Journal of Perinatology (2015) 35, 223–228 © 2015 Nature America, Inc. All rights reserved 0743-8346/15 www.nature.com/jp
ORIGINAL ARTICLE
End-of-life care in a regional level IV neonatal intensive care unit after implementation of a palliative care initiative C Samsel1,2 and BE Lechner1,3 OBJECTIVE: We hypothesized that the implementation of a neonatal palliative care initiative will result in improved markers of end-of-life care. STUDY DESIGN: A retrospective and prospective chart review of neonatal intensive care unit deaths was performed for 24 months before, 16 months during and 24 months after the implementation of palliative care provider education and practice guidelines (n = 106). Ancillary care, redirection of care, palliative medication usage and outcome meetings in the last 48 h of life and basic demographic data were compared between epochs. Parametric and nonparametric analysis was performed. RESULT: There was an increase in redirection of care and palliative medication usage and a decrease in variability of use of end-of-life interventions (P = 0.012, 0.022 and o0.001). CONCLUSION: The implementation of a neonatal palliative care initiative was associated with increases in palliative interventions for neonates in their final 48 h of life, suggesting that such an initiative may enhance end-of-life care. Journal of Perinatology (2015) 35, 223–228; doi:10.1038/jp.2014.189; published online 23 October 2014
INTRODUCTION Pediatric palliative care aims to improve the quality-of-life of children faced with life-threatening or life-limiting illness. Of children who die in the United States, over half are infants (o 1 year) and of those, over 65% are neonates.1 Most neonates and infants who die do so in the intensive care unit setting.2 Thus, a significant number of neonates require palliative care services in the NICU (neonatal intensive care unit). A recent study of 653 neonatologists showed that over 95% believe palliative care programs are important and are needed to improve quality of care but cited difficulties with support including stigma, funding, implementation and lack of evidence of palliative care efficacy in the literature.3 While the numbers of pediatric palliative care programs in the United States are increasing in response to the need,4 dying neonates are receiving less palliative care than pediatric patients5 and little is known about neonatal palliative care programs or interventions. At the same time, there is a clear need for quality palliative care in the NICU.6 Training of neonatology fellows in end-of-life care7,8 is also lacking, as clinicians are often not comfortable with providing palliative care to neonates.9 While the development of guidelines for the provision of palliative care in the NICU have been reported,10,11 as well as the impact of a palliative care consultation,12 to our knowledge, there are no studies evaluating the impact of the implementation of a palliative care intervention within the NICU on outcomes of dying infants. We hypothesized that the implementation of a neonatal palliative care intervention in a level IV NICU setting will result in improved end-of-life care for dying neonates as evidenced by improved discussion of prognosis with parents, increased care redirection, increased palliative medicine use at the end of life and greater utilization of supportive ancillary care teams at the end of life.
METHODS Design A retrospective and prospective chart review was performed of deaths at an 80-bed regional level IV NICU for 24 months before, 16 months during intervention implementation and 24 months after the implementation of a neonatal palliative care initiative from January 2008 through April 2013. The pre-implementation group underwent a retrospective chart review, while the during and post-implementation groups underwent a prospective chart review. Inclusion criterion for the study was death of the neonate in the NICU. The 16-month epoch during the implementation of the intervention was necessary due to the stepwise nature of the implementation of the study. The initial educational lectures were given at the beginning of this 16-month period and the final approval and implementation of the end-of-life guidelines and the electronic order set were at the end of the 16-month period.
Intervention description Prior to the development of this intervention, a consultative model was used as the standard approach to palliative and end-of-life care in our NICU, in which dying patients received palliative interventions on an asneeded basis. The disadvantage of this approach is a lack of consistency over shifts. Similarly to the model described by others,13 the moral distress experienced by care providers in some difficult cases led to the development of a NICU palliative care initiative with the goal of shifting care of dying neonates from the consultative model to a team collaborative model, as described by others.13 A multidisciplinary committee was formed that consisted of representatives of all disciplines that are involved in the care of neonates in our NICU (attending physicians, fellows, residents, nurse practitioners, nurses, nurse managers, respiratory therapists, occupational therapists, lactation consultants, pharmacists, nutritionists, social workers, chaplains and bereaved family members). This committee developed three main foci for the NICU palliative care intervention: provider education, formal practice guideline development
1 Department of Neonatology, Women and Infants Hospital, Providence, RI, USA; 2Triple Board Residency Program, Brown University and Rhode Island Hospitals, Providence, RI, USA and 3Warren Alpert Medical School of Brown University, Providence, RI, USA. Correspondence: Dr B Lechner, Department of Pediatrics, Women & Infants' Hospital of Rhode Island, 101 Dudley Street, Providence 02905, RI, USA. E-mail: [email protected] Received 11 July 2014; revised 28 August 2014; accepted 2 September 2014; published online 23 October 2014
Neonatal end-of-life care initiative results C Samsel and BE Lechner
224 and communication skills training. A discussion of the communication skills training and its outcomes is beyond the scope of this study. The provider education component and formal practice guidelines were developed as follows: As part of the educational component of the initiative, the intervention was launched with a conference on neonatal palliative care aimed at the entire Department of Pediatrics at Women and Infants Hospital of Rhode Island. This conference was aimed at educating providers on the current state of perinatal and neonatal palliative and end-of-life care. The conference was held jointly by a local neonatologist and an outside pediatric palliative care specialist. Further educational interventions included multiple smaller conferences on the basis of neonatal palliative care aimed at neonatology fellows as well as the NICU nursing staff. Most neonatologists, fellows and ancillary staff attended at least one such conference. Additionally, all nurses had access to an intranet based learning module recapitulating the conference material as well as the order set. For the practice guideline development component, a mission statement for the NICU palliative care initiative, NICU end-of-life care guidelines, an order set (Supplementary Appendix 1) as well as a local pediatric hospice program discharge resource guide were developed by the aforementioned multidisciplinary committee. The guidelines were developed based on committee discussions, while various components were adapted and modified from neonatal palliative care guidelines in the literature,10,11 the AAP palliative care statement,14 and a protocol from CHOP (shared by D. Munson). The medication protocol was developed in conjunction with a perinatal pharmacist. The work product of the committee was circulated among physicians, nurse practitioners, fellows, nursing and all other ancillary staff in the NICU and made available on all NICU computer stations. The end-of-life order set was made available within the NICU's computer ordering system and all staff who write orders were in service. The multidisciplinary NICU palliative care group continues to meet on a bimonthly basis.
