Hospital-Based Palliative and End-of-Life Care in the COVID-19 Pandemic: A Scoping Review

Aim: To identify the nature of the evidence reporting hospital-based palliative and end-of-life care during the COVID-19 pandemic. Background: The COVID-19 pandemic has seen an increase in the numbers of seriously ill people being cared for across all health services worldwide. Due to the rapid progression of severe symptoms, the majority of staff working in hospitals and other healthcare centres were providing end-of-life care. Little is known about the level of hospital-based palliative care service provided during the COVID-19 pandemic, particularly during surges in admission rates with an increased number of deaths accruing. Methods: A scoping review was conducted to search and select potential studies. The scoping review was guided by the framework of Arskey and O’Malley and advanced by the use of the methodology of the Joanna Briggs Institute. Results: Eighteen studies published between March 2020 and July 2021 were identified. Three broad categories included overall management strategy and logistics, symptom prevalence and management of patients with COVID-19 and end-of-life care needs within the current pandemic. Conclusions: This review highlights increased awareness and knowledge of palliative and end-of-life care provided in hospitals. The review also highlights the response of hospital-based palliative care teams to an evolving crisis, within the context of developed health systems under sustained and overwhelming pressure. Implications: Newly established clinical links and referral pathways developed during the initial COVID-19 surge between hospital-based palliative care and other healthcare teams, be continued and further enhanced. Understanding of the role of specialist palliative care providers in supporting palliative and end-of-life care within the hospital setting needs further investigation.


Introduction
The COVID-19 pandemic has seen a significant increase in the numbers of seriously ill people being cared for across all health services worldwide. Given the rapid progression of severe symptoms associated with a diagnosis of COVID-19, end-of-life care became the everyday work of the majority of staff working in hospitals and other health care centres during this time.
Palliative care is provided across a range of settings including hospital, community and in designated palliative care units or hospices. To date, hospital-based palliative care services provide a consultation service to assist in the management of complex symptoms and provide end-of-life care, and in some countries provide a link between hospital and the community. Little is known about the level of hospitalbased palliative care service provision in the context of the COVID-19 pandemic, particularly when surges in admissions and deaths occurred. While it is reasonable to assume that palliative care services would be called upon to assist with complex symptom management and end-of-life care for those suffering with COVID-19, the benefit of specialised palliative care has not been visible within such an extreme environment to date or reported on.

Aim of the Review
The aim of this scoping review was to evaluate the evidence about the use of palliative and end-of-life care during the COVID-19 pandemic in order to consider the gaps in knowledge and issues that require further investigation.

Methods
A scoping review was conducted to identify and map the available evidence as well as to consider what future research may be needed. 1,2 While this scoping study was conducted iteratively, Arksey and O'Malley 3 methodological framework enhanced by Levac et al 4 and formally adopted and developed further by the Joanna Briggs Institute 5 was applied and Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)-ScR standards were used. 6

Stage 1-Identifying the Research Question
The research question was to scope the nature of the evidence concerning hospital-based palliative and end-of-life care in the COVID-19 pandemic. Key stakeholders from general hospital/tertiary care services helped to inform the research question and search strategy.

Stage 2-Identifying the Relevant Studies
In collaboration with our specialist librarian and key stakeholders, a comprehensive search strategy was developed. Given the novel emergence of the COVID-19 pandemic, the focus of the literature search was restricted from March 2020 to July 2021.
The inclusion and exclusion criteria were refined iteratively among the team and after performing the search. The recommended Population, Concept and Context pneumonic for scoping reviews was used to structure the eligibility criteria 5,7 (Table 1). The focus was on hospital-based palliative care during the COVID-19 pandemic. There were no restrictions to design or control. However, the search was limited to articles published in English. The inclusion criteria were further amended to specifically include the term hospital-based palliative care. Exclusion criteria included all papers that addressed non-hospitalbased palliative care in a non-hospital setting during the COVID-19 pandemic and any papers that discussed related sub elements of palliative care with no reference to the COVID-19 pandemic.
Database searches were undertaken in PUBMED, Psy-chINFO via ProQuest and CINAHL Complete. The search terms were related to hospital-based palliative care and COVID-19 and were searched as keywords as well as subject headings. For example, for hospital based, search terms used included acute setting, acute ward, inpatient, ward setting, acute care and ward. While the purpose of the searches was to identify the breadth of literature, 8 as a consequence of limited researcher resource and time restrictions, other research techniques such as exploring the grey literature or reference checking of identified articles was not conducted.
The specialist librarian in the team stored the retrieved records on EndNote X9. Subsequently, Covidence, a webbased literature review software platform, was used to assist the screening and selection of records.

