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Journal of Clinical Oncology, Vol 26, No 10 (April 1), 2008: pp. 1717-1723 © 2008 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.14.0277 Easing of Suffering in Children With Cancer at the End of Life: Is Care Changing?
From the Departments of Pediatric Oncology and Medical Oncology, and the Center for Outcomes and Policy Research, Dana-Farber Cancer Institute; Departments of Medicine and Anesthesia, Children's Hospital Boston; Departments of Psychiatry and Medicine, Brigham and Women's Hospital; and Harvard Medical School, Boston, MA Corresponding author: Joanne Wolfe, MD, MPH, Dana-Farber Cancer Institute, 44 Binney St, SM-205, Boston, MA 02115; e-mail: Joanne_wolfe{at}dfci.harvard.edu
Purpose In the past decade studies have documented substantial suffering among children dying of cancer, prompting national attention on the quality of end-of-life care and the development of a palliative care service in our institutions. We sought to determine whether national and local efforts have led to changes in patterns of care, advanced care planning, and symptom control among children with cancer at the end of life. Methods Retrospective cohort study from a US tertiary level pediatric institution. Parent survey and chart review data from 119 children who died between 1997 and 2004 (follow-up cohort) were compared with 102 children who died between 1990 and 1997 (baseline cohort). Results In the follow-up cohort, hospice discussions occurred more often (76% v 54%; adjusted risk difference [RD], 22%; P < .001) and earlier (adjusted geometric mean 52 days v 28 days before death; P = .002) compared with the baseline cohort. Do-not-resuscitate orders were also documented earlier (18 v 12 days; P = .031). Deaths in the intensive care unit or other hospitals decreased significantly (RD, 16%; P = .024). Parents reported less child suffering from pain (RD, 19%; P = .018) and dyspnea (RD, 21%; P = .020). A larger proportion of parents felt more prepared during the child's last month of life (RD, 29%; P < .001) and at the time of death (RD, 24%; P = .002). Conclusion Children dying of cancer are currently receiving care that is more consistent with optimal palliative care and according to parents, are experiencing less suffering. With ongoing growth of the field of hospice and palliative medicine, further advancements are likely.
We previously reported on the experience of children who died of cancer between 1990 and 1997, demonstrating that they experienced substantial suffering at the end of life, and that communication with parents was often deficient.1,2 The need for extensive improvements in the care of children with advanced illness has been confirmed in other studies.3-14 Spurred in part by the publication of these studies, international attention has been focused on end-of-life quality of care both for adults and children with cancer.15-20 A consistent recommendation that has emerged from this discussion is the need to better integrate palliative care into the treatment of patients with life-threatening illness. Attempts to achieve this goal have occurred at the local level (eg, through development of palliative care services21-24) and nationally (eg, through educational programs for oncologists25-27 and formalized training programs in hospice and palliative medicine28,29). Clinicians at the Dana-Farber Cancer Institute (DFCI) and Children's Hospital Boston (CHB) have been exposed to both local and national efforts to improve the care of children with advanced cancer over the past decade. Prompted by our study findings,1,2 the Pediatric Advanced Care Team (PACT) was developed in 1997. The goals of this interdisciplinary palliative care service are to improve communication, symptom control, and quality of life in children with advanced cancer and their families. PACT's development was facilitated through participation in a 1 year-long national initiative to improve end-of-life care.30 Three strategies have been used by the service to improve the care of children and families. First, PACT clinicians provide ongoing education about palliative care to pediatric oncology practitioners through PACT rounds, a monthly interdisciplinary case-based conference, as well as through discipline-specific educational sessions. Second, PACT provides clinical consultations to the medical team and the patient and/or family in the inpatient, outpatient, and home settings. A PACT consult team typically involves a physician, nurse, and social worker working with the primary team and family to delineate goals of care; subsequent recommendations stem from these goals. Third, PACT clinicians have led efforts to develop system-wide improvements designed to foster a more consistent, yet flexible approach to caring for children with advanced cancer. Examples include the direct admission policy, which allows dying children to be admitted directly to the oncology ward, rather than first being attended to in the emergency department, and the comfort corner, a home-like suite on the inpatient oncology ward. An in-depth description of PACT activities is beyond the scope of this article but has been previously published.31 We sought to determine whether these national and local efforts have led to changes in patterns of care, advanced care planning, and symptom control among children cared for at the end of life in our centers.