Procedure Data were collected via Institutional review board-approved chart review from Women and Infants Hospital paper and electronic patient records. All data were reviewed and analyzed after primary collection. Data were collected on gender, gestational age, NICU length of stay, time of death, diagnosis, birth weight, ethnicity, race, religion, maternal age and primary diagnosis. In the last 48 h of life, data were collected on the documentation of redirection of care, outcome expectation meetings between providers and families, palliative medication usage and ancillary service consultation. The final 48 h period was chosen as the timeframe to assess end-of-life care, as adapted from a study examining the role of palliative care consultation in neonatal end-of-life care,12 given the pathophysiology of the typical dying infant in the NICU setting. The disease processes that lead to death in the NICU often cause death in a more rapidly progressive manner than in older children or adults, typically leading to shorter periods of the dying process than in older patients. Redirection of care to comfort care was defined as at least one of the following: a change in Do Not Resuscitate status, documentation of redirection of care to comfort care, use of the palliative care order set or compassionate extubation. In addition to at least one of the above indicators, the absence of all of the following aggressive life-sustaining interventions was necessary in the 48 h prior to death for redirection of care to comfort care to occur: cardiopulmonary resuscitation, the use of epinephrine, transfusions, inotropic agents, intubation and central line placement. Outcome expectation meetings were defined as documented meetings between a physician or nurse practitioner and at least one guardian, in which disclosure and education of poor clinical status or outcomes was disseminated with an option of redirection of care goals to comfort care only. Palliative medications were defined as medication documented to assist with the comfort of a neonate at the end of life. Furthermore, in two cases, the use of morphine in 3 h prior to death without documentation of reasoning was deemed to exhibit a clear pattern of redirection of care based on consensus of the investigators in reviewing other orders and documentation (that is, discontinuation of ventilation, nutrition, antibiotics, so on, followed by morphine administration). To reach this conclusion in these two cases, the investigators independently assessed relevant information, including chart documentation and orders as well as the Journal of Perinatology (2015), 223 – 228
timing thereof, and then compared the two independent assessments, both of which came to the same conclusion. Ancillary service consultation was defined as documented contact with the departments of social work or chaplaincy. We only included this measure as present, if a note or document from the ancillary service or other team member's note documented contact with one of these services in the last 48 h of life. Theoretically, the fact that the authors were also involved in patient care may introduce a bias to the data. However, one author was involved in roughly 3% of deaths as a resident, all of which took place before he became involved in the project, and the other author was involved in o10% of deaths as an attending physician. Given the large number of staff of various disciplines that provide care in the NICU, the overlap between intervention planning group and clinical care providers was minimal (range of 1–12% per discipline).
Data analysis Parametric testing was used for normally distributed continuous variables and nonparametric testing was used for non-normally distributed variables. Specifically, analysis of variance, Kruskal–Wallis one-way analysis of variance on ranks and χ2 testing were performed using SigmaPlot 11 (San Jose, CA, USA).
RESULTS A total of 106 neonates were included in the study, of whom 44 were captured in the 'pre-implementation' epoch, 40 in the 'during implementation' epoch and 22 in the 'post-implementation' epoch. No statistically significant differences were noted in gestational age, birth weight, gender, NICU length of stay, maternal age, race, ethnicity or religion, noted between the preimplementation, during implementation and post-implementation epochs (Table 1). Similarly, the primary diagnosis did not differ between epochs (P = 0.28; Table 2). We assessed the presence or absence of the following interventions within the last 48 h of the neonates' life: the decision to implement redirection of care (the absence of life-sustaining treatments), outcome expectation meetings between providers and families, the use of palliative medications and the presence of ancillary service consultation between the three epochs (Figure 1). Redirection of care increased over the course of the intervention epochs from 34% during the pre-implementation epoch to 45% during the implementation and 73% post implementation. These findings were statistically significant (P = 0.01). The occurrence of outcome expectation meetings stayed nearly the same in the pre-implementation and during implementation epochs at 54 and 52% and was 77% during the post-implementation epoch. However, these findings did not bear statistical significance (P = 0.13). Palliative medication increased over the epochs from 36% pre-implementation and 37% during implementation to 64% post implementation. These findings were statistically significant (P = 0.02). Ancillary service consultation did not show statistical significance (P = 0.16) with 70% occurrence in the pre-implementation epoch, 80% occurrence during implementation, and 91% post implementation (Figure 1). Next, we assessed the variability in the use of specific end-of-life palliative care interventions. Variability was defined as a statistically significant difference in the likelihood that certain end-of-life interventions would be utilized for a patient compared with other end-of-life interventions. Thus, a lack of variability would imply that each possible end-of-life intervention would be offered to a patient with similarly high (or low) frequency. In the preimplementation epoch, there was a significant difference in the usage of various interventions (P = o0.001). Redirection of care was present in only 34% of deaths, palliative medication usage was present in only 36% and an outcome meeting was held in only 54% of deaths. Ancillary care, however, was provided in 70% of deaths. In the post-implementation epoch, the differences between the usage of each of these four interventions was not © 2015 Nature America, Inc.
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225 Table 1.
