proportion of cases. From the family’s perspective, to have professionals who have been with their child throughout the hospital stay advocating for them can only be beneficial.
The evolution of pediatric NCC practice Acute, severe neurological and neurosurgical diseases are significant causes of death in the PICU (18–20). The type of critical condition encountered in this population includes brain tissue herniation, hypoxic-ischemic injury, hemorrhage, trauma, tumor, epilepsy, and peripheral neuromuscular disorders (18–25). The specific conditions that have been formative in our development and engaged our research in the past include Reye syndrome, traumatic brain injury (TBI), drowning, postresuscitation neurologic disease and cardiac arrest, and meningitis. Models of pediatric NCC practice Over recent years, most of our focus has been on better care for severe TBI and three potential models have © 2014 John Wiley & Sons Ltd
Present day scope of pediatric NCC practice In general, pediatric NCC practice is now a collective expertise of multiple disciplines (e.g., critical care, neuroanesthesia, neurology, neurosurgery, neuroradiology, and neurorehabilitation) and the issue that we deal with each day is how best to coordinate patient care throughout the child’s hospital admission. Whether the local caseload and referral pattern warrant specialization and management of patients in a cohort or a separate unit is a local decision, and to date there are no stand-alone pediatric NCCUs. Rather, around the US, some PICUs have developed a subsidiary team within their faculty focused on the care of patients suffering TBI, other PICUs have a team focused on monitoring and developing designated beds for seizure care and continuous electroencephalography (cEEG), and others have a team 3
Neurocritical care
focused on postoperative neurosurgery and cerebrovascular care. Traumatic brain injury Tasker et al. (30) examined the healthcare system in England and Wales from 2004 to 2008 for 2575 critically ill children with severe TBI admitted to any of 27 PICUs. The authors found that the lowest-volume sector, with little or no pediatric neurosurgical activity on the unit, exhibited worse than expected outcome, particularly in those patients undergoing intracranial pressure (ICP) monitoring. The best outcomes were seen in PICUs in the mid-volume sector (i.e., 20–40 cases per year) rather than the highest-volume sector. It was not clear what accounted for this hierarchy in performance. The major difference in outcomes was seen in those undergoing ICP monitoring, yet there was no difference in the surrogate markers of this practice such as use of inotropes or duration of stay. The authors were not able to address system factors such as co-location with an adult neurotrauma center, the nature of neurosurgical involvement and supervision of intensive care, staffing levels, or standardized medical management. Recently, Pineda et al. (28) reported the results of their pediatric NCC program within the PICU focused on patients with severe TBI. The program was implemented in 2005, and involved ‘a coordinated communication and activity of PICU staff and physician faculty and trainees in several disciplines (critical care, neurosurgery, surgery, anesthesia, and radiology) and was implemented through a detailed training program, an explicit process for maintenance of pathway fidelity, and continuous quality improvement.’ The supplementary appendix to the paper describes the details of the pathway and the approach taken by the team at St Louis Children’s Hospital. The center cares for 20–40 patients with severe TBI each year, and the report focused on a before-and-after analysis using data from 123 patients (~10 per year after excluding those with abusive head trauma, Glasgow Coma Scale score 3 and fixed and dilated pupils at presentation, preadmission cardiac arrest, and gunshot wounds to the head). By using an ordered probit statistical model to assess adjusted outcome as a function of initial severity, the authors came to the conclusion that outcomes for children with TBI can be improved by altering the system of care. Monitoring and treatment of seizures and status epilepticus Continuous EEG monitoring is being used in adult NCC practice with increasing frequency, and up to 48% 4
R.C. Tasker
