Palliative care utilization in oncology and hemato-oncology: a systematic review of cognitive barriers and facilitators from the perspective of healthcare professionals, adult patients, and their families

Background Despite the high potential to improve the quality of life of patients and families, palliative care services face significant obstacles to their use. In countries with high-resource health systems, the nonfinancial and nonstructural obstacles to palliative care services are particularly prominent. These are the cognitive barriers -knowledge and communication barriers- to the use of palliative care. To date no systematic review has given the deserved attention to the cognitive barriers and facilitators to palliative care services utilization. This study aims to synthesize knowledge on cognitive barriers and facilitators to palliative care use in oncology and hemato-oncology from the experiences of health professionals, patients, and their families. Methods A systematic review was conducted. PubMed, PsycINFO, International Association for Hospice and Palliative Care/Cumulative Index of Nursing and Allied Health Literature (IAHPC/CINAHL), and Communication & Mass Media Complete (CMMC) were systematically searched for the main core concepts: palliative care, barriers, facilitators, perspectives, points of view, and related terms and synonyms. After screening of titles, abstracts, and full-texts, 52 studies were included in the qualitative thematic analysis. Results Four themes were identified: awareness of palliative care, collaboration and communication in palliative care-related settings, attitudes and beliefs towards palliative care, and emotions involved in disease pathways. The results showed that cognitive barriers and facilitators are involved in the educational, social, emotional, and cultural dimensions of palliative care provision and utilization. In particular, these barriers and facilitators exist both at the healthcare professional level (e.g. a barrier is lack of understanding of palliative care applicability, and a facilitator is strategic visibility of the palliative care team in patient floors and hospital-wide events) and at the patient and families level (e.g. a barrier is having misconceptions about palliative care, and a facilitator is patients’ openness to their own needs). Conclusions To optimize palliative care services utilization, awareness of palliative care, and healthcare professionals’ communication and emotion management skills should be enhanced. Additionally, a cultural shift, concerning attitudes and beliefs towards palliative care, should be encouraged.


Background
The relevance of palliative care services and their integration into the traditional medical model is widely recognized. In 2014, the World Health Assembly urged countries to integrate palliative care into their health care systems [1]. This goal has not yet been achieved, as palliative care services are not available, due to several various reasons, to all those patients experiencing a serious chronic disease in most countries, even in high-resource systems [2,3].
According to the Health Care Access Barriers Model [4], barriers to health services use include Financial barriers, that is cost of care and health insurance status barrier, Structural barriers, namely institutional and organizational barriers, and Cognitive barriers, including knowledge and communication barriers. The three categories of barriers affect health care utilization individually and in concert, and are associated with late presentation to care, and lack of treatment, which translates in poor health outcomes [4].
Particularly in developed countries, where palliative care services are part of the healthcare system [3], the nonfinancial and nonstructural barriers and facilitators to palliative care use highly affect the utilization of palliative care for patients and their families. Additionally, even in developing countries, where resources are limited, cognitive barriers are prominent, as financial choices and organizational decisions are affected by cognitive aspects of the type of services in which to invest both at the system and the organizational levels [3]. Moreover, cognitive barriers are directly modifiable through targeted strategies.
In the specific case of palliative care services, referrer reluctance as well as patients and families reluctance are related to cognitive barriers, such as lack of understanding of the benefits of referral or avoidance of talking about end of life and death with the belief that this will allow avoidance of death itself [3].
Systematic literature reviews have synthesized research on barriers and facilitators to palliative care from a general perspective, without going into depth on cognitive barriers. Potential barriers include patients' and doctors' (e.g., general practitioners [GPs]') ambivalence about discussing 'bad news' of a diagnosis [5], which is relevant as it may affect the GP-patient relationship. Other barriers include lack of human resources, financial constraints, limited infrastructure for palliative care [6], and lack of standardized referral criteria for palliative care services [7]. Potential facilitators for palliative care use include the availability of relevant specialized secondary services in integrated palliative care, which were shown to be highly valuable both for the hospital (lower costs) and for the patient (better use to certain palliative care services including improving functional status) [8]. In addition, these studies found that stakeholder engagement, financial support, a supportive learning environment for HPs, and community networks might facilitate palliative care use [6], as well as appropriate communication styles, perceptions of patient readiness [9], knowledge of palliative care [7,9], and education on palliative care among HPs [7].
In particular, this review aims at identifying the cognitive barriers and facilitators to the use of palliative care, and at giving to these a deserved attention including a deeper exploration compared to previous broad systematic reviews. More specifically, we aim at analyzing perceived cognitive barriers and facilitators, to the utilization of palliative care, from the perspective of healthcare professionals, oncology patients and their families. The broad goal of this review is to identify targets to overcome the obstacles and encourage the enablers in order to reinforce health care systems towards an optimal utilization of palliative care.

