ecancermedicalscience

Review

Progress in palliative care for cancer in Turkey: a review of the literature

Tezer Kutluk1, Fahad Ahmed1, Mustafa Cemaloğlu1, Burça Aydın1, Meltem Şengelen2, Meral Kirazli1, Sema Yurduşen1, Richard Sullivan3 and Richard Harding4

1Department of Pediatric Oncology, Hacettepe University Faculty of Medicine and Cancer Institute, 06100 Ankara, Turkey

2Department of Public Health, Hacettepe University Faculty of Medicine, 06100 Ankara, Turkey

3King’s College London, Institute of Cancer Policy, Conflict & Health Research Group, London, UK

4Florence Nightingale Faculty of Nursing, Midwifery and Palliative Care, Cicely Saunders Institute, King’s College London, London, UK


Abstract

Background: The demographic transition in Turkey is shifting the burden of diseases towards non-communicable diseases including cancer. Palliative care (PC) as a component of Universal Health Coverage assures patient and family-centred care provision throughout the spectrum of cancer.

Objectives: This study aimed to make a detailed evaluation of the progress achieved since the mid-90s and the current situation of cancer PC in Turkey.

Methods: A literature review was conducted in PubMed, Scopus, Embase, ScienceDirect, Web of Science, Google Scholar, The Turkish Academic Network and Information Centre databases, Ministry of Health documents, Council of Higher Education’s thesis 01/1995 to 07/2020. The information was categorised into the six domains: history of the cancer PC; law and regulations; education and research; opioid use; patient care and palliative centres; public awareness, psychosocial support and end of life ethics.

Results: Of 27,489 studies, 331 met the inclusion criteria. The majority were published in the Turkish language and were journal articles. The findings showed that the development of PC in Turkey can be divided into three stages: early initiatives before 2000, the dissemination stage, 2000–2010 and the advanced stage after 2010. There is evidence of progress in terms of legal regulations, opioid use and number of PC services and research output. However, there is still a need for improvement in professional education, public awareness and end of life care.

Conclusion: There is evidence of progress, barriers and opportunities. However, bringing research into practice is needed for scale-up and integration of PC in cancer care in Turkey.

Keywords: palliative care, cancer, capacity building, systematic review, Turkey

Correspondence to: Tezer Kutluk
Email: tezerkutluk@gmail.com

Published: 25/11/2021
Received: 09/10/2021

Copyright: © the authors; licensee ecancermedicalscience. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Background

Demographic and disease transition has amplified the challenges for cancer care globally [13]. Palliative care (PC) aims to relieve the suffering of patients facing life-limiting conditions. Although PC is a newer component in the modern healthcare system, it is increasingly recognised as an essential part of it. The PC resolution adopted at the World Health Assembly in May 2014, urged governments to ‘integrate palliative care services in the continuum of care, across all levels, with emphasis on primary care, community and home-base care, and universal health coverage (UHC) schemes’ [4]. Moreover, the recommendations of the Worldwide Palliative Care Alliance stress that all governments must integrate PC along with preventive and curative health care into their national health system [5].

It is estimated that more than 56.8 million people need end of life PC every year globally [5]. If it is considered that for every terminally ill patient requiring PC, there are at least one or two caregivers involved, the total need of PC will be twice or thrice than the above estimates. Owing to physical symptoms, psycho-social and treatment effects, cancer patients are in greater need of PC and it is estimated that cancer patients only require more than one-quarter of global PC need [5].

Considering the need of PC, it is also worth noting that only a few countries have comprehensive PC programmes through a public health approach [6]. According to the most recent global survey conducted among 194 countries, funding for PC was available in 68% of countries and only 40% of countries reported that the PC services reached at least half of the patients in need [7].

Turkey is home to about 83.6 million people [8] and additionally hosts about 3.6 million refugees [9]. Based on the Global Cancer Observatory (GLOBOCAN) 2020 data, the estimated number of annual cancer cases in Turkey is 233,834 and 126,335 people die due to cancer [10]. Considering the burden of cancer and other non-communicable diseases (NCDs) along with an increase in life expectancy at birth [11], the real need for PC will be much greater in the near future. The concept of PC was developed in Turkey along with the cancer control programme. The Turkish Ministry of Health (MoH) had brought together all stakeholders under the umbrella of a National Cancer Advisory Board and ignited the Palliaturk project which became a turning point to create a national policy for PC [12]. Despite the decade long effort for establishment of the national PC programme and the progress which has been made, it is widely acknowledged that there is still a need for improvement for further dissemination and to take PC to a higher level in Turkey [13]. The aim of this review is to make a detailed evaluation of the progress achieved since the mid-90s and the current situation of cancer PC in Turkey.


