Pediatric Palliative Care: Current Evidence and Evidence Gaps Elissa G. Miller, MD1,2, Carly Levy, MD1,2, Jennifer S. Linebarger, MD3, Jeffrey C. Klick, MD4, and Brian S. Carter, MD3
H
ospice and palliative medicine (HPM) is an emerging medical subspecialty initially recognized by the American Board of Medical Specialties in 2006. As the Institute of Medicine reported in 2014, health care delivery and the challenges of care at the end of children’s lives have evolved significantly over the past 15 years.1 The last decade has seen the growth of pediatric palliative care (PPC) programs at children’s hospitals and a transformation of the field.2 Fifty percent of children’s hospitals nationwide have a PPC program, with a peak in new program development occurring in 2008.3 New programs are almost immediately impactful, experience high referral volumes, and must quickly expand their workforce.4 Although HPM has a growing body of literature, the evidence for PPC appears to lag behind the clinical growth. Here we provide a focused and practical summary of evidence in pediatric HPM as a primer for those practicing in other subspecialties. Specifically, we review evidence by focusing on a few of the domains in HPM : (1) communication and psychosocial support; (2) pain and symptom management; (3) end-of-life care; and (4) ways to build a better health care system. We hope to strengthen understanding and partnerships between HPM and non-HPM clinicians and investigators and thereby improve patient care for children with serious illnesses.
Case 1 An 18-day-old, term infant presented to the emergency department unresponsive with sepsis and presumed meningitis. Blood and cerebrospinal fluid cultures confirmed group-B streptococcus infection. Given the serious nature of the infant’s condition, the pediatric intensive care unit (PICU) team consulted the PPC team on hospital day 3. With aggressive life-sustaining measures, the infant survived, but sustained significant brain injury, remaining comatose with absent gag reflex and insufficient respiratory effort. The PPC team met with family frequently during the infant’s hospitalization to provide support around understanding of disease and coping with critical illness as well as to address goals of care. Initially, goals were focused on life-sustaining measures. As the severity of the infant’s neurologic condition became clear, family goals slowly shifted toward a comfort-focused approach. Ultimately, after
ACP DNR HPM PICU PPC
Advance care planning Do not resuscitate Hospice and palliative medicine Pediatric intensive care unit Pediatric palliative care
a family meeting with extended family present, the parents chose to focus solely on the infant’s comfort and discontinue all interventions that were prolonging suffering, including the ventilator. The infant died peacefully in his mother’s arms shortly thereafter.
Case 2 A 15-year-old male with Hunter syndrome was well known to his hospital’s PPC team. Many years earlier, his family, knowing the progressive nature of the disease, had chosen to focus on his comfort and quality of life. Enzyme infusions successfully reduced his pain and symptom burden, and he was rarely hospitalized during his first decade of life. Recently, however, he had experienced increased seizures with frequent aspiration events. After an episode of severe pneumonia requiring hospitalization and noninvasive ventilation, his parents asked to speak with the PPC team. Together, they devised an advance care plan for their son that included an out-of-hospital do not resuscitate (DNR) order. Utilizing the Concurrent Care for Children Requirement from the Affordable Care Act, the family chose to continue enzyme infusions while he also received home hospice care. Nine months later, the child had not been rehospitalized and was doing well, so the family discontinued hospice care but maintained the out-of-hospital DNR order. His parents continue to focus on his comfort and quality of life. These cases present different but common scenarios facing PPC teams. A multidisciplinary approach to care allowed 2 different children—1 child with sudden, critical illness and another with chronic disease—to live what their families felt was the best quality of life for as long as possible under the circumstances of their illness. It is important to examine the evidence guiding the practices discussed in these cases.
Communication and Psychosocial Support The literature within the communication domain of HPM focuses on family meetings, decision making, advance care planning (ACP), family coping, and the impact of bereavement. Although there is significant literature focused on adult patients, pediatrics necessitates a stronger focus on the child’s cognitive development and how he or she fits into
From the 1Department of Pediatrics, Nemours/Alfred I. duPont Hospital for Children, Wilmington, DE; 2Sidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, PA; 3Children’s Mercy Hospital and Clinics, Kansas City, MO; and 4 Department of Pediatrics, Children’s Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2015.02.019
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Vol. 166, No. 6 June 2015 the social structure of the family. These differences make it difficult to extrapolate from the adult-based literature. Family Meetings As in our case 1 example, family meetings are a cornerstone tool of HPM, but they have been minimally studied in pediatrics. Nonetheless, it seems clear that these meetings are infrequently used, even for the sickest children.5 In one study, meetings were focused on information exchange and future management. Conferences occurred predominantly for sicker patients, those with complex chronic conditions, and those with PPC consultation.5 Although many clinicians believe that the family meeting is key to the practice of palliative medicine,6 there is minimal evidence regarding families’ perception of such meetings. Decision Making Clinicians can facilitate families’ decision making. Hinds et al7 interviewed parents faced with making noncurative treatment decisions. The families identified components of being a “good parent” to include focusing on their child’s quality of life, advocating for their child with the medical team, and putting their child’s needs above their own.8 By working to define a family’s priorities and values, the clinician can help them fulfill their wishes to “be a good parent” through dire circumstances.8 In a study of parents of PICU patients, 40% of parents preferred sharing decision making with their doctors, 41% preferred autonomous decision making, and 18.9% preferred delegating these decisions to their doctors.9 ACP ACP involves the patient, family, and providers sharing information on the natural course of the child’s disease, individualized prognostic information including trajectory, and the expected experiences of the child.10,11 ACP is a common task for palliative care teams; however, conversations are most productive when the family and clinicians have a common understanding of the child’s disease and prognosis. On average, oncologists recognize 100 days sooner than parents that there is no realistic chance of cure.12 When the poor prognosis for survival is disclosed early, there are earlier discussions of hospice care, earlier DNR orders, and decreased use of chemotherapy in the last month of life. Importantly, there are also better parental ratings of the quality of care in the home. It is also important to include the child in ACP in appropriate ways. Teenagers with HIV/AIDS and those with advanced cancer overwhelmingly express the desire to participate in their own ACP.13-16 Families who decide to speak with their children about death report that they are happy with that decision, and nearly one-third of families who did not discuss death with their child regretted that decision later.16 A single-center study examined generally perceived barriers to ACP and DNR discussions. The top 3 barriers to ACP discussions identified were clinician perception of
unrealistic parental expectations, lack of parent readiness to have the discussion, and discrepancies between clinician and patient/parent understanding of the prognosis.17 The clinicians at that center overwhelmingly felt that ACP/DNR discussions should be initiated on presentation/diagnosis or during a period of stability. Family Coping Families cope and accommodate to their child’s illness using a multitude of supports, coping strategies, and resources. Religion, spirituality, and life philosophy are some tools that can help families cope with adversity.18-20 Hopeful thoughts and language play a major role; many parents use hopeful language about outcomes for their child, even when death is inevitable.18 Impact of Bereavement The death of a child or sibling has a significant effect on the entire family. Youngblut et al21 reported significant negative physical and mental health outcomes in parents 13 months after their child’s death, including newly diagnosed chronic health conditions, posttraumatic stress disorder, and hospitalizations. Psychiatric comorbidities, previous loss, economic hardship, duration and intensity of the child’s treatment, perceptions of medical care, child’s quality of life, and parent preparedness for death all impact parental outcomes.22 Siblings are affected as well and often recognize their parents’ grief.23 Survivor guilt, parental overprotection, and idealization of the deceased child affect sibling bereavement.24 Siblings may be affected by how their parents engage them, allow them to see/hold/touch their ill siblings, and even participate in their care,25,26 although few evidence-based bereavement interventions have been published.27-29
Physical Aspects of Care In contrast to the large body of evidence on palliative pain and symptom management in adults, studies on pediatric patients are scant. Much of the evidence that pediatric HPM clinicians use is drawn from the adult literature, and the medications used are often off-label. Although many of the principles of pain management are consistent across the age spectrum, there are important differences in neonatal and pediatric patients that merit more careful study. Even though the clinical practice of PPC includes symptom management integrated into life-sustaining therapies, much of the PPC literature focuses on pain and symptom management at the end of life. Symptoms at End of Life Children with terminal cancer have a significant burden of pain and symptoms in their last 30 days of life.30 PPC has been shown to lessen this burden, and to help parents feel more prepared during their child’s last months of life and at the time of death.31 Prominent symptoms in the last 24 hours of life include respiratory distress, pain, nausea, vomiting, and anxiety.32 One study found that children who die of advanced 1537
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heart disease also carry a significant symptom burden and poor quality of life in their last 30 days,33 suggesting the need for improved symptom assessment and management in many children with noncancer diagnoses.
