REVIEW URRENT C OPINION
Integrating palliative care in the ICU May Hua a and Hannah Wunsch a,b,c
Purpose of review Although providing palliative care in the ICU has become a priority, the success of different methods to integrate palliative care into the ICU has varied. This review examines the current evidence supporting the different models of palliative care delivery and highlights areas for future study. Recent findings The need for palliative care for ICU patients is substantial. A large percentage of patients meet criteria for palliative care consultation and there is frequent use of intensive care and other nonbeneficial care at the end of life. Overall, the consultative model of palliative care appears to have more of an impact on patient care. However, given the current workforce shortage of palliative care providers, a sustainable model of delivering palliative care requires both an effective integrative model, in which palliative care is delivered by ICU clinicians, and appropriate use of the consultative model, in which palliative care consultation is reserved for patients at highest risk of having unmet or long-term palliative care needs. Summary Developing a mixed model of palliative care delivery is necessary to meet the palliative care needs of critically ill patients. Efforts focused on improving integrative models and appropriately targeting the use of palliative care consultants are needed. Keywords critical care, end-of-life care, palliative care, palliative care consultation, quality improvement
INTRODUCTION For decades intensive care providers focused primarily on increasing short-term survival. But in recent years, the purview of critical care has expanded to improving long-term outcomes associated with critical illness and improving quality of life for patients who are dying. Previously, ICU clinicians were largely concerned with rescuing patients from their disease process. Now, avoiding unnecessary medicalization and striving for a ‘good’ death have become increasingly important. There is little debate that the delivery of palliative care and endof-life care in the ICU requires improvement. Multiple professional societies endorse the need for palliative care in the ICU [1,2], and one of the five recommendations made by the Critical Care Societies Collaborative as a part of the ‘Choosing Wisely’ campaign was ‘don’t continue life support for patients at high risk of death or severely impaired functional recovery without offering. . . the alternative of care focused entirely on comfort’ [3]. As the provision of palliative care has become a priority, we must determine which methods are most effective for delivering palliative care in the ICU. In this review, we discuss different models of palliative care delivery and consider the benefits
and drawbacks of each model and areas for improvement.
UNDERSTANDING THE NEED FOR IMPROVED PALLIATIVE CARE IN THE ICU Despite efforts in the last decade and a half to improve palliative care and end-of-life care, patients with critical illness continue to be at high risk of having unmet palliative care needs. Mortality for ICU patients during hospitalization remains high [4], and long-term mortality is increased for survivors of critical illness, particularly in the 6 months following hospital discharge [5]. Although the use of hospice at the end of life in the United States has
a
Department of Anesthesiology, Columbia University, New York, New York, USA, bDepartment of Critical Care Medicine, Sunnybrook Hospital and cDepartment of Anesthesia, University of Toronto, Toronto, Ontario, Canada Correspondence to May Hua, MD, Department of Anesthesiology, Columbia University, 622 West 168th Street PH5, Room 535 New York, NY 10032, USA. Tel: +1 212 305 1982; fax: +1 212 305 3204; e-mail: [email protected] Curr Opin Crit Care 2014, 20:673–680 DOI:10.1097/MCC.0000000000000149
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
KEY POINTS There is a large need for palliative care in the ICU, but successful models of delivery in varied practice settings have yet to be well defined. Available evidence suggests that the consultative model may be more effective.
In addition, survivors of critical illness may have significant palliative care needs. A study of elderly ICU patients discharged to postacute care facilities in the United States found that 88% of patients had at least one potential palliative care need [21 ]. ICU survivors suffer from cognitive dysfunction, psychiatric disorders, functional disability and increased long-term mortality [5,22 ,23,24 ]. This constellation of problems has been labeled a ‘postintensive care syndrome’ [25] and thus far, few interventions have been shown to improve outcomes. Palliative care, a specialty that focuses on improving symptomatology and quality of life, may be best poised to provide long-term care for many of these patients. Substantial variation exists in the delivery of palliative care in the ICU. Although this variation is likely partially driven by patient preferences, some of it may be related to differences in the culture of individual providers as well as institutional and organizational factors. In a study of decisions to forego life-sustaining treatment in US ICUs the predicted probability of making such decisions varied greatly, even after adjustment for patient-level and ICU-level effects [26]. These findings are similar to that of European ICUs, in which limitations in therapy were much more common, but also geographically variable [27]. This unexplained variation suggests that there may be differences in physician practice that alter the likelihood of making these decisions. One study found that ratings of the quality of dying varied between physicians of different specialties [28 ]. Furthermore, clinicians’ practice may be influenced by the environment. Intensivists practicing in ‘low’ and ‘high’ intensity institutions were found to differ in their approaches to decisionmaking regarding life-sustaining treatments and prognosis [29], and medical ICU patients are more likely to have treatment limitations placed than those cared for in surgical ICUs [7 ,12 ]. ICU staffing models also may affect palliative care delivery, as the use of 24-h nighttime intensivist staffing was associated with a decrease in the time to end-of-life decision making [30 ], and differences in both physician and nurse staffing altered the likelihood of making decisions to forego life-sustaining treatment in European ICUs [31]. &
&&
Methods to improve the quality of integrative palliative care delivered in ICUs, as well as more stringent evaluation of the consultative model of palliative care with regards to the improvement of patient-centered outcomes, are necessary. Given the workforce shortage of palliative care providers, sustainable models of palliative care delivery in the ICU will need to include a combination of the integrative and consultative models.
gone up, the use of ICU within the last 30 days of life has concomitantly increased [6 ]. In US ICUs, it is estimated that approximately 15% of all patients meet screening triggers for palliative care consultation [7 ], and this is likely underestimating the overall need, given that referrals for reasons such as refractory symptom management, conflict resolution and existential distress were not captured. Yet, in a study of a multifaceted educational intervention to improve palliative care in the ICU, there did not appear to be any improvement in the quality of palliative care, as assessed by the quality of death and dying, over time [8 ]. Furthermore, the provision of treatment perceived to be futile remains common in both the United States and Europe, and was estimated in a single center study in the United States to make up 3.5% of the hospital costs for ICU patients [9 ,10 ]. Futile care not only places a financial strain on the healthcare system without benefit, it also may not be in line with patients’ preferences, as patients and family often wish to avoid burdensome treatments in the face of a poor prognosis [11,12 ]. The use of palliative care has been reported to improve this misalignment between the care that is provided and the care that patients actually desire. Benefits of palliative care in the ICU include decreased use of nonbeneficial life-sustaining therapies, increased use of hospice and increased establishment of advanced directives [13–15]. Furthermore, palliative care consultation has been associated with decreased ICU length of stay, and decreased costs at the end of life in a generalized hospital setting [16–18]. However, it is important to note that cost savings may be dependent on both the timing of palliative care involvement and overall length of hospital stay [19,20]. &&
&
&
&&
&
&
674
www.co-criticalcare.com
&&
&
&
&
&
MODELS OF DELIVERING PALLIATIVE CARE There are several major challenges to adequately meeting the palliative care needs of critically ill patients, including first, the difficulty of identifying which patients are appropriate for palliative care and/ or hospice services, second, the variability associated with the initiation and quality of palliative care that Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch Table 1. Example of a checklist of an integrative palliative care intervention Within 24 h of admission
Within 72 h
End-of-life care
No time frame
Bereavement and psychosocial support for patients and families
Family meeting with physician and nurse within 72 h of admission to the surgical ICU
Implementation of palliative care standing order set and ventilator withdrawal guidelines for patients who are identified as imminently dying
Integration of palliative care performance into morbidity and mortality conferences and peer review
Interdisciplinary palliative care assessment
Comprehensive palliative care plan by 72 h including:
Assessment of pain and symptoms
Goals of care
Assessment of psychosocial, spiritual and bereavement needs of family
Pain and symptom management
Identify surrogate decision-maker
Psychosocial support for the family
Solicit and clarify advanced directives
Discussion about do-not-resuscitate orders or withdrawal or withholding of life-sustaining treatments if appropriate
Assessment of likely outcome and prognosis (discharge from ICU, discharge from hospital) from the current illness with regards to mortality and quality of life Adapted from [34].
is provided and third, a lack of appropriately trained providers of palliative care. These are issues that the current models of delivering palliative care must address. The two main models of delivering palliative care in the ICU are the integrative model and the consultative model [32], reflecting the division between generalist and specialist palliative care [33]. Generalist palliative care is delivered by primary providers, and involves basic palliative care skills, including knowledge of uncomplicated pain and symptom management, elicitation of preferences and basic discussions regarding goals of care. Specialized palliative care, which is delivered by consultants, is appropriate for patients who are in need of assistance with complex decision-making, refractory pain and symptom management, significant psychological distress or conflict resolution regarding goals of care [33]. These models can, and likely should, be combined in practice.
and palliative care needs are routinely assessed as a part of ICU care and communication with families regarding prognosis and goals of care is structured and standardized, regardless of prognosis. This can be applied universally to all ICU patients, or to subgroups meeting particular criteria that can be chosen to meet the needs of an individual ICU [32]. Examples of these models and methods for implementation have been described previously (Table 1) [32,34]. The main tool for this type of quality improvement lies in protocolization of aspects of palliative care, such as routine pain and symptom assessment, documentation of surrogate decision-makers and advanced directives, conducting family meetings within a prescribed amount of time and the use of palliative care order sets. Although protocolization of care is common in critical care, the success of such palliative care initiatives may be highly dependent on the culture of an individual ICU and training of individual physicians.