Stage 3-Study Selection
MC and MB screened all the titles and abstracts and undertook full-text review of the potentially relevant studies against the inclusion criteria. Any disagreements were discussed and resolved by consensus. The results are reported in the PRISMA flowchart 9 (Figure 1).

Stage 4-Charting the Data
MB undertook data extraction and initially drafted a charting table to reflect the relevant characteristics of the data. Charting the data became an iterative process, given the ongoing review and discussion with MC. It was further refined, reviewed and synthesised in accordance with Joanna Briggs Institute guidelines. 5 Finally, the following agreed characteristics of the data were charted including author, year, country, journal, aim, population, methodology and key findings ( Table 2).

Stage 5-Collating, Summarising and Reporting the Results
The analysis of the extracted data incorporated 2 steps: the first being a descriptive numerical summary of the relevant

Selection of Studies
The search initially yielded 145 articles ( Figure 1). With 27 duplicates removed and when title and abstracts were reviewed another 87 were excluded as they did not meet the inclusion criteria. The remaining 31 studies were assessed for full-text eligibility resulting in a further 13 being excluded as these were not specific to hospital-based palliative care. The remaining 18 underwent full-text review and were included in the study.

Description of Studies
Overall, this review process gleaned a broad variety of articles that focussed on different aspects of data capturing palliative   28 The predominant methodological approach adopted was retrospective patient chart review or care plan analysis reported in 9 articles. 10,13,[19][20][21][22][23]25,26 Of 6 discussion articles identified, 2 examined bereavement risk 17,24 1 presented the challenges experienced in delivering palliative services during a pandemic 12 and 3 discussed the implementation of a strategy or plan that was developed in their hospital to address the impact of the surge in palliative care patients. 15,18,27 One article presented a patient case study of the challenges and difficulties that were identified in a non-ICU setting. 11 Fiorentino et al. (2020) 16 conducted a retrospective observational study using the Palliative Performance Scale (PPS) to predict mortality in 334 hospitalised patients with COVID-19. Cook et al. (2021) 14 used mixed methodology to investigate clinicians' perspectives on the adaptation to end-of-life care for dying patients and their families during the pandemic.
The sample sizes used in the 9 chart reviews ranged from 36 26 to 1071 patients. 22 Two of these studies compared palliative care services needs of 2 groups of patients. Chidiac et al. (2020) 13 compared 60patients with COVID-19 and another 61 without, to evaluate the impact of COVID-19 on symptoms, clinical characteristics and outcomes for patients in a hospitalbased palliative care service. Moriyama et al. (2021) 22 compared 678 patients, the pre-COVID group, to 1071, the COVID-19 group regarding their demographics, comorbidities and rates of mortality.
Following an analysis of the extracted data, 3 broad categories were identified reflecting the predominant perspectives of addressing palliative and end-of-life care needs during a pandemic within hospital settings. These included overall management strategy and logistics, symptom prevalence and management of patients with COVID-19 and end-of-life care needs/consultation demands within the current pandemic.