End-of-Life Care Resuscitation Status In a study of deaths of hospitalized children at 1 institution, few children had DNR orders before admission, and often orders that were written were done so less than 1 day before death.34 The incidence of DNR orders increased when parents had more education (>15 years) or a higher monthly income.35 On the other hand, a recent report on PICU deaths suggested that DNR orders may be used less often today than in the past.36 We do not know whether PPC involvement increases the frequency of DNR or limited code orders. How and Where Patients Die As access to PPC has increased, the location of death for children dying from oncologic diseases and complex chronic conditions has shifted.37 Nonetheless, children with advanced heart, lung, immune, and infectious diseases continue to die in the PICU after receiving highly technical medical support at the end of life and after the withdrawal of life-sustaining interventions.33,36,38 Patients and families vary in terms of preference for location of end-of-life care,39 and the majority of children die in a hospital setting.40 This can actively change to home deaths with PPC involvement.41 Among patients with advanced cancer, having open discussions about the location of death is associated with increased home deaths.42 Although adult HPM providers use a shift in location of death as an impactful outcome of palliative care involvement, whether PPC will, or even should, have the same impact is less clear. Many children and families become comfortable with the hospital environment over the disease trajectory and actively choose the hospital for end-of-life care.43
Building a Better Health Care System Barriers to Palliative Care A survey of pediatric staff members at the University of California San Francisco identified an uncertain patient prognosis as the primary barrier to PPC referral.44 Additional barriers included the clinician’s perception of the family’s unwillingness to acknowledge the incurable nature of their child’s disease, language barriers, and time constraints. Many pediatricians still associate PPC with hospice care, used only for the end of life.45 In reality, most PPC consults are for facilitating communication; in 1 study, only 30% of consults ended in the patient’s death.46 Cost of Care By clarifying and focusing on individual patient goals of care, adult palliative care teams not only save money by decreasing hospital length of stay, but also help reduce 30-day hospital 1538
Vol. 166, No. 6 readmission rates and decrease emergency department and intensive care unit utilization.47 Pediatric data are currently lacking, however, and some argue that cost avoidance is not a relevant topic in PPC.48 Children with life-limiting diseases experience multiple hospitalizations and spend on average more than 39 days in the hospital in the last year of life.49 Outpatient PPC programs can decrease hospital and emergency department charges and shift care to an in-home setting through a community-based PPC program.50,51 However, to date no study has examined the overall health care costs and potential savings realized by PPC involvement with medically complex hospitalized pediatric patients. Care Delivery Systems There are multiple reports of novel models of PPC delivery, from perinatal palliative care to automated PPC consult triggers to the use of telemedicine. Pediatric hospice patients are eligible for concurrent care (ie, hospice in addition to disease-directed therapy, as in our case 2) through the Affordable Care Act. The use of concurrent care has been reported, but cost savings remain unclear.52,53 Use of the PPC Team Although palliative care offers a variety of expertise, previous studies have demonstrated that the specific services requested of the palliative care team vary and depend largely on the referring service. A survey of PICU physicians identified continuity between hospitalizations, transition to the community setting, and provision of bereavement care for family and staff was the most valuable services offered by the PPC team.54 Critical care physicians were more likely to consult palliative care for psychosocial support of patients and families, and oncologists were more likely to consult for symptom management. In addition, clinicians with self-reported palliative care education were more likely to involve PPC in the care of their patients.55 Best Practices/Quality Improvement Measures Most notably lacking from the PPC literature are data confirming quality metrics and establishing evidence-based best practices for PPC clinicians. Barriers to PPC Research There are many barriers to producing high-quality palliative care research, including funding, institutional capacity, researcher workforce, challenges related to the topic and population (eg, attrition, rare disease entities, heightened human subjects protections), and public and professional misunderstanding of palliative care and aversion to topics related to serious illness and the end of life.56 It is important to focus PPC research on areas that are unique to pediatric patients (eg, developmentally appropriate communication, family coping), those that are unique to PPC (eg, concurrent hospice care, care coordination), and those that cannot be easily extrapolated from adult literature (eg, pain and symptom management). Miller et al
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Discussion The evidence shows that PPC teams improve patient care, and it is no longer acceptable for pediatric patients with access to PPC to die without PPC involvement. It is striking that data on costs of care, best practices, and management lag behind those for ACP. Ullrich and Morrison suggested opportunities for collaboration for future research, stating that PPC “research priorities.should fall into one of two categories. They should be either issues related specifically to children, from which lessons learned from adult research cannot be extrapolated, or unique opportunities for PPC research to inform the provision of palliative care for people of all ages.”57 The Institute of Medicine’s 2014 report echoes this sentiment.1 Pediatric-specific research efforts intended to directly impact clinical care should focus on such areas as developmental considerations to optimize patient and family communication, evidence-based interventions to maximally support family members and aid in decision making, families’ perspective on family meetings, and models for delivery of out-of-hospital PPC (Table; available at www.jpeds.com). Broad application of the current evidence should result in decreased patient suffering and less discrepancy in palliative care between adult and pediatric patients. Such application across pediatric subspecialties will allow clinical and research collaboration to fill in the disease-specific evidence gaps that remain. With approximately 250 pediatricians boardcertified in HPM, we have few practitioners of clinical PPC and even fewer clinician-investigators. New HPM fellows are graduating from 1-year clinical HPM training programs and generally are not being trained to become academic clinician-investigators; consequently, growth of the evidence base for PPC likely will continue to rely on relatively few pediatric investigators and to lean heavily on other fields as partners in advancing this young field. n Submitted for publication Nov 12, 2014; last revision received Jan 30, 2015; accepted Feb 6, 2015. Reprint requests: Elissa G. Miller, MD, Nemours/Alfred I. duPont Hospital for Children, PO Box 269, Wilmington, DE 19899. E-mail: [email protected]
References 1. Institute of Medicine. Dying in America: Improving quality and honoring individual preferences near the end of life. Washington, DC: National Academies Press; 2014. 2. Kang TI, Feudtner C. Advances in pediatric palliative medicine in the United States. Prog Palliat Care 2012;20:331-6. 3. Feudtner C, Womer J, Augustin R, Remke S, Wolfe J, Friebert S, et al. Pediatric palliative care programs in children’s hospitals: a crosssectional national survey. Pediatrics 2013;132:1063-70. 4. Frizzola M, Miller EG. Referrals to a new pediatric palliative care team: details of the first 12 months of operation. J Palliat Med 2014;17:585-8. 5. Michelson KN, Clayman ML, Haber-Barker N, Ryan C, Rychlik K, Emanuel L, et al. The use of family conferences in the pediatric intensive care unit. J Palliat Med 2013;16:1595-601. 6. Fox D, Brittan M, Stille C. The pediatric inpatient family care conference: a proposed structure toward shared decision-making. Hosp Pediatr 2014;4:305-10.