Method

Search strategy

The methods for this review were based on Arksey and O’Malley’s scoping review methodology [14]. The databases were retrieved through a search of MEDLINE, Scopus, Embase, ScienceDirect and Web of Science, Google Scholar, ULAKBIM (The Turkish Academic Network and Information Centre), Turkish MoH documents, The Thesis Database of the Turkish Council of Higher Education and renowned national and international PC as well as cancer conferences. Articles were explored for PC for cancer patients in Turkey. The search was made by using three Medical Subject Headings (MeSH) categories – palliative care (palliative care, palliative therapy, end of life care, terminal care, supportive care, palliative medicine), cancer (cancer, oncology, malignancy, neoplasm, tumours, neoplasia) and Turkey (Turkey, Turkish) – combined using ‘and’ statements. The local database was also searched using the translation of the above term in Turkish. The search was limited to literature published between the year 01/1995 and 07/2020. Searches were performed on article titles, abstracts and full text. Additional studies were identified through the references of relevant studies.

Data selection procedure

Articles/studies were included in the review if they were in either the English or Turkish language and focused on PC in cancer. Articles which did not focus on Turkey, or were focused on surgical or radiological interventions for palliation of symptoms were excluded. Following the database search, duplicates were removed. Titles and abstracts were inspected jointly by all authors for inclusion in the review. Irrelevant studies were removed and the full text was examined if necessary. A Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram was used to provide information regarding the selection of the articles in this review.

Data extraction and analysis

The following information was extracted from articles: author names, the institution of affiliation of the first and corresponding author, title, name of the journal/conference/publisher, year of publication, type of publication, language of the article, study design and setting, national or international collaboration, aim/objective of the study, aspect of PC being studied and the main findings.

The main text of all articles included in this review was read by authors independently, the key findings were extracted and assigned into categories. Later these categories were examined and conceptualised in the research team meetings and were condensed into major themes; history of PC in Turkey, law and regulations, education & training, research trend, pain management, patient care and psychosocial support. The summary findings are presented in the results section.


Results

Search results

A total of 27,489 papers (7,989 research papers, 19,388 abstracts of conference presentation/poster, 101 postgraduate theses and 11 governmental documents) were identified. After removing duplicates, 24,788 papers met the condition for full-text screening. In all, 24,374 pieces of literature (the large majority of conference abstracts) were excluded based on the title or abstract. The remaining 414 were retrieved and screened in detail. Out of these, 83 were removed (there was insufficient information regarding PC for cancer in the full text of 67 literatures, five studies were specific to ethical considerations at the end of life, four were about the specific surgical procedures to palliate the obstructive symptoms due to cancer, other four were regarding PC needs of neonates with congenital malformation/birth defects, two studies were regarding geriatric health without cancer, one was about burnout of healthcare workers at oncology services). Figure 1 describes the PRISMA flowchart of the literature reviewed in this study and the details of the included 331 articles are shown in Supplementary Table 1.

Figure 1. PRISMA flowchart.

Characteristics of included studies

Of these 331 articles included in this review, the majority 161 (48.6%) are journal articles, 96 (29.0%) conference abstracts, 56 (16.9%) post-grad theses, 13 (3.9%) gray literature (mostly from the Turkish Ministry of Health), 3 (0.9%) book chapters and 2 (0.6%) are letter to a journal editor. Regarding journal articles – more than half, 98, articles were published in international journals, whereas 63 were published in Turkish/national journals.

About 193 (58.3%) literatures were published in the Turkish language, whereas 138 (41.7%) were in English. Among all the literature included in this review, 194 (58.6%) used cross-sectional surveys or retrospective analysis of datasets, 59 (17.8%) were review articles, letter to the editors, book chapters, 19 (5.7%) employed either interventional design or randomised control trials or quasi-experimental design, 14 (4.2%) studies evaluated validity and reliability of specific questionnaires among Turkish PC cancer patients, 13 (3.9%) were gray literature, 12 (3.6%) used qualitative research methods, 5 (1.5%) were case studies or case series evaluating a specific dimension of PC for cancer patients, 4 (1.2%) employed methodological design, 3 (0.9%) mixed methods research design, 3 (0.9%) articles used either prospective or cohort design and other 3 (0.9%) were cost analysis studies. Only 2 (0.6%) used a case–control design. Furthermore, 11 articles were published in collaboration with the Middle East Cancer Consortium (MECC). As shown in Figure 2, only two articles included in this review were published before the year 2000. Most of the articles were published between the year 2018 and 2019. The major themes were presented below.