Neonate characteristics Pre-implementation (n = 44)
During implementation (n = 40)
Post implementation (n = 22)
P-value
30.3 (5.2) 1265 (936) 61 18.9 (32) 30.0 (6.3)
30.9 (5.8) 1185 (1002) 40 23.4 (41) 29.0 (6.0)
32.4 (5.9) 1448 (953) 68 16.0 (28) 27.2 (5.9)
0.52 0.23 0.20 0.19 0.23
Race Caucasian African American Asian Unknown Mixed/other
30 6 2 3 3
19 10 1 4 6
14 2 0 1 5
Ethnicity Hispanic Non-hispanic Unknown
11 30 3
8 18 14
8 6 8
Religion Catholic Christian Jehovah witness None Unknown
10 5 0 2 27
5 4 1 3 27
4 3 0 1 14
Characteristic Gestational age, weeks (s.d.) Birth weight, g (s.d.) Male, % Days in NICU (s.d.) Maternal age (s.d.)
0.23
0.55
0.13
Abbreviation: NICU, neonatal intensive care unit.
Table 2. Comparison of diagnoses between epochs in implementation of palliative care Primary diagnosis Congenitala Geneticb Extreme prematurity
Preimplementation (n = 44)
During implementation (n = 40)
Post implementation (n = 22)
9 5 30
5 6 29
5 4 13
a
Congenital malformations: malformations not associated with documented chromosomal abnormalities. bGenetic syndromes: documented chromosomal abnormalities.
statistically significant, with percentages ranging from 64% palliative medication usage to 91% ancillary care usage (Figure 2). DISCUSSION A disproportionately large fraction of pediatric deaths2,15,16 occurs in the neonatal period, and most of these occur in the hospital, specifically in the NICU setting. Yet NICUs often do not have sufficient access to palliative care programs and funding for such programs is lacking,17 while sufficient scientific evidence supporting best practices in neonatal palliative care interventions is unavailable. To our knowledge, this study is the first to evaluate the impact of the implementation of a NICU palliative care intervention on specific markers of end-of-life care in neonates. Although a neonatal palliative care program has been described in Argentina,18 and another study described in detail the implementation of a perinatal palliative care program that is very similar to the intervention we developed,13 this study takes that work one step further by measuring markers of the intervention. © 2015 Nature America, Inc.
Figure 1. Percentage of patients receiving each end-of-life intervention in the last 48 h of life. Redirection of care and palliative medication use increased after implementation of palliative care intervention. Redirection of care, P = 0.012; outcome meetings, P = 0.13; palliative medication, P = 0.022; ancillary care, P = 0.16 (χ2-test).
A number of components have a role in the delivery of quality end-of-life care when infants die in the NICU. In the unique setting of the NICU, where patients do not typically have the developmental maturity and self-awareness to experience significant psychological, emotional, psychosocial or spiritual suffering, measures of end-of-life quality aimed at the patient consist of appropriate pain management as well as ensuring the opportunity Journal of Perinatology (2015), 223 – 228
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226
Figure 2. Variability in the percentage of patients receiving specific interventions pre- and post-implementation of the palliative care intervention. Individual interventions were more uniformly offered after the Variability in the percentage of patients receiving specific interventions pre- and post-implementation implementation of the palliative care intervention. Pre-implementation, P ⩽ 0.001; post implementation, P = 0.132 (χ2-test).
for parental bonding. Possible interventions at the psychological, emotional, psychosocial and spiritual level are aimed at the infant's family, typically including the parents and siblings. In this study, we have chosen to specifically assess pain management as the major component of neonatal palliative care focusing directly on the patient. Although successful management of the infant to ensure comfort, including pain control, is paramount, adequate pain control has been lacking in the neonatal population.19,20 Furthermore, NICU infants of lower birth weight receive less comfort medication prior to death21 and there is significant regional variation in end-of-life medication usage.22 However, our results indicate that a palliative care intervention is correlated with an increase in the use of palliative medication during the final 48 h of the neonate's life. Thus, the combination of formal teaching sessions, the existence of written end-of-life clinical practice guidelines, and the presence of an electronic palliative care order set, including dosing for palliative medication, was associated with the increased usage of palliative medication for dying infants. The existence of policies or guidelines supporting palliative care in the NICU has been identified as a facilitator of end-of-life care in the NICU.23 It is likely that this association was dependent on the combination of interventions leading to a higher level of staff education and awareness, as well as to an operationally more efficient process, more than any individual intervention in the bundle. Future directions might include assessing pain scores at the end of life. Our data indicate that redirection of care to comfort measures only increased in the infants that died in the NICU after the implementation of the perinatal palliative care intervention. Thus, after the implementation of the intervention, infants were less likely to die on the ventilator undergoing aggressive curative treatment in the last 48 h of their life than before the implementation. Due to the typical velocity of events in the NICU setting in the 48 h prior to death, it is often difficult to retrospectively parse out decision-making and redirection of care in detail. Thus, to allow for robust data, we utilized the stringent criteria of a change in Do Not Resuscitate status, documentation of comfort care, use of the palliative care order set or compassionate extubation, as well as the absence of cardiopulmonary resuscitation, epinephrine usage or other resuscitative measures in the final 48 h of life in determining redirection of care to comfort measures only. Defining redirection of care to comfort care is challenging, and while the definition used is quite specific, it is generalizable within Journal of Perinatology (2015), 223 – 228
the NICU population when common 'real world' neonatal end-oflife scenarios are taken into account. Redirection of care to comfort measures and away from curative measures at the appropriate time is important. If this is achieved, the balance in the infants' final hours can shift from unnecessary and painful interventions to more quality time with the parents. Thus, redirection of care at the appropriate time may be a reasonable marker of quality palliative and end-of-life care, as it reflects that the care team has addressed the infant's impending death with the family before the death became imminent. However, the concept of appropriate time is amenable to a broad range of interpretations and the decision of when it is time to redirect care is fraught with difficulties, given the almost infinite variations in medical condition, family wishes and beliefs, as well as physician beliefs.24–27 Thus, conversations with parents about therapeutic choices at the limits of viability, devastating long-term outcomes, and redirection of care to comfort measures are necessary. Approaches to communicating with parents in end-oflife discussions in the NICU have received attention recently.28 In fact, parents of children who have died view communication with the medical team as a priority29 and good communication between parents and physicians leads to indicators of a 'letter death'.30 It is likely that the changes in practice that we measured are associated with better staff awareness of the goals of palliative as well as end-of-life care, as well as possible better