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Table 2 Overview of the Studies included in the Systematic Review

From: How views of oncologists and haematologists impacts palliative care referral: a systematic review

Author (Year) Country Research question Participants/Setting Method Key findings Hawker Score
Horlait et al. (2016) [36]
What are the barriers to introduce palliative care into discussion with patients with advanced cancer? 15 medical oncologists from academic and non-academic hospitals Grounded theory Following were the barriers identified by the oncologists. Physician related barriers were emotional bonding with the patients, feeling of professional failure, discomfort with death and dying and lack of experience and training in managing patients with advanced illness. Patient related barriers were language and culture, denial, and unrealistic expectations. Family related barriers were protection of patients, and family disputes. Disease related barriers were lack of clear guidelines for palliative care referral, unpredictable trajectory of illness and unexpected progression. Organisation related barriers were lack of availability of palliative care services, excessive focus on cure, lack of space and time to discuss palliative care, and excessive workload. The societal barrier was the stigma associated with palliative care and palliative care referral. 34
Charalambous et al. (2014) [37]
What are the attitudes and referral patterns of lung cancer specialists to palliative care? 50 cancer specialists from the EORTC Lung Cancer Group representing 14 countries. Survey Oncologists like to refer to palliative care when they have difficult to control symptoms or when no treatment is available. Some refer during the diagnosis of metastatic disease or during cancer treatment. Non-availability of palliative care physicians is a major barrier. Oncologists feel that patients do not like to be referred to palliative care and referral means abandoning their patients. Moreover, oncologists have concerns about expertise of palliative care physicians and feel that they may discourage or interfere with oncological treatment. 29
Cherny et al. (2003) [38]
What is the practice and attitudes of ESMO oncologists in relation to the supportive and palliative management of patients with advanced and incurable cancer and what are the oncologist-related barriers to the provision of optimal supportive and palliative care? 895 ESMO member oncologists representing 64 countries. Survey All advanced cancer patients should receive concurrent palliative care. Oncologists should coordinate the care at all stages of disease including end of life care. Prefer to manage advanced cancer and dying patients themselves. They felt they have acquired some knowledge of palliative care during their training and feel confident about managing symptoms. Palliative care physicians do not have enough understanding of oncology to counsel patients with advanced cancer regarding treatment options. 33
Morikawa et al. (2016) [39]
What are the barriers to collaboration between haematologists and palliative care teams in relapse or refractory leukaemia and malignant lymphoma patients’ care? 11 Haematologists from
University Hospital
Content Analysis Barriers for referral were a. treatment provided by palliative care providers were not as preferred by the haematologists b. treatment of primary disease given priority over palliative care c. Lack of aggressive approach by the palliative care team d. negative image of palliative care, palliative care is equated by the patients to imminent death e. palliative care team may not be able to support the haematology patients and they have a different perspective on assessment f. lack of interdisciplinary communication and g. lack of palliative care human resources. 25
Johnson et al. (2008) [40]
What are the triggers that initiate referral to palliative care and what are the reasons for non-referral? 699 cancer specialists practicing at various hospitals in Australia Survey Patients with advanced cancer should be referred early. Early referral is beneficial, and patients will benefit from palliative care while receiving anti-cancer treatment. Patients are often referred when they have a terminal illness, uncontrolled physical symptoms, complex patient needs and when they are not coping with the physical care. They prefer integrated care and would like to be involved in the care even after palliative care referral. They are confident about managing symptoms and unlikely to refer if patient’s symptoms are well controlled and prognosis is good. 34
Ward et al. (2009) [41]
What are the attitudes of Australian medical oncologists towards palliative care and collaboration with palliative care services? 115 Medical Oncologists who are members of Medical Oncology Group of Australia. Mixed Method
(Survey and thematic analysis)
Provision of palliative care is central, rewarding and adds value. Have adequate palliative care training and confident in managing symptoms and communication. Palliative care rotation should be part of medical oncology and vice-versa. Major reason for referral is symptom management, community support, hospice and terminal care. Prefer concurrent model over sequential model. Barriers to referral are, a. inadequate palliative care resources b. refusal by palliative care to take patients receiving anti-cancer therapy c. lack of clear guidelines regarding timing of referral 33
Hay et al. (2017) [42]
What are the Gynaec-oncologist’s views that influences the utilisation of outpatient specialist palliative care? 34 Gynaec-oncologists working at NCI designated cancer centres Grounded theory Long term relationship with the patients helps in convincing the patients to access palliative care. They value the communication skills of the palliative care provider, emotional support, help in navigating difficult circumstances, goals of care discussion and prognostic awareness. Prefer embedded clinics and better inter-disciplinary communication. Have concerns about losing control and awareness of patients receiving palliative care. 27
Wright et al. (2017) [43]
What are the views and perceptions of haematologists towards palliative care and the factors that helped or hindered referral to palliative care? 8 Haematologists working in a
tertiary referral cancer centre
Grounded theory Equated palliative care with worsening prognosis, death and dying. Hospice has a negative connotation, and hospice referral requires sensitive and proactive explanation. Symptom control was the most common reason to refer. Barriers for referral were a. inadequate number of palliative care beds b. palliative care lack resources to provide blood products c. inflexible referral criteria d. prejudice by the palliative care providers against haematology patients d. difficult timing and transition due to complex and unpredictable nature of illness e. uncomfortable to refer curative patients f. mixed messages g. loss of control g. sense of professional failure h. feelings of abandoning patients. Prefer joint care approach. 32