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GRAND ROUNDS 7. Hinds PS, Oakes LL, Hicks J, Powell B, Srivastava DK, Spunt SL, et al. “Trying to be a good parent” as defined by interviews with parents who made phase I, terminal care, and resuscitation decisions for their children. J Clin Oncol 2009;27:5979-85. 8. October TW, Fisher KR, Feudtner C, Hinds PS. The parent perspective: “being a good parent” when making critical decisions in the PICU. Pediatr Crit Care Med 2014;15:291-8. 9. Madrigal VN, Carroll KW, Hexem KR, Faerber JA, Morrison WE, Feudtner C. Parental decision-making preferences in the pediatric intensive care unit. Crit Care Med 2012;40:2876-82. 10. Lotz JD, Jox RJ, Borasio GD, F€ uhrer M. Pediatric advance care planning from the perspective of health care professionals: a qualitative interview study. Palliat Med 2015;29:212-22. 11. Heckford E, Beringer AJ. Advance care planning: challenges and approaches for pediatricians. J Palliat Med 2014;17:1049-53. 12. Wolfe J, Klar N, Grier HE, Duncan J, Salem-Schatz S, Emanuel EJ, et al. Understanding of prognosis among parents of children who died of cancer: impact on treatment goals and integration of palliative care. JAMA 2000;284:2469-75. 13. Wiener L, Zadeh S, Battles H, Baird K, Ballard E, Osherow J, et al. Allowing adolescents and young adults to plan their end-of-life care. Pediatrics 2012;130:897-905. 14. Hinds PS, Oakes LL, Hicks J, Anghelescu DL. End-of-life care for children and adolescents. Semin Oncol Nurs 2005;21:53-62. 15. Lyon ME, McCabe MA, Patel KM, D’Angelo LJ. What do adolescents want? An exploratory study regarding end-of-life decision-making. J Adolesc Health 2004;35:529.e1-6. 16. Kreicbergs U, Valdimarsdottir U, Onelov E, Henter JI, Steineck G. Talking about death with children who have severe malignant disease. N Engl J Med 2004;351:1175-86. 17. Sanderson A, Zurakowski D, Wolfe J. Clinician perspectives regarding the do-not-resuscitate order. JAMA Pediatr 2013;167:954-8. 18. Hexem KR, Miller VA, Carroll KW, Faerber JA, Feudtner C. Putting on a happy face: emotional expression in parents of children with serious illness. J Pain Symptom Manage 2013;45:542-51. 19. Hexem KR, Mollen CJ, Carroll K, Lanctot DA, Feudtner C. How parents of children receiving pediatric palliative care use religion, spirituality, or life philosophy in tough times. J Palliat Med 2011;14:39-44. 20. Robinson MR, Thiel MM, Backus MM, Meyer EC. Matters of spirituality at the end of life in the pediatric intensive care unit. Pediatrics 2006;118: e719-29. 21. Youngblut JM, Brooten D, Cantwell GP, del Moral T, Totapally B. Parent health and functioning 13 months after infant or child NICU/PICU death. Pediatrics 2013;132:e1295-301. 22. Rosenberg AR, Baker KS, Syrjala K, Wolfe J. Systematic review of psychosocial morbidities among bereaved parents of children with cancer. Pediatr Blood Cancer 2012;58:503-12. 23. Youngblut JM, Brooten D. Parents’ report of child’s response to sibling’s death in a neonatal or pediatric intensive care unit. Am J Crit Care 2013; 22:474-81. 24. Wender E, Committee on Psychosocial Aspects of Child and Family Health. Supporting the family after the death of a child. Pediatrics 2012;130:1164-9. 25. Gaab EM, Owens GR, MacLeod RD. Siblings caring for and about pediatric palliative care patients. J Palliat Med 2014;17:62-7. 26. Fanos JH, Little GA, Edwards WH. Candles in the snow: ritual and memory for siblings of infants who died in the intensive care nursery. J Pediatr 2009;154:849-53. 27. Forte AL, Hill M, Pazder R, Feudtner C. Bereavement care interventions: a systematic review. BMC Palliat Care 2004;3:3. 28. Cortezzo DE, Sanders MR, Brownell EA, Moss K. End-of-life care in the neonatal intensive care unit: experiences of staff and parents. Am J Perinatol 2014; http://dx.doi.org/10.1055/s-0034-1395475. 29. Capitulo KL. Evidence for healing interventions with perinatal bereavement. MCN Am J Matern Child Nurs 2005;30:389-96. 30. Wolfe J, Grier HE, Klar N, Levin SB, Ellenbogen JM, Salem-Schatz S, et al. Symptoms and suffering at the end of life in children with cancer. N Engl J Med 2000;342:326-33. 1539
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31. Wolfe J, Hammel JF, Edwards KE, Duncan J, Comeau M, Breyer J, et al. Easing of suffering in children with cancer at the end of life: is care changing? J Clin Oncol 2008;26:1717-23. 32. Ho C, Straatman L. A review of pediatric palliative care service utilization in children with a progressive neuromuscular disease who died on a palliative care program. J Child Neurol 2013;28:40-4. 33. Blume ED, Balkin EM, Aiyagari R, Ziniel S, Beke DM, Thiagarajan R, et al. Parental perspectives on suffering and quality of life at end-oflife in children with advanced heart disease: an exploratory study. Pediatr Crit Care Med 2014;15:336-42. 34. McCallum DE, Byrne P, Bruera E. How children die in hospital. J Pain Symptom Manage 2000;20:417-23. 35. Hileli I, Weyl Ben Arush M, Hakim F, Postovsky S. Association between religious and socio-economic background of parents of children with solid tumors and DNR orders. Pediatr Blood Cancer 2014;61:265-8. 36. Burns JP, Sellers DE, Meyer EC, Lewis-Newby M, Truog RD. Epidemiology of death in the PICU at five US teaching hospitals. Crit Care Med 2014;42:2101-8. 37. Feudtner C, Feinstein JA, Satchell M, Zhao H, Kang TI. Shifting place of death among children with complex chronic conditions in the United States, 1989-2003. JAMA 2007;297:2725-32. 38. Lee KJ, Tieves K, Scanlon MC. Alterations in end-of-life support in the pediatric intensive care unit. Pediatrics 2010;126:e859-64. 39. Kassam A, Skiadaresis J, Alexander S, Wolfe J. Parent and clinician preferences for location of end-of-life care: home, hospital or freestanding hospice? Pediatr Blood Cancer 2014;61:859-64. 40. Brandon D, Docherty SL, Thorpe J. Infant and child deaths in acute care settings: implications for palliative care. J Palliat Med 2007;10: 910-8. 41. Gupta N, Harrop E, Lapwood S, Shefler A. Journey from pediatric intensive care to palliative care. J Palliat Med 2013;16:397-401. 42. Dussel V, Kreicbergs U, Hilden JM, Watterson J, Moore C, Turner BG, et al. Looking beyond where children die: determinants and effects of planning a child’s location of death. J Pain Symptom Manage 2009;37: 33-43. 43. Lowton K. “A bed in the middle of nowhere”: parents’ meanings of place of death for adults with cystic fibrosis. Soc Sci Med 2009;69:1056-62. 44. Davies B, Sehring SA, Partridge JC, Cooper BA, Hughes A, Philp JC, et al. Barriers to palliative care for children: perceptions of pediatric health care providers. Pediatrics 2008;121:282-8. 45. Thompson LA, Knapp C, Madden V, Shenkman E. Pediatricians’ perceptions of and preferred timing for pediatric palliative care. Pediatrics 2009;123:e777-82. 46. Feudtner C, Kang TI, Hexem KR, Friedrichsdorf SJ, Osenga K, Siden H, et al. Pediatric palliative care patients: a prospective multicenter cohort study. Pediatrics 2011;127:1094-101. 47. Ranganathan A, Dougherty M, Waite D, Casarett D. Can palliative home care reduce 30-day readmissions? Results of a propensity score-matched cohort study. J Palliat Med 2013;16:1290-3.