Design
A systematic review was conducted following established guidelines to ensure rigour and transparency [10]. The Preferred Reporting Items for Systematic Reviews and Meta-Analysis: PRISMA statement [11] was followed to standardize the reporting. Qualitative, quantitative and mixed-method studies were included. A textual narrative synthesis [12] approach was adopted to present the results, more specifically, this review main goal was to explore diverse types of studies with no scope to explore relationships within and between studies. This approach included thematic analysis, used to extract the main themes [13], and tabulation in order to analyze the findings. Barriers and facilitators pertaining to areas other than personal and relational aspects, such as institutional and organizational barriers and facilitators, were not included in the analysis. Search terms covered the concepts of palliative care and barriers and facilitators to referral and use (Additional file 1). Terms to cover palliative care in the included 'palliative', 'supportive', 'end of life', 'terminal', and 'hospice', which were searched with 'care' or 'medicine' or 'treatment' or 'therapy', as these have been used with similar meanings internationally. For each study, we checked that the type of care described matched with the concept of palliative care adopted here [14] and was relevant to the research question. Other terms included were 'facilitator' and 'barrier' (and synonyms) and 'attitude', 'point of view', 'perspective', 'angle', 'position', 'thought', 'belief', and 'idea' (for details see Additional file 1). Keywords were generated by examining other review papers in the palliative care literature and using an English thesaurus. Keywords were combined with standard MeSH terms from PubMed and subject headings for the other databases. Moreover, the definitions of barriers and facilitators used were the following: barriers are actual or perceived factors such as a perception or belief that make it difficult or impossible for patients to access palliative care; facilitators are actual or perceived factors as a perception or belief that make it easier or more likely for patients to access palliative care.

Eligible studies
Papers focusing on palliative care and oncology or hemato-oncology were included. Inclusion criteria were the following: Study types: peer-reviewed studies presenting original qualitative, quantitative, and mixed-method studies with an exploratory descriptive approach. Systematic reviews, commentaries, editorials, newspaper articles, and other forms of popular media were excluded. Population or participants: papers from all over the world were examined. Studies including HPs, patients with cancer and families were eligible. Studies including patients with disease other than cancer were excluded. This review was limited to studies on adults, since perceived barriers and facilitators to use pediatric palliative care differ from those to use adult palliative care [15,16]. Setting: oncology, hemato-oncology, and general practice which includes oncology/hemato-oncology patients. Outcome measures: primary outcomes of interest were palliative care use, access, provision, implementation, and integration. Studies with diverse perspectives were included (e.g., hematooncologists' and GPs' perspectives). Studies that included palliative care as a range of services provided by a multidisciplinary team were examined; studies focusing on a single aspect of palliative care services (e.g., spiritual care only) were not considered. Language: studies in English only were included.
There is no consistency in defining palliative care in the literature [17,18]. We refer to the WHO definition: "Palliative care is an approach that improves the quality of life of patients and their families facing the problem associated with life-threatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial and spiritual" [14]. Studies were included if they explicitly specified that the patients or health professionals were receiving, providing, or referring to palliative care services. Some studies referring to hospice care (or other terms, see Identification of relevant literature) that also investigated palliative care provision were considered, but only those in which palliative care was specifically addressed were finally included in the review.