of critically ill patients have nonconvulsive seizures (31,32). In recent overviews of pediatric NCC practice, EEG was needed in 35% and 50% of cases, as reported by Bell et al.(23) and LaRovere et al.(25), respectively. LaRovere et al. (25) also reported that cEEG was used in one-quarter of their EEG studies. Seizures may be difficult to detect in comatose critically ill children, especially if the episode is subtle or when neuromuscular blocking agents are used during mechanical ventilation. In these and similar situations, brief EEG seizure (ES) activity or more prolonged episodes of EEG status epilepticus (ESE) may occur. However, to date, the clinical significance of ES and ESE remains largely unknown, including, for example, whether the relationship of such activity to outcome is independent of the underlying cause or even whether treatment is advisable. There is a wide range in prevalence of ES and ESE in the recent PICU literature, which likely reflects the case-mix in different series (33–44). Groups at high risk for ES are patients with epilepsy, central nervous system infection, structural brain lesions, encephalopathy after cardiac arrest, and TBI. Recently, Topjian et al. (44) reported a PICU series of 200 patients undergoing cEEG monitoring during acute encephalopathy (in the setting of primary brain disorder), ESE was observed in 21.5% and ES alone was found in 20.5% of cases. Prevalence of ESE and ES also depended on diagnosis (56% in epilepsy, 45% in encephalitis, 36% in hypoxic-ischemic encephalopathy after cardiac arrest, and 31% in TBI), and in the whole series, ESE rather than ES alone was associated with worsened outcome. The implication was that controlling or treating these events by first identifying them and then administering medications would lead to better outcomes. At present, however, this logic and the need for such monitoring is undertaken only to some and not all of us in the field (45). Imagine the consequences of deciding that all comatose and deeply sedated patients on the PICU necessitated cEEG monitoring. Instituting such a service would require significant resources, and if we think it is really necessary, then it ought to be available nights and weekends. Also, as it is not cEEG monitoring per se that improves outcome, but possibly our interventions guided by this technology, we would also need to focus on the value of ES/ESE goal-directed therapy. Who is going to provide the technical and diagnostic support? In some PICUs this support is provided by the extended NCC consult service, but not all units have this resource. Alternatively, is it time that some epileptologists in training develop an interest in cEEG monitoring in the PICU? © 2014 John Wiley & Sons Ltd
R.C. Tasker
Other special interest populations and practices The other specialist practices that are developing in some centers of pediatric NCC include neurooncology, perioperative neurosurgery, and neurovascular. These developments depend on referral practice. For example, 30% of cases described by LaRovere et al. (25) were perioperative neurosurgical patients. The future of pediatric NCC as a discipline The brain is the vital organ and, unfortunately, all too vulnerable during critical illness (46). Hence, the future of pediatric critical care medicine is intricately linked to the future of pediatric NCC—the brain is our final frontier. However, the mere presence of a neurointensivist will not of itself lead to improvements in outcomes. Rather, if we think about this field as a development in the PICU, then a significant volume of practice is needed to justify this focus; that is, developing a pathway of care, improving communications, auditing practice, and championing innovations in practice. Training a specialist for pediatric NCC Each of the models and scope of practice in so-called pediatric NCC described in the previous section has to be applicable to the educational needs of specialists in training and their likely future practice. Certain clinical realities need to be addressed at each institution. Higher professional training in pediatric critical care medicine, neurology, neuroanesthesia, or neurosurgery is not sufficient for the needs of ‘neurocritical care’ patients as they follow a clinical pathway from admission to hospital discharge. For example, these patients have high-acuity illness that is not usually managed by pediatric neurology trainees: 57% of patients are supported by mechanical ventilation, 45% have coexisting general medical or surgical diagnoses, and 7% die, which is four times the rate of death observed in the general pediatric intensive care unit population (25). A significant proportion of these patients remain in the hospital for a prolonged period, have poor outcome, and require neurology and rehabilitative inpatient support not usually managed by trainees in pediatric critical care or neuroanesthesia. These realities have significant implications for education and training for the main stakeholders in the fields of NCC, critical care, neurology, neuroanesthesia and neurosurgery. Training programs in pediatric critical care medicine, neurology, neuroanesthesia, neurosurgery, and other interested disciplines may consider devising curriculum and practice tracks/pathways. For example, the © 2014 John Wiley & Sons Ltd
Neurocritical care