INTEGRATIVE MODEL The integrative model of palliative care delivery is one in which principles of palliative care are incorporated into everyday ICU care, and palliative care is delivered by the ICU team. In this model, symptoms
ADVANTAGES OF THE INTEGRATIVE MODEL One of the greatest benefits of the integrative approach is that patients ‘in need of palliative care’
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
675
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
do not need to be identified, as all patients receive a basic palliative care needs assessment and have a palliative care treatment plan that is carried out in conjunction with the rest of their ICU care. The question to answer is not ‘who needs palliative care?’, but ‘how much palliative care does a particular patient need?’. In the most successful models, these practices are not tied to prognosis, as prognostication remains difficult for clinicians. However, a recent study showed that physicians were still largely influenced by functional prognosis in their decisions to initiate withdrawal of life-sustaining treatment with families, and were more influenced by their own assessment of prognosis than by the preferences of the patient or family [35 ]. Another advantage of this model is that it does not require additional staffing and is not dependent on a palliative care service. This advantage is important, as many hospitals do not have palliative care services [36], and there is a workforce shortage of palliative care specialists [37]. Lastly, the integrative approach, if implemented, may shift the culture of an ICU, as it requires staff to prioritize palliative care as a problem that needs to be addressed daily, similar to ventilator weaning, or interruption of sedation. &&
DISADVANTAGES OF THE INTEGRATIVE MODEL Although the integrative model has many potential benefits, empirically, there have been difficulties with implementation and effectiveness. First, there is significant provider variability in the delivery of palliative care. In a study of a quality improvement intervention for palliative care in the ICU, the quality of death as rated by nurses and families differed significantly between specialties, with neurologists and neurosurgeons having the best ratings and general and other subspecialty surgeons having the worst ratings [28 ]. This variability may be related in part to the prominence of palliative care education among different specialties, as education in palliative care has been associated with variation in end-of-life care practices in the ICU [38]. Certain specialty training programs, such as general surgery, have been noted to be particularly deficient in palliative care education [39,40]. However, better education of clinicians in palliative care skills may not translate to improved outcomes, as a randomized controlled trial of a multifaceted palliative care intervention that included several educational components for clinicians did not affect ICU length of stay or improve quality of death and dying [41]. Particular skills that are crucial to palliative care, such as communication, are difficult to teach. A trial of a simulation intervention to improve trainees’
communication skills did not improve the quality of communication about end-of-life care or the quality of end-of-life care, but was associated with a small increase in depressive symptoms among patients in the intervention arm [42 ]. Some interventions have been successful at demonstrating long-term improvements in process measures such as documentations of care goals and daily family updates [43], but the effect of an intervention may also differ across institutions. A multifaceted intervention to improve communication in a statewide ICU collaborative found significant variation among different ICU types, with closed units and teaching units being more likely to improve in comparison with open and nonteaching units [44 ]. Overall, the effectiveness and generalizability of quality improvement interventions to deliver integrative palliative care have been difficult to demonstrate [45]. Despite this lack of success, there are some general lessons that can be learned. First, it is very difficult to effect change. The failure of welldesigned interventions to impact outcomes is likely partly because of the fact that physicians may be relatively recalcitrant to changing their practices in this area, although this remains speculative. A consistent finding is that quality improvement interventions are most likely to succeed if they are ‘home-grown,’ arising from within the institution. One reason provided for the failure of an intervention to improve outcomes in a multicenter trial (but that did initially achieve an effect in a single-center study) was that it was difficult to achieve the same level of commitment and buy-in from clinicians at other institutions with different cultures of care [41]. Despite these difficulties, it is essential that we improve the integrative model of palliative care, as this constitutes, and will remain, the majority of palliative care delivery to critically ill patients. &&
&
&
676
www.co-criticalcare.com
CONSULTATIVE MODEL In the consultative model of palliative care delivery, palliative care is provided by consultants. With this approach, identifying which patients are appropriate for palliative care presents a greater challenge, and consultation can be facilitated by choosing appropriate screening criteria, or triggers, for palliative care consultation. Triggers have been designed (largely through consensus criteria) to select patients at high risk of poor outcomes who may benefit from earlier discontinuation of life-sustaining therapies, as well as patients with chronic severe illness requiring aggressive symptom management [14,46,47]. Multiple sets of triggers for ICU palliative care consultation have been published [14,15,47–50], but success in implementation has varied. In one study in a medical ICU, Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch
the use of triggers was associated with a decrease in ICU length of stay, whereas another study, using different triggers in a surgical ICU, failed to even increase the number of consultations. This difference was likely because of the fact that in the first study, referral to palliative care was automatic upon meeting a trigger, whereas in the surgical ICU study, information was relayed to the ICU team who ultimately decided whether or not to refer patients [14,15,49]. These studies demonstrate that simply screening patients for palliative care needs is insufficient; if triggers are not used to their full potential, the consultative model may be ineffective. There are also differences between published triggers that may influence their efficacy; certain triggers are objective (status post cardiac arrest) whereas others are more subjective (death expected during ICU stay). A recent study pooled many triggers together and found that five ‘efficient’ triggers (all of which were objective or ‘concrete’) were able to capture 85% of all patients meeting any trigger across different types of ICUs. Efficient triggers for palliative care consultation (adapted from Hua et al. [7 ] with permission of the American Thoracic Society. Copyright ß 2014 American Thoracic Society) are as follows: &
(1) ICU admission after hospital stay at least 10 days, (2) multisystem organ failure at least three systems, (3) diagnosis of active stage IV malignancy (metastatic disease), (4) status post cardiac arrest, (5) diagnosis of intracerebral hemorrhage requiring mechanical ventilation. Despite the finding of relatively little variation when current triggers were applied across different ICUs [7 ] it is unlikely that there will be universal agreement on triggers for palliative care consultation in the ICU. More likely (and perhaps appropriate) is the development of triggers tailored to the individual patient population and culture of an institution [51]. &
ADVANTAGES OF THE CONSULTATIVE MODEL The main advantage of the consultative model is that there is stronger literature supporting its effectiveness. Use of palliative care consultation in the ICU has been associated with decreased ICU length of stay and decreased use of nonbeneficial lifesustaining treatments [13–15], and meta-analyses of interventions to improve communication have also suggested that the consultative model appears
to be more effective, particularly for decreasing healthcare utilization [52,53]. This clearer impact from specialized palliative care may be due to less variability in the delivery of care. The consultative model also may be particularly helpful in moderating conflict between families and the ICU team, and in offsetting some of the work burden of intensivists. This division of time may be beneficial for other ICU patients, as increases in ‘ICU strain,’ as measured by increases in the number of admissions, patients’ severity of illness and increases in overall census, have been associated with small, but real, increases in mortality [54]. Lastly, palliative care consultants may also provide continuity of care for a patient through different ICU teams and after discharge from the ICU [32]. This final point is potentially an important key strength of the consultative model, as delivery of palliative care with an integrative model may end upon ICU discharge. Many patients who may be appropriate for palliative care will not die in the ICU, and therefore require these services beyond the ICU and often after hospital discharge as well; provision of appropriate palliative care in the post-ICU discharge setting may be equally (or more) important than its provision during the ICU stay.
DISADVANTAGES OF CONSULTATIVE MODEL The largest drawback to the consultative model is its reliance on palliative care specialists. Significant disparity exists in the availability of palliative care services internationally [55]. The presence of palliative care services in hospitals varies throughout the United States and Europe [36,56], and throughout Asia and Africa, palliative care services are still in various stages of development [57,58]. In some countries, there is also reticence to the idea of mandatory palliative care consultation [59]. These issues make it unlikely that this model will suffice on its own to meet the palliative care needs of critically ill patients globally. Another disadvantage is that having an additional consulting team may further fragment patient care and introduce conflict with intensivists and other primary providers, such as surgeons or oncologists. ICU clinicians in particular may not look favorably upon the introduction of palliative care consultants, as they view palliative care as part of the scope of their practice [60] and may not always be willing to cede this part of care [61]; the success of the consultative approach is highly dependent on the culture of an ICU and whether or not a collaborative environment can be established [51].