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Vol. 166, No. 6 48. Meier DE, Beresford L. Pediatric palliative care offers opportunities for collaboration. J Palliat Med 2007;10:284-9. 49. Chavoshi N, Miller T, Siden H. Resource utilization among individuals dying of pediatric life-threatening diseases. J Palliat Med 2013; 16:1210-4. 50. Postier A, Chrastek J, Nugent S, Osenga K, Friedrichsdorf SJ. Exposure to home-based pediatric palliative and hospice care and its impact on hospital and emergency care charges at a single institution. J Palliat Med 2014;17:183-8. 51. Gans D, Kominski GF, Roby DH, Diamant AL, Chen X, Lin W, et al. Better outcomes, lower costs: palliative care program reduces stress, costs of care for children with life-threatening conditions. Policy Brief UCLA Cent Health Policy Res 2012;1-8. 52. Miller EG, Laragione G, Kang TI, Feudtner C. Concurrent care for the medically complex child: lessons of implementation. J Palliat Med 2012;15:1281-3. 53. Lindley LC, Edwards S, Bruce DJ. Factors influencing the implementation of health care reform: an examination of the concurrent care for children provision. Am J Hosp Palliat Care 2013; 31:527-33. 54. Jones PM, Carter BS. Pediatric palliative care: feedback from the pediatric intensivist community. Am J Hosp Palliat Care 2010;27: 450-5. 55. Atwood MA, Hoffmann RG, Yan K, Lee KJ. Attitudes about palliative care: a comparison of pediatric critical care and oncology providers. Am J Hosp Palliat Care 2013;31:665-71. 56. Chen EK, Riffin C, Reid MC, Adelman R, Warmington M, Mehta SS, et al. Why is high-quality research on palliative care so hard to do? Barriers to improved research from a survey of palliative care researchers. J Palliat Med 2014;17:782-7. 57. Ullrich C, Morrison RS. Pediatric palliative care research comes of age: what we stand to learn from children with life-threatening illness. J Palliat Med 2013;16:334-6. 58. October TW, Watson AC, Hinds PS. Characteristics of family conferences at the bedside versus the conference room in pediatric critical care. Pediatr Crit Care Med 2013;14:e135-42. 59. Young B, Dixon-Woods M, Windridge KC, Heney D. Managing communication with young people who have a potentially life threatening chronic illness: qualitative study of patients and parents. BMJ 2003;326:305. 60. Liberman DB, Pham PK, Nager AL. Pediatric advance directives: parents’ knowledge, experience, and preferences. Pediatrics 2014;134:e436-43. 61. Pritchard M, Burghen EA, Gattuso JS, West NK, Gajjar P, Srivastava DK, et al. Factors that distinguish symptoms of most concern to parents from other symptoms of dying children. J Pain Symptom Manage 2010;39: 627-36. 62. Keele L, Keenan HT, Sheetz J, Bratton SL. Differences in characteristics of dying children who receive and do not receive palliative care. Pediatrics 2013;132:72-8.
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Table. Summary of progress to date and needed future investigations Topic Communication and psychosocial support Family meetings
Decision making
ACP
Family coping Bereavement support
Physical aspects of care Pain and symptom management
Symptoms at end of life End of life care Resuscitation status
How and where patients die Building a better healthcare system Barriers to palliative care
Cost of care
Research progress to date Family meetings rarely occur.5 Effective in aiding decision making.58 An evidence-based structure for family conferences exists.6 Families differ in their approach to decision making (shared vs autonomous vs delegation).9 Parents differ in what it means to be a “good parent,” making it challenging to best to support families with difficult treatment decisions.7,8 Teens want to participate in ACP.13-16 Teens feel marginalized when excluded from ACP discussions.59 Families who discussed dying with their children did not regret it after the death of their child.16 Family caregivers view the advance directive as a way to have more control over what happened to their child.60 Families rely on various coping strategies when their child has a serious illness.18,19 Families use spirituality in their coping after the death of a child,20 although they often have negative physical and mental health outcomes.21 Siblings are affected as well.23-25 There are few evidence-based bereavement interventions for siblings.27
Ideal timing/frequency of family meetings Whether routine family meetings affect patient-level outcomes (eg, length of stay, family and/or provider satisfaction with care) Evidence-based methods of providing decision support, including how to clearly communicate patient’s clinical status, review the benefits/harms of medical interventions, and discuss goals of care1
The most distressing symptoms have been identified by patients and families.30,61 All palliative symptom management research to date has been in adult populations. PPC helps decrease patients’ suffering at end of life and improves parents’ sense of preparedness before the death of the child.30,31,33
Pharmacologic and nonpharmacologic interventions merit robust study, including effectiveness of different medications and potential problems of polypharmacy
Best time for prognostic revelation and ACP discussions Best ways to communicate and document ACP discussions
Evidence-based strategies for providers to elicit and support family coping strategies Complicated bereavement risk-group identification Evidence-based parent and sibling bereavement interventions
Tools for symptom assessment in non–cancer patient populations
DNR orders are commonly placed just prior to a child’s death.34,35 Death in the PICU continues to be common in children after withdrawal of technological support.38 PPC teams help shift the location of death away from PICU and inpatient settings to home and hospice settings.37,39,41,62
Whether the involvement of a PPC team leads to earlier limits on resuscitative efforts Technology-based decision aids (eg, videos, apps) for parents and pediatric patients Identification and clarification of factors that influence the preferred location of death
Uncertain patient prognosis.44 Clinician perception of family “readiness” for PPC/ACP discussions.17 Misperception that palliative care is equivalent to hospice or only for the end of life.45 Adult palliative care programs reduce emergency department and intensive care unit utilization, decrease hospital length of stay, and cut costs,47 as do outpatient PPC programs.50,51
Comparison of clinician perception of parent readiness to engage with PPC vs parent report of readiness Interventions to facilitate earlier PPC involvement and earlier ACP
Care delivery systems
There are multiple proof-of-concept descriptions, but no studies of novel modes of PPC delivery.
Use of the PPC team
Clinicians from different subspecialties consult PPC for different reasons.54 Clinicians with self-reported PPC education are more likely to involve PPC in the care of their patients.55 None exist.