Study Design As previously reported,1,2 we interviewed 102 parents of children cared for at the DFCI and CHB, who died of cancer between January 1990 and June 1997, and reviewed the charts. The findings from that study serve as the baseline cohort in this analysis. We subsequently used similar methods and a subset of items from the original study instrument to survey parents of children who died of cancer between July 1997 and December 2004 (follow-up cohort). Surveys were conducted by telephone, in person, or by paper and pencil format, at the parent's discretion. For parents whose child died between 2000 and 2004, we invited both the mother and father to participate. However, for this analysis, only responses from the parent who first completed the survey were included. Parents were considered eligible if they were English-speaking, lived in North America, and their child's former oncologist permitted us to contact them (such permission was denied in the instance of 16 families). Eligible parents were sent a letter containing a postage-paid opt-out card that they could return if they did not want to participate. Of the 223 eligible families, 168 had viable addresses and were contacted, and 119 agreed to participate, for an overall response rate of 71% (as compared with 72% for the baseline cohort). There were no statistically significant differences in sex, diagnosis, and duration of disease between the children of respondents and nonrespondents; however, children of nonresponders were older (mean age at death, 13.2 v 10.4 years; P = .01). The institutional review board of the DFCI/CHB approved the study. All parents gave oral informed consent. Parents were informed in the introductory letter and interview that psychosocial support was available if desired.
Data Collection Parent survey. Parents were asked whether the child experienced pain, dyspnea, fatigue, and anxiety during the last month of life and were also asked to rate the degree to which the child suffered from these symptoms. Response categories included "a great deal", "a lot", "some", "a little", or "no" suffering. In the baseline cohort, the item asking about suffering from anxiety was added toward the end of this study and is only available for a subset of parents (n = 29). Parents were also asked how prepared they felt for the kinds of medical problems experienced by the child during the end-of-life care period ("very prepared", "somewhat prepared", "a little prepared", "not at all prepared") and for the circumstances at the time of death.
Statistical Analysis
Characteristics of Participants The characteristics of the children and the responding parents are summarized in Table 1. Characteristics of the children did not differ significantly between cohorts. In the follow-up cohort, a significantly greater number of parent respondents were male and interviews were conducted 1 year earlier on average as compared with the baseline cohort.
Patterns of Care at the End of Life Table 2 presents crude and adjusted results related to patterns of care at the end of life comparing the follow-up with the baseline cohort. In multivariate analyses, there was no significant difference between cohorts in the proportion of children whose charts documented discussions about poor prognosis and there was also no difference in the time before death that cancer-directed therapy was discontinued. However, there was a 22 percentage point increase in the documentation of discussion about hospice in the follow-up cohort (76% [95% CI, 73 to 79] v 54% [95% CI, 51 to 57] for the baseline cohort; P < .001), after accounting for physician clustering and adjusted by type of death. Relative to date of death, hospice discussions occurred earlier in the follow-up cohort (adjusted geometric mean, 52 days [95% CI, 41 to 65] v 28 days [95% CI, 21 to 38] before death for the baseline cohort; P = .002). DNR orders were more commonly documented among children in the follow-up cohort (78% [95% CI, 77 to 80] v 67% [95% CI, 65 to 68] for the baseline cohort; P = .051) and were also documented earlier (geometric mean, 18 days [95% CI, 13 to 25] compared with 12 days [95% CI, 9 to 15] before death for the baseline cohort; P = .031). There was no statistically significant difference in the proportion of children dying at home (44% in the follow-up cohort v 49% in the baseline cohort). However, among children who died in hospitals, there was a 16% absolute decrease in the proportion of deaths occurring in the intensive care unit or an outside hospital in the follow-up cohort (22% [95% CI, 19 to 26] v 38% [95% CI, 35 to 42] in the baseline cohort; P = .024). There was no significant difference in the proportion of children who were seen by the pain team. In the follow-up cohort, almost half of all children received direct palliative care consultation from PACT.