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
677
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
FUTURE DIRECTIONS Palliative care in the ICU is impaired by numerous barriers, and problems exist with both models of delivery. Integrative models are hindered by the fact that proven methods of improving palliative care skills of generalist providers are lacking. The education to truly integrate palliative care into generalist practice may need to begin as early as medical school. Also, the effect of interventions may be impacted by many different factors pertaining to patients, providers and the individual institutions in which they are implemented. Despite this, there may be value in determining if parts of these complex interventions are generalizable; perhaps a methodology for implementation, protocols for performing needs assessments or process measures may be portable from one institution to another. Similarly, aspects of using the consultative model require further study. Existing triggers have not been validated against an objective benchmark, and may need to be refined. Trying to identify these high-risk patients should be a priority, as it may allow for targeting of specialized palliative care to patients most likely to derive benefit, and can maximize the utility of a scarce resource. This may be accomplished by defining new triggers, or by combining existing ones with other factors associated with a poor prognosis, such as frailty [62,63,64 ]. Another approach to dealing with the shortage of palliative care providers may be to use methods for extending scarce resources, such as telemedicine, which has already been used in some ICU settings to provide intensivist coverage. Using telemedicine to deliver palliative care has been demonstrated to be feasible for both cancer and ICU patients [65,66], and a cluster-randomized trial using telemedicine to deliver home palliative care is underway in the Netherlands [67]. We also have yet to determine which model will operate best under different ICU organizational characteristics and staffing models. It may be that integrative palliative care may be more successful with a closed staffing model, as these ICUs may have a greater ability to change ICU culture and practice [34,44 ]. Another area that merits considerable focus is the use of palliative care to improve the long-term sequelae of critical illness for survivors. Given the high burden of symptoms affecting the quality of life in this population, the initiation of palliative care during an ICU stay, or perhaps even upon ICU discharge, may improve these outcomes, which have been difficult to improve thus far. Perhaps most importantly, comparisons of both integrative and consultative interventions in the ICU have been hampered by the use of heterogeneous outcomes, such as ICU length of stay, clinician satisfaction and &
&
678
www.co-criticalcare.com
family ratings of death and dying [68]. Studies thus far lack the use of outcomes that truly measure improvements for patients, and evaluations of palliative care delivery cannot exclude this important stakeholder. Appropriate patient-centered outcomes that are both sensitive and responsive need to be developed and standardized so that palliative care interventions can be effectively studied.
CONCLUSION As the benefits of palliative care during, and potentially after, an ICU stay are elucidated, the adequate delivery of palliative care to critically ill patients should be a priority for healthcare. Given that there are advantages and disadvantages of both the integrative and consultative models, improving access to palliative care in the ICU will likely require the use of a mixed model that combines both approaches. In the current milieu, meeting the palliative care needs of critically ill patients will depend on tailoring integrative and consultative models to meet the needs of a particular ICU. In certain institutions, palliative care consultants may be required simply to perform a basic needs assessment, whereas in ICUs with well-developed integrative models, consultants may be reserved for only the highest risk cases. Finding an appropriate balance of these two models for an individual ICU, as well as at regional and national levels, is necessary to improve delivery of palliative care to critically ill patients. Acknowledgements Support: Dr Hua is supported by a Mentored-Training Research Grant from the Foundation in Anesthesia Education and Research. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Truog RD, Campbell ML, Curtis JR, et al. Recommendations for end-of-life care in the intensive care unit: a consensus statement by the American College [corrected] of Critical Care Medicine. Crit Care Med 2008; 36:953–963. 2. Lanken PN, Terry PB, Delisser HM, et al. An official American Thoracic Society clinical policy statement: palliative care for patients with respiratory diseases and critical illnesses. Am J Respir Crit Care Med 2008; 177:912–927. 3. Critical Care Societies Collaborative. Five things physicians and patients should question 2014 [cited 4 June 2014]. Available from: http://www.choo singwisely.org/doctor-patient-lists/critical-care-societies-collaborative-criticalcare/. 4. Lilly CM, Zuckerman IH, Badawi O, Riker RR. Benchmark data from more than 240 000 adults that reflect the current practice of critical care in the United States. Chest 2011; 140:1232–1242. 5. Wunsch H, Guerra C, Barnato AE, et al. Three-year outcomes for Medicare beneficiaries who survive intensive care. JAMA 2010; 303:849–856.
Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch 6. Teno JM, Gozalo PL, Bynum JP, et al. Change in end-of-life care for Medicare beneficiaries: site of death, place of care, and healthcare transitions in 2000, 2005, and 2009. JAMA 2013; 309:470–477. This study determined that the use of intensive care and the number of healthcare transitions at the end of life have both increased over time. This observation helps to define the urgent need to improve the delivery of palliative care in the ICU. 7. Hua MS, Li G, Blinderman CD, Wunsch H. Estimates of the need for palliative & care consultation across United States intensive care units using a triggerbased model. Am J Respir Crit Care Med 2014; 189:428–436. This study provided the first estimate of the percentage of ICU patients meeting published criteria for palliative care consultation in US ICUs, highlighting the need for palliative care specialists in the ICU. 8. DeCato TW, Engelberg RA, Downey L, et al. Hospital variation and temporal & trends in palliative and end-of-life care in the ICU. Crit Care Med 2013; 41:1405–1411. This study found signficant differences in the intensity of treatment at the end of life in ICUs, but did not find evidence of improved palliative care delivery over time. 9. Huynh TN, Kleerup EC, Wiley JF, et al. The frequency and cost of treatment && perceived to be futile in critical care. JAMA Intern Med 2013; 173:1887– 1894. This study found that the provision of futile care in the ICU was both common and costly. This observation highlights the need for palliative care, which may help to reduce this type of care. 10. Piers RD, Azoulay E, Ricou B, et al. Inappropriate care in European ICUs: & confronting views from nurses, junior and senior physicians. Chest 2014; 146:267–275. This study found that inappropriate care was common in European ICUs, and investigates differences in the perception of inappropriate care among different ICU providers. 11. Fried TR, Bradley EH, Towle VR, Allore H. Understanding the treatment preferences of seriously ill patients. N Engl J Med 2002; 346:1061– 1066. 12. Turnbull AE, Ruhl AP, Lau BM, et al. Timing of limitations in life support in & acute lung injury patients: a multisite study. Crit Care Med 2014; 42:296– 302. This study of patients with acute lung injury determined that persistent organ failure was associated with an increase in limitations in life support. This highlights one factor that may be associated with poor prognosis and a need for palliative care. 13. O’Mahony S, McHenry J, Blank AE, et al. Preliminary report of the integration of a palliative care team into an intensive care unit. Palliat Med 2010; 24:154– 165. 14. Norton SA, Hogan LA, Holloway RG, et al. Proactive palliative care in the medical intensive care unit: effects on length of stay for selected high-risk patients. Crit Care Med 2007; 35:1530–1535. 15. Campbell ML, Guzman JA. Impact of a proactive approach to improve end-oflife care in a medical ICU. Chest 2003; 123:266–271. 16. Penrod JD, Deb P, Dellenbaugh C. Hospital-based palliative care consultation: effects on hospital cost. J Palliat Med 2010; 13:973–979. 17. Morrison RS, Penrod JD, Cassel JB, et al. Cost savings associated with US hospital palliative care consultation programs. Arch Intern Med 2008; 168:1783–1790. 18. Morrison RS, Dietrich J, Ladwig S, et al. Palliative care consultation teams cut hospital costs for Medicaid beneficiaries. Health Aff (Millwood) 2011; 30:454–463. 19. Nevadunsky NS, Gordon S, Spoozak L, et al. The role and timing of palliative medicine consultation for women with gynecologic malignancies: association with end of life interventions and direct hospital costs. Gynecol Oncol 2014; 132:3–7. 20. Starks H, Wang S, Farber S, et al. Cost savings vary by length of stay for inpatients receiving palliative care consultation services. J Palliat Med 2013; 16:1215–1220. 21. Baldwin MR, Wunsch H, Reyfman PA, et al. High burden of palliative needs & among older ICU survivors transferred to post-acute care facilities: a single center study. Ann Am Thorac Soc 2013; 10:458–465. This single-center study determined that the majority of patients from a cohort of elderly ICU survivors discharged to postacute care facilities had at least one potential palliative care need, suggesting that the burden of palliative care needs of ICU survivors is large. 22. Wunsch H, Christiansen CF, Johansen MB, et al. Psychiatric diagnoses and && psychoactive medication use among nonsurgical critically ill patients receiving mechanical ventilation. JAMA 2014; 311:1133–1142. This cohort study determined that the rate of new psychiatric diagnoses and the use for psychoactive medications is increased for survivors of critical illness in comparison to hospital and general population controls. This study helps to elucidate another potential palliative care need in ICU survivors. 23. Herridge MS, Tansey CM, Matte A, et al. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med 2011; 364:1293–1304. 24. Pandharipande PP, Girard TD, Jackson JC, et al. Long-term cognitive impair&& ment after critical illness. N Engl J Med 2013; 369:1306–1316. This cohort study determined that survivors of critical illness were at high risk for long-term cognitive impairment, and that a longer period of delirium in the hospital was associated with worse cognitive function. This study helps to elucidate another potential palliative care need in ICU survivors. &&