communication with families. It is also possible that a component of the increase in redirection of care to comfort measures is due to better awareness and thus better documentation of the process in the chart. While this is an alternate explanation for the results, it does not detract from the significance of the findings, since it is possible that heightened awareness of the need for comfort care that leads to an increase in documentation will also lead to an increase in actual comfort care to the patient. Similar educational approaches have been found to increase awareness of end-of-life issues among NICU staff31 and weaknesses in documentation are a well described phenomenon.32 Furthermore, some of the markers of care we assessed in the last 48 h of life, including the utilization of medications and the utilization of services, improve with outside palliative care team consultation.12 Although a consult service with experienced palliative care practitioners brings with it a myriad of advantages for the patient and family that are beyond the scope of this discussion, it could be argued that a palliative care intervention as described in this study may at least partially shoulder a palliative care team consultation's role in raising awareness within the NICU care team in the absence of a neonatal or pediatric palliative care team. However, the number of documented multidisciplinary family outcome meetings about the goals of care did not increase. One possible explanation for the increase in redirection of care to comfort care without a concomitant increase in family meetings is the conversations were in fact taking place but the documentation was not in place. Although others have shown a national trend toward withholding or withdrawing curative support over a decade in Portugal,33 our study indicates an increase in redirecting care to comfort measures and an increase in palliative medication usage at the end-of-life associated with the implementation of a perinatal palliative care intervention. We did not note an increase in the usage of ancillary services as an additional support for families. This finding is in line with our clinical experience that most families experienced social work or chaplaincy support in the days leading up to the death of their infant in the NICU even before the implementation of the intervention. Furthermore, our results indicate that there were significant differences in the level of usage of the four end-of-life interventions measured before the implementation of the palliative care intervention. Although almost three-fourths of dying infants received ancillary consults, only a third received palliative © 2015 Nature America, Inc.
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227 medication. After the implementation of the intervention, these differences evened out, and there was no longer a statistical difference in the usage of each of the measures. This may be attributable to an increased understanding among care providers of the importance of providing multiple aspects of end-of-life care in a holistic manner. It is important to note that our institution does not have a separate pediatric palliative care consultative team. The interventions described were developed by a team from within the NICU. An intriguing future direction of study would be whether the embeddedness of a perinatal palliative care intervention within the NICU compared with the existence of an ancillary pediatric palliative care team performing palliative consults in the NICU12 is associated with better ease of implementation/effectiveness and thus better quality of end of life, given that multiple experts have discussed the difficulty of increasing acceptance and integration of palliative care consult teams into the NICU.34 Although the intervention was aimed at providing palliative care in general, the outcome measure we assessed was restricted to the end-of-life phase in the final 48 h of life. We chose to focus on this period of time instead of a broader period because the manner in which this important phase is managed clinically provides significant insight into opportunities for improvement in terms of both staff education and medical management process. Others have similarly found that the final 48 h of life are an important time period in assessing palliative care interventions that occurred prior to the 48 h period in the NICU.12 However, we recognize that the infants that would benefit the most from palliative care interventions are the infants that have lifethreatening illness for an extended period of time. Important future directions will be to study the relationship between the palliative care intervention and actual palliative care provided to neonates with life-threatening illness over the course of their illness, as well as specific quality-of-life measures, beyond the concrete measures that were used as a proxy by us, as well as others as indicators of quality-of-life at the end of life.12 This study focused on the care given to the infants. An additional future direction may include studying the impact of the implementation of palliative care interventions on the care directed at the families of neonates, given the central role that families have in the care of their infants. Providing care to dying infants and infants with life-threatening disease is challenging and sometimes fraught with conflict for care providers. Provider moral distress in the NICU is a welldescribed phenomenon.35–38 Others have shown that palliative care educational interventions lead to an increase in nursing comfort levels in caring for dying infants in the NICU.39 Also, lack of education has been identified as a barrier to the provision of end-of-life care in the NICU.23 Thus, the implementation of the educational component of the palliative care interventions may have led to a higher level of nursing comfort in caring for dying infants and thus may have contributed to the increase in redirection of care and palliative medication usage. It is also important to note that it cannot be assumed that the goal must be the attainment of the measure of 100% for each of the interventions tested. Although it is reasonable to assume that most infants will benefit from these end-of-life interventions, there will always be specific cases, in which our 'standard' end-of-life care, or specific components thereof, is not what is needed given the patient's medical status or the family's set of goals and values. Furthermore, a prospective chart review coupled with a retrospective chart review is not the ideal format for a study comparing two epochs. However, refraining from introducing a palliative care intervention for a period of time to allow for the prospective collection of data on a group of infants as a pre-implementation group was not deemed ethically feasible. Similarly, a limitation of the study is that the ideal washout period between epochs would be one in which the final interven© 2015 Nature America, Inc.
tion occurred before the beginning of the washout period. However, it was beyond the scope of this study to wait for that. In summary, our findings indicate that the implementation of a perinatal palliative care intervention in a regional level IV NICU, including staff teaching, written guidelines and an electronic medical record order set, is correlated with a measurable increase in redirection of care to comfort care and palliative medication usage provided to infants in their final 48 h of life. Thus, palliative care initiatives in the NICU may contribute to improving end-oflife care of dying neonates. Future studies should address this question on a prospective manner. CONFLICT OF INTEREST The authors declare no conflict of interest.
ACKNOWLEDGEMENTS We would like to thank the Women and Infants Hospital NICU Palliative Care working group for their critical input.