Data extraction and data synthesis
Included studies were heterogeneous, not allowing meta-analysis of quantitative studies or meta-synthesis of qualitative studies. A textual narrative synthesis, which aims to describe studies, by arranging these into homogeneous groups, through thematic analysis, and compares similarities and differences across studies [12] was conducted. The textual narrative synthesis of the results [12,19] was performed by extracting relevant characteristics from the selected studies, charting them in tables (Tables 2, and Additional file 2: Table 3), and producing a textual summary of the results. Each study was coded using an ad-hoc data extraction sheet according to the following characteristics: Author name, year of publication, aim, design, participants (number and type), country, data collection method and sample, barriers or facilitators to palliative care services use, strategies, and outcome(s). Extracted barriers and facilitators were tabulated and synthesized thematically through a thematic analysis. The thematic analysis was used to identify and develop themes across studies, by using line-by-line coding, developing descriptive themes, and generating analytical themes [12]. Emergent themes are included in Table 1, and Additional file 2, Table 3. The criteria for the inclusion of barriers and facilitators in the relevant themes are reported in the paragraph "Thematic Analysis" in the results section. Regular debriefings and discussion of the themes among the three reviewers (M.B., N.D. and S.R.) and discussions with the other co-authors (C.G., P.S., I.C., and G.S.) were used to validate the findings.

Identification and selection of the literature
The search and screening process are presented in a standard diagram flow (Fig. 1). After deduplication, 8259 studies were screened to retain only original research about barriers and facilitators to the use of palliative care. Following this process, 165 studies were identified as eligible for the next selection step. Many of these studies, rather than focusing on perceived barriers or facilitators to palliative care use, had a focus on intervention evaluation or on end-of-life care in general, or on a specific area of palliative care. Fifty-two studies were retained for analysis.

Characteristics of included studies
Characteristics of included studies are displayed in Table 2. Studies were published between 1995 and 2018. Most of the studies were conducted in North America (22/52, 42.3%) or Oceania (16/52, 30.7%). In Europe 6 studies (11.6%) were conducted, as well as in Asia (6/52, 11.6%), and 1 study (1.9%) was completed in South America. Only one study (1.9%) included an international sample, in which all the continents were represented. Five studies focused uniquely on hematooncology (5/52, 9.6%), and the rest focused either on oncology in general or on solid tumor oncology. The studies' populations ranged from HPs from various medical disciplines and HPs, and patients, to patients' families. Sample sizes ranged from 1 to 984 participants. All Improving education on PC for HPs in general, including experiencing observation and receiving support [39].

Awareness among patients and families
Patient and families do not know the purpose of PC involvement [64].
Increase of opportunities of patient education on PC for instance videos [64]. Health care professionals' difficulty in communicating patients' prognoses [54].
The use of short assessment scales, communication note-books and medical files with non-physical information [23].

Collaboration and communication between health care professionals
Difficulty in dealing with conflicting information about the goals of care which are them given among nurses [26].
PC team strategic visibility in patient floors and hospital-wide events and PC team unintentional visibility like being present around the hospital [64].

Theme 3: Emotions involved in disease paths
Emotions among health care professionals Barriers to discuss PC: emotional bond, emotional discomfort among oncologists [34].
Further education and training focused on dealing properly with patient psychosocial and emotional problems for HPs [52].

Emotions among patients and their families
Emotions in patients such as sadness/suppression, unrealistic expectations, infinite trust and faith in medicine, giving up hope, overly optimistic about life expectation [34].
Assessing psychological condition and treating mental disorders of patient [65].

Theme 4: Attitudes and beliefs towards palliative care
Attitudes and beliefs among health care professionals Belief that PC is not appropriate for those who have complex problems without physical symptoms among HPs [38].
Provision of clear, convincing, scientific support, concerning palliative care, for recommendations from the PC team [64].

Attitudes and beliefs among patients and their families
Interpretation of earlier and broader PC consultations as a cost saving measure (rather than clinically beneficial measure) among patients and their families [58].
Renaming 'palliative care' to 'supportive care', as patients were more receptive to the second name [57].