principles, fundamental practices and skills needed to create a multidisciplinary group of healthcare providers with a common understanding of each other’s perspective and language. How each subspecialty ultimately dovetails with critical care will likely depend on local resources and needs. Creating a group of providers who can ensure high-quality care for critically ill children and their families from admission through followup in the outpatient setting should be one overarching goal for the delivery of pediatric NCC. In essence, borrowing a framework from the cardiac intensive care model. Addressing the question of benefit of NCC practices Does care differ for neurological patients admitted to a PICU that has a neurointensivist vs one that does not? What is the impact of a specialized NCC team on the outcome of critically ill patients? Does the NCC team improve resource utilization and fiscal benefits? These questions are impossible to answer in the pediatric field as we have no data. However, there are data in adults. Kramer and Zygun systematically searched the literature and identified 12 studies, involving almost 25 000 patients, which presented original data comparing models of care for adult NCC patients (47). The results showed that in specialized NCCUs mortality was lower and neurologic outcomes were improved. Elsewhere, others have described additional benefits to having a neurointensivist-led team for NCC patients; these include reduced length of stay, cost savings, less need for ventriculoperitoneal shunts in subarachnoid patients, improved documentation, and increased organ and tissue donation rates. Pediatric ‘neurointensivists’ now need to demonstrate the same. Developing a patient-centered pediatric NCC research agenda Undertaking RCTs helped adult NCC practice thrive, and resulted in better care for patients. For example, current clinical projects involve patients with stroke, status epilepticus, neuromuscular respiratory failure, intracerebral hemorrhage, intraventricular hemorrhage, hydrocephalus, subarachnoid hemorrhage, TBI, and spinal cord injury (13). In contrast to adult practice, even though pediatric critical care specialists have undertaken RCTs (236 in the period 1986–2012) (48), there are too few in pediatric NCC. For example, in the best-studied area—pediatric TBI—there have been five RCTs of hypothermia therapy (49) involving, in total, only 400 patients (which is grossly underpowered (50)). Taking these studies 5
Neurocritical care
R.C. Tasker
together, the risk ratio of death in the hypothermia group compared with the normothermia group was not statistically significant, and there was a suggestion of increased risk of death with hypothermia therapy. Therefore hypothermia for severe TBI is not recommended. So where does that leave us for the future? Recently, the US National Institutes of Health has started a comparative effectiveness research (CER) study (UO1NS081041) in severe TBI that aims to recruit 1000 children managed in the US and Europe over the next three years. CER measures difference in outcome and relates it to the package of care and its constituent components. The idea is to capture what actually happens in patients and identify future best practices and hypotheses for research.
Acknowledgments RC Tasker receives support from the NIH (UO1N S081041). Funding This research was carried out without funding. Conflicts of interest RC Tasker has no conflicts of interest.
References 1 Paediatric Intensive Care Audit Network. PICANet 2013 summary report. Available at: http://www.picanet.org.uk. Accessed 5 March, 2014. 2 Tasker RC. Pediatric neurocritical care: is it time to come of age? Curr Opin Pediatr 2009; 21: 724–730. 3 Drinker PA, McKhann CF. The iron lung: first practical means of respiratory support. JAMA 1986; 255: 1476–1480. 4 Drinker P, Shaw LA. An apparatus for the prolonged administration of artificial respiration: I. A design for adults and children. J Clin Invest 1929; 7: 229–247. 5 Drinker P, McKhann CF. The use of a new apparatus for prolonged administration of artificial respiration: I. A fatal case of poliomyelitis. JAMA 1929; 92: 1658–1660. 6 Dr John Spalding in Conversation. Oxford Medicine, 2005: 4–6. Available at: http:// www.medsci.ox.ac.uk/oma/oxmed/oxmedjul2005. Accessed 19 March, 2014. 7 Richmond C. Obituaries: Bjørn Ibsen. BMJ 2007; 335: 674. 8 Lassen HCA. A preliminary report on the 1952 epidemic of poliomyelitis in Copenhagen with special reference to the treatment of acute respiratory failure. Lancet 1953; 1: 37– 41. 9 Severinghaus JW, Astrup P, Murray JF. Blood gas analysis and critical care medicine. Am J Respir Crit Care Med 1998; 157: S114– S122. 10 West JB. The physiological challenges of the 1952 Copenhagen poliomyelitis epidemic and a renaissance in clinical respiratory physiology. J Appl Physiol 2005; 99: 424–432. 11 Trubuhovich RV. In the beginning: the 1952–1953 Danish epidemic of poliomyelitis and Bjørn Ibsen. Crit Care Resusc 2003; 5: 227–230.