25. Harvey MA. The truth about consequences: postintensive care syndrome in intensive care unit survivors and their families. Crit Care Med 2012; 40:2506–2507. 26. Quill CM, Ratcliffe SJ, Harhay MO, Halpern SD. Variation in decisions to forgo life-sustaining therapies in US intensive care units. Chest 2014; 146:573– 582. 27. Sprung CL, Cohen SL, Sjokvist P, et al. End-of-life practices in European intensive care units: the Ethicus Study. JAMA 2003; 290:790–797. 28. Kross EK, Engelberg RA, Downey L, et al. Differences in end-of-life care in the & ICU across patients cared for by medicine, surgery, neurology, and neurosurgery physicians. Chest 2014; 145:313–321. This study found that the quality of palliative care varied by providers of different specialties, highlighting one aspect contributing to the variability of palliative care delivery in ICUs. 29. Barnato AE, Tate JA, Rodriguez KL, et al. Norms of decision making in the ICU: a case study of two academic medical centers at the extremes of end-of-life treatment intensity. Intensive Care Med 2012; 38:1886–1896. 30. Wilson ME, Samirat R, Yilmaz M, et al. Physician staffing models impact the & timing of decisions to limit life support in the ICU. Chest 2013; 143:656– 663. This retrospective study found that the institution of 24-h intensivist staffing improved the quality of end-of-life care and decreased time to limitations in life support. 31. Azoulay E, Metnitz B, Sprung CL, et al. End-of-life practices in 282 intensive care units: data from the SAPS 3 database. Intensive Care Med 2009; 35:623–630. 32. Nelson JE, Bassett R, Boss RD, et al. Models for structuring a clinical initiative to enhance palliative care in the intensive care unit: a report from the IPAL-ICU Project (improving palliative care in the ICU). Crit Care Med 2010; 38:1765– 1772. 33. Quill TE, Abernethy AP. Generalist plus specialist palliative care: creating a more sustainable model. N Engl J Med 2013; 368:1173–1175. 34. Mosenthal AC, Murphy PA. Interdisciplinary model for palliative care in the trauma and surgical intensive care unit: Robert Wood Johnson Foundation Demonstration Project for improving palliative care in the intensive care unit. Crit Care Med 2006; 34 (Suppl 11):S399–S403. 35. Turnbull AE, Krall JR, Ruhl AP, et al. A scenario-based, randomized trial of && patient values and functional prognosis on intensivist intent to discuss withdrawing life support. Crit Care Med 2014; 42:1455–1462. This scenario-based trial found that intensivists’ likelihood of discussing withdrawal of life-sustaining therapies was not influenced by patients’ values, but was influenced by the recording of patients’ functional prognosis. This highlights that physician decision-making regarding end-of-life care continues to be influenced by prognosis and may not be patient-centered. 36. Goldsmith B, Dietrich J, Du Q, Morrison RS. Variability in access to hospital palliative care in the United States. J Palliat Med 2008; 11:1094– 1102. 37. Lupu D; American Academy of Hospice. Palliative Medicine Workforce Task Force. Estimate of current hospice and palliative medicine physician workforce shortage. J Pain Symptom Manage 2010; 40:899–911. 38. Forte DN, Vincent JL, Velasco IT, Park M. Association between education in EOL care and variability in EOL practice: a survey of ICU physicians. Intensive Care Med 2012; 38:404–412. 39. Galante JM, Bowles TL, Khatri VP, et al. Experience and attitudes of surgeons toward palliation in cancer. Arch Surg 2005; 140:873–878. 40. Brasel KJ, Weissman DE. Palliative care education for surgeons. J Am Coll Surg 2004; 199:495–499. 41. Curtis JR, Nielsen EL, Treece PD, et al. Effect of a quality-improvement intervention on end-of-life care in the intensive care unit: a randomized trial. Am J Respir Crit Care Med 2011; 183:348–355. 42. Curtis JR, Back AL, Ford DW, et al. Effect of communication skills training && for residents and nurse practitioners on quality of communication with patients with serious illness: a randomized trial. JAMA 2013; 310:2271– 2281. This trial of a communication skills intervention did not find improved quality of communication or improved quality of end-of-life care with the intervention. This highlights the difficulty in teaching certain skills necessary for the provision of palliative care, such as communication. 43. Wysham NG, Mularski RA, Schmidt DM, et al. Long-term persistence of quality improvements for an intensive care unit communication initiative using the VALUE strategy. J Crit Care 2014; 29:450–454. 44. Black MD, Vigorito MC, Curtis JR, et al. A multifaceted intervention to improve & compliance with process measures for ICU clinician communication with ICU patients and families. Crit Care Med 2013; 41:2275–2283. This study implementing a multifaceted communication intervention found significant variation in the effect of the intervention in different types of ICUs, suggesting that the institutional and organizational characteristics may modify the effect of interventions on process measures of palliative care. 45. Lau BD, Aslakson RA, Wilson RF, et al. Methods for improving the quality of palliative care delivery: a systematic review. Am J Hosp Palliat Care 2014; 31:202–210. 46. Bradley CT, Brasel KJ. Developing guidelines that identify patients who would benefit from palliative care services in the surgical intensive care unit. Crit Care Med 2009; 37:946–950.
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
679
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU 47. Weissman DE, Meier DE. Identifying patients in need of a palliative care assessment in the hospital setting: a consensus report from the Center to Advance Palliative Care. J Palliat Med 2011; 14:17–23. 48. Campbell ML, Guzman JA. A proactive approach to improve end-of-life care in a medical intensive care unit for patients with terminal dementia. Crit Care Med 2004; 32:1839–1843. 49. Bradley C, Weaver J, Brasel K. Addressing access to palliative care services in the surgical intensive care unit. Surgery 2010; 147:871–877. 50. Sihra L, Harris M, O’Reardon C. Using the improving palliative care in the intensive care unit (IPAL-ICU) project to promote palliative care consultation. J Pain Symptom Manage 2011; 42:672–675. 51. Nelson JE, Curtis JR, Mulkerin C, et al. Choosing and using screening criteria for palliative care consultation in the ICU: a report from the Improving Palliative Care in the ICU (IPAL-ICU) Advisory Board. Crit Care Med 2013; 41:2318– 2327. 52. Scheunemann LP, McDevitt M, Carson SS, Hanson LC. Randomized, controlled trials of interventions to improve communication in intensive care: a systematic review. Chest 2011; 139:543–554. 53. Fawole OA, Dy SM, Wilson RF, et al. A systematic review of communication quality improvement interventions for patients with advanced and serious illness. J Gen Intern Med 2013; 28:570–577. 54. Gabler NB, Ratcliffe SJ, Wagner J, et al. Mortality among patients admitted to strained intensive care units. Am J Respir Crit Care Med 2013; 188:800–806. 55. Lynch T, Connor S, Clark D. Mapping levels of palliative care development: a global update. J Pain Symptom Manage 2013; 45:1094–1106. 56. Pivodic L, Pardon K, Van den Block L, et al. Palliative care service use in four European countries: a cross-national retrospective study via representative networks of general practitioners. PLoS One 2013; 8:e84440. 57. Yamaguchi T, Kuriya M, Morita T, et al. Palliative care development in the AsiaPacific region: an international survey from the Asia Pacific Hospice Palliative Care Network (APHN). BMJ Support Palliat Care 2014. [Epub ahead of print] 58. Clark D, Wright M, Hunt J, Lynch T. Hospice and palliative care development in Africa: a multimethod review of services and experiences. J Pain Symptom Manage 2007; 33:698–710.
680
www.co-criticalcare.com
59. Koper I, van der Heide A, Janssens R, et al. Consultation with specialist palliative care services in palliative sedation: considerations of Dutch physicians. Support Care Cancer 2014; 22:225–231. 60. Rodriguez KL, Barnato AE, Arnold RM. Perceptions and utilization of palliative care services in acute care hospitals. J Palliat Med 2007; 10:99–110. 61. White DB, Cua SM, Walk R, et al. Nurse-led intervention to improve surrogate decision making for patients with advanced critical illness. Am J Crit Care 2012; 21:396–409. 62. Baldwin MR, Reid MC, Westlake AA, et al. The feasibility of measuring frailty to predict disability and mortality in older medical intensive care unit survivors. J Crit Care 2014; 29:401–408. 63. Azevedo LC, Caruso P, Silva UV, et al. Outcomes for patients with cancer admitted to the ICU requiring ventilatory support: results from a prospective multicenter study. Chest 2014; 146:257–266. 64. Bagshaw SM, Stelfox HT, McDermid RC, et al. Association between frailty & and short- and long-term outcomes among critically ill patients: a multicentre prospective cohort study. CMAJ 2014; 186:E95–102. This study determined that frailty in ICU patients is common, and frail patients were at increased risk of adverse events and mortality, suggesting that frailty may be an important additional prognostic factor to consider. 65. Watanabe SM, Fairchild A, Pituskin E, et al. Improving access to specialist multidisciplinary palliative care consultation for rural cancer patients by videoconferencing: report of a pilot project. Support Care Cancer 2013; 21:1201–1207. 66. Menon PR, Stapleton RD, McVeigh U, Rabinowitz T. Telemedicine as a tool to provide family conferences and palliative care consultations in critically III patients at rural healthcare institutions: a pilot study. Am J Hosp Palliat Care 2014. [Epub ahead of print] 67. Duursma F, Schers HJ, Vissers KC, Hasselaar J. Study protocol: optimization of complex palliative care at home via telemedicine. A cluster randomized controlled trial. BMC Palliat Care 2011; 10:13. 68. Aslakson RA, Bridges JF. Assessing the impact of palliative care in the intensive care unit through the lens of patient-centered outcomes research. Curr Opin Crit Care 2013; 19:504–510.
Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU May Hua a and Hannah Wunsch a,b,c
Purpose of review Although providing palliative care in the ICU has become a priority, the success of different methods to integrate palliative care into the ICU has varied. This review examines the current evidence supporting the different models of palliative care delivery and highlights areas for future study. Recent findings The need for palliative care for ICU patients is substantial. A large percentage of patients meet criteria for palliative care consultation and there is frequent use of intensive care and other nonbeneficial care at the end of life. Overall, the consultative model of palliative care appears to have more of an impact on patient care. However, given the current workforce shortage of palliative care providers, a sustainable model of delivering palliative care requires both an effective integrative model, in which palliative care is delivered by ICU clinicians, and appropriate use of the consultative model, in which palliative care consultation is reserved for patients at highest risk of having unmet or long-term palliative care needs. Summary Developing a mixed model of palliative care delivery is necessary to meet the palliative care needs of critically ill patients. Efforts focused on improving integrative models and appropriately targeting the use of palliative care consultants are needed. Keywords critical care, end-of-life care, palliative care, palliative care consultation, quality improvement
INTRODUCTION For decades intensive care providers focused primarily on increasing short-term survival. But in recent years, the purview of critical care has expanded to improving long-term outcomes associated with critical illness and improving quality of life for patients who are dying. Previously, ICU clinicians were largely concerned with rescuing patients from their disease process. Now, avoiding unnecessary medicalization and striving for a ‘good’ death have become increasingly important. There is little debate that the delivery of palliative care and endof-life care in the ICU requires improvement. Multiple professional societies endorse the need for palliative care in the ICU [1,2], and one of the five recommendations made by the Critical Care Societies Collaborative as a part of the ‘Choosing Wisely’ campaign was ‘don’t continue life support for patients at high risk of death or severely impaired functional recovery without offering. . . the alternative of care focused entirely on comfort’ [3]. As the provision of palliative care has become a priority, we must determine which methods are most effective for delivering palliative care in the ICU. In this review, we discuss different models of palliative care delivery and consider the benefits
and drawbacks of each model and areas for improvement.
UNDERSTANDING THE NEED FOR IMPROVED PALLIATIVE CARE IN THE ICU Despite efforts in the last decade and a half to improve palliative care and end-of-life care, patients with critical illness continue to be at high risk of having unmet palliative care needs. Mortality for ICU patients during hospitalization remains high [4], and long-term mortality is increased for survivors of critical illness, particularly in the 6 months following hospital discharge [5]. Although the use of hospice at the end of life in the United States has
a
Department of Anesthesiology, Columbia University, New York, New York, USA, bDepartment of Critical Care Medicine, Sunnybrook Hospital and cDepartment of Anesthesia, University of Toronto, Toronto, Ontario, Canada Correspondence to May Hua, MD, Department of Anesthesiology, Columbia University, 622 West 168th Street PH5, Room 535 New York, NY 10032, USA. Tel: +1 212 305 1982; fax: +1 212 305 3204; e-mail: [email protected] Curr Opin Crit Care 2014, 20:673–680 DOI:10.1097/MCC.0000000000000149
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
KEY POINTS There is a large need for palliative care in the ICU, but successful models of delivery in varied practice settings have yet to be well defined. Available evidence suggests that the consultative model may be more effective.
In addition, survivors of critical illness may have significant palliative care needs. A study of elderly ICU patients discharged to postacute care facilities in the United States found that 88% of patients had at least one potential palliative care need [21 ]. ICU survivors suffer from cognitive dysfunction, psychiatric disorders, functional disability and increased long-term mortality [5,22 ,23,24 ]. This constellation of problems has been labeled a ‘postintensive care syndrome’ [25] and thus far, few interventions have been shown to improve outcomes. Palliative care, a specialty that focuses on improving symptomatology and quality of life, may be best poised to provide long-term care for many of these patients. Substantial variation exists in the delivery of palliative care in the ICU. Although this variation is likely partially driven by patient preferences, some of it may be related to differences in the culture of individual providers as well as institutional and organizational factors. In a study of decisions to forego life-sustaining treatment in US ICUs the predicted probability of making such decisions varied greatly, even after adjustment for patient-level and ICU-level effects [26]. These findings are similar to that of European ICUs, in which limitations in therapy were much more common, but also geographically variable [27]. This unexplained variation suggests that there may be differences in physician practice that alter the likelihood of making these decisions. One study found that ratings of the quality of dying varied between physicians of different specialties [28 ]. Furthermore, clinicians’ practice may be influenced by the environment. Intensivists practicing in ‘low’ and ‘high’ intensity institutions were found to differ in their approaches to decisionmaking regarding life-sustaining treatments and prognosis [29], and medical ICU patients are more likely to have treatment limitations placed than those cared for in surgical ICUs [7 ,12 ]. ICU staffing models also may affect palliative care delivery, as the use of 24-h nighttime intensivist staffing was associated with a decrease in the time to end-of-life decision making [30 ], and differences in both physician and nurse staffing altered the likelihood of making decisions to forego life-sustaining treatment in European ICUs [31]. &
&&
Methods to improve the quality of integrative palliative care delivered in ICUs, as well as more stringent evaluation of the consultative model of palliative care with regards to the improvement of patient-centered outcomes, are necessary. Given the workforce shortage of palliative care providers, sustainable models of palliative care delivery in the ICU will need to include a combination of the integrative and consultative models.
gone up, the use of ICU within the last 30 days of life has concomitantly increased [6 ]. In US ICUs, it is estimated that approximately 15% of all patients meet screening triggers for palliative care consultation [7 ], and this is likely underestimating the overall need, given that referrals for reasons such as refractory symptom management, conflict resolution and existential distress were not captured. Yet, in a study of a multifaceted educational intervention to improve palliative care in the ICU, there did not appear to be any improvement in the quality of palliative care, as assessed by the quality of death and dying, over time [8 ]. Furthermore, the provision of treatment perceived to be futile remains common in both the United States and Europe, and was estimated in a single center study in the United States to make up 3.5% of the hospital costs for ICU patients [9 ,10 ]. Futile care not only places a financial strain on the healthcare system without benefit, it also may not be in line with patients’ preferences, as patients and family often wish to avoid burdensome treatments in the face of a poor prognosis [11,12 ]. The use of palliative care has been reported to improve this misalignment between the care that is provided and the care that patients actually desire. Benefits of palliative care in the ICU include decreased use of nonbeneficial life-sustaining therapies, increased use of hospice and increased establishment of advanced directives [13–15]. Furthermore, palliative care consultation has been associated with decreased ICU length of stay, and decreased costs at the end of life in a generalized hospital setting [16–18]. However, it is important to note that cost savings may be dependent on both the timing of palliative care involvement and overall length of hospital stay [19,20]. &&
&
&
&&
&
&
674
www.co-criticalcare.com
&&
&
&
&
&
MODELS OF DELIVERING PALLIATIVE CARE There are several major challenges to adequately meeting the palliative care needs of critically ill patients, including first, the difficulty of identifying which patients are appropriate for palliative care and/ or hospice services, second, the variability associated with the initiation and quality of palliative care that Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch Table 1. Example of a checklist of an integrative palliative care intervention Within 24 h of admission
Within 72 h
End-of-life care
No time frame
Bereavement and psychosocial support for patients and families
Family meeting with physician and nurse within 72 h of admission to the surgical ICU
Implementation of palliative care standing order set and ventilator withdrawal guidelines for patients who are identified as imminently dying
Integration of palliative care performance into morbidity and mortality conferences and peer review
Interdisciplinary palliative care assessment
Comprehensive palliative care plan by 72 h including:
Assessment of pain and symptoms
Goals of care
Assessment of psychosocial, spiritual and bereavement needs of family
Pain and symptom management
Identify surrogate decision-maker
Psychosocial support for the family
Solicit and clarify advanced directives
Discussion about do-not-resuscitate orders or withdrawal or withholding of life-sustaining treatments if appropriate
Assessment of likely outcome and prognosis (discharge from ICU, discharge from hospital) from the current illness with regards to mortality and quality of life Adapted from [34].
is provided and third, a lack of appropriately trained providers of palliative care. These are issues that the current models of delivering palliative care must address. The two main models of delivering palliative care in the ICU are the integrative model and the consultative model [32], reflecting the division between generalist and specialist palliative care [33]. Generalist palliative care is delivered by primary providers, and involves basic palliative care skills, including knowledge of uncomplicated pain and symptom management, elicitation of preferences and basic discussions regarding goals of care. Specialized palliative care, which is delivered by consultants, is appropriate for patients who are in need of assistance with complex decision-making, refractory pain and symptom management, significant psychological distress or conflict resolution regarding goals of care [33]. These models can, and likely should, be combined in practice.
and palliative care needs are routinely assessed as a part of ICU care and communication with families regarding prognosis and goals of care is structured and standardized, regardless of prognosis. This can be applied universally to all ICU patients, or to subgroups meeting particular criteria that can be chosen to meet the needs of an individual ICU [32]. Examples of these models and methods for implementation have been described previously (Table 1) [32,34]. The main tool for this type of quality improvement lies in protocolization of aspects of palliative care, such as routine pain and symptom assessment, documentation of surrogate decision-makers and advanced directives, conducting family meetings within a prescribed amount of time and the use of palliative care order sets. Although protocolization of care is common in critical care, the success of such palliative care initiatives may be highly dependent on the culture of an individual ICU and training of individual physicians.