Parents' Perception of Child's End-of-Life Course The proportion of children who, according to their parents, experienced fatigue, pain, dyspnea, and anxiety did not differ between baseline and follow-up cohorts (Fig 1). However, reports of "a great deal" or "a lot" of suffering decreased in the follow-up cohort for all symptoms except fatigue. Accounting for physician clustering, and adjusting by cause of death and parent sex, there was a decrease in the proportion of parents reporting "a great deal" or "a lot" of suffering from pain (47% [95% CI, 45 to 48] compared with 66% [95% CI, 65 to 67] in the baseline cohort; adjusted risk difference [RD], 19%; P = .018) and dyspnea (37% [95% CI, 37 to 38] v 58% [95% CI, 57 to 58]; RD, 21%; P = .020), and a trend toward decreased suffering from anxiety (39% [95% CI, 38 to 40] v 58% [95% CI, 57 to 59]; RD, 19%; P = .093).
In the follow-up cohort, 29% more parents reported feeling "very prepared" for the medical problems experienced by the child at the end of life (56% [95% CI, 54 to 57]) as compared with the baseline cohort (27% [95% CI, 26 to 28]; P < .001) and 24% more parents felt "very prepared" for the circumstances at the time of death (49% [95% CI, 49 to 51] v 25% [95% CI, 24 to 26]; P = .002; Table 3).
For all multivariate models, further adjustment by time elapsed since death including a sensitivity analysis did not significantly alter results.
Given widespread national and local initiatives to improve the care of children with cancer at the end of life, we sought to discern what changes, if any, occurred in the end-of-life experience of children at our institutions. We found positive changes in several key domains of care identified as high priorities by the National Consensus Project for Quality Palliative Care,33 as well as by parents and physicians of children at the end of life.34 Notably, elements of advanced care planning improved as reflected in more frequent and earlier discussions by physicians about hospice and earlier documentation of DNR orders before death. While some of the statistically significant differences found were small (eg, DNR orders were written an average of 6 days earlier) and others, such as discussion of incurability, while larger did not reach statistical significance, all patterns of care investigated showed a consistent trend toward earlier and/or more frequent documentation, which seems to support the hypothesis that advanced planning is now often part of the care process. Parents also appear to have been better prepared for their child's end-of-life course, a quality of care outcome highly valued by bereaved parents.34 We also found that according to parents, children are experiencing significantly less suffering related to prevalent symptoms, such as pain and dyspnea at the end of life, and at least one indicator of psychological distress, anxiety, also improved. That distress related to fatigue did not improve, a complex symptom known to be less mutable, provides compelling, if indirect evidence, that improvements do not simply reflect a shift in reporting. Relief of child's end-of-life distress may have long-lasting implications for bereaved parents, who are negatively affected by the child's experience of pain years beyond the death.13 Also worth noting, significantly fewer children died in the intensive care unit. Although death in the intensive care unit is not necessarily an indicator of poor quality of care, the change in location of death may indicate that when given choices, parents and children opt for alternative settings.35 In our setting, the comfort corner, a home-like suite in the hospital with care provided by clinicians well known to the family, may represent a preferred choice. Increasing opportunities for death outside the intensive care unit may also be associated with cost savings.36 Finally, findings suggest that outcomes may even have been improved among children who died of treatment-related complications. In the earlier cohort, we identified little, if any, advanced care planning for children who died a toxic death, despite the fact that all had serious, life-threatening illnesses. Current understanding of parent goals of care suggest there is continued hope for life extension even until the very end of life for most children with advanced cancer2,37 and this may account for why there was no change in use of cancer-directed therapy in the follow-up cohort. For certain types of childhood malignancies, this hope can result in pursuing more intensive interventions, such as stem-cell transplantation, with associated higher risks of life-threatening complications.38 Given our small sample size, a true stratified analysis was not possible; however, findings suggest that further evaluation of the impact of palliative care interventions in children at risk for life-threatening, treatment-related complications is warranted. It is important to emphasize that we cannot determine the relative contributions of specific components of our quality improvement efforts in leading to improved outcomes. In all likelihood, the changes we observed are attributable to a combination of secular trends and local quality improvement efforts. Increased focus on end-of-life care in the medical field and mass media, and the presence of national recommendations advocating for palliative care as an expected standard of care17 are likely to have impacted clinical practice at an individual level. In addition, hospital-based palliative care teams such as PACT involve a myriad of strategies that extend beyond direct clinical care.31 In order to isolate the effects of local from more global