Thematic analysis
Four themes emerged: awareness of palliative care, collaboration and communication in palliative care-related settings (e.g., hospital oncological wards), attitudes and beliefs towards palliative care, and emotions involved in disease pathways among HPs, patients and their families (see Table 1, Fig. 3, and Table 3 in the Additional file 2).
The following categorization was developed in order to avoid potential overlapping barriers or facilitators between different themes. In particular, we included in the theme "awareness", barriers and facilitator related to knowledge and understanding (e.g. resulting from the participants' assessment of knowledge about palliative care), and those related to education (resulting from courses, practical trainings or experience in palliative    care units or related settings). We included in the theme "attitudes and beliefs", all those barriers and facilitators reported as attitudes or beliefs in the relevant studies, and, additionally, all other aspects related to opinions, views, thoughts, rules, assumptions, interpretations, ideas (regarded as absolute truths) [66] and subjective evaluations (that range from good to bad) that are represented in memory [67]. In the theme "Emotions", we included barriers or facilitators referring to emotions, in particular referring to primary emotions (e.g. anger, sadness, fear, and surprise), secondary emotions (e.g. optimism), and tertiary emotions (e.g. frustration) [68,69].
In the theme "Communication and collaboration" barriers and facilitators referring to collaboration as any mutually beneficial and well-defined relationship entered into by two or more people to achieve common goals [70] and those referring to transferring information, sharing meaning, and boundary negotiation [71]. Often a single study identified numerous barriers or facilitators; therefore, the number of barriers and facilitators is greater than the total number of the studies included in each theme. In the following section the results are presented by actor involved in palliative care use pathways: barriers and facilitators related to healthcare

Awareness of palliative care
Within this theme we included studies on knowledge of palliative care (e.g., knowledge of palliative care's scope and benefits), education on palliative care, and experience in the palliative care field (e.g., palliative care training or practical experience). In most of these studies (e.g., [22,39,46]), HPs' lack of knowledge of palliative care in general (e.g. how and when initiate palliative care, and lack of familiarity with the basic principles of palliative care, including pain management, among medical students), or lack of one or more areas pertaining to it, such as existential issues [23] represent a serious obstacle to palliative care utilization. Some studies also reported a lack of understanding of palliative care services [22,25,43,54], their scope [29,64], or their applicability [51,64]. Others showed a lack of knowledge of locally available palliative care services among HPs [22,62]. Often physicians (e.g., oncologists), nurses, and other HPs specifically reported a lack of education in palliative care [21,22,40,45,51,64]. Other studies reported a lack of practical training [22,27,34,64] or working experience [23,34] in palliative care. Potential facilitators to palliative care use were identified; some studies showed that the provision of education on palliative care, including education on the initiation phase, improved utilization [38,39,46,52,58,64]. One study focused on family physicians and highlighted that the use of specific tools for palliative care needs assessment was useful to address those needs in a timely manner [23]. Finally, several of quantitative studies showed that previous experience, general knowledge of end-of-life care, palliative care education provision for HPs (e.g., workshops and practical training) [35,51,52,58,64] as well as clinical guidelines on palliative care delivery [51] led to greater utilization of palliative care services.

Collaboration and communication between health care professionals
Eighteen studies reported poor communication between HPs, particularly between palliative care specialists and oncologists [30]. Reasons to explain this suboptimal communication included poor information exchange [22,48,72], lack of effective team communication (e.g., concerning communication of the prognosis between palliative care specialists and oncologists) [45,64], as well as lack of clarity [63] and consensus [34,48,73] on palliative care initiation. Ineffective communication can be due to lack of opportunity of conversations between cancer care and palliative care providers [64]. A study showed that the relationships between cancer and palliative care providers solely focused on patient care not representing trusted relationships which facilitate collaboration [64]. Several potential facilitators, such as improving collaboration between oncologists and the palliative care team [30], involving other HPs (e.g., nurses) in the negotiation phase with patients and their family, and joining other HPs at multidisciplinary meetings [23], were reported to improve palliative care use. A study reported that palliative care team strategic visibility in patient floors and hospital-wide events, as well as unintentional visibility, such as being present around the hospital, would nurture casual relationships between palliative care team and nonpalliative providers and hinder palliative care consultations [64]. Additionally, this study highlighted that an active marketing of the utility of palliative care consultations and education about the expertise of palliative care team to nonpalliative providers, as well as providing scientific support for recommendations during consultations represent facilitators for the receipt new palliative care consultations [64].