INTEGRATIVE MODEL The integrative model of palliative care delivery is one in which principles of palliative care are incorporated into everyday ICU care, and palliative care is delivered by the ICU team. In this model, symptoms
ADVANTAGES OF THE INTEGRATIVE MODEL One of the greatest benefits of the integrative approach is that patients ‘in need of palliative care’
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
675
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
do not need to be identified, as all patients receive a basic palliative care needs assessment and have a palliative care treatment plan that is carried out in conjunction with the rest of their ICU care. The question to answer is not ‘who needs palliative care?’, but ‘how much palliative care does a particular patient need?’. In the most successful models, these practices are not tied to prognosis, as prognostication remains difficult for clinicians. However, a recent study showed that physicians were still largely influenced by functional prognosis in their decisions to initiate withdrawal of life-sustaining treatment with families, and were more influenced by their own assessment of prognosis than by the preferences of the patient or family [35 ]. Another advantage of this model is that it does not require additional staffing and is not dependent on a palliative care service. This advantage is important, as many hospitals do not have palliative care services [36], and there is a workforce shortage of palliative care specialists [37]. Lastly, the integrative approach, if implemented, may shift the culture of an ICU, as it requires staff to prioritize palliative care as a problem that needs to be addressed daily, similar to ventilator weaning, or interruption of sedation. &&
DISADVANTAGES OF THE INTEGRATIVE MODEL Although the integrative model has many potential benefits, empirically, there have been difficulties with implementation and effectiveness. First, there is significant provider variability in the delivery of palliative care. In a study of a quality improvement intervention for palliative care in the ICU, the quality of death as rated by nurses and families differed significantly between specialties, with neurologists and neurosurgeons having the best ratings and general and other subspecialty surgeons having the worst ratings [28 ]. This variability may be related in part to the prominence of palliative care education among different specialties, as education in palliative care has been associated with variation in end-of-life care practices in the ICU [38]. Certain specialty training programs, such as general surgery, have been noted to be particularly deficient in palliative care education [39,40]. However, better education of clinicians in palliative care skills may not translate to improved outcomes, as a randomized controlled trial of a multifaceted palliative care intervention that included several educational components for clinicians did not affect ICU length of stay or improve quality of death and dying [41]. Particular skills that are crucial to palliative care, such as communication, are difficult to teach. A trial of a simulation intervention to improve trainees’
communication skills did not improve the quality of communication about end-of-life care or the quality of end-of-life care, but was associated with a small increase in depressive symptoms among patients in the intervention arm [42 ]. Some interventions have been successful at demonstrating long-term improvements in process measures such as documentations of care goals and daily family updates [43], but the effect of an intervention may also differ across institutions. A multifaceted intervention to improve communication in a statewide ICU collaborative found significant variation among different ICU types, with closed units and teaching units being more likely to improve in comparison with open and nonteaching units [44 ]. Overall, the effectiveness and generalizability of quality improvement interventions to deliver integrative palliative care have been difficult to demonstrate [45]. Despite this lack of success, there are some general lessons that can be learned. First, it is very difficult to effect change. The failure of welldesigned interventions to impact outcomes is likely partly because of the fact that physicians may be relatively recalcitrant to changing their practices in this area, although this remains speculative. A consistent finding is that quality improvement interventions are most likely to succeed if they are ‘home-grown,’ arising from within the institution. One reason provided for the failure of an intervention to improve outcomes in a multicenter trial (but that did initially achieve an effect in a single-center study) was that it was difficult to achieve the same level of commitment and buy-in from clinicians at other institutions with different cultures of care [41]. Despite these difficulties, it is essential that we improve the integrative model of palliative care, as this constitutes, and will remain, the majority of palliative care delivery to critically ill patients. &&
&
&
676
www.co-criticalcare.com
CONSULTATIVE MODEL In the consultative model of palliative care delivery, palliative care is provided by consultants. With this approach, identifying which patients are appropriate for palliative care presents a greater challenge, and consultation can be facilitated by choosing appropriate screening criteria, or triggers, for palliative care consultation. Triggers have been designed (largely through consensus criteria) to select patients at high risk of poor outcomes who may benefit from earlier discontinuation of life-sustaining therapies, as well as patients with chronic severe illness requiring aggressive symptom management [14,46,47]. Multiple sets of triggers for ICU palliative care consultation have been published [14,15,47–50], but success in implementation has varied. In one study in a medical ICU, Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch
the use of triggers was associated with a decrease in ICU length of stay, whereas another study, using different triggers in a surgical ICU, failed to even increase the number of consultations. This difference was likely because of the fact that in the first study, referral to palliative care was automatic upon meeting a trigger, whereas in the surgical ICU study, information was relayed to the ICU team who ultimately decided whether or not to refer patients [14,15,49]. These studies demonstrate that simply screening patients for palliative care needs is insufficient; if triggers are not used to their full potential, the consultative model may be ineffective. There are also differences between published triggers that may influence their efficacy; certain triggers are objective (status post cardiac arrest) whereas others are more subjective (death expected during ICU stay). A recent study pooled many triggers together and found that five ‘efficient’ triggers (all of which were objective or ‘concrete’) were able to capture 85% of all patients meeting any trigger across different types of ICUs. Efficient triggers for palliative care consultation (adapted from Hua et al. [7 ] with permission of the American Thoracic Society. Copyright ß 2014 American Thoracic Society) are as follows: &
(1) ICU admission after hospital stay at least 10 days, (2) multisystem organ failure at least three systems, (3) diagnosis of active stage IV malignancy (metastatic disease), (4) status post cardiac arrest, (5) diagnosis of intracerebral hemorrhage requiring mechanical ventilation. Despite the finding of relatively little variation when current triggers were applied across different ICUs [7 ] it is unlikely that there will be universal agreement on triggers for palliative care consultation in the ICU. More likely (and perhaps appropriate) is the development of triggers tailored to the individual patient population and culture of an institution [51]. &
ADVANTAGES OF THE CONSULTATIVE MODEL The main advantage of the consultative model is that there is stronger literature supporting its effectiveness. Use of palliative care consultation in the ICU has been associated with decreased ICU length of stay and decreased use of nonbeneficial lifesustaining treatments [13–15], and meta-analyses of interventions to improve communication have also suggested that the consultative model appears
to be more effective, particularly for decreasing healthcare utilization [52,53]. This clearer impact from specialized palliative care may be due to less variability in the delivery of care. The consultative model also may be particularly helpful in moderating conflict between families and the ICU team, and in offsetting some of the work burden of intensivists. This division of time may be beneficial for other ICU patients, as increases in ‘ICU strain,’ as measured by increases in the number of admissions, patients’ severity of illness and increases in overall census, have been associated with small, but real, increases in mortality [54]. Lastly, palliative care consultants may also provide continuity of care for a patient through different ICU teams and after discharge from the ICU [32]. This final point is potentially an important key strength of the consultative model, as delivery of palliative care with an integrative model may end upon ICU discharge. Many patients who may be appropriate for palliative care will not die in the ICU, and therefore require these services beyond the ICU and often after hospital discharge as well; provision of appropriate palliative care in the post-ICU discharge setting may be equally (or more) important than its provision during the ICU stay.
DISADVANTAGES OF CONSULTATIVE MODEL The largest drawback to the consultative model is its reliance on palliative care specialists. Significant disparity exists in the availability of palliative care services internationally [55]. The presence of palliative care services in hospitals varies throughout the United States and Europe [36,56], and throughout Asia and Africa, palliative care services are still in various stages of development [57,58]. In some countries, there is also reticence to the idea of mandatory palliative care consultation [59]. These issues make it unlikely that this model will suffice on its own to meet the palliative care needs of critically ill patients globally. Another disadvantage is that having an additional consulting team may further fragment patient care and introduce conflict with intensivists and other primary providers, such as surgeons or oncologists. ICU clinicians in particular may not look favorably upon the introduction of palliative care consultants, as they view palliative care as part of the scope of their practice [60] and may not always be willing to cede this part of care [61]; the success of the consultative approach is highly dependent on the culture of an ICU and whether or not a collaborative environment can be established [51].