Best practices/quality improvement measures Barriers to PPC research
Proposed needed investigation
Barriers to PPC research include lack of funding, institutional capacity, and research workforce. Additional challenges include public and professional misunderstanding of the field.56
Pediatric Palliative Care: Current Evidence and Evidence Gaps
Overall health care cost and potential savings of PPC involvement with medically complex, hospitalized pediatric patients Cost of PPC team (eg, salaries) weighed against healthcare dollars saved through outpatient PPC Evidence-based PPC team structure/staffing Effect of concurrent care on cost of care, family perceptions of care, and treatment decisions Evidence-based educational models for practicing physicians to improve understanding and use of PPC Evidence-based quality metrics Evidence-based best practice guidelines
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H
ospice and palliative medicine (HPM) is an emerging medical subspecialty initially recognized by the American Board of Medical Specialties in 2006. As the Institute of Medicine reported in 2014, health care delivery and the challenges of care at the end of children’s lives have evolved significantly over the past 15 years.1 The last decade has seen the growth of pediatric palliative care (PPC) programs at children’s hospitals and a transformation of the field.2 Fifty percent of children’s hospitals nationwide have a PPC program, with a peak in new program development occurring in 2008.3 New programs are almost immediately impactful, experience high referral volumes, and must quickly expand their workforce.4 Although HPM has a growing body of literature, the evidence for PPC appears to lag behind the clinical growth. Here we provide a focused and practical summary of evidence in pediatric HPM as a primer for those practicing in other subspecialties. Specifically, we review evidence by focusing on a few of the domains in HPM : (1) communication and psychosocial support; (2) pain and symptom management; (3) end-of-life care; and (4) ways to build a better health care system. We hope to strengthen understanding and partnerships between HPM and non-HPM clinicians and investigators and thereby improve patient care for children with serious illnesses.
Case 1 An 18-day-old, term infant presented to the emergency department unresponsive with sepsis and presumed meningitis. Blood and cerebrospinal fluid cultures confirmed group-B streptococcus infection. Given the serious nature of the infant’s condition, the pediatric intensive care unit (PICU) team consulted the PPC team on hospital day 3. With aggressive life-sustaining measures, the infant survived, but sustained significant brain injury, remaining comatose with absent gag reflex and insufficient respiratory effort. The PPC team met with family frequently during the infant’s hospitalization to provide support around understanding of disease and coping with critical illness as well as to address goals of care. Initially, goals were focused on life-sustaining measures. As the severity of the infant’s neurologic condition became clear, family goals slowly shifted toward a comfort-focused approach. Ultimately, after
ACP DNR HPM PICU PPC
Advance care planning Do not resuscitate Hospice and palliative medicine Pediatric intensive care unit Pediatric palliative care
a family meeting with extended family present, the parents chose to focus solely on the infant’s comfort and discontinue all interventions that were prolonging suffering, including the ventilator. The infant died peacefully in his mother’s arms shortly thereafter.
Case 2 A 15-year-old male with Hunter syndrome was well known to his hospital’s PPC team. Many years earlier, his family, knowing the progressive nature of the disease, had chosen to focus on his comfort and quality of life. Enzyme infusions successfully reduced his pain and symptom burden, and he was rarely hospitalized during his first decade of life. Recently, however, he had experienced increased seizures with frequent aspiration events. After an episode of severe pneumonia requiring hospitalization and noninvasive ventilation, his parents asked to speak with the PPC team. Together, they devised an advance care plan for their son that included an out-of-hospital do not resuscitate (DNR) order. Utilizing the Concurrent Care for Children Requirement from the Affordable Care Act, the family chose to continue enzyme infusions while he also received home hospice care. Nine months later, the child had not been rehospitalized and was doing well, so the family discontinued hospice care but maintained the out-of-hospital DNR order. His parents continue to focus on his comfort and quality of life. These cases present different but common scenarios facing PPC teams. A multidisciplinary approach to care allowed 2 different children—1 child with sudden, critical illness and another with chronic disease—to live what their families felt was the best quality of life for as long as possible under the circumstances of their illness. It is important to examine the evidence guiding the practices discussed in these cases.
Communication and Psychosocial Support The literature within the communication domain of HPM focuses on family meetings, decision making, advance care planning (ACP), family coping, and the impact of bereavement. Although there is significant literature focused on adult patients, pediatrics necessitates a stronger focus on the child’s cognitive development and how he or she fits into
From the 1Department of Pediatrics, Nemours/Alfred I. duPont Hospital for Children, Wilmington, DE; 2Sidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, PA; 3Children’s Mercy Hospital and Clinics, Kansas City, MO; and 4 Department of Pediatrics, Children’s Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2015.02.019
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Vol. 166, No. 6 June 2015 the social structure of the family. These differences make it difficult to extrapolate from the adult-based literature. Family Meetings As in our case 1 example, family meetings are a cornerstone tool of HPM, but they have been minimally studied in pediatrics. Nonetheless, it seems clear that these meetings are infrequently used, even for the sickest children.5 In one study, meetings were focused on information exchange and future management. Conferences occurred predominantly for sicker patients, those with complex chronic conditions, and those with PPC consultation.5 Although many clinicians believe that the family meeting is key to the practice of palliative medicine,6 there is minimal evidence regarding families’ perception of such meetings. Decision Making Clinicians can facilitate families’ decision making. Hinds et al7 interviewed parents faced with making noncurative treatment decisions. The families identified components of being a “good parent” to include focusing on their child’s quality of life, advocating for their child with the medical team, and putting their child’s needs above their own.8 By working to define a family’s priorities and values, the clinician can help them fulfill their wishes to “be a good parent” through dire circumstances.8 In a study of parents of PICU patients, 40% of parents preferred sharing decision making with their doctors, 41% preferred autonomous decision making, and 18.9% preferred delegating these decisions to their doctors.9 ACP ACP involves the patient, family, and providers sharing information on the natural course of the child’s disease, individualized prognostic information including trajectory, and the expected experiences of the child.10,11 ACP is a common task for palliative care teams; however, conversations are most productive when the family and clinicians have a common understanding of the child’s disease and prognosis. On average, oncologists recognize 100 days sooner than parents that there is no realistic chance of cure.12 When the poor prognosis for survival is disclosed early, there are earlier discussions of hospice care, earlier DNR orders, and decreased use of chemotherapy in the last month of life. Importantly, there are also better parental ratings of the quality of care in the home. It is also important to include the child in ACP in appropriate ways. Teenagers with HIV/AIDS and those with advanced cancer overwhelmingly express the desire to participate in their own ACP.13-16 Families who decide to speak with their children about death report that they are happy with that decision, and nearly one-third of families who did not discuss death with their child regretted that decision later.16 A single-center study examined generally perceived barriers to ACP and DNR discussions. The top 3 barriers to ACP discussions identified were clinician perception of
unrealistic parental expectations, lack of parent readiness to have the discussion, and discrepancies between clinician and patient/parent understanding of the prognosis.17 The clinicians at that center overwhelmingly felt that ACP/DNR discussions should be initiated on presentation/diagnosis or during a period of stability. Family Coping Families cope and accommodate to their child’s illness using a multitude of supports, coping strategies, and resources. Religion, spirituality, and life philosophy are some tools that can help families cope with adversity.18-20 Hopeful thoughts and language play a major role; many parents use hopeful language about outcomes for their child, even when death is inevitable.18 Impact of Bereavement The death of a child or sibling has a significant effect on the entire family. Youngblut et al21 reported significant negative physical and mental health outcomes in parents 13 months after their child’s death, including newly diagnosed chronic health conditions, posttraumatic stress disorder, and hospitalizations. Psychiatric comorbidities, previous loss, economic hardship, duration and intensity of the child’s treatment, perceptions of medical care, child’s quality of life, and parent preparedness for death all impact parental outcomes.22 Siblings are affected as well and often recognize their parents’ grief.23 Survivor guilt, parental overprotection, and idealization of the deceased child affect sibling bereavement.24 Siblings may be affected by how their parents engage them, allow them to see/hold/touch their ill siblings, and even participate in their care,25,26 although few evidence-based bereavement interventions have been published.27-29
Physical Aspects of Care In contrast to the large body of evidence on palliative pain and symptom management in adults, studies on pediatric patients are scant. Much of the evidence that pediatric HPM clinicians use is drawn from the adult literature, and the medications used are often off-label. Although many of the principles of pain management are consistent across the age spectrum, there are important differences in neonatal and pediatric patients that merit more careful study. Even though the clinical practice of PPC includes symptom management integrated into life-sustaining therapies, much of the PPC literature focuses on pain and symptom management at the end of life. Symptoms at End of Life Children with terminal cancer have a significant burden of pain and symptoms in their last 30 days of life.30 PPC has been shown to lessen this burden, and to help parents feel more prepared during their child’s last months of life and at the time of death.31 Prominent symptoms in the last 24 hours of life include respiratory distress, pain, nausea, vomiting, and anxiety.32 One study found that children who die of advanced 1537
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heart disease also carry a significant symptom burden and poor quality of life in their last 30 days,33 suggesting the need for improved symptom assessment and management in many children with noncancer diagnoses.