History of cancer PC in Turkey

The history of PC in cancer is evaluated in three stages as summarised below and also shown in a timeline (Figure 3).

The first stage: Early initiatives (Before 2000): The earliest available information regarding PC is the establishment of the first outpatient pain unit in Istanbul University in 1986, and the establishment of the Turkish Society of Algology and the launch of the Turkish Journal of Pain in 1987. Soon after, in 1990, an inpatient pain department was established in Istanbul University and in the same year, algology was accepted as a speciality by Higher Education Council [15].

By the end of the 90s, there were no modern PC services. A lack of trained health care professionals, low public/professional awareness, limited access to opioids and opiophobia were the major barriers [16, 17]. In 2000, 13.1% of all deaths in Turkey were due to cancer and future projections showed that it would continue to rise [18]. Generally, PC was not a priority. By 2005, there were only seven supportive care units for pain and symptom management. Opioid consumption was relatively low and physicians as well as pharmacists faced legislative and practical obstacles in prescribing and dispensing opioid analgesics [19].

Figure 2. The evolution of the number of articles regarding PC for cancer in Turkey published per year, 1996–2020.

Figure 3. The evolution of the PC in Turkey from the mid-1980s to 2020. PC, Palliative care; MECC, Middle East Cancer Consortium; MASCC, Multinational Association of Supportive Care in Cancer; MoH, Ministry of Health; TOG, Turkish Oncology Group; TSMO, Turkish Society of Medical Oncology; ESMO, European Society of Medical Oncology.

The second stage: Dissemination of PC concept and awareness among the medical and scientific community (2000–2010): The new millennium witnessed interest from governmental and non-governmental stakeholders. The Turkish Oncology Group (TOG) established a supportive care working group in 1999 [16]. The National Cancer Advisory Board of MoH sets a psychosocial sub-committee in 2003. The Turkish Society of Medical Oncology started training courses [16, 20], organised a joint meeting with the Multinational Association of Supportive Care in Cancer (MASCC) in 2004 [20] and the European Society for Medical Oncology (ESMO) in 2006 [21]. The MECC, founded in 1996 in collaboration with MoH from member countries, became a platform bringing together clinical professionals and researchers [22]. As soon as Turkey became a member of MECC in 2004 [21], MECC & MoH collaboration started to organise meetings in cancer control including PC courses and workshops. PC awareness and engagement of different stakeholders were raised in the mid-2000s; The establishments of Hope Lodge by Hacettepe University Oncology Institute Foundation in 2006 [23, 24], the Palliative Care Association (PCA) in 2005 [23, 25], PC units in Ege University and Anadolu Hospital in 2006 [20] and a PC unit at MoH Oncology Hospital in 2007 [26] are examples of progress in this period. Based on a survey by MoH in 2009, there were only 10 PC units and 72 pain units in the country. Morphine use was less than in the USA and many Middle Eastern countries. Legal restrictions and lack of trained PC staff were the major barriers [12, 27, 28].

The third stage: Advancement with government and societal engagement (After 2010): MoH brought the first Cancer Control Programme in 2008 [29]. Soon after, MoH Cancer Control Department started the Palliaturk project in 2010, which was implemented in 2011 [12]. The Palliaturk project had two main objectives – namely targeting the availability of opioids and implementation of a community based PC model [12, 28]. The model included primary, secondary and tertiary level PC centres. MoH also started collaborations with international and national stakeholders (World Health Organization (WHO), Union for International Cancer Control (UICC), national non-governmental organisations (NGOs) and professional organisations, etc.) [12, 28]. Since the 2010s, new regulations and rules were set by the government; stakeholder involvement and awareness of the medical community as well as the public had increased. New PC centres were opened around the country. In 2015, the ‘Palliative Care Nursing Certificate Program’ was started by the MoH [30]. In 2017, The Home and Palliative Care section was established under MoH Public Health Directorate [31, 32]. According to the international PC scale ranking, Turkey was in group 2 (capacity-building PC activity) in 2006, and moved up to group 3b (generalised PC provision) in 2011, then in group 3a (isolated PC provision) in 2017. There were no countries except Israel in group 4 from the Middle Eastern Countries [6, 3335].