Overall Management Strategy and Logistics
The overall strategies and logistics adopted to address the surge in demand for palliative care was reported by 3 articles from the USA and 1 from Canada. 12,15,18,27 Each outlined a strategic plan that was adopted and focussed primarily on how to increase the numbers of palliative care staff as well as optimising the use of existing palliative care specialists. Some novel ways of addressing this problem were reported. For example, Xu et al. (2021) 27 described how 12 volunteer clinicians (11 physicians and 1 nurse practitioner) each shadowed a palliative care team member for 1 day, given a manual with communication guidance, received targeted training on advanced care planning and was then embedded within a team led by a palliative care provider. Consequently, it emerged that 6 of these physicians were psychiatrists and could quickly use their own communication skills to support family and staff. What was also apparent from these papers was the necessity for very quick training of staff not specialised in palliative care that worked in key areas such as ED or ICU to enhance their frontline skills via new tailored communication trainings. 18 Fausto et al. (2020) 15 reported that all teams in ED, ICU and acute care services were provided with clinician discussion tools and access to consultation with the specialist palliative care team for assistance with complex communication. These frontline staff were provided with resources that included an informed assent strategy for discussing do-not-resuscitate orders as well as resources for COVID-19 ready communication skills. Arya et al. (2020) 12 presented 2 short scripts capturing the suggested language that clinicians should use when providing support to a patient or family member who was denied access to intensive care due to resource scarcity and when discussing treatment when a patient is unlikely to survive a critical illness but could include life-sustaining therapies if needed.
Besides redeployment of non-specialist staff into the palliative care team, cognisance of the most efficient and effective use of specialist palliative care clinicians were also evident. A triage tool for referral to specialist palliative care was adopted as part of the mass casualty critical care framework by Arya et al. (2020), 12 while Fausto et al. (2020) 15 described how routine palliative care consultations were triaged and postponed when possible. A palliative care specialist was also embedded in the ED and ICU to address and screen high volumes of patients, to coach staff and to assist with goals of care. 15 Xu et al. (2021) 27 reported how specialist palliative care teams expanded their role and saw every patient with multi-organ failure in ICU and took over the communication with families. They also acknowledged that due to the urgency of the situation and the swift nature of the implementation of their interventions to address the COVID-19, outcomes could not be effectively measured at that time. 27 New services were also developed to address the many challenges that arose due to surges in COVID-19 admission. A 24-hour/afterhours telephone service was established to provide additional palliative care capacity to primary care teams in relation to symptom guidance and coaching 15 and to patient's families. 18 Specific end-of-life care units for patients dying with COVID-19 staffed by palliative care clinicians and advanced practice specialists were created 15 or modified 18 to maximise patient comfort and staff safety.

Symptom Prevalence and Management of Patients With COVID-19
Five articles reported on symptom prevalence and descriptive statistics of patients admitted to hospital during with COVID-19. 13,16,19,21,23 Dyspnoea and agitation were the 2 most prevalent symptom reported by 3 studies. 13,19,21 By contrast, an Italian study reported that 41% of patients' predominant symptom was restlessness/agitation, 26% was emotional issues but only 20% presented with dyspnoea as the most prevalent symptom. 23 Comparisons were made between referral patterns for those admitted with COVID-19 and those referred to specialist palliative eservices pre-COVID-19. There were some notable observations. The time from referral to palliative care to death was shorter 13,19,21,23 ; specifically, 2 days for patients with COVID vs 5 days for those without. Fiorentino et al. (2020) 16 used the PPS and found that frailty was an independent predictor of mortality. In addition, patients with COVID-19 had a lower PPS found in older patients and predominantly black patients with comorbidities. The most common comorbidities for patients with COVID-19 were hypertension, diabetes mellitus and COPD. 19 However, age and the Charlson Comorbidity Index did not predict mortality in the Fiorentino et al.'s (2020) 16 25 examined the utilisation rates and characteristics of consultations to palliative care during the initial wave of the pandemic. Not surprisingly, new consults increased significantly. Three quarters (75%) of referrals to palliative care were for goals of care and advanced care planning while less than 10% were for symptom management. 20 Both of these studies showed that less than ten percent had documented Advance Care Directives despite the sample population age being older. It is noteworthy that Chidiac et al. (2020) 13 reported that 40% (n = 24) of patients who were referred to palliative care for symptom control were evidently in the dying phase of COVID-19 illness. In addition, Sheehan et al. 25 study focussed on patients in the ICU setting and found that there was an underutilisation of palliative care services.
PC consultations varied in how they were managed. Sheehan et al. (2020) 25 indicated that 39% (n = 59) received inpatient PC consultation, 16 received a one-time telemedicine consultation, 39 received continued telemedicine and follow-up and MDT involvement and 4 patients initially received one-time telemedicine followed by continued telemedicine.
It is worth noting that 1 study found that patients dying from COVID-19 experience similar end-of-life care needs and problems to other groups of patients as well as responding to standard interventions for those end-of-life problems. 10