efforts, a randomized controlled trial would have been needed. However, we chose a time series design rather than a randomized trial for several reasons. First, given that palliative care services had already been associated with small but positive improvements in end-of-life outcomes,24,39-42 a nonintervention control arm would have raised ethical concerns. Second, data suggested that clinicians were responding to the evidence that dying children were experiencing unacceptably high level of suffering with "trial and error" strategies43 warranting immediate action; there was a need for systematic clinician education. Finally, compelling single-site results were needed before undertaking a multi-institutional cluster randomized trial, the only design possible given the system-wide interventions involved. We made every effort to protect against bias. The evaluation methods used were rigorous and combined professionally determined outcomes44 with family-centered standards as advocated by experts in the field.45,46 Recruitment and surveys in the baseline and follow-up cohorts used the same methods. Finally, child and parent characteristics that might affect outcomes were accounted for in the analyses. Other limitations should be considered. Given the retrospective nature of this study, the child's perspective was not included although we aim to do so in future prospective studies. In the interim, parents remain the primary voice, which is consistent with care approaches throughout pediatrics. Interestingly, Russell et al47 found a strong agreement and consistency between parent and child reports across multiple quality-of-life domains, which led to the conclusion that when the child is too ill to provide a self-report, parent-reported quality of life can be a reliable substitute. Another potential limitation could be selection bias. Families who opted out or whose doctor denied us permission may have had worse outcomes than those enrolled. However, both the baseline and follow-up surveys had a similar proportion of nonresponders (29% for both cohorts) and therefore we believe the cohorts remain comparable. Can the palliative care prototype at our institution be exported to other institutions? PACT has been fortunate to benefit from a strong level of support from the leadership at both institutions, as well as strong collaboration with other pediatric subspecialists, essential prerequisite components for successful implementation and acceptance of such a program. A number of major pediatric centers throughout North America have recently implemented programs48 with components similar to PACT, suggesting that this is a feasible strategy. Our results suggest that increased focus on the palliative care needs of children with advanced cancer and their families creates an environment that fosters significantly improved end-of-life care, with parents reporting better preparedness for the end-of-life course and decreased suffering in their children, as well as substantial improvements in advanced care planning. The field of hospice and palliative medicine has gained formal recognition, and subspecialty training and certification is now being sponsored by 10 specialty boards of the American Board of Medical Specialties, including pediatrics.49 With time, and a growing academic community, pediatric palliative care experts will promote the evaluation and development of more targeted interventions to further ease suffering in children with cancer at the end of life. The potential benefits of such labors could be substantial and long lasting.
The author(s) indicated no potential conflicts of interest.
Conception and design: Joanne Wolfe, Jim F. Hammel, Kelly E. Edwards, Holcombe E. Grier, Charles Berde, Veronica Dussel, Jane C. Weeks Financial support: Joanne Wolfe Administrative support: Sarah A. Aldridge Provision of study materials or patients: Janet Duncan Collection and assembly of data: Joanne Wolfe, Jim F. Hammel, Kelly E. Edwards, Michael Comeau, Joanna Breyer, Sarah A. Aldridge Data analysis and interpretation: Joanne Wolfe, Jim F. Hammel, Veronica Dussel Manuscript writing: Joanne Wolfe, Jim F. Hammel, Holcombe E. Grier, Charles Berde, Veronica Dussel, Jane C. Weeks Final approval of manuscript: Joanne Wolfe, Jim F. Hammel, Kelly E. Edwards, Janet Duncan, Michael Comeau, Joanna Breyer, Sarah A. Aldridge, Holcombe E. Grier, Charles Berde, Veronica Dussel, Jane C. Weeks
We are appreciative of the collaborative care of children with advanced cancer provided by PACT clinicians, including Tamara Vesel, MD, and Marsha Joselow, MSW, and primary oncology teams. We are immensely grateful for participating parents' willingness to share cherished perspectives about their child's end-of-life experience.
Supported by Grant No. NCI 5 K07 CA096746 from the National Cancer Institute and a Child Health Research Grant from the Charles H. Hood Foundation Inc (J.W.); by the Office of Enrichment Programs, Harvard Medical School (J.H.); by the Alexandra Miliotis Fellowship in Pediatric Oncology and the Neil Samuel Ghiso Foundation also through the Office of Enrichments Programs, Harvard Medical School (K.E.E.); and by a fellowship from the Agency for Health Research and Quality (T32HP10018; V.D.). The Pediatric Advanced Care Team has been generously supported by grants from the Hasbro Children's Foundation (1998 to 2000), the Education Development Center's Initiative for Pediatric Palliative Care (2000 to 2002), and the Stephen E. and Catherine Pappas Palliative Care Fund (2004 to 2014). Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2008 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