6
12 Spalding JMK, Crampton Smith A. Clinical Practice and Physiology of Artificial Respiration. Oxford: Blackwell Scientific Publications, 1963. 13 Neurocritical Care Society. Available at: http://maps.google.com/maps/ms? ie=UTF8&hl=en&msa=0&msid=108542175118493601623. 00047fcc91780cd976daf&ll=33.000884,-111. 965918&spn=29.210936,91.784334&source=embed. Accessed 5 March, 2014. 14 Ward MJ, Shutter LA, Branas CC et al. Geographical access to US neurocritical care units registered with the Neurocritical Care Society. Neurocrit Care 2012; 16: 232–240. 15 Howard RS, Kullmann DM, Hirsch NP. Admission to neurological intensive care: who, when, and why? J Neurol Neurosurg Psychiatry 2003; 74: 2–9. 16 Howard RC. Neurological problems on the ICU. Clin Med 2007; 7: 148–153. 17 Mirski MA. Leapfrog jumps on board with neuro-intensivists. Currents 2008; 3: 1–9. 18 Sands R, Manning JC, Vyas H et al. Characteristics of deaths in paediatric intensive care: a 10-year study. Nurs Crit Care 2009; 14: 235–240. 19 Au AK, Carcillo JA, Clark RS et al. Brain injuries and neurological system failure are the most common proximate causes of death in children admitted to a pediatric intensive care unit. Pediatr Crit Care Med 2011; 12: 566–571. 20 Namachivayam P, Shann F, Shekerdemian L et al. Three decades of pediatric intensive care: who was admitted, what happened in intensive care, and what happened afterward. Pediatr Crit Care Med 2010; 11: 549–555. 21 Michaud LJ, Rivara FP, Grady MS et al. Predictors of survival and severity of disability after severe brain injury in children. Neurosurgery 1992; 31: 254–264.
22 Lopez Pison J, Galvan Manso M, Rubio Morales L et al. Descriptive analysis of neurological disorders in the pediatric intensive care unit of a regional reference hospital. An Esp Pediatr 2000; 53: 119–124. 23 Bell MJ, Carpenter J, Au AK et al. Development of a pediatric neurocritical care service. Neurocrit Care 2009; 10: 4–10. 24 Spentzas T, Escue JE, Patters AB et al. Brain tumor resection in children: neurointensive care unit course and resource utilization. Pediatr Crit Care Med 2010; 11: 718–722. 25 LaRovere KL, Graham RJ, Tasker RC; Pediatric Central Nervous System program (pCNSp). Pediatric neurocritical care: a neurology consultation model and implication for education and training. Pediatr Neurol 2013; 48: 206–211. 26 Suarez JI, Zaidat OO, Suri MF et al. Length of stay and mortality in neurocritically ill patients: impact of a specialized neurocritical care team. Crit Care Med 2004; 32: 2311– 2317. 27 Varelas PN, Conti MM, Spanaki MV et al. The impact of a neurointensivist-led team on a semiclosed neurosciences intensive care unit. Crit Care Med 2004; 32: 2191–2198. 28 Pineda JA, Leonard JR, Mazotas IG et al. Effect of implementation of a paediatric neurocritical care programme on outcomes after severe traumatic brain injury: a retrospective cohort study. Lancet Neurol 2013; 12: 45–52. 29 Scher M. Proposed cross-disciplinary training in pediatric neurointensive care. Pediatr Neurol 2008; 39: 1–5. 30 Tasker RC, Fleming TJ, Young AE et al. Severe head injury in children: intensive care unit activity and mortality in England and Wales. Br J Neurosurg 2011; 25: 68–77. 31 Claassen J, Mayer SA, Kowalski RG et al. Detection of electrographic seizures with © 2014 John Wiley & Sons Ltd