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
677
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU
FUTURE DIRECTIONS Palliative care in the ICU is impaired by numerous barriers, and problems exist with both models of delivery. Integrative models are hindered by the fact that proven methods of improving palliative care skills of generalist providers are lacking. The education to truly integrate palliative care into generalist practice may need to begin as early as medical school. Also, the effect of interventions may be impacted by many different factors pertaining to patients, providers and the individual institutions in which they are implemented. Despite this, there may be value in determining if parts of these complex interventions are generalizable; perhaps a methodology for implementation, protocols for performing needs assessments or process measures may be portable from one institution to another. Similarly, aspects of using the consultative model require further study. Existing triggers have not been validated against an objective benchmark, and may need to be refined. Trying to identify these high-risk patients should be a priority, as it may allow for targeting of specialized palliative care to patients most likely to derive benefit, and can maximize the utility of a scarce resource. This may be accomplished by defining new triggers, or by combining existing ones with other factors associated with a poor prognosis, such as frailty [62,63,64 ]. Another approach to dealing with the shortage of palliative care providers may be to use methods for extending scarce resources, such as telemedicine, which has already been used in some ICU settings to provide intensivist coverage. Using telemedicine to deliver palliative care has been demonstrated to be feasible for both cancer and ICU patients [65,66], and a cluster-randomized trial using telemedicine to deliver home palliative care is underway in the Netherlands [67]. We also have yet to determine which model will operate best under different ICU organizational characteristics and staffing models. It may be that integrative palliative care may be more successful with a closed staffing model, as these ICUs may have a greater ability to change ICU culture and practice [34,44 ]. Another area that merits considerable focus is the use of palliative care to improve the long-term sequelae of critical illness for survivors. Given the high burden of symptoms affecting the quality of life in this population, the initiation of palliative care during an ICU stay, or perhaps even upon ICU discharge, may improve these outcomes, which have been difficult to improve thus far. Perhaps most importantly, comparisons of both integrative and consultative interventions in the ICU have been hampered by the use of heterogeneous outcomes, such as ICU length of stay, clinician satisfaction and &
&
678
www.co-criticalcare.com
family ratings of death and dying [68]. Studies thus far lack the use of outcomes that truly measure improvements for patients, and evaluations of palliative care delivery cannot exclude this important stakeholder. Appropriate patient-centered outcomes that are both sensitive and responsive need to be developed and standardized so that palliative care interventions can be effectively studied.
CONCLUSION As the benefits of palliative care during, and potentially after, an ICU stay are elucidated, the adequate delivery of palliative care to critically ill patients should be a priority for healthcare. Given that there are advantages and disadvantages of both the integrative and consultative models, improving access to palliative care in the ICU will likely require the use of a mixed model that combines both approaches. In the current milieu, meeting the palliative care needs of critically ill patients will depend on tailoring integrative and consultative models to meet the needs of a particular ICU. In certain institutions, palliative care consultants may be required simply to perform a basic needs assessment, whereas in ICUs with well-developed integrative models, consultants may be reserved for only the highest risk cases. Finding an appropriate balance of these two models for an individual ICU, as well as at regional and national levels, is necessary to improve delivery of palliative care to critically ill patients. Acknowledgements Support: Dr Hua is supported by a Mentored-Training Research Grant from the Foundation in Anesthesia Education and Research. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Truog RD, Campbell ML, Curtis JR, et al. Recommendations for end-of-life care in the intensive care unit: a consensus statement by the American College [corrected] of Critical Care Medicine. Crit Care Med 2008; 36:953–963. 2. Lanken PN, Terry PB, Delisser HM, et al. An official American Thoracic Society clinical policy statement: palliative care for patients with respiratory diseases and critical illnesses. Am J Respir Crit Care Med 2008; 177:912–927. 3. Critical Care Societies Collaborative. Five things physicians and patients should question 2014 [cited 4 June 2014]. Available from: http://www.choo singwisely.org/doctor-patient-lists/critical-care-societies-collaborative-criticalcare/. 4. Lilly CM, Zuckerman IH, Badawi O, Riker RR. Benchmark data from more than 240 000 adults that reflect the current practice of critical care in the United States. Chest 2011; 140:1232–1242. 5. Wunsch H, Guerra C, Barnato AE, et al. Three-year outcomes for Medicare beneficiaries who survive intensive care. JAMA 2010; 303:849–856.
Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Integrating palliative care in the ICU Hua and Wunsch 6. Teno JM, Gozalo PL, Bynum JP, et al. Change in end-of-life care for Medicare beneficiaries: site of death, place of care, and healthcare transitions in 2000, 2005, and 2009. JAMA 2013; 309:470–477. This study determined that the use of intensive care and the number of healthcare transitions at the end of life have both increased over time. This observation helps to define the urgent need to improve the delivery of palliative care in the ICU. 7. Hua MS, Li G, Blinderman CD, Wunsch H. Estimates of the need for palliative & care consultation across United States intensive care units using a triggerbased model. Am J Respir Crit Care Med 2014; 189:428–436. This study provided the first estimate of the percentage of ICU patients meeting published criteria for palliative care consultation in US ICUs, highlighting the need for palliative care specialists in the ICU. 8. DeCato TW, Engelberg RA, Downey L, et al. Hospital variation and temporal & trends in palliative and end-of-life care in the ICU. Crit Care Med 2013; 41:1405–1411. This study found signficant differences in the intensity of treatment at the end of life in ICUs, but did not find evidence of improved palliative care delivery over time. 9. Huynh TN, Kleerup EC, Wiley JF, et al. The frequency and cost of treatment && perceived to be futile in critical care. JAMA Intern Med 2013; 173:1887– 1894. This study found that the provision of futile care in the ICU was both common and costly. This observation highlights the need for palliative care, which may help to reduce this type of care. 10. Piers RD, Azoulay E, Ricou B, et al. Inappropriate care in European ICUs: & confronting views from nurses, junior and senior physicians. Chest 2014; 146:267–275. This study found that inappropriate care was common in European ICUs, and investigates differences in the perception of inappropriate care among different ICU providers. 11. Fried TR, Bradley EH, Towle VR, Allore H. Understanding the treatment preferences of seriously ill patients. N Engl J Med 2002; 346:1061– 1066. 12. Turnbull AE, Ruhl AP, Lau BM, et al. Timing of limitations in life support in & acute lung injury patients: a multisite study. Crit Care Med 2014; 42:296– 302. This study of patients with acute lung injury determined that persistent organ failure was associated with an increase in limitations in life support. This highlights one factor that may be associated with poor prognosis and a need for palliative care. 13. O’Mahony S, McHenry J, Blank AE, et al. Preliminary report of the integration of a palliative care team into an intensive care unit. Palliat Med 2010; 24:154– 165. 14. Norton SA, Hogan LA, Holloway RG, et al. Proactive palliative care in the medical intensive care unit: effects on length of stay for selected high-risk patients. Crit Care Med 2007; 35:1530–1535. 15. Campbell ML, Guzman JA. Impact of a proactive approach to improve end-oflife care in a medical ICU. Chest 2003; 123:266–271. 16. Penrod JD, Deb P, Dellenbaugh C. Hospital-based palliative care consultation: effects on hospital cost. J Palliat Med 2010; 13:973–979. 17. Morrison RS, Penrod JD, Cassel JB, et al. Cost savings associated with US hospital palliative care consultation programs. Arch Intern Med 2008; 168:1783–1790. 18. Morrison RS, Dietrich J, Ladwig S, et al. Palliative care consultation teams cut hospital costs for Medicaid beneficiaries. Health Aff (Millwood) 2011; 30:454–463. 19. Nevadunsky NS, Gordon S, Spoozak L, et al. The role and timing of palliative medicine consultation for women with gynecologic malignancies: association with end of life interventions and direct hospital costs. Gynecol Oncol 2014; 132:3–7. 20. Starks H, Wang S, Farber S, et al. Cost savings vary by length of stay for inpatients receiving palliative care consultation services. J Palliat Med 2013; 16:1215–1220. 21. Baldwin MR, Wunsch H, Reyfman PA, et al. High burden of palliative needs & among older ICU survivors transferred to post-acute care facilities: a single center study. Ann Am Thorac Soc 2013; 10:458–465. This single-center study determined that the majority of patients from a cohort of elderly ICU survivors discharged to postacute care facilities had at least one potential palliative care need, suggesting that the burden of palliative care needs of ICU survivors is large. 22. Wunsch H, Christiansen CF, Johansen MB, et al. Psychiatric diagnoses and && psychoactive medication use among nonsurgical critically ill patients receiving mechanical ventilation. JAMA 2014; 311:1133–1142. This cohort study determined that the rate of new psychiatric diagnoses and the use for psychoactive medications is increased for survivors of critical illness in comparison to hospital and general population controls. This study helps to elucidate another potential palliative care need in ICU survivors. 23. Herridge MS, Tansey CM, Matte A, et al. Functional disability 5 years after acute respiratory distress syndrome. N Engl J Med 2011; 364:1293–1304. 24. Pandharipande PP, Girard TD, Jackson JC, et al. Long-term cognitive impair&& ment after critical illness. N Engl J Med 2013; 369:1306–1316. This cohort study determined that survivors of critical illness were at high risk for long-term cognitive impairment, and that a longer period of delirium in the hospital was associated with worse cognitive function. This study helps to elucidate another potential palliative care need in ICU survivors. &&
