Navigating the Road “Less Traveled”: Death by Neurologic Criteria*

Death is an event that no one is immune to and an inevitable consequence of life, from which no one can return. Determining if a patient has died is a fundamental responsibility of our practice in critical care medicine. Death signifies the end of the person’s life. Medical treatments usually cease as they are no longer indicated because the physician-patient relationship ends, although our care of families continues. However, evolving and advanced mechanical technology has allowed for continued circulation during severe organ failure, whether mechanical ventilation or extracorporeal support adding additional layers of complexity and challenges to the accurate determination of death, whether by circulatory or neurologic criteria. Regardless of the pathway, the determination of death relies on a complete clinical examination of the patient to ensure established criteria are met. Further complicating the determination of death in children are physiologic and anatomic differences, mechanisms of injury, and disease processes based on the age difference between a newborn and adolescent patient. These differences have resulted in specific guidelines addressing the determination of neurologic death in children (1,2). Previous guidelines in the United States to determine death by neurologic criteria (DNC) have been revised to address advances in technology for children and adults (3). The World Brain Death Guidelines examined practices of death determination using neurologic criteria (4). The United Kingdom, Cyprus, and India are exceptions to the whole brain death criteria where DNC is primarily determined by loss of brainstem criteria (5). Regardless of the definition used, minimum clinical criteria are required to determine DNC, and the bedside examination is the foundation of this process. The World Brain Death Guidelines summarized many essential aspects of the neurologic examination highlighting consistency in the minimal criteria to determine neurologic death. Common practices to determine DNC in children include two clinical examinations separated by a fixed or random observation period and a Paco2 threshold for apnea testing. Variability in the use and type of ancillary studies, number of examinations, observation periods between examinations, and experience required to perform DNC testing were also noted (6). In this issue of Pediatric Critical Care Medicine, Aziz et al (7) report their retrospective examination of 824 children suspected of DNC in the United Kingdom. DNC was rare over the 8-year study period, with 565 children tested and 548 confirmed DNC. There were 43 children two months to 1 year of age and only 12 infants younger than 2 months of age declared with DNC in this study. Importantly, DNC in term infants younger than 2 months of age has only been permitted in the United Kingdom since 2015. DNC accounted for 2.5–3.5% of all pediatric deaths in the United Kingdom and 9.7–12.2% of all PICU deaths. Although most children with suspected DNC were cared for in a PICU (74.1%), almost 25% were cared for in an adult ICU (most children older than 16 y are cared for in an adult ICU in the United Kingdom), with only 1% cared for in a neonatal ICU. The authors concluded that DNC was a relatively infrequent occurrence, particularly in the neonatal and infant age group, and proposed the need for a national registry to facilitate clinical practice in the United Kingdom. This study highlights significant gaps in knowledge, lack of standardization, and significant variation in testing for determination of DNC, despite clearly defined U.K. national standards from the Academy of Medicine Royal Colleges, National Health Service Blood and Transplant, and the Royal College of pediatrics and Child Health documents (2,8,9). Although criteria were outlined and followed based on current standards, there were instances where testing for neurologic death did not occur. Although the vast majority of patients who did not progress to testing for DNC were hemodynamically unstable, family pressure to not test (15%) and issues related to organ donation (12.5%) were also cited as reasons to not perform testing for DNC. 19.5% of the patients in this survey had confounding variables affecting the DNC examination. This is depressingly unchanged since being reported as part of the overall U.K. donation experience 6 years ago (10). Most adults and children who die in an ICU do so following loss of circulation after the withdrawal of life-sustaining medical therapies. Determination of DNC, especially in children, is relatively infrequent. This necessitates caution to avoid diagnostic errors, especially in younger children. The authors note that across the 30 PICUs in the United Kingdom, only one to two children would undergo DNC per ICU annually if deaths were equally distributed. Furthermore, for children younger than 2 y, DNC testing would occur less than once every 2 y (6). This infrequency is compounded by younger physicians and trainees having fewer opportunities to perform practical procedures such as examinations to determine death, limited clinical experience due to work hour restrictions, and more specialists that dilute clinical time in the ICU (11). Seventeen children underwent DNC testing and were not confirmed dead. This complies with national policy to always perform DNC if “brain death” is suspected. However, further information about why DNC was not confirmed in these patients would be helpful. Was there an inability to complete the neurologic examination, failed apnea testing, or other medical or technical reasons for not declaring DNC? What happened to these children and did any satisfy DNC criteria later, was death verified using circulatory criteria, or did they survive? This study also highlighted a significant number of children where organ donation appeared to be a motivating factor in determining DNC. This contradicts the United Kingdom and other national and international policies. Determination of death is not the driving factor for organ donation. Organ donation must remain a separate and secondary consideration following death and can never be the primary reason to determine DNC. Determination of death is a critical part of patient care and our responsibility as healthcare providers. Delaying this process can consume valuable critical care resources and may further delay the grieving process for the family. When the DNC has been certified, death has occurred and artificial support is terminated whether by the medical team or the legal system, depending on jurisdiction when families may object to the DNC. This contrasts the family having to decide to withdraw life-sustaining medical therapies in a situation when death has not occurred. In this situation, families may experience guilt for having participated or caused the death of their child. Additionally, one must consider religious beliefs which for some families may preclude DNC in some jurisdictions. Irrespective of faith and culture, all dying children in the ICU should be cared for compassionately and respectfully. It is vital to allow families to participate in the care of their child at the end of life. There is a clear necessity to standardize the process of determining DNC in the United Kingdom and other parts of the world. Diagnostic errors leading to premature determination of death result in continued mistrust of the medical community. Consistency in the examination process, standardization of observation periods between examinations, use of ancillary studies, and documentation are clearly required and should be achievable. Such global consistency would augment confidence in DNC for both the medical community and the broader public, by ensuring that the determination of death is performed uniformly to avoid diagnostic error and minimize the false determination of death. A standardized protocolized checklist exists in the United Kingdom (12) and should be used to ensure consistency in the examination process to determine DNC which is essential and can reduce the likelihood of diagnostic error (13). However, as exemplified in this study, merely having such a checklist is inadequate. Policies and procedures must be used consistently and audited in a meaningful way with oversight for compliance to be beneficial for this most crucial of intensive care activities. Although a national database will provide information regarding various aspects of DNC in children, it does not address critical issues of consistency and standardization to determine DNC. Having a clearly defined, standardized process to determine death will help families and the medical team ensure that no matter where a child is cared for (pediatric, adult, or neonatal ICU) death is determined by a consistent process. There is a clear opportunity and need to improve and standardize this process to ensure accuracy when determining DNC. Managing the death of a child is one of our most important duties and there is no room for error. Death determination must be made correctly and in a consistent and efficient manner to ensure we are appropriately treating children and not prolonging death. What continues to remain true from the past and present is that some of our most difficult medical and ethical decisions are when life begins, and when life ends.