Emotions involved in cancer care pathways
Six qualitative studies reported that HPs in oncological and hemato-oncological settings had issues with managing the emotions involved in the discussions of diagnosis, prognosis and palliative care options with patients and families. In the selected studies, emotional discomfort with death and dying [32,53], discomfort preceded by a feeling of failure and defeat (when palliative care discussion is brought up or when referring to palliative care) [34,63], difficulty in managing the close emotional bond of patients or family members (sometimes resulting in personal identification with the patient) [26,34,52], and difficulty in addressing their reactions to prognosis disclosure (e.g. patient shock or anger) [26,52] were reported to be experienced by HPs. From these studies a lack of available psychological support for HPs who experience an high emotional involvement emerged [34,52]. Narrative-based training for HPs, in particular for nurses, may represent a facilitator to properly process emotions during discussions of diagnosis, prognosis and palliative care options, additionally, to help building therapeutic alliances with patients and colleagues, and to improve communication skills [26].

Attitudes and beliefs towards palliative care
Thirty-four studies identified attitudes and beliefs towards palliative care, which may represent barriers or facilitators to palliative care utilization. Common beliefs were the association of palliative care or hospice with death [28,51], the inappropriateness of palliative care for complex problems if physical symptoms were not present [38,74], the only palliative care goal being symptom management [46,74], incompatibility of palliative care and cancer therapy [57,62], suitability of palliative care for certain types of cancer such as lung cancer (less suitable for others e.g., breast cancer) [42], and suitability for older patients [25,53]. In addition, specific beliefs among hemato-oncologists included inappropriateness of palliative care for onco-hematologic patients (e.g., specific needs, such as transfusions, not being addressed) [44,53], the development of palliative care services specifically for solid tumor cancer rather than for blood cancer [53] and talking about palliative care at an early stage not being appropriate due to the large amount of other issues to address [47]. Additionally, some studies found that hemato-oncologists perceived palliative care as end-of-life care, preferred to maintain control also on palliative care, and had lack of trust in other professionals' oncology knowledge [44]. Moreover, further studies showed that hemato-oncologists had lower comfort levels towards palliative care referral compared to oncologists [35] and were conducive to referral with the service name supportive care instead of palliative care [36]. In these studies the difficulty of accepting death and avoiding discussing death was reported [25,29,34]. A recent study showed how HPs felt compelled to fully exhaust disease-directed treatment options prior to referring patients to palliative care providers [54]. HPs' beliefs in the selected studies also included earlier palliative care introduction in the disease trajectory representing a source of confusion over roles [75], increasing care fragmentation [75], and threat to palliative care patient autonomy [45,58]. Overall, attitudes of HPs included beliefs about losing patient care management [25,44,52], unconsciously avoiding admitting failure [25,63,64], personal crusades for the disease [76], curefocused attitudes and over-emphasis on the treatment [34,44,45,54], palliative care incompatibility with the hospital life-saving culture, including beliefs that hospital reputation can be damaged [58], and considering palliative care referring as the last resort [64]. Other studies found that oncologists were reluctant to refer to the palliative care team [28,37], due to a negative view of the palliative care team involvement [27,30,44,45,77] or past negative experiences [44,77]. A qualitative study highlighted that nonpallitive providers were reluctant to refer to palliative care team for consultations because they felt capable of providing palliative care, without the involvement of the palliative care team, or because they were hesitant about specific medications for pain/symptom management prescribed by the palliative care team [64]. Other reasons for the lack of palliative care referral included beliefs that patients or their family might have inappropriate reactions to the referral [54,77], that discussions or referral upset patients and families [34,54,75], or simply because of a lack of interest in palliative care [38,56]. Attitudes which might represent facilitators to palliative care use, in particular palliative care provision and palliative care needs identification, were the hospital team paying attention to ethical differences and acting according to patient values [21,23].

Barriers and facilitators related to the relationship between health care professionals and patients
This section shows barriers and facilitators for both HPs and patients and families, with a focus on communication issues between HPs and patients and/or families. Seventeen studies reported on these issues.