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Supplementary Information accompanies the paper on the Journal of Perinatology website (http://www.nature.com/jp)
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© 2015 Nature America, Inc.
ORIGINAL ARTICLE
End-of-life care in a regional level IV neonatal intensive care unit after implementation of a palliative care initiative C Samsel1,2 and BE Lechner1,3 OBJECTIVE: We hypothesized that the implementation of a neonatal palliative care initiative will result in improved markers of end-of-life care. STUDY DESIGN: A retrospective and prospective chart review of neonatal intensive care unit deaths was performed for 24 months before, 16 months during and 24 months after the implementation of palliative care provider education and practice guidelines (n = 106). Ancillary care, redirection of care, palliative medication usage and outcome meetings in the last 48 h of life and basic demographic data were compared between epochs. Parametric and nonparametric analysis was performed. RESULT: There was an increase in redirection of care and palliative medication usage and a decrease in variability of use of end-of-life interventions (P = 0.012, 0.022 and o0.001). CONCLUSION: The implementation of a neonatal palliative care initiative was associated with increases in palliative interventions for neonates in their final 48 h of life, suggesting that such an initiative may enhance end-of-life care. Journal of Perinatology (2015) 35, 223–228; doi:10.1038/jp.2014.189; published online 23 October 2014
INTRODUCTION Pediatric palliative care aims to improve the quality-of-life of children faced with life-threatening or life-limiting illness. Of children who die in the United States, over half are infants (o 1 year) and of those, over 65% are neonates.1 Most neonates and infants who die do so in the intensive care unit setting.2 Thus, a significant number of neonates require palliative care services in the NICU (neonatal intensive care unit). A recent study of 653 neonatologists showed that over 95% believe palliative care programs are important and are needed to improve quality of care but cited difficulties with support including stigma, funding, implementation and lack of evidence of palliative care efficacy in the literature.3 While the numbers of pediatric palliative care programs in the United States are increasing in response to the need,4 dying neonates are receiving less palliative care than pediatric patients5 and little is known about neonatal palliative care programs or interventions. At the same time, there is a clear need for quality palliative care in the NICU.6 Training of neonatology fellows in end-of-life care7,8 is also lacking, as clinicians are often not comfortable with providing palliative care to neonates.9 While the development of guidelines for the provision of palliative care in the NICU have been reported,10,11 as well as the impact of a palliative care consultation,12 to our knowledge, there are no studies evaluating the impact of the implementation of a palliative care intervention within the NICU on outcomes of dying infants. We hypothesized that the implementation of a neonatal palliative care intervention in a level IV NICU setting will result in improved end-of-life care for dying neonates as evidenced by improved discussion of prognosis with parents, increased care redirection, increased palliative medicine use at the end of life and greater utilization of supportive ancillary care teams at the end of life.
METHODS Design A retrospective and prospective chart review was performed of deaths at an 80-bed regional level IV NICU for 24 months before, 16 months during intervention implementation and 24 months after the implementation of a neonatal palliative care initiative from January 2008 through April 2013. The pre-implementation group underwent a retrospective chart review, while the during and post-implementation groups underwent a prospective chart review. Inclusion criterion for the study was death of the neonate in the NICU. The 16-month epoch during the implementation of the intervention was necessary due to the stepwise nature of the implementation of the study. The initial educational lectures were given at the beginning of this 16-month period and the final approval and implementation of the end-of-life guidelines and the electronic order set were at the end of the 16-month period.
Intervention description Prior to the development of this intervention, a consultative model was used as the standard approach to palliative and end-of-life care in our NICU, in which dying patients received palliative interventions on an asneeded basis. The disadvantage of this approach is a lack of consistency over shifts. Similarly to the model described by others,13 the moral distress experienced by care providers in some difficult cases led to the development of a NICU palliative care initiative with the goal of shifting care of dying neonates from the consultative model to a team collaborative model, as described by others.13 A multidisciplinary committee was formed that consisted of representatives of all disciplines that are involved in the care of neonates in our NICU (attending physicians, fellows, residents, nurse practitioners, nurses, nurse managers, respiratory therapists, occupational therapists, lactation consultants, pharmacists, nutritionists, social workers, chaplains and bereaved family members). This committee developed three main foci for the NICU palliative care intervention: provider education, formal practice guideline development
1 Department of Neonatology, Women and Infants Hospital, Providence, RI, USA; 2Triple Board Residency Program, Brown University and Rhode Island Hospitals, Providence, RI, USA and 3Warren Alpert Medical School of Brown University, Providence, RI, USA. Correspondence: Dr B Lechner, Department of Pediatrics, Women & Infants' Hospital of Rhode Island, 101 Dudley Street, Providence 02905, RI, USA. E-mail: [email protected] Received 11 July 2014; revised 28 August 2014; accepted 2 September 2014; published online 23 October 2014
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224 and communication skills training. A discussion of the communication skills training and its outcomes is beyond the scope of this study. The provider education component and formal practice guidelines were developed as follows: As part of the educational component of the initiative, the intervention was launched with a conference on neonatal palliative care aimed at the entire Department of Pediatrics at Women and Infants Hospital of Rhode Island. This conference was aimed at educating providers on the current state of perinatal and neonatal palliative and end-of-life care. The conference was held jointly by a local neonatologist and an outside pediatric palliative care specialist. Further educational interventions included multiple smaller conferences on the basis of neonatal palliative care aimed at neonatology fellows as well as the NICU nursing staff. Most neonatologists, fellows and ancillary staff attended at least one such conference. Additionally, all nurses had access to an intranet based learning module recapitulating the conference material as well as the order set. For the practice guideline development component, a mission statement for the NICU palliative care initiative, NICU end-of-life care guidelines, an order set (Supplementary Appendix 1) as well as a local pediatric hospice program discharge resource guide were developed by the aforementioned multidisciplinary committee. The guidelines were developed based on committee discussions, while various components were adapted and modified from neonatal palliative care guidelines in the literature,10,11 the AAP palliative care statement,14 and a protocol from CHOP (shared by D. Munson). The medication protocol was developed in conjunction with a perinatal pharmacist. The work product of the committee was circulated among physicians, nurse practitioners, fellows, nursing and all other ancillary staff in the NICU and made available on all NICU computer stations. The end-of-life order set was made available within the NICU's computer ordering system and all staff who write orders were in service. The multidisciplinary NICU palliative care group continues to meet on a bimonthly basis.