Law and regulations

The major PC regulations and laws were released after 1998. The first regulations relating to patient’s rights were released in 1998 [36]. The first home care regulation was released in 2005 [37]. PC services were mentioned in the 2010 update of the home care directive [20, 24, 38]. The first National Cancer Control Programme was released in 2008 [29] and became a turning point – the MoH Cancer Control Department started to work on PC Projects. With the aim of PC provisions, MoH established the PC Directive in 2014 and implemented it in 2015. It became a strong legal support to the establishment of PC centres to provide and promote PC in Turkey [39]. The PC directive described inpatient PC centres within the established hospitals. The involvement of family physicians and home care services in the outpatient setting were also included. The PC coverage includes examination, evaluation, care, rehabilitation, psychosocial support, nutritional support, pain management, legal support for the patients & relatives. Social Security Administration accepted the reimbursement of the inpatient PC costs in 2014 [20, 40]. An update of the home care regulation was released in 2015 [41]. In parallel to this legal progress, the first morphine sulphate tablet was officially produced by a Turkish pharmaceutical company in 2014 [42].

Professional education, training and research

The first PC fellow of Turkey was a medical oncologist trained in the USA in 1997–1998. Between 2001 and 2010, the Supportive Care in Cancer Committee of the TOG organised 18 national/international training meetings. This committee also contributed to the development of PC within the National Cancer Control Programme after 2008 [16]. Turkish Medical Oncology Society organised the first postgraduate education on PC in 2003, joint meeting with MASCC in 2004, PC course with ESMO in 2006 [20]. More PC courses and meetings have been organised after 2013 by different stakeholders [20]. A nursing academic was trained in the USA for PC in 2006 [20]. MECC & MoH collaborations became a driving force for PC education in Turkey and regional countries. They jointly organised meetings and workshops between 2004 and 2014, training 434 health care professionals [2022, 43, 44].

The interest in PC research and education from Medical & Nursing Schools appeared after 2010. PC lectures were included in Nursing schools under the postgraduate curriculum [20]. PC centres were established in Ege and Dokuz Eylul Universities in 2011 and 2012, respectively. The centre in Dokuz Eylul University was approved by the Higher Education Council [24, 45, 46].

Stakeholders including the Turkish Medical Oncology Society, the anaesthesiology/algology, nursing community and PCA made a significant contribution. The inclusion of a Psychosocial Committee within the National Cancer Advisory Board in 2003 also helped to increase stakeholders’ engagement [47]. In 2019, the Palliative Care Nursing Association was established [48]. The increasing number of reports from various stakeholders including medical specialities [4951] nurses [20, 5257], physiotherapists [5862], social workers [47, 63], hospital managers [64], nursing students [6568] shows the progress in the PC field in Turkey. However, there were an insufficient number of PC healthcare workers. The lack of PC training among medical, nursing, midwifery, students, physicians and nurses, healthcare staff, emergency care staff was within the range of 50%–80% [6983].

The number of research outputs on PC increased after 2015. The different areas of PC were investigated. The need assessment and adaptation of the ENABLE (Educate, Nurture, Advise, Before Life Ends) evidence-based early PC model were also investigated for Turkish family caregivers of older persons with cancer [84]. Ulus State Hospital, MoH first comprehensive PC centre, reported that 38.4% PC patients had a cancer diagnosis [85]. A previous study found that pain was the most common symptom (27.1%) among hospitalized patients [86]. Along with an increase in PC services, burnout was also found to be a significant problem among healthcare workers working in PC units [87]. Complementary and alternative medicine (CAM) use is also a common practice in Turkey. CAM use was found to be 57% among cancer patients [88]. In another study, at least one CAM method was used by 62% [89]. Irmak et al [90] found that 46.4% of cancer patients were CAM users, however no significant difference was found with respect to quality-of-life (QoL) score among CAM users and non-users. A randomised trial found that listening to music was effective in controlling pain and anxiety among cancer patients [91]. Several studies focused on the validity, reliability and adaptation of various scales among PC and cancer patients [92119] (See Supplementary Table 2).

