The Challenges of Caring for People Dying From COVID-19: A Multinational, Observational Study (CovPall)

Context Systematic data on the care of people dying with COVID-19 are scarce. Objectives To understand the response of and challenges faced by palliative care services during the COVID-19 pandemic, and identify associated factors. Methods We surveyed palliative care and hospice services, contacted via relevant organizations. Multivariable logistic regression identified associations with challenges. Content analysis explored free text responses. Results A total of 458 services responded; 277 UK, 85 rest of Europe, 95 rest of the world; 81% cared for patients with suspected or confirmed COVID-19, 77% had staff with suspected or confirmed COVID-19; 48% reported shortages of Personal Protective Equipment (PPE), 40% staff shortages, 24% medicines shortages, 14% shortages of other equipment. Services provided direct care and education in symptom management and communication; 91% changed how they worked. Care often shifted to increased community and hospital care, with fewer admissions to inpatient palliative care units. Factors associated with increased odds of PPE shortages were: charity rather than public management (OR 3.07, 95% CI 1.81–5.20), inpatient palliative care unit rather than other settings (OR 2.34, 95% CI 1.46–3.75). Being outside the UK was associated with lower odds of staff shortages (OR 0.44, 95% CI 0.26–0.76). Staff described increased workload, concerns for their colleagues who were ill, whilst expending time struggling to get essential equipment and medicines, perceiving they were not a front-line service. Conclusion Palliative care services were often overwhelmed, yet felt ignored in the COVID-19 response. Palliative care needs better integration with health care systems when planning and responding to future epidemics/pandemics.


Introduction
COVID-19 evolved from a mystery illness to a pandemic in 93 days, overwhelming services in many countries (1). The World Health Organisation rapidly issued guidance on maintaining essential health services during the pandemic, highlighting prevention, maternity, emergency care and chronic diseases, without mention of palliative care (2).
Palliative care is multidisciplinary, holistic and person-centred treatment, care and support for people with life-limiting illness, and those important to them, such as family and friends. It is recommended in respiratory (5,6) and infectious diseases (7), and in recent guidance from the European Respiratory Society in COVID-19 (8,9). In the COVID-19 pandemic, palliative care has an important role in ensuring symptom control, training of non-specialists in symptom management and care of dying patients, compassionate communication, psychosocial support for patients, carers and health care professionals, advanced care planning and bereavement support (8,10), supporting patients wherever they want to be cared for (11) (see box 1).
The only review published on the role and response of palliative care and hospice services during pandemics included 10 observational studies (12) from single units or countries: West Africa, Taiwan, Hong Kong, Singapore, the U.S. (a simulation), and Italy (the only one considering . The review concluded hospice and palliative care services are essential in the response to COVID-19 but systematic data are urgently needed to inform how to improve care for those who are likely to die, and/or have severe symptoms.
Palliative care services are often managed separately from other medical services and may be exceptionally vulnerable to disruption in pandemics as they often rely on charity funding.
During the COVID-19 pandemic there were media reports of acute shortages of Personal Protective Equipment (PPE) and medicines that limited care (13). There is little systematic data about these situations (12,14). This study aimed to understand the response of and challenges faced by palliative care services during the COVID-19 pandemic, and to identify factors associated with challenges experienced, in particular shortages of equipment, medicines and staff. We tested two a priori null hypotheses: there are no differences in shortages between services with different management types (e.g. charity and public) -there are no differences in shortages between settings; e.g. between hospital based and non-hospital based; or community and non-community settings.

Study design and participants
CovPall is a multicentre multinational observational study of palliative care during the Free text comments were explored in Excel using content analysis to understand the impact of COVID-19 and the strategies, enablers and actions deployed by services.

Results
In total, 489 questionnaires were commenced, 477 completed (completion rate 97.5%); of these 15 were duplicates and 2 triplicates of entries with the same name/email; 2 were invalid being from one researcher without a palliative care service, leaving 458 valid responses: 277 UK, 85 rest of Europe, 95 rest of the world, 1 missing country (Table 1; supplementary  Table   S2).

Overall impact of COVID-19 on palliative and hospice services
Of all responding services, 91% changed how they worked as a result of COVID-19; 77% had staff who had suspected or confirmed cases of COVID-19. 81% of services had cared for patients with suspected or confirmed COVID-19, or both; of these, three main groups were cared for: patients with pre-existing illness or morbidities who were severely ill or dying from COVID-19 not previously known to palliative care (70% of services); patients dying from COVID-19 already known to palliative care services (47%); and patients severely ill or dying from COVID-19 but without pre-existing illness or morbidities (37%) ( Table 1, supplementary   Table S1).

Activities and changes in services
Free text responses revealed that inpatient palliative care units reported reduced activity; patients who did not have COVID-19 did not want to be admitted for fear of contracting the infection. There was increased home and hospital palliative care team activity. Assistance from volunteers plummeted; of responding services who used volunteers, 79% used them much less. Many volunteers were from older age groups and therefore high risk. Other activities and changes highlighted in free text comments included (supplementary tables S1,

S3):
 a surge in the number of patients cared for;  developing guidelines and education materials as none existed nationally;  training and supporting other health professionals;  increasing virtual and telephone monitoring (84% of services increased this type of support for patients, and 95% of services in supporting other professionals);  directly supporting continuous positive airway pressure or other ventilatory withdrawal;  delivering or supporting community or district nursing services;  switching from pro-active to reactive care because of the demand on services.
Free text comments described how staff were stressed by concerns for the patient's health and their own, being unable to visit patients and adapting to new practices. Services were frustrated by how their time and energy were consumed trying to source equipment, including PPE; without which staff got ill or could not deliver care ( Figure 1). The lack of timely PPE and the ethical challenges this presented, in terms of whom they could visit, made them fearful and anxious. There were financial considerations, with some staff especially from charities, concerned for the viability of services (Figure 1; supplementary   table S3).