Procedure Data were collected via Institutional review board-approved chart review from Women and Infants Hospital paper and electronic patient records. All data were reviewed and analyzed after primary collection. Data were collected on gender, gestational age, NICU length of stay, time of death, diagnosis, birth weight, ethnicity, race, religion, maternal age and primary diagnosis. In the last 48 h of life, data were collected on the documentation of redirection of care, outcome expectation meetings between providers and families, palliative medication usage and ancillary service consultation. The final 48 h period was chosen as the timeframe to assess end-of-life care, as adapted from a study examining the role of palliative care consultation in neonatal end-of-life care,12 given the pathophysiology of the typical dying infant in the NICU setting. The disease processes that lead to death in the NICU often cause death in a more rapidly progressive manner than in older children or adults, typically leading to shorter periods of the dying process than in older patients. Redirection of care to comfort care was defined as at least one of the following: a change in Do Not Resuscitate status, documentation of redirection of care to comfort care, use of the palliative care order set or compassionate extubation. In addition to at least one of the above indicators, the absence of all of the following aggressive life-sustaining interventions was necessary in the 48 h prior to death for redirection of care to comfort care to occur: cardiopulmonary resuscitation, the use of epinephrine, transfusions, inotropic agents, intubation and central line placement. Outcome expectation meetings were defined as documented meetings between a physician or nurse practitioner and at least one guardian, in which disclosure and education of poor clinical status or outcomes was disseminated with an option of redirection of care goals to comfort care only. Palliative medications were defined as medication documented to assist with the comfort of a neonate at the end of life. Furthermore, in two cases, the use of morphine in 3 h prior to death without documentation of reasoning was deemed to exhibit a clear pattern of redirection of care based on consensus of the investigators in reviewing other orders and documentation (that is, discontinuation of ventilation, nutrition, antibiotics, so on, followed by morphine administration). To reach this conclusion in these two cases, the investigators independently assessed relevant information, including chart documentation and orders as well as the Journal of Perinatology (2015), 223 – 228
timing thereof, and then compared the two independent assessments, both of which came to the same conclusion. Ancillary service consultation was defined as documented contact with the departments of social work or chaplaincy. We only included this measure as present, if a note or document from the ancillary service or other team member's note documented contact with one of these services in the last 48 h of life. Theoretically, the fact that the authors were also involved in patient care may introduce a bias to the data. However, one author was involved in roughly 3% of deaths as a resident, all of which took place before he became involved in the project, and the other author was involved in o10% of deaths as an attending physician. Given the large number of staff of various disciplines that provide care in the NICU, the overlap between intervention planning group and clinical care providers was minimal (range of 1–12% per discipline).
Data analysis Parametric testing was used for normally distributed continuous variables and nonparametric testing was used for non-normally distributed variables. Specifically, analysis of variance, Kruskal–Wallis one-way analysis of variance on ranks and χ2 testing were performed using SigmaPlot 11 (San Jose, CA, USA).
RESULTS A total of 106 neonates were included in the study, of whom 44 were captured in the 'pre-implementation' epoch, 40 in the 'during implementation' epoch and 22 in the 'post-implementation' epoch. No statistically significant differences were noted in gestational age, birth weight, gender, NICU length of stay, maternal age, race, ethnicity or religion, noted between the preimplementation, during implementation and post-implementation epochs (Table 1). Similarly, the primary diagnosis did not differ between epochs (P = 0.28; Table 2). We assessed the presence or absence of the following interventions within the last 48 h of the neonates' life: the decision to implement redirection of care (the absence of life-sustaining treatments), outcome expectation meetings between providers and families, the use of palliative medications and the presence of ancillary service consultation between the three epochs (Figure 1). Redirection of care increased over the course of the intervention epochs from 34% during the pre-implementation epoch to 45% during the implementation and 73% post implementation. These findings were statistically significant (P = 0.01). The occurrence of outcome expectation meetings stayed nearly the same in the pre-implementation and during implementation epochs at 54 and 52% and was 77% during the post-implementation epoch. However, these findings did not bear statistical significance (P = 0.13). Palliative medication increased over the epochs from 36% pre-implementation and 37% during implementation to 64% post implementation. These findings were statistically significant (P = 0.02). Ancillary service consultation did not show statistical significance (P = 0.16) with 70% occurrence in the pre-implementation epoch, 80% occurrence during implementation, and 91% post implementation (Figure 1). Next, we assessed the variability in the use of specific end-of-life palliative care interventions. Variability was defined as a statistically significant difference in the likelihood that certain end-of-life interventions would be utilized for a patient compared with other end-of-life interventions. Thus, a lack of variability would imply that each possible end-of-life intervention would be offered to a patient with similarly high (or low) frequency. In the preimplementation epoch, there was a significant difference in the usage of various interventions (P = o0.001). Redirection of care was present in only 34% of deaths, palliative medication usage was present in only 36% and an outcome meeting was held in only 54% of deaths. Ancillary care, however, was provided in 70% of deaths. In the post-implementation epoch, the differences between the usage of each of these four interventions was not © 2015 Nature America, Inc.
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225 Table 1.