End-of-Life Care Resuscitation Status In a study of deaths of hospitalized children at 1 institution, few children had DNR orders before admission, and often orders that were written were done so less than 1 day before death.34 The incidence of DNR orders increased when parents had more education (>15 years) or a higher monthly income.35 On the other hand, a recent report on PICU deaths suggested that DNR orders may be used less often today than in the past.36 We do not know whether PPC involvement increases the frequency of DNR or limited code orders. How and Where Patients Die As access to PPC has increased, the location of death for children dying from oncologic diseases and complex chronic conditions has shifted.37 Nonetheless, children with advanced heart, lung, immune, and infectious diseases continue to die in the PICU after receiving highly technical medical support at the end of life and after the withdrawal of life-sustaining interventions.33,36,38 Patients and families vary in terms of preference for location of end-of-life care,39 and the majority of children die in a hospital setting.40 This can actively change to home deaths with PPC involvement.41 Among patients with advanced cancer, having open discussions about the location of death is associated with increased home deaths.42 Although adult HPM providers use a shift in location of death as an impactful outcome of palliative care involvement, whether PPC will, or even should, have the same impact is less clear. Many children and families become comfortable with the hospital environment over the disease trajectory and actively choose the hospital for end-of-life care.43
Building a Better Health Care System Barriers to Palliative Care A survey of pediatric staff members at the University of California San Francisco identified an uncertain patient prognosis as the primary barrier to PPC referral.44 Additional barriers included the clinician’s perception of the family’s unwillingness to acknowledge the incurable nature of their child’s disease, language barriers, and time constraints. Many pediatricians still associate PPC with hospice care, used only for the end of life.45 In reality, most PPC consults are for facilitating communication; in 1 study, only 30% of consults ended in the patient’s death.46 Cost of Care By clarifying and focusing on individual patient goals of care, adult palliative care teams not only save money by decreasing hospital length of stay, but also help reduce 30-day hospital 1538
Vol. 166, No. 6 readmission rates and decrease emergency department and intensive care unit utilization.47 Pediatric data are currently lacking, however, and some argue that cost avoidance is not a relevant topic in PPC.48 Children with life-limiting diseases experience multiple hospitalizations and spend on average more than 39 days in the hospital in the last year of life.49 Outpatient PPC programs can decrease hospital and emergency department charges and shift care to an in-home setting through a community-based PPC program.50,51 However, to date no study has examined the overall health care costs and potential savings realized by PPC involvement with medically complex hospitalized pediatric patients. Care Delivery Systems There are multiple reports of novel models of PPC delivery, from perinatal palliative care to automated PPC consult triggers to the use of telemedicine. Pediatric hospice patients are eligible for concurrent care (ie, hospice in addition to disease-directed therapy, as in our case 2) through the Affordable Care Act. The use of concurrent care has been reported, but cost savings remain unclear.52,53 Use of the PPC Team Although palliative care offers a variety of expertise, previous studies have demonstrated that the specific services requested of the palliative care team vary and depend largely on the referring service. A survey of PICU physicians identified continuity between hospitalizations, transition to the community setting, and provision of bereavement care for family and staff was the most valuable services offered by the PPC team.54 Critical care physicians were more likely to consult palliative care for psychosocial support of patients and families, and oncologists were more likely to consult for symptom management. In addition, clinicians with self-reported palliative care education were more likely to involve PPC in the care of their patients.55 Best Practices/Quality Improvement Measures Most notably lacking from the PPC literature are data confirming quality metrics and establishing evidence-based best practices for PPC clinicians. Barriers to PPC Research There are many barriers to producing high-quality palliative care research, including funding, institutional capacity, researcher workforce, challenges related to the topic and population (eg, attrition, rare disease entities, heightened human subjects protections), and public and professional misunderstanding of palliative care and aversion to topics related to serious illness and the end of life.56 It is important to focus PPC research on areas that are unique to pediatric patients (eg, developmentally appropriate communication, family coping), those that are unique to PPC (eg, concurrent hospice care, care coordination), and those that cannot be easily extrapolated from adult literature (eg, pain and symptom management). Miller et al
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Discussion The evidence shows that PPC teams improve patient care, and it is no longer acceptable for pediatric patients with access to PPC to die without PPC involvement. It is striking that data on costs of care, best practices, and management lag behind those for ACP. Ullrich and Morrison suggested opportunities for collaboration for future research, stating that PPC “research priorities.should fall into one of two categories. They should be either issues related specifically to children, from which lessons learned from adult research cannot be extrapolated, or unique opportunities for PPC research to inform the provision of palliative care for people of all ages.”57 The Institute of Medicine’s 2014 report echoes this sentiment.1 Pediatric-specific research efforts intended to directly impact clinical care should focus on such areas as developmental considerations to optimize patient and family communication, evidence-based interventions to maximally support family members and aid in decision making, families’ perspective on family meetings, and models for delivery of out-of-hospital PPC (Table; available at www.jpeds.com). Broad application of the current evidence should result in decreased patient suffering and less discrepancy in palliative care between adult and pediatric patients. Such application across pediatric subspecialties will allow clinical and research collaboration to fill in the disease-specific evidence gaps that remain. With approximately 250 pediatricians boardcertified in HPM, we have few practitioners of clinical PPC and even fewer clinician-investigators. New HPM fellows are graduating from 1-year clinical HPM training programs and generally are not being trained to become academic clinician-investigators; consequently, growth of the evidence base for PPC likely will continue to rely on relatively few pediatric investigators and to lean heavily on other fields as partners in advancing this young field. n Submitted for publication Nov 12, 2014; last revision received Jan 30, 2015; accepted Feb 6, 2015. Reprint requests: Elissa G. Miller, MD, Nemours/Alfred I. duPont Hospital for Children, PO Box 269, Wilmington, DE 19899. E-mail: [email protected]
References 1. Institute of Medicine. Dying in America: Improving quality and honoring individual preferences near the end of life. Washington, DC: National Academies Press; 2014. 2. Kang TI, Feudtner C. Advances in pediatric palliative medicine in the United States. Prog Palliat Care 2012;20:331-6. 3. Feudtner C, Womer J, Augustin R, Remke S, Wolfe J, Friebert S, et al. Pediatric palliative care programs in children’s hospitals: a crosssectional national survey. Pediatrics 2013;132:1063-70. 4. Frizzola M, Miller EG. Referrals to a new pediatric palliative care team: details of the first 12 months of operation. J Palliat Med 2014;17:585-8. 5. Michelson KN, Clayman ML, Haber-Barker N, Ryan C, Rychlik K, Emanuel L, et al. The use of family conferences in the pediatric intensive care unit. J Palliat Med 2013;16:1595-601. 6. Fox D, Brittan M, Stille C. The pediatric inpatient family care conference: a proposed structure toward shared decision-making. Hosp Pediatr 2014;4:305-10.