Smith et al. (2012) [44]
What influences lung cancer physician’s decision to refer their patients to experts in palliative care? 155 Lung Cancer Physicians practising at various teaching hospitals in USA Survey Patients and families would be alarmed by mention of palliative care. Patients prefer to focus on curative therapies than palliative care. Patients do not want to discuss prognosis. Palliative care providers are good in discussing complex issues and goals of care. They help in reducing symptoms, provide spiritual support and decrease the length of stay. 32
Rhondali et al. (2013) [45]
What are medical oncologists’ perceptions of the supportive care service and whether changing the name “palliative care” to “supportive care” influenced communication with patients and their families about palliative care and the referral? 17 medical oncologists working in a
tertiary referral cancer centre
Grounded Theory Symptom control is the primary function of palliative care. Palliative care communication helps in transitioning patients to end of life care. Psychological support provided by palliative care decreases caregiver anxiety and facilitates communication. Palliative care involvement has time saving benefit and helps patients to complete treatment due to better symptom control. Earlier referral is better as it will facilitate better therapeutic relationship. Triggers for referral are terminal nature of illness, metastatic disease and exhaustion of treatment. Barriers for referral are no clear-cut point to stop treatment, communication involved in referral is challenging, conflicts in goals of care and physician ownership. Prefer name to be changed as supportive care as patients perceive it better and will be more receptive for referral. 33
Schenker et al.
(2014) [46]
What are the oncologist factors that influence referral decisions? 74 Oncologists practising at various hospitals in USA Qualitative data analysis Palliative care is an alternative to chemotherapy and cannot have both. Palliative care referral decision based on disease stage and treatment option. Palliative care has a different philosophy of care not compatible with active disease modifying care. PC providers create conflict and provide dismal prognosis. Referral to palliative care means abandoning, giving up. They are territorial and would like to provide treatment till the end and do not like others interfering with the care. They have palliative care skills and refer patients for symptom control. Having more A positive referral experience may facilitate referral. 25
LeBlanc et al. (2015) [47]
What are the differences in referral practice and views of palliative care among haematologists and solid tumour oncologists? 23 Haematologists
43 Solid tumour oncologists practicing at academic cancer centres
Mixed Method Study
(Survey + Qualitative Data Analysis)
Haematologists view palliative care as end of life care and as antithetical to cancer care. Solid tumour oncologists feel palliative care expertise is useful and believe in co-management of patients. Haematologists expressed distrust, need to maintain control, avoiding involvement of other consultants, mixed messages, and prognostic uncertainty. Palliative care is inconsistent with treatment goals and a major barrier for referral. Solid tumour oncologists felt lack of palliative care resources, logistics of accessing, insurance as barriers for referral 28
Wentlandt et al.
(2012) [48]
What are the referral practices of Canadian oncologists to palliative care, particularly with respect to the timing of referral and to identify factors that were associated with timely versus late referral? 603 medical, radiation and surgical oncologists from the Canadian oncology societies Survey Diagnosis of an incurable cancer, uncontrolled physical symptoms and prognosis less than 1 year were the likely reason for referral. Referrals are also made for discharge planning and psychosocial support. The term palliative care has a negative perception and would refer if the name is changed to supportive care. They will refer the patients early if there are more palliative care services and palliative care providers accept patients receiving chemotherapy. 32
Wentlandt et al.
(2014) [49]
What are the attitudes and referral practices of paediatric oncologists to specialized palliative care services and to compare their practices and opinions with those of adult oncologists? 48 Paediatric Oncologists & 595 Adult Oncologists practising at various hospitals in Canada Survey Paediatric oncologists refer terminally ill patients, metastatic disease, prognosis of less than 6 months, and with uncontrolled symptoms to palliative care. Paediatric oncologists feel palliative care has a negative perception and prefer name change to supportive care. They are comfortable treating advanced patients at end of life. Adult oncologists refer earlier, when prognosis is < 1 year, for discharge planning, psychosocial and spiritual support. 30
Suwanabol et al. (2018) [50]
How surgeons who care for patients with colorectal cancers approach end-of-life care and engage palliative care specialists? 131 Cancer Surgeons belonging to the American Society of Colon & Rectal Surgeons Mixed Method Study
(Survey + Qualitative Data Analysis)
Oncologists have lack of knowledge, training and opportunities for delivery of palliative care. Barriers are inadequate communication between teams, unrealistic expectation in a poor prognosis situation and effectiveness of treatment, uncertainty in decision making, legal liability, opioid phobia, family conflict, lack of time, lack of palliative care services and culture of continuing life sustaining treatment in the hospital. 28
Gidwani et al. (2017) [51]
What are the oncologist’s views and attitudes towards palliative care referral? 31 Medical Oncologists practicing at academic cancer centres and Veteran Affairs hospitals in USA Thematic Analysis Palliative care is an important layer of support, should be provided early and unavailability of the palliative care provider is the barrier. Excessive focus on inpatient palliative care and absence of outpatient and community palliative care is the barrier. Palliative care provider is perceived as outsider, unable to understand oncology patients, oncology treatment and unable to recognise a recoverable sick oncology patient from a dying patient. Issues with care coordination and oncologists being left out of crucial discussions and lack of interdisciplinary communication is a barrier for referral. Palliative care has a narrow focus and palliative care providers excessively rely on sedation and analgesics. 25
Cripe et al. (2019)
USA [52]
What are the perceived
barriers to integrate specialty palliative care into gynaecologic cancer care?