Neonate characteristics Pre-implementation (n = 44)
During implementation (n = 40)
Post implementation (n = 22)
P-value
30.3 (5.2) 1265 (936) 61 18.9 (32) 30.0 (6.3)
30.9 (5.8) 1185 (1002) 40 23.4 (41) 29.0 (6.0)
32.4 (5.9) 1448 (953) 68 16.0 (28) 27.2 (5.9)
0.52 0.23 0.20 0.19 0.23
Race Caucasian African American Asian Unknown Mixed/other
30 6 2 3 3
19 10 1 4 6
14 2 0 1 5
Ethnicity Hispanic Non-hispanic Unknown
11 30 3
8 18 14
8 6 8
Religion Catholic Christian Jehovah witness None Unknown
10 5 0 2 27
5 4 1 3 27
4 3 0 1 14
Characteristic Gestational age, weeks (s.d.) Birth weight, g (s.d.) Male, % Days in NICU (s.d.) Maternal age (s.d.)
0.23
0.55
0.13
Abbreviation: NICU, neonatal intensive care unit.
Table 2. Comparison of diagnoses between epochs in implementation of palliative care Primary diagnosis Congenitala Geneticb Extreme prematurity
Preimplementation (n = 44)
During implementation (n = 40)
Post implementation (n = 22)
9 5 30
5 6 29
5 4 13
a
Congenital malformations: malformations not associated with documented chromosomal abnormalities. bGenetic syndromes: documented chromosomal abnormalities.
statistically significant, with percentages ranging from 64% palliative medication usage to 91% ancillary care usage (Figure 2). DISCUSSION A disproportionately large fraction of pediatric deaths2,15,16 occurs in the neonatal period, and most of these occur in the hospital, specifically in the NICU setting. Yet NICUs often do not have sufficient access to palliative care programs and funding for such programs is lacking,17 while sufficient scientific evidence supporting best practices in neonatal palliative care interventions is unavailable. To our knowledge, this study is the first to evaluate the impact of the implementation of a NICU palliative care intervention on specific markers of end-of-life care in neonates. Although a neonatal palliative care program has been described in Argentina,18 and another study described in detail the implementation of a perinatal palliative care program that is very similar to the intervention we developed,13 this study takes that work one step further by measuring markers of the intervention. © 2015 Nature America, Inc.
Figure 1. Percentage of patients receiving each end-of-life intervention in the last 48 h of life. Redirection of care and palliative medication use increased after implementation of palliative care intervention. Redirection of care, P = 0.012; outcome meetings, P = 0.13; palliative medication, P = 0.022; ancillary care, P = 0.16 (χ2-test).
A number of components have a role in the delivery of quality end-of-life care when infants die in the NICU. In the unique setting of the NICU, where patients do not typically have the developmental maturity and self-awareness to experience significant psychological, emotional, psychosocial or spiritual suffering, measures of end-of-life quality aimed at the patient consist of appropriate pain management as well as ensuring the opportunity Journal of Perinatology (2015), 223 – 228
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226
Figure 2. Variability in the percentage of patients receiving specific interventions pre- and post-implementation of the palliative care intervention. Individual interventions were more uniformly offered after the Variability in the percentage of patients receiving specific interventions pre- and post-implementation implementation of the palliative care intervention. Pre-implementation, P ⩽ 0.001; post implementation, P = 0.132 (χ2-test).
for parental bonding. Possible interventions at the psychological, emotional, psychosocial and spiritual level are aimed at the infant's family, typically including the parents and siblings. In this study, we have chosen to specifically assess pain management as the major component of neonatal palliative care focusing directly on the patient. Although successful management of the infant to ensure comfort, including pain control, is paramount, adequate pain control has been lacking in the neonatal population.19,20 Furthermore, NICU infants of lower birth weight receive less comfort medication prior to death21 and there is significant regional variation in end-of-life medication usage.22 However, our results indicate that a palliative care intervention is correlated with an increase in the use of palliative medication during the final 48 h of the neonate's life. Thus, the combination of formal teaching sessions, the existence of written end-of-life clinical practice guidelines, and the presence of an electronic palliative care order set, including dosing for palliative medication, was associated with the increased usage of palliative medication for dying infants. The existence of policies or guidelines supporting palliative care in the NICU has been identified as a facilitator of end-of-life care in the NICU.23 It is likely that this association was dependent on the combination of interventions leading to a higher level of staff education and awareness, as well as to an operationally more efficient process, more than any individual intervention in the bundle. Future directions might include assessing pain scores at the end of life. Our data indicate that redirection of care to comfort measures only increased in the infants that died in the NICU after the implementation of the perinatal palliative care intervention. Thus, after the implementation of the intervention, infants were less likely to die on the ventilator undergoing aggressive curative treatment in the last 48 h of their life than before the implementation. Due to the typical velocity of events in the NICU setting in the 48 h prior to death, it is often difficult to retrospectively parse out decision-making and redirection of care in detail. Thus, to allow for robust data, we utilized the stringent criteria of a change in Do Not Resuscitate status, documentation of comfort care, use of the palliative care order set or compassionate extubation, as well as the absence of cardiopulmonary resuscitation, epinephrine usage or other resuscitative measures in the final 48 h of life in determining redirection of care to comfort measures only. Defining redirection of care to comfort care is challenging, and while the definition used is quite specific, it is generalizable within Journal of Perinatology (2015), 223 – 228
the NICU population when common 'real world' neonatal end-oflife scenarios are taken into account. Redirection of care to comfort measures and away from curative measures at the appropriate time is important. If this is achieved, the balance in the infants' final hours can shift from unnecessary and painful interventions to more quality time with the parents. Thus, redirection of care at the appropriate time may be a reasonable marker of quality palliative and end-of-life care, as it reflects that the care team has addressed the infant's impending death with the family before the death became imminent. However, the concept of appropriate time is amenable to a broad range of interpretations and the decision of when it is time to redirect care is fraught with difficulties, given the almost infinite variations in medical condition, family wishes and beliefs, as well as physician beliefs.24–27 Thus, conversations with parents about therapeutic choices at the limits of viability, devastating long-term outcomes, and redirection of care to comfort measures are necessary. Approaches to communicating with parents in end-oflife discussions in the NICU have received attention recently.28 In fact, parents of children who have died view communication with the medical team as a priority29 and good communication between parents and physicians leads to indicators of a 'letter death'.30 It is likely that the changes in practice that we measured are associated with better staff awareness of the goals of palliative as well as end-of-life care, as well as possible better communication with families. It is also possible that a component of the increase in redirection of care to