Collaboration and communication between health care professionals and patients and/or their families
A large number of the selected studies' samples included doctors (20/52 [38.5%], including oncologists, hematooncologists, GPs, and residents), followed by HPs (17/52 [32.7%] that included various health professions including nurses), and patients and families (15/52 [28.8%], including studies that also included HPs). Some studies reported difficulties in negotiating the transition to palliative care [29] which was chaotic and frequently occurred a short time prior to death [72], due to lack of open communication between HPs and patients and families [31,55,72,74], as well as lack of information on patient prognosis [22,72] or available support and services [61,72,74]. A study found that long-term relationships between hemato-oncologists and patients result in considerable difficulty conducting end-of-life discussions [53]. Three recent studies showed that further barriers to palliative care use included receiving conflicting information on goals of care by HPs [26,61,72], lack of shared perspectives on patient conditions by HPs [72], no discussions on end of life between patients and family and oncologists [54,72], no preparation of the patient and family to the imminent deterioration of the patient conditions [72]. Several aspects related to the lack of open communication were reported in these studies, such as absence of training in communication skills [23,34], problems with communication of a bad prognosis [45,54,78], lack of communication skills [22,61] and difficulty discussing spiritual, psychosocial, and emotional issues [52]. Lack of effective communication and collaboration between HPs and patients and families [31,39,55] and not using communication tools [23] were further obstacles to palliative care utilization. From some studies it emerged that collaboration and communication could be influenced by the unwillingness of the patient's family to openly communicate with the patient about diagnosis and prognosis (thus influencing the communication between the HPs and the patient) [55] as well as language or cultural barriers [34] or family emotional reactions [34], and difficulty in dealing with these for HPs [26]. Finally, a patient with impaired communication ability might represent a barrier to early identification of palliative care needs [23].
On the contrary, early identification of palliative care needs could be facilitated by effective communication [43], a gentle exploration of the topic, and the use of communication notebooks and medical files with nonphysical information by the GP [23], as well as 'reinforcing' the relationship with the patient (e.g., making regular contacts with him/her or creating trust in the patient) [23,64]. Additionally, designing proactive approaches for non-face-to-face communication with patients and family [54], interacting and collaborating with home care professionals by patients and family (home palliative care services) [50] and conducting regular follow-ups, with direct contact with patients, by the palliative care team [64].
Moreover, providing information on the medical condition and palliative care options to the patients or family [51,65], the family involvement in care trajectories and decision-making [65,76], medical language translated into more simple language for patients and families [76], and HPs receiving training on communication skills [23,26], were reported as aspects that improved palliative care utilization (provision or increased palliative care referrals). Additionally, training in communication skills could improve transition to specialized palliative care [41]. Finally, some studies showed that proposing palliative care with a new name ('supportive care') might increase palliative care services referral [37,57].

Barriers and facilitators related to patients and their families
Only a limited number of studies included patients and/ or families in the sample (only patients and/or families, 10/52 [19.2%]; patients and/or families and HPs, 5/52 [9.6%]). However, some studies that included only HP samples also reported perceived barriers and facilitators to palliative care use among patients and their families and these are also reported below.

Awareness of palliative care
Eleven studies which showed lack of palliative care knowledge in the patient population and in families were identified. In particular, low awareness about palliative care [38,42,51], and lack of knowledge of palliative care and local services [33,46,61,64] were recurrent barriers. Other studies reported uncertainty about palliative care scope [30], difficulty in defining palliative care [48], and lack of patient education [40] or lack of guidelines for patient education [22] as obstacles to palliative care use. Recent studies reported lack of information on hospital and home palliative care services by HPs [61] and difficulty in navigating the home palliative care system among patients [50] as barriers to palliative care use.
A greater level of education in patients, including increased knowledge of palliative care benefits [38,47,64] and demonstration of palliative care utility via exposure [64], provision of clear information on end of life [50], with the integration of a lay health coach into oncology teams [54] has been found to be associated with greater palliative care use.

Emotions involved in cancer care pathways
Some qualitative studies have shown that emotions involved (e.g., sadness and suppression) and psychological reactions (e.g., unrealistic optimism and unrealistic expectations especially among hemato-oncology patients [53]) in the disease path experienced by the patients and families might make early identification of palliative care needs difficult [23] as well as palliative care referrals [34]. Recent studies highlighted that feelings of frustration and anger due to unpreparedness of the family to patient transition to palliative care [72], fear of palliative care [59], and resistance or denial to accept the actual medical condition and/or palliative care options [25,64] represent barriers. In particular, one case study highlighted how assessing the psychological condition, in particular patients' emotions, contributed to improved palliative care utilization [65].