174 Gynaec-oncologists who are members of the Society of Gynaecologic-
Oncology in USA
Survey Barriers to specialty palliative care in Gynaecologic Oncology practice were unrealistic expectations of families and patients, limited access to specialty palliative care, poor insurance reimbursement, time constraints, and concern of reducing hope or trust. 34
NyirÖ et al. (2018) [53]
What is the timing and circumstances of implementing paediatric palliative care in the Hungarian paediatric oncology practice? 22 physicians from the Hungarian Paediatric Oncology Group Survey Barriers for early palliative care implementation were increase in parental anxiety, detrimental effects on the doctor-family-patient relationship and equating palliation with end-of-life care. Oncologists preferred discussing with the parent’s first before referral, gradual information disclosure, and waiting till the end of child’s life for making referral. They preferred to have a psychologist in the earlier discussions. Avoided using the term palliative care and used euphemisms to communicate death/dying. 33
Ethier et al. (2018) [54]
What are the various perceived barriers for having goals of care (GOC) discussions and palliative care referral? 127 oncologists from 12 cancer centres in Ontario, Canada Survey Barriers were patients have difficulty in accepting prognosis, and desire for aggressive treatment due to inflated expectation of treatment benefit. Other barriers were lack of time to have conversations, prognostic uncertainty, desire to maintain hope, uncertainty of the benefits of further active cancer therapy, difficulty in recommending discontinuation of treatment in younger population and patient and family refusals 34
Feld et al. (2019) [55]
What are the practices and attitudes regarding the role of early palliative care referral among oncologists and patients with metastatic non-small cell lung cancer? 279 Oncologists from the International Association for the Study of Lung Cancer Survey Common factors influencing participants to refer patients to palliative care were inadequately managed pain, no further or dwindling treatment options, other cancer-related symptoms, depression/anxiety. The common reasons for not referring patients to palliative care include lack of time to address palliative care needs
lack of patient symptoms, belief that oncologists can manage palliative care needs independently, not wanting to burden patients with additional appointments, concern that referral may not be well-received by patients, and long wait times.
Prodhomme (2018) [56]
What are the perceptions of haematologists on end of life discussion in patients and families with relapsed haematological malignancies? 10 haematologists from haematology centres of northern France and Belgium Grounded Theory Reluctance to discuss death and dying. Talking about death and dying is stressful, difficult and a taboo. Primary role is to cure and save from death. Responsibility is to reassure, motivate and infuse confidence. End of life discussion is not compatible with the physician’s role. Treatment effectiveness is proof of physician’s performance and death is a professional failure. End of life discussion causes loss of physician credibility and jeopardises patient compliance. Will initiate discussion only when there is an explicit request and would like to protect patients from violent discussions on end of life. Initiating palliative care and end of life care is incompatible with hope. Palliative care can be initiated when all the treatment is discontinued. 32
(2019) [57]
What are the barriers for referring to specialist palliative care from the perspectives of the haematologists? 14 haematologists from two haematology centres at Lyon, France Grounded
Referral only when there are difficult to control symptoms like severe pain, complex situations and therapeutic decision making. Early referral beneficial in an asymptomatic patient for facilitating smooth transition. The term palliative care has a negative connotation and patients/families react negatively to palliative care. Preferred to use the term supportive care instead of palliative care. Short time frame from appearance of symptoms and end of life hinders referral 28
Sarradon-Eck (2019) [58]
What are the perceptions and attitudes of oncologists on early referral to palliative care and working with the palliative care services? 13 Oncologists working at 10 cancer treatment sites across France Grounded
The term palliative care has a negative connotation. The term is unsuitable, scares people, harms them. Term palliative care elicits feelings of abandonment, stopping treatment and euthanasia. Prefer to use euphemisms life supportive care, comfort care instead of palliative care. More likely to refer if it is called supportive care. Referral to palliative care causes loss of patient compliance, loss of hope, elicits distress and equivalent to announcing poor prognosis. Palliative care is a last recourse and restricted for patients with less than three months life expectancy. Palliative care assessment is vague, not evidence based, and oncologists are experienced in symptom management. 28