Neurocritical care
R.C. Tasker
32
33
34
35
36
37
continuous EEG monitoring in critically ill patients. Neurology 2004; 62: 1743–1748. Friedman D, Claassen J, Hirsch LJ. Continuous electroencephalogram monitoring in the intensive care unit. Anesth Analg 2009; 109: 506–523. Hosain SA, Solomon GE, Kobylarz EJ. Electroencephalographic patterns in unresponsive pediatric patients. Pediatr Neurol 2005; 32: 162–165. Jette N, Claassen J, Emerson RG et al. Frequency and predictors of nonconvulsive seizures during continuous electroencephalographic monitoring in critically ill children. Arch Neurol 2006; 63: 1750– 1755. Saengpattrachai M, Sharma R, Hunjan A et al. Nonconvulsive seizures in the pediatric intensive care unit: etiology, EEG, and brain imaging findings. Epilepsia 2006; 47: 1510– 1518. Hyllienmark L, Amark P. Continuous EEG monitoring in a paediatric intensive care unit. Eur J Paediatr Neurol 2007; 11: 70–75. Carrera E, Claassen J, Oddo M et al. Continuous electroencephalographic monitoring in critically ill patients with central nervous sys-
© 2014 John Wiley & Sons Ltd
38
39
40
41
42
43
44
tem infections. Arch Neurol 2008; 65: 1612– 1618. Shahwan A, Bailey C, Shekerdemian L et al. The prevalence of seizures in comatose children in the pediatric intensive care unit: a prospective video-EEG study. Epilepsia 2010; 51: 1198–1204. Abend NS, Gutierrez-Colina AM, Topjian AA et al. Nonconvulsive seizures are common in critically ill children. Neurology 2011; 76: 1071–1077. McCoy B, Sharma R, Ochi A et al. Predictors of nonconvulsive seizures among critically ill children. Epilepsia 2011; 52: 1973–1978. Greiner HM, Holland K, Leach JL et al. Nonconvulsive status epilepticus: the encephalopathic pediatric patient. Pediatrics 2012; 129: e748–e755. Kirkham FJ, Wade AM, McElduff F et al. Seizures in 204 comatose children: incidence and outcome. Intensive Care Med 2012; 38: 853–862. Schreiber JM, Zelleke T, Gaillard WD et al. Continuous video EEG for patients with acute encephalopathy in a pediatric intensive care unit. Neurocrit Care 2012; 17: 31–38. Topjian AA, Gutierrez-Colina AM, Sanchez SM et al. Electrographic status epilepticus is
45
46
47
48
49
50
associated with mortality and worse shortterm outcome in critically ill children. Crit Care Med 2013; 41: 215–223. Abend NS, Dlugos DJ, Hahn CD et al. Use of EEG monitoring and management of nonconvulsive seizures in critically ill patients: a survey of neurologists. Neurocrit Care 2010; 12: 382–389. Tasker RC. Pediatric critical care, glycemic control, and hypoglycemia: what is the real target? JAMA 2012; 308: 1687–1688. Kramer AH, Zygun DA. Do neurocritical care units save lives? Measuring the impact of specialized ICUs. Neurocrit Care 2011; 14: 329–333. Duffett M, Choong K, Hartling L et al. Randomized controlled trials in pediatric critical care: a scoping review. Crit Care 2013; 17: R256. Hutchison JS, Guerguerian AM. Cooling of children with severe traumatic brain injury. Lancet Neurol 2013; 12: 527–529. Forsyth RJ, Parslow RC, Tasker RC et al. Prediction of raised intracranial pressure complicating severe traumatic brain injury in children: implications for trial design. Pediatr Crit Care Med 2008; 9: 8–14.
7