Attitudes and beliefs towards palliative care
This theme emerged in eighteen studies. The most recurrent themes were family or patient reluctance [34,63], willingness to continue the active treatment [72], a negative view of palliative care [33,34,75], misconceptions about palliative care [39,51], palliative care being viewed as terminal care [20,49,59], and beliefs about losing hope [24,34,77] or differing perspectives about hope (overoptimism versus hopelessness) when discontinuation of active treatment was communicated [60]. A qualitative study reported that patients wished to receive care from family physicians or nurses rather than from unknown HPs in a palliative care unit [33]. Additional beliefs reported by the selected studies were the perception of palliative care as a lesser care alternative and cost-saving option [58], and palliative care options which must not be brought up at the diagnosis or prognosis discussions [47,79]. Patient or family attitudes that were reported included infinite trust and faith in medicine [34], as well as family forbidding discussion of palliative care during conversations about diagnosis or prognosis [55]. On the contrary, one study found that patients' openness to their own needs was reported as a facilitator to early identification of palliative care needs [23].

Discussion
This study systematically reviewed current literature on using palliative care in oncology and hemato-oncology. The focus was on cognitive barriers and facilitators influencing the use of palliative care services from the perspectives of HPs, adult patients with cancer, and their families. Literature on this topic is very heterogeneous in objectives and focus, mainly addressing palliative care use, palliative care provision, and palliative care service referral. Findings show that barriers and facilitators can be summarized in four areas: awareness of palliative care; collaboration and communication in palliative care-related settings; attitudes and beliefs towards palliative care; and emotions involved in disease pathways. To note that no relevant differences regarding the themes emerging in the most recent studies, conducted between 2009 and 2019, and in the previous studies, conducted between 1995 and 2008, were observed. Overall, the studies revealed that lacking awareness of palliative care, having incorrect beliefs, negative attitudes and negative emotions towards palliative care among HPs or patients and families, as well as lack of collaboration and communication skills among HPs, poor communication and consensus on palliative care between HPs and palliative care team, and lack of open communication between HPs and patients and families represented the most common barriers to providing, asking for PC consultations or referring to, and consequently using palliative care services. In addition, it should be noted that specific barriers in hemato-oncology include HPs' lack of trust regarding the appropriateness of palliative care services for hemato-oncology patients, and lower comfort levels towards palliative care referrals compared to oncologists. These studies suggested that enhancing HPs' education about and clinical experience of palliative care as well as patients and families' education could facilitate palliative care utilization.
This study deeply exploring cognitive barriers and facilitators to palliative care provided an adequate understanding and specific nuances regarding palliative care access. In particular, this study showed that emotions play a key role for palliative care utilization, not only among patients and their families, but also among healthcare professionals. Moreover, this work highlighted that not only collaboration and communication between HPs contribute significantly to palliative care utilization, but also collaboration and communication between HPs and patients, and their families. With this regards, we strongly believe that the information on cognitive barriers and facilitators is highly relevant due to the fact that these represent directly addressable aspects. By intervening on cognitive barriers and facilitators potentially leads to directly enhance the utilization of palliative care services, as well as to partially overcome the other two types of barriers (e.g. more general awareness of palliative care benefits, including awareness among local health authority services, can encourage changes at systematic and organizational levels towards palliative care services optimization).
A way to interpret the meaning and the implications of these results refers back to the idea that health professionals, and medical doctors especially, are trained in the so-called curative model. In the curative model, health care practitioners treat patients with the sole intent of curing them, and do not consider other aspects such as reducing pain or stress [80]. By definition, palliative care has no curative goal, and intends neither to hasten nor postpone death [13]. What it can and should achieve is to improve the quality of life [13]. Our review suggests that cure-focused cultural aspects in health care settings may constitute a barrier to palliative care provision and referral. In particular, the predominance of a curative model [23,34] may explain the incorrect belief about palliative care as mostly conceived only to address physical symptoms [46]. In other cases, the cure-focused culture may influence the HPs' perception and confidence towards palliative care and its team's holistic approach [81]. Confidence was reported as being low or lacking among HPs [77], in line with a recent study [82], mainly because palliative care was seen as 'external' to the curefocused culture. In agreement with this, a recent American study showed that the palliative care team was perceived as being a 'team of outsiders' by oncologists [30]. In this cure-focused culture, dealing with emotions [32,53], being highly involved in chronic conditions as well as discussing spiritual issues [52] may be very challenging. Therefore, a discrepant view about palliative care utility [43], no consensus on appropriate timing of palliative care service initiation [48,74] as well as poor information exchange [30,48] have all been found to make the negotiation of palliative care transition extremely arduous [29].