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GRAND ROUNDS 7. Hinds PS, Oakes LL, Hicks J, Powell B, Srivastava DK, Spunt SL, et al. “Trying to be a good parent” as defined by interviews with parents who made phase I, terminal care, and resuscitation decisions for their children. J Clin Oncol 2009;27:5979-85. 8. October TW, Fisher KR, Feudtner C, Hinds PS. The parent perspective: “being a good parent” when making critical decisions in the PICU. Pediatr Crit Care Med 2014;15:291-8. 9. Madrigal VN, Carroll KW, Hexem KR, Faerber JA, Morrison WE, Feudtner C. Parental decision-making preferences in the pediatric intensive care unit. Crit Care Med 2012;40:2876-82. 10. Lotz JD, Jox RJ, Borasio GD, F€ uhrer M. Pediatric advance care planning from the perspective of health care professionals: a qualitative interview study. Palliat Med 2015;29:212-22. 11. Heckford E, Beringer AJ. Advance care planning: challenges and approaches for pediatricians. J Palliat Med 2014;17:1049-53. 12. Wolfe J, Klar N, Grier HE, Duncan J, Salem-Schatz S, Emanuel EJ, et al. Understanding of prognosis among parents of children who died of cancer: impact on treatment goals and integration of palliative care. JAMA 2000;284:2469-75. 13. Wiener L, Zadeh S, Battles H, Baird K, Ballard E, Osherow J, et al. Allowing adolescents and young adults to plan their end-of-life care. Pediatrics 2012;130:897-905. 14. Hinds PS, Oakes LL, Hicks J, Anghelescu DL. End-of-life care for children and adolescents. Semin Oncol Nurs 2005;21:53-62. 15. Lyon ME, McCabe MA, Patel KM, D’Angelo LJ. What do adolescents want? An exploratory study regarding end-of-life decision-making. J Adolesc Health 2004;35:529.e1-6. 16. Kreicbergs U, Valdimarsdottir U, Onelov E, Henter JI, Steineck G. Talking about death with children who have severe malignant disease. N Engl J Med 2004;351:1175-86. 17. Sanderson A, Zurakowski D, Wolfe J. Clinician perspectives regarding the do-not-resuscitate order. JAMA Pediatr 2013;167:954-8. 18. Hexem KR, Miller VA, Carroll KW, Faerber JA, Feudtner C. Putting on a happy face: emotional expression in parents of children with serious illness. J Pain Symptom Manage 2013;45:542-51. 19. Hexem KR, Mollen CJ, Carroll K, Lanctot DA, Feudtner C. How parents of children receiving pediatric palliative care use religion, spirituality, or life philosophy in tough times. J Palliat Med 2011;14:39-44. 20. Robinson MR, Thiel MM, Backus MM, Meyer EC. Matters of spirituality at the end of life in the pediatric intensive care unit. Pediatrics 2006;118: e719-29. 21. Youngblut JM, Brooten D, Cantwell GP, del Moral T, Totapally B. Parent health and functioning 13 months after infant or child NICU/PICU death. Pediatrics 2013;132:e1295-301. 22. Rosenberg AR, Baker KS, Syrjala K, Wolfe J. Systematic review of psychosocial morbidities among bereaved parents of children with cancer. Pediatr Blood Cancer 2012;58:503-12. 23. Youngblut JM, Brooten D. Parents’ report of child’s response to sibling’s death in a neonatal or pediatric intensive care unit. Am J Crit Care 2013; 22:474-81. 24. Wender E, Committee on Psychosocial Aspects of Child and Family Health. Supporting the family after the death of a child. Pediatrics 2012;130:1164-9. 25. Gaab EM, Owens GR, MacLeod RD. Siblings caring for and about pediatric palliative care patients. J Palliat Med 2014;17:62-7. 26. Fanos JH, Little GA, Edwards WH. Candles in the snow: ritual and memory for siblings of infants who died in the intensive care nursery. J Pediatr 2009;154:849-53. 27. Forte AL, Hill M, Pazder R, Feudtner C. Bereavement care interventions: a systematic review. BMC Palliat Care 2004;3:3. 28. Cortezzo DE, Sanders MR, Brownell EA, Moss K. End-of-life care in the neonatal intensive care unit: experiences of staff and parents. Am J Perinatol 2014; http://dx.doi.org/10.1055/s-0034-1395475. 29. Capitulo KL. Evidence for healing interventions with perinatal bereavement. MCN Am J Matern Child Nurs 2005;30:389-96. 30. Wolfe J, Grier HE, Klar N, Levin SB, Ellenbogen JM, Salem-Schatz S, et al. Symptoms and suffering at the end of life in children with cancer. N Engl J Med 2000;342:326-33. 1539
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31. Wolfe J, Hammel JF, Edwards KE, Duncan J, Comeau M, Breyer J, et al. Easing of suffering in children with cancer at the end of life: is care changing? J Clin Oncol 2008;26:1717-23. 32. Ho C, Straatman L. A review of pediatric palliative care service utilization in children with a progressive neuromuscular disease who died on a palliative care program. J Child Neurol 2013;28:40-4. 33. Blume ED, Balkin EM, Aiyagari R, Ziniel S, Beke DM, Thiagarajan R, et al. Parental perspectives on suffering and quality of life at end-oflife in children with advanced heart disease: an exploratory study. Pediatr Crit Care Med 2014;15:336-42. 34. McCallum DE, Byrne P, Bruera E. How children die in hospital. J Pain Symptom Manage 2000;20:417-23. 35. Hileli I, Weyl Ben Arush M, Hakim F, Postovsky S. Association between religious and socio-economic background of parents of children with solid tumors and DNR orders. Pediatr Blood Cancer 2014;61:265-8. 36. Burns JP, Sellers DE, Meyer EC, Lewis-Newby M, Truog RD. Epidemiology of death in the PICU at five US teaching hospitals. Crit Care Med 2014;42:2101-8. 37. Feudtner C, Feinstein JA, Satchell M, Zhao H, Kang TI. Shifting place of death among children with complex chronic conditions in the United States, 1989-2003. JAMA 2007;297:2725-32. 38. Lee KJ, Tieves K, Scanlon MC. Alterations in end-of-life support in the pediatric intensive care unit. Pediatrics 2010;126:e859-64. 39. Kassam A, Skiadaresis J, Alexander S, Wolfe J. Parent and clinician preferences for location of end-of-life care: home, hospital or freestanding hospice? Pediatr Blood Cancer 2014;61:859-64. 40. Brandon D, Docherty SL, Thorpe J. Infant and child deaths in acute care settings: implications for palliative care. J Palliat Med 2007;10: 910-8. 41. Gupta N, Harrop E, Lapwood S, Shefler A. Journey from pediatric intensive care to palliative care. J Palliat Med 2013;16:397-401. 42. Dussel V, Kreicbergs U, Hilden JM, Watterson J, Moore C, Turner BG, et al. Looking beyond where children die: determinants and effects of planning a child’s location of death. J Pain Symptom Manage 2009;37: 33-43. 43. Lowton K. “A bed in the middle of nowhere”: parents’ meanings of place of death for adults with cystic fibrosis. Soc Sci Med 2009;69:1056-62. 44. Davies B, Sehring SA, Partridge JC, Cooper BA, Hughes A, Philp JC, et al. Barriers to palliative care for children: perceptions of pediatric health care providers. Pediatrics 2008;121:282-8. 45. Thompson LA, Knapp C, Madden V, Shenkman E. Pediatricians’ perceptions of and preferred timing for pediatric palliative care. Pediatrics 2009;123:e777-82. 46. Feudtner C, Kang TI, Hexem KR, Friedrichsdorf SJ, Osenga K, Siden H, et al. Pediatric palliative care patients: a prospective multicenter cohort study. Pediatrics 2011;127:1094-101. 47. Ranganathan A, Dougherty M, Waite D, Casarett D. Can palliative home care reduce 30-day readmissions? Results of a propensity score-matched cohort study. J Palliat Med 2013;16:1290-3.