25. Harvey MA. The truth about consequences: postintensive care syndrome in intensive care unit survivors and their families. Crit Care Med 2012; 40:2506–2507. 26. Quill CM, Ratcliffe SJ, Harhay MO, Halpern SD. Variation in decisions to forgo life-sustaining therapies in US intensive care units. Chest 2014; 146:573– 582. 27. Sprung CL, Cohen SL, Sjokvist P, et al. End-of-life practices in European intensive care units: the Ethicus Study. JAMA 2003; 290:790–797. 28. Kross EK, Engelberg RA, Downey L, et al. Differences in end-of-life care in the & ICU across patients cared for by medicine, surgery, neurology, and neurosurgery physicians. Chest 2014; 145:313–321. This study found that the quality of palliative care varied by providers of different specialties, highlighting one aspect contributing to the variability of palliative care delivery in ICUs. 29. Barnato AE, Tate JA, Rodriguez KL, et al. Norms of decision making in the ICU: a case study of two academic medical centers at the extremes of end-of-life treatment intensity. Intensive Care Med 2012; 38:1886–1896. 30. Wilson ME, Samirat R, Yilmaz M, et al. Physician staffing models impact the & timing of decisions to limit life support in the ICU. Chest 2013; 143:656– 663. This retrospective study found that the institution of 24-h intensivist staffing improved the quality of end-of-life care and decreased time to limitations in life support. 31. Azoulay E, Metnitz B, Sprung CL, et al. End-of-life practices in 282 intensive care units: data from the SAPS 3 database. Intensive Care Med 2009; 35:623–630. 32. Nelson JE, Bassett R, Boss RD, et al. Models for structuring a clinical initiative to enhance palliative care in the intensive care unit: a report from the IPAL-ICU Project (improving palliative care in the ICU). Crit Care Med 2010; 38:1765– 1772. 33. Quill TE, Abernethy AP. Generalist plus specialist palliative care: creating a more sustainable model. N Engl J Med 2013; 368:1173–1175. 34. Mosenthal AC, Murphy PA. Interdisciplinary model for palliative care in the trauma and surgical intensive care unit: Robert Wood Johnson Foundation Demonstration Project for improving palliative care in the intensive care unit. Crit Care Med 2006; 34 (Suppl 11):S399–S403. 35. Turnbull AE, Krall JR, Ruhl AP, et al. A scenario-based, randomized trial of && patient values and functional prognosis on intensivist intent to discuss withdrawing life support. Crit Care Med 2014; 42:1455–1462. This scenario-based trial found that intensivists’ likelihood of discussing withdrawal of life-sustaining therapies was not influenced by patients’ values, but was influenced by the recording of patients’ functional prognosis. This highlights that physician decision-making regarding end-of-life care continues to be influenced by prognosis and may not be patient-centered. 36. Goldsmith B, Dietrich J, Du Q, Morrison RS. Variability in access to hospital palliative care in the United States. J Palliat Med 2008; 11:1094– 1102. 37. Lupu D; American Academy of Hospice. Palliative Medicine Workforce Task Force. Estimate of current hospice and palliative medicine physician workforce shortage. J Pain Symptom Manage 2010; 40:899–911. 38. Forte DN, Vincent JL, Velasco IT, Park M. Association between education in EOL care and variability in EOL practice: a survey of ICU physicians. Intensive Care Med 2012; 38:404–412. 39. Galante JM, Bowles TL, Khatri VP, et al. Experience and attitudes of surgeons toward palliation in cancer. Arch Surg 2005; 140:873–878. 40. Brasel KJ, Weissman DE. Palliative care education for surgeons. J Am Coll Surg 2004; 199:495–499. 41. Curtis JR, Nielsen EL, Treece PD, et al. Effect of a quality-improvement intervention on end-of-life care in the intensive care unit: a randomized trial. Am J Respir Crit Care Med 2011; 183:348–355. 42. Curtis JR, Back AL, Ford DW, et al. Effect of communication skills training && for residents and nurse practitioners on quality of communication with patients with serious illness: a randomized trial. JAMA 2013; 310:2271– 2281. This trial of a communication skills intervention did not find improved quality of communication or improved quality of end-of-life care with the intervention. This highlights the difficulty in teaching certain skills necessary for the provision of palliative care, such as communication. 43. Wysham NG, Mularski RA, Schmidt DM, et al. Long-term persistence of quality improvements for an intensive care unit communication initiative using the VALUE strategy. J Crit Care 2014; 29:450–454. 44. Black MD, Vigorito MC, Curtis JR, et al. A multifaceted intervention to improve & compliance with process measures for ICU clinician communication with ICU patients and families. Crit Care Med 2013; 41:2275–2283. This study implementing a multifaceted communication intervention found significant variation in the effect of the intervention in different types of ICUs, suggesting that the institutional and organizational characteristics may modify the effect of interventions on process measures of palliative care. 45. Lau BD, Aslakson RA, Wilson RF, et al. Methods for improving the quality of palliative care delivery: a systematic review. Am J Hosp Palliat Care 2014; 31:202–210. 46. Bradley CT, Brasel KJ. Developing guidelines that identify patients who would benefit from palliative care services in the surgical intensive care unit. Crit Care Med 2009; 37:946–950.
1070-5295 ß 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
www.co-criticalcare.com
679
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Ethical, legal and organizational issues in the ICU 47. Weissman DE, Meier DE. Identifying patients in need of a palliative care assessment in the hospital setting: a consensus report from the Center to Advance Palliative Care. J Palliat Med 2011; 14:17–23. 48. Campbell ML, Guzman JA. A proactive approach to improve end-of-life care in a medical intensive care unit for patients with terminal dementia. Crit Care Med 2004; 32:1839–1843. 49. Bradley C, Weaver J, Brasel K. Addressing access to palliative care services in the surgical intensive care unit. Surgery 2010; 147:871–877. 50. Sihra L, Harris M, O’Reardon C. Using the improving palliative care in the intensive care unit (IPAL-ICU) project to promote palliative care consultation. J Pain Symptom Manage 2011; 42:672–675. 51. Nelson JE, Curtis JR, Mulkerin C, et al. Choosing and using screening criteria for palliative care consultation in the ICU: a report from the Improving Palliative Care in the ICU (IPAL-ICU) Advisory Board. Crit Care Med 2013; 41:2318– 2327. 52. Scheunemann LP, McDevitt M, Carson SS, Hanson LC. Randomized, controlled trials of interventions to improve communication in intensive care: a systematic review. Chest 2011; 139:543–554. 53. Fawole OA, Dy SM, Wilson RF, et al. A systematic review of communication quality improvement interventions for patients with advanced and serious illness. J Gen Intern Med 2013; 28:570–577. 54. Gabler NB, Ratcliffe SJ, Wagner J, et al. Mortality among patients admitted to strained intensive care units. Am J Respir Crit Care Med 2013; 188:800–806. 55. Lynch T, Connor S, Clark D. Mapping levels of palliative care development: a global update. J Pain Symptom Manage 2013; 45:1094–1106. 56. Pivodic L, Pardon K, Van den Block L, et al. Palliative care service use in four European countries: a cross-national retrospective study via representative networks of general practitioners. PLoS One 2013; 8:e84440. 57. Yamaguchi T, Kuriya M, Morita T, et al. Palliative care development in the AsiaPacific region: an international survey from the Asia Pacific Hospice Palliative Care Network (APHN). BMJ Support Palliat Care 2014. [Epub ahead of print] 58. Clark D, Wright M, Hunt J, Lynch T. Hospice and palliative care development in Africa: a multimethod review of services and experiences. J Pain Symptom Manage 2007; 33:698–710.
680
www.co-criticalcare.com
59. Koper I, van der Heide A, Janssens R, et al. Consultation with specialist palliative care services in palliative sedation: considerations of Dutch physicians. Support Care Cancer 2014; 22:225–231. 60. Rodriguez KL, Barnato AE, Arnold RM. Perceptions and utilization of palliative care services in acute care hospitals. J Palliat Med 2007; 10:99–110. 61. White DB, Cua SM, Walk R, et al. Nurse-led intervention to improve surrogate decision making for patients with advanced critical illness. Am J Crit Care 2012; 21:396–409. 62. Baldwin MR, Reid MC, Westlake AA, et al. The feasibility of measuring frailty to predict disability and mortality in older medical intensive care unit survivors. J Crit Care 2014; 29:401–408. 63. Azevedo LC, Caruso P, Silva UV, et al. Outcomes for patients with cancer admitted to the ICU requiring ventilatory support: results from a prospective multicenter study. Chest 2014; 146:257–266. 64. Bagshaw SM, Stelfox HT, McDermid RC, et al. Association between frailty & and short- and long-term outcomes among critically ill patients: a multicentre prospective cohort study. CMAJ 2014; 186:E95–102. This study determined that frailty in ICU patients is common, and frail patients were at increased risk of adverse events and mortality, suggesting that frailty may be an important additional prognostic factor to consider. 65. Watanabe SM, Fairchild A, Pituskin E, et al. Improving access to specialist multidisciplinary palliative care consultation for rural cancer patients by videoconferencing: report of a pilot project. Support Care Cancer 2013; 21:1201–1207. 66. Menon PR, Stapleton RD, McVeigh U, Rabinowitz T. Telemedicine as a tool to provide family conferences and palliative care consultations in critically III patients at rural healthcare institutions: a pilot study. Am J Hosp Palliat Care 2014. [Epub ahead of print] 67. Duursma F, Schers HJ, Vissers KC, Hasselaar J. Study protocol: optimization of complex palliative care at home via telemedicine. A cluster randomized controlled trial. BMC Palliat Care 2011; 10:13. 68. Aslakson RA, Bridges JF. Assessing the impact of palliative care in the intensive care unit through the lens of patient-centered outcomes research. Curr Opin Crit Care 2013; 19:504–510.
Volume 20 Number 6 December 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