Shortages and associated factors
Of responding services, overall 48% reported shortages of PPE, 40% shortages of staff, 24% shortages of medicines, and 14% shortages of other equipment, commonly battery operated syringe drivers (  Figure 2). In free text fields, shortages were reported most commonly for masks (filtering facepiece, FFP2, FFP3), FIT testing kits for FFP3 masks, hospital scrubs, aprons, gloves, face shields, long sleeve gowns, hand gels, goggles and eye protection.
Insert Table 2  Other factors were not significantly associated with staff shortages in regression analysis.
Free text comments described shortages in specialist palliative care teams, of doctors (consultants, specialty doctors, middle grade and junior doctors), nurses (advanced practitioners, clinical nurse specialists, community nurses, community palliative care nurses, registered general nurses, ward managers), allied health professionals (healthcare assistants, occupational therapists, pharmacists, pharmacy assistants, physiotherapists, social workers), administrative and housekeeping staff.

Medicines shortages
The top three medicine shortages reported in free text comments were: levomepromazine, midazolam (used for symptoms of agitation and delirium) and alfentanil (used for pain and breathlessness, commonly used in the UK in severe renal impairment, when morphine is contra-indicated). Shortages of medicines affected 20-27% of settings ( Figure 2). Only one variable (inpatient palliative care unit) met our criteria for inclusion from the univariable analysis (at P=0.07), so multiple regression analysis was not attempted.
Other equipment shortages

Response to shortages
Free text comments revealed that services expended huge efforts to procure PPE, some deployed staff to find PPE as their main role. Services contacted local vets, schools, dentists, universities, hospitals, businesses, health services, national supply lines, the government, professional organisations and the wider public. Some made their own supplies, crowd sourced and ran social media campaigns ( Figure 3). In response to medicine shortages, services contacted local services and pharmacists ( Figure 3). Some used alternative medicines even as first line, alternative strengths (lower or higher concentrations), or reduced the numbers of vials when prescribing home medications. In response to shortages of other equipment, services tried to get loans from other teams and settings ( Figure 3). The teams explored alternative ways to manage symptoms and administer medication to require less use of limited equipment. For example, faced with a shortage of syringe drivers (small, portable, battery powered infusion pumps suitable to give medicines for breathlessness, pain and agitation), services carried out risk assessments, programmed alternative pumps, such as 50 ml infusion devices, gave four hourly subcutaneous injections, or considered using transdermal patches rather than subcutaneous infusions.

Discussion
We report the first multinational survey on the response of and challenges to palliative care  (8,9).
Palliative care clinicians adapted and innovated quickly (19), possibly helped by prior experience with patients with different diseases and with multimorbidity. Palliative care puts the person before their disease wherever they are cared for: it is neither disease nor setting specific. The symptoms and problems of severe COVID-19 are commonly breathlessness and agitation (20,21), both familiar to palliative care clinicians. Current case reports suggest that these symptoms in end stage COVID-19 can be alleviated with low doses of opioids and benzodiazepines, delivered subcutaneously with a battery operated syringe driver (8,9,20,21). Palliative care has expertise in holistic end of life care, care for older people and those with multimorbidity (22). This flexibility, expertise and learning will be crucial to the international response to COVID-19, especially as cases of COVID-19 continue to rise across the globe.
Our study identified three different groups of patients, and these may require different approaches. A parallel planning approach may be needed for patients with uncertain trajectories, as is often used among patients with other uncertain prognosis in serious illness (23,24). Parallel planning provides for two sets of plans, run side by side. Both plans aim to ensure symptom management and the best in care: one plan is towards improvement or recovery, the second plan is in case the patient deteriorates or begins to die (24  In all publications, presentations and when the name of the survey is used, relevant CovPall papers should be references, and permission for use of the survey should be acknowledged.

Data sharing
Applications for use of the survey data can be made for up to 10 years, and will be considered on a case by case basis on receipt of a methodological sound proposal to achieve aims in line with the original protocol. The study protocol is available on request. All requests for data access should be addressed to the Chief Investigator via the details on the CovPall website (https://www.kcl.ac.uk/cicelysaunders/research/evaluating/covpall-study, and palliativecare@kcl.ac.uk) and will be reviewed by the Study Steering Group. 3. Home palliative care teamprovides specialist palliative care to patients who need it at home, or in care homes or residential homes, and support their families and carers. They also provide specialist advice to general practitioners, family doctors and nurses caring for the patients.

Figure captions
4. Home nursingprovides intensive home nursing care for the patient at home, sometimes referred to as hospice or hospital at home, often supporting patients whose care needs are such that without this they would be admitted to an inpatient palliative care unit or hospital. Includes data from the one missing country c Response for "yes" and "sometimes" both coded as "yes" d Not applicable includes those services who did not have shortages