Limitations
Although this is one of the few systematic reviews that included studies at any time and from any country with a specific focus on cognitive barriers and facilitators to palliative care, limitations exist.
First, we included non-interventional studies, whose quality should be considered lower than that of interventional [83]. However, due to our explorative aim, they were the most appropriate to answer our research question. Second, integrating qualitative and quantitative studies in one review was a challenge. However, both qualitative and quantitative results increased our understanding of the factors involved in palliative care utilization, the qualitative results gave a context for these factors from the perspectives of patients, formal and informal caregivers. This is a relatively new path of research which we have enriched with the present study. Finally, the inclusion of studies focused on palliative care in general, rather than also including studies on the specific palliative care areas (e.g., spiritual care) may represent a limitation. However, the scope of this review was to focus on palliative care as a typology of services, and explore how HPs, patients and families perceived palliative care as a whole.

Directions for future research
Most of the studies included in the review were conducted in the USA and Oceania, leaving space for international, European, African, and Asian studies. This is necessary due to country-specific characteristics of health care systems and cultures (e.g., beliefs, religion) which influence palliative care services' utilization, as this review showed.
Terminology issues emerged while conducting this review, due mainly to lack of consistency in the use of the term palliative care, hospice care and related terms across countries and over time. Making consistent the terms so that the meaning of palliative care is equal all around the globe is necessary for public health services to be informed by relevant studies and in order to make study comparisons possible.
Palliative care use between 'solid' and 'liquid' cancers might be quite different in terms of timing. Even though a small number of studies investigating palliative care in hemato-oncology exist, most literature concentrates on 'solid' oncology, leaving room for more research in this area.
Overall, there was a limited variety in participant sample types, as they were mostly composed of medical doctors or nurses, missing the perspectives of patients and families. A large number of studies on factors influencing palliative care use for patients included only HP samples, rather than patients and families. In future, qualitative studies especially need to explore these factors by making patients and families' voices heard.

Clinical implications
One of the main reasons impeding patients with oncological conditions experiencing physical suffering and high distress, who certainly would benefit from palliative care services, to use these can be attributed to the lack of collaboration and communication skills necessary to properly address discussions with patients and family, as well as to the general stigma attached to palliative care. Therefore, discussion of palliative care options is often avoided, especially due to lack of openness of communication on diagnosis and prognosis between patients and family [55], or between HPs and patients [31,45]. Training to increase collaboration and communication skills in palliative care settings should be available to HPs [84,85]. In addition, it might be relevant to implement the use of relevant tools for disclosing unfavorable information, such as SPIKES [80] or BREAKS [86], and to implement guidelines and recommendations for how doctors should prepare to delivering bad news [86,87].
Second, studies reported that the trajectory of the illness might be an obstacle to palliative care referral. In line with the principle of co-existence between disease treatment and palliative care, triggers for referral to palliative care services should be activated when transitions in care are verified (e.g., metastases discovered) or by the emergence of distress recognized with specific screening tools [3]. Therefore, referral for specialist palliative care support should be conducted at any time when physical, psychological, social or spiritual unmet needs cannot be satisfactorily resolved by the primary care team, even when the main goal of disease management is curative in intent. Interprofessional collaboration skills (e.g. to learn to be comfortable with performance review by team members of different professional background and with dilution of the traditional one-to-one relationship with patient [88]) should be enhanced.
Overall, strategies to encourage collaboration between oncologists and the palliative care team, to define a clear division of responsibility, and to encourage sharing of expertise of nonphysician palliative care team members should be applied in order to improve the interface between oncologists and palliative care providers [30].

Conclusions
Being aware of the existing cognitive barriers to palliative care utilization can help to address them in practice, particularly when strategies aimed at increasing the recognition of the importance of palliative care and at introducing it early on to patients are implemented. This would provide patients with continuity of care, allowing them to gain the possible benefits from palliative care when they are in need.