Opioid use and pain management

Opioid consumption at the global level started to increase in the mid-90s. A survey on the availability and accessibility of opioids among Middle East countries showed that opioid availability was low throughout most of the Middle East countries except Israel. In 2011, Turkey was in the 10th rank as regards morphine consumption mg per capita [120]. For many years, opioids are available but the process for prescribing was complicated with a colour-coded system; red prescription for strong opioids, green for sedatives and weak opioids and white for all non-restricted prescription [16].

Opioid consumption in total morphine equivalence, milligrams per capita, in Turkey in 1980 was 0.0937 and it increased to 12.2204 in 2011. Although there was a significant increase by the time, 2011 Eastern Mediterranean Regional Office (EMRO) average was 10.56, global average was 61.66 [34, 43]. A study published in 2010 showed that the consumption of morphine has been fluctuating at doses around 0.1 mg/capita in Turkey for the period of 2004–2007. This was higher than Saudi Arabia and Egypt but lower than Israel, Cyprus, Jordan and Lebanon. Morphine consumption in Turkey was 447 times less than the USA in 2007. In the USA, the consumption was 76 mg/capita in the year 2007. The global mean was 5.57 mg/capita [121]. There was a big disparity among the Middle East countries including Turkey in terms of opioid use compared with western World and the USA. Turkey was at number 50th in the world for consumption of opioids analgesics during 2007–2009 [22]. Access to Opioid Medicine in a European Project (ATOME) in 2016 reported that Turkey had more than 40 potential barriers in different categories [122].

A number of studies have been published with a focus on pain management in cancer patients [123132]. A study among 52 metastatic cancer patients found that the use of morphine was 5.7%; codeine 3.8% and tramadol 75% [130]. In another study, interventional procedure was used to control pain in 11% of cancer patients [131]. It was also reported that 82% of hospitalised cancer patients for PC were given different analgesic treatment of whom 50% received third step pain medicines [124]. A study among 1,467 cancer patients utilising analgesic step ladder approach showed the use of nonopioid+/−weak opioid+strong opioid in 31.5% and interventional procedures in 14.5% of patients [125].

Patient care and PC centres

PC activity was very limited in Turkey before 2010 [21]. The European Association for Palliative Care (EAPC) survey in 2007 showed that PC services are provided in ten centres with a total of 241 beds, and there was only one hospice centre in Turkey. Most of the PC centres were within oncology clinics with a major focus on pain control [133]. The earliest PC units were established in 2006 at Anadolu and Ege University Hospitals [20]. MoH Abdurrahman Yurtaslan Hospital established the comprehensive PC services in 2007 with 18 inpatient beds [26]. New PC centres in MoH Hospitals were established following 2010 [20]. A multidisciplinary PC team in 2010 and first PC unit for children in 2011 were established in Dokuz Eylul University [134, 135]. The first ‘Comprehensive PC Center’ in the Turkish MoH, Ulus State Hospital was opened in December 2012. One third of patients treated in this centre within a year had a cancer diagnosis [23].

PC services were included in home care services in 2010 [20, 38]. By the year 2014, there were a total of 834 home care teams providing services to 416,175 patients. In 2013, there were 18 PC centres in the Turkey [43]. By 2017, the number of PC services increased to 227 PC Units, 947 home care teams and trained 21,696 family physicians within the MoH organisation [44]. A study in 2018, presented that there were four paediatric PC hospital services in Turkey [136]. As of February 2020, there were 415 PC centres, with 5,577 bed capacity and 6,011 PC workers in 81 Provinces. Among these, there were 10 paediatric PC services with 119 bed capacity. More than 290,000 patients got support from these services [137] (Figure 4).

Figure 4. Number of PC beds in Turkey, 2012–2021.

The increase in PC centres also resulted in an increased number of research outputs. A study showed that 9% of 214 patients receiving home care health services in Kirikkale city had a diagnosis of cancer [138]. A study reported 45,838 out of 409,337 patients with respiratory problems benefitting from home care services had a diagnosis of lung cancer during 2011–2017 and the number of lung cancer patients increased from 1,346 in 2011 to 9,206 in 2017 [139]. Another study showed that cancer was the fourth most common diagnosis among patients receiving home care services. During the period of 2011 and 2017, total number of home care visits increased from 3,440,144 to 10,917,965; the number of home care teams increased from 593 to 662. Among home care visits, number of cancer patients increased from 7,278 to 74,261 [140].