comfort measures is due to better awareness and thus better documentation of the process in the chart. While this is an alternate explanation for the results, it does not detract from the significance of the findings, since it is possible that heightened awareness of the need for comfort care that leads to an increase in documentation will also lead to an increase in actual comfort care to the patient. Similar educational approaches have been found to increase awareness of end-of-life issues among NICU staff31 and weaknesses in documentation are a well described phenomenon.32 Furthermore, some of the markers of care we assessed in the last 48 h of life, including the utilization of medications and the utilization of services, improve with outside palliative care team consultation.12 Although a consult service with experienced palliative care practitioners brings with it a myriad of advantages for the patient and family that are beyond the scope of this discussion, it could be argued that a palliative care intervention as described in this study may at least partially shoulder a palliative care team consultation's role in raising awareness within the NICU care team in the absence of a neonatal or pediatric palliative care team. However, the number of documented multidisciplinary family outcome meetings about the goals of care did not increase. One possible explanation for the increase in redirection of care to comfort care without a concomitant increase in family meetings is the conversations were in fact taking place but the documentation was not in place. Although others have shown a national trend toward withholding or withdrawing curative support over a decade in Portugal,33 our study indicates an increase in redirecting care to comfort measures and an increase in palliative medication usage at the end-of-life associated with the implementation of a perinatal palliative care intervention. We did not note an increase in the usage of ancillary services as an additional support for families. This finding is in line with our clinical experience that most families experienced social work or chaplaincy support in the days leading up to the death of their infant in the NICU even before the implementation of the intervention. Furthermore, our results indicate that there were significant differences in the level of usage of the four end-of-life interventions measured before the implementation of the palliative care intervention. Although almost three-fourths of dying infants received ancillary consults, only a third received palliative © 2015 Nature America, Inc.
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227 medication. After the implementation of the intervention, these differences evened out, and there was no longer a statistical difference in the usage of each of the measures. This may be attributable to an increased understanding among care providers of the importance of providing multiple aspects of end-of-life care in a holistic manner. It is important to note that our institution does not have a separate pediatric palliative care consultative team. The interventions described were developed by a team from within the NICU. An intriguing future direction of study would be whether the embeddedness of a perinatal palliative care intervention within the NICU compared with the existence of an ancillary pediatric palliative care team performing palliative consults in the NICU12 is associated with better ease of implementation/effectiveness and thus better quality of end of life, given that multiple experts have discussed the difficulty of increasing acceptance and integration of palliative care consult teams into the NICU.34 Although the intervention was aimed at providing palliative care in general, the outcome measure we assessed was restricted to the end-of-life phase in the final 48 h of life. We chose to focus on this period of time instead of a broader period because the manner in which this important phase is managed clinically provides significant insight into opportunities for improvement in terms of both staff education and medical management process. Others have similarly found that the final 48 h of life are an important time period in assessing palliative care interventions that occurred prior to the 48 h period in the NICU.12 However, we recognize that the infants that would benefit the most from palliative care interventions are the infants that have lifethreatening illness for an extended period of time. Important future directions will be to study the relationship between the palliative care intervention and actual palliative care provided to neonates with life-threatening illness over the course of their illness, as well as specific quality-of-life measures, beyond the concrete measures that were used as a proxy by us, as well as others as indicators of quality-of-life at the end of life.12 This study focused on the care given to the infants. An additional future direction may include studying the impact of the implementation of palliative care interventions on the care directed at the families of neonates, given the central role that families have in the care of their infants. Providing care to dying infants and infants with life-threatening disease is challenging and sometimes fraught with conflict for care providers. Provider moral distress in the NICU is a welldescribed phenomenon.35–38 Others have shown that palliative care educational interventions lead to an increase in nursing comfort levels in caring for dying infants in the NICU.39 Also, lack of education has been identified as a barrier to the provision of end-of-life care in the NICU.23 Thus, the implementation of the educational component of the palliative care interventions may have led to a higher level of nursing comfort in caring for dying infants and thus may have contributed to the increase in redirection of care and palliative medication usage. It is also important to note that it cannot be assumed that the goal must be the attainment of the measure of 100% for each of the interventions tested. Although it is reasonable to assume that most infants will benefit from these end-of-life interventions, there will always be specific cases, in which our 'standard' end-of-life care, or specific components thereof, is not what is needed given the patient's medical status or the family's set of goals and values. Furthermore, a prospective chart review coupled with a retrospective chart review is not the ideal format for a study comparing two epochs. However, refraining from introducing a palliative care intervention for a period of time to allow for the prospective collection of data on a group of infants as a pre-implementation group was not deemed ethically feasible. Similarly, a limitation of the study is that the ideal washout period between epochs would be one in which the final interven© 2015 Nature America, Inc.
tion occurred before the beginning of the washout period. However, it was beyond the scope of this study to wait for that. In summary, our findings indicate that the implementation of a perinatal palliative care intervention in a regional level IV NICU, including staff teaching, written guidelines and an electronic medical record order set, is correlated with a measurable increase in redirection of care to comfort care and palliative medication usage provided to infants in their final 48 h of life. Thus, palliative care initiatives in the NICU may contribute to improving end-oflife care of dying neonates. Future studies should address this question on a prospective manner. CONFLICT OF INTEREST The authors declare no conflict of interest.
ACKNOWLEDGEMENTS We would like to thank the Women and Infants Hospital NICU Palliative Care working group for their critical input.
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Supplementary Information accompanies the paper on the Journal of Perinatology website (http://www.nature.com/jp)
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