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Vol. 166, No. 6 48. Meier DE, Beresford L. Pediatric palliative care offers opportunities for collaboration. J Palliat Med 2007;10:284-9. 49. Chavoshi N, Miller T, Siden H. Resource utilization among individuals dying of pediatric life-threatening diseases. J Palliat Med 2013; 16:1210-4. 50. Postier A, Chrastek J, Nugent S, Osenga K, Friedrichsdorf SJ. Exposure to home-based pediatric palliative and hospice care and its impact on hospital and emergency care charges at a single institution. J Palliat Med 2014;17:183-8. 51. Gans D, Kominski GF, Roby DH, Diamant AL, Chen X, Lin W, et al. Better outcomes, lower costs: palliative care program reduces stress, costs of care for children with life-threatening conditions. Policy Brief UCLA Cent Health Policy Res 2012;1-8. 52. Miller EG, Laragione G, Kang TI, Feudtner C. Concurrent care for the medically complex child: lessons of implementation. J Palliat Med 2012;15:1281-3. 53. Lindley LC, Edwards S, Bruce DJ. Factors influencing the implementation of health care reform: an examination of the concurrent care for children provision. Am J Hosp Palliat Care 2013; 31:527-33. 54. Jones PM, Carter BS. Pediatric palliative care: feedback from the pediatric intensivist community. Am J Hosp Palliat Care 2010;27: 450-5. 55. Atwood MA, Hoffmann RG, Yan K, Lee KJ. Attitudes about palliative care: a comparison of pediatric critical care and oncology providers. Am J Hosp Palliat Care 2013;31:665-71. 56. Chen EK, Riffin C, Reid MC, Adelman R, Warmington M, Mehta SS, et al. Why is high-quality research on palliative care so hard to do? Barriers to improved research from a survey of palliative care researchers. J Palliat Med 2014;17:782-7. 57. Ullrich C, Morrison RS. Pediatric palliative care research comes of age: what we stand to learn from children with life-threatening illness. J Palliat Med 2013;16:334-6. 58. October TW, Watson AC, Hinds PS. Characteristics of family conferences at the bedside versus the conference room in pediatric critical care. Pediatr Crit Care Med 2013;14:e135-42. 59. Young B, Dixon-Woods M, Windridge KC, Heney D. Managing communication with young people who have a potentially life threatening chronic illness: qualitative study of patients and parents. BMJ 2003;326:305. 60. Liberman DB, Pham PK, Nager AL. Pediatric advance directives: parents’ knowledge, experience, and preferences. Pediatrics 2014;134:e436-43. 61. Pritchard M, Burghen EA, Gattuso JS, West NK, Gajjar P, Srivastava DK, et al. Factors that distinguish symptoms of most concern to parents from other symptoms of dying children. J Pain Symptom Manage 2010;39: 627-36. 62. Keele L, Keenan HT, Sheetz J, Bratton SL. Differences in characteristics of dying children who receive and do not receive palliative care. Pediatrics 2013;132:72-8.
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Table. Summary of progress to date and needed future investigations Topic Communication and psychosocial support Family meetings
Decision making
ACP
Family coping Bereavement support
Physical aspects of care Pain and symptom management
Symptoms at end of life End of life care Resuscitation status
How and where patients die Building a better healthcare system Barriers to palliative care
Cost of care
Research progress to date Family meetings rarely occur.5 Effective in aiding decision making.58 An evidence-based structure for family conferences exists.6 Families differ in their approach to decision making (shared vs autonomous vs delegation).9 Parents differ in what it means to be a “good parent,” making it challenging to best to support families with difficult treatment decisions.7,8 Teens want to participate in ACP.13-16 Teens feel marginalized when excluded from ACP discussions.59 Families who discussed dying with their children did not regret it after the death of their child.16 Family caregivers view the advance directive as a way to have more control over what happened to their child.60 Families rely on various coping strategies when their child has a serious illness.18,19 Families use spirituality in their coping after the death of a child,20 although they often have negative physical and mental health outcomes.21 Siblings are affected as well.23-25 There are few evidence-based bereavement interventions for siblings.27
Ideal timing/frequency of family meetings Whether routine family meetings affect patient-level outcomes (eg, length of stay, family and/or provider satisfaction with care) Evidence-based methods of providing decision support, including how to clearly communicate patient’s clinical status, review the benefits/harms of medical interventions, and discuss goals of care1
The most distressing symptoms have been identified by patients and families.30,61 All palliative symptom management research to date has been in adult populations. PPC helps decrease patients’ suffering at end of life and improves parents’ sense of preparedness before the death of the child.30,31,33
Pharmacologic and nonpharmacologic interventions merit robust study, including effectiveness of different medications and potential problems of polypharmacy
Best time for prognostic revelation and ACP discussions Best ways to communicate and document ACP discussions
Evidence-based strategies for providers to elicit and support family coping strategies Complicated bereavement risk-group identification Evidence-based parent and sibling bereavement interventions
Tools for symptom assessment in non–cancer patient populations
DNR orders are commonly placed just prior to a child’s death.34,35 Death in the PICU continues to be common in children after withdrawal of technological support.38 PPC teams help shift the location of death away from PICU and inpatient settings to home and hospice settings.37,39,41,62
Whether the involvement of a PPC team leads to earlier limits on resuscitative efforts Technology-based decision aids (eg, videos, apps) for parents and pediatric patients Identification and clarification of factors that influence the preferred location of death
Uncertain patient prognosis.44 Clinician perception of family “readiness” for PPC/ACP discussions.17 Misperception that palliative care is equivalent to hospice or only for the end of life.45 Adult palliative care programs reduce emergency department and intensive care unit utilization, decrease hospital length of stay, and cut costs,47 as do outpatient PPC programs.50,51
Comparison of clinician perception of parent readiness to engage with PPC vs parent report of readiness Interventions to facilitate earlier PPC involvement and earlier ACP
Care delivery systems
There are multiple proof-of-concept descriptions, but no studies of novel modes of PPC delivery.
Use of the PPC team
Clinicians from different subspecialties consult PPC for different reasons.54 Clinicians with self-reported PPC education are more likely to involve PPC in the care of their patients.55 None exist.
Best practices/quality improvement measures Barriers to PPC research
Proposed needed investigation
Barriers to PPC research include lack of funding, institutional capacity, and research workforce. Additional challenges include public and professional misunderstanding of the field.56
Pediatric Palliative Care: Current Evidence and Evidence Gaps
Overall health care cost and potential savings of PPC involvement with medically complex, hospitalized pediatric patients Cost of PPC team (eg, salaries) weighed against healthcare dollars saved through outpatient PPC Evidence-based PPC team structure/staffing Effect of concurrent care on cost of care, family perceptions of care, and treatment decisions Evidence-based educational models for practicing physicians to improve understanding and use of PPC Evidence-based quality metrics Evidence-based best practice guidelines
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