Identified Impact
It is clear that the infection, prevention and control restrictions during the COVID-19 pandemic led to a number of adverse impacts to patients and staff in a number of articles. A German case study reported how 1 patient expressed distress at having no visitors and was profoundly lonely. 11 In order to respond to the impact of visiting restrictions, clinicians in a Canadian study took on advocacy roles for patients. 14 For example, these clinicians ascertained the final wishes of patients and their families and implemented them, setup new ways of connecting patients with their relatives and actively tried to ensure that no patient death was unmarked. Social workers in Australia assisted the bereavement process for families by changing their practice using memory making as a tool to support families through letters, photos and hand-drawn pictures and music. 17 Cook et al. (2021) 14 also reported how the burden on clinicians associated with visitor restrictions led to clinicians reporting moral distress. Indeed, Selman et al. (2020) 24 identified several risk factors for poor bereavement outcomes for relatives including dying in the ICU, severe breathlessness, patient isolation and significant patient and family emotional distress. The impact of these deaths on staff led to self-reported moral distress/injury, depression, anxiety and post-traumatic distress.
Uniquely, Turner et al. (2020) 26 from a chart review observed that there were 3 different ways of dying from COVID-19 labelled as fulminant COVID-19, longer illness and slower death or long illness, stability and rapid death. However, many of these studies reported a shorter average dying phase for those with COVID-19 of about 38.25 hours compared to 74 hours with no COVID-19.

Discussion
Eighteen studies were identified for inclusion which used a variety of methods to detail varying different experiences of hospital-based palliative teams' response to COVID-19.
The studies articulated a comprehensive response to COVID-19 provided by hospital-based palliative care teams, including interventions to manage symptoms, providing supportive care to patients, families and staff and a novel solution to providing palliative and end-of-life care by appropriately triaging those with worsening COVID-19 symptoms. This process of triage saw palliative and end-of-life care being centrally located in the planning and provision of care to patients with COVID-19.
While palliative and end-of-life care have received attention in the past, this review clearly articulates the immediate and ongoing response of hospital-based palliative care to a continually emerging health care emergency which resulted in a significant increase of patients needing specialist palliative and end-of-life care. It also highlights the role that hospital-based palliative care played in supporting staff caring for the dying, including staff who have not experienced this type of care provision before, while also recognising the large numbers of dying patients being cared for. It is evident from this review that palliative care became more visible during surges in admissions due to COVID-19.
This review highlights the response of hospital-based palliative care in the context of a pandemic. It demonstrates the myriad ways in which hospital-based palliative care responded to the pandemic, for example, symptom management advice, communication with patients and families about change in focus of care and end-of-life care planning. This review adhered to the relevant reporting framework and was rigorous in its methodology.
The majority of studies included were small single centred with small population samples. Only 6 of the studies had a sample population greater than 100. While a comprehensive research strategy was conducted, the studies included are all English language, so the experience of hospital-based palliative care not reported in English could not have been included.

Conclusion
This review has highlighted the increased awareness and knowledge of palliative and end-of-life care provided in hospitals. The COVID-19 pandemic and subsequent increased admission to hospitals has led to increased referral rates to these services, which in turn has the potential to improve patients and family care and assist with greater interaction and consultation with specialist palliative care in the future. The review has also highlighted the rapid response of hospitalbased palliative care teams to an evolving crisis, within the context of developed health systems under sustained and overwhelming pressure.

Implications for Practice
It is imperative that newly established clinical links and referral pathways developed during the initial COVID-19 surge between hospital-based palliative care and other health care teams be continued and further enhanced to ensure that patients' palliative and end of life remains a focus for those with life-limiting illnesses and be included as part of their planned care.
Understanding of the role of specialist palliative care providers in supporting palliative and end-of-life care within the hospital setting needs investigation.

Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.