With the increase in the number of services, PC units around the country started to report their experiences [141145]. Most of the studies focused on symptom management [146171]. Different aspects of supportive care were investigated in many studies including quality of life [172181], care dependency [182], nutritional aspects [160, 183, 184]; complementary approaches like acupress [185], reflexology [186], lymphedema management [187], bio-resonance [188] and music therapy [189]. A study from a PC centre showed 87.8% of 327 patients had cancer during 2015 and 2017. The most common reason for hospitalisation was oral intake impairment in 34.6%, pain control in 25.5% and both in 16.2% [190]. Ozcelik et al [191] prepared a PC guideline in 2014. Erkal et al [192] discussed the cost, management, satisfaction and other issues in PC services.

A few studies investigating emergency department admissions showed that 20%–60% of patients had a diagnosis of cancer [193195]. A mortality analysis of 373 stage 4 cancer cases showed that 23.9% were given chemotherapy during a month before their death [196]. A study investigated the last 2 weeks of 422 terminal cancer patients in hospital; the invasive pain management was used in 25%, terminal sedation in 12%, chemotherapy in 9%, central catheters in 38%, transfusion in 43% and MR imaging in 13% [197]. Another study in cancer patients showed that 42% of patients were given palliative chemotherapy in the last 3 months of life [198]. There are similar studies that focused on the interventions and investigations during the last weeks of life [199201]. These studies highlight unnecessary procedures at the terminal stage and emphasise the need for PC among cancer patients.

Symptom control was not at the optimal level. A multicentre study in 1,245 lung cancer patients found that pain was controlled in only 21.7% cases, while dyspnoea in only 12.4% of cases [202].

Poor symptom control also affects home based care. A study among caregivers of terminal cancer care presented that most participants expressed that they would like to look after their patients at home, however they preferred hospital care at the end [203]. A study shows that the health literacy level of care givers has a significant effect on bedsore occurrence and survival [204]. A positive correlation between ‘the time from diagnosis to palliative care application’ and the quality of life was found in a cohort study [205].

An analysis on the nosocomial infections in PC unit showed that the average cost of antibiotics was 1,252.79 ± 1,616.50 Turkish Lira (TRY) [206]. A cost comparison was made among cancer patients treated at comprehensive PC; hospital in-patient PC and home health care services, and it was found that the mean total indirect costs were $164.10, $778.43, $344.62, respectively. The mean total direct costs were $2,384.57 and $4,775.68 in comprehensive palliative care services (CPCC) and hospital inpatient palliative care services (HIS), respectively [207]. A cost analysis in a medical intensive care unit where 77% of the patients had terminal cancer found that the median cost was 2,841 TRY, and the total cost was 581,353.2 TRY [208]. A cost analysis in Denizli State Hospital PC Centre revealed that total cost of the PC centre was 1.034.235,26 TRY [209]. In another study, the direct cost per patient per day in a PC centre was found as 391 TRY [210].

A survey showed that the patient satisfaction was higher in oncology centres having PC units [211]. A study showed that PC centre was less effective in reducing symptom levels in cancer patients compared with patients in general care at the public hospital, but provided greater patient satisfaction [212].

Public awareness, psychosocial support and end of life ethics

A low level of public awareness was identified in many studies. It was found that 60%–87% of cancer patients and their caregivers had no prior knowledge about PC [203, 210, 213, 214]. Home care awareness was found as 57% [119]. Another study presented that patient preference for home care increased from 12% at admission to 47% at discharge [215]. Quality of life for care givers was also investigated in a study, and it was found that 53% of the study subjects did not meet routine responsibilities [216].

Do not resuscitate (DNR) is an important element of PC and end of life. However, there is no DNR Law in Turkey. Many researchers stressed the need for legal arrangements for end of life care and DNR policies [20, 217220].

Along with progress on PC at national level, many studies were conducted on the subjects of psychosocial issues [221234], patient and professional satisfaction [235237], burden of the caregivers [238247] and end of life [248251]. A survey among doctors and nurses in Middle Eastern Countries including Turkey showed that 44% of participants provided spiritual care less often than they think they should [252]. A study among PC nurses found that they perceive death as a natural and inevitable process and as their experience increases, they become desensitised [253]. A study showed that 55.7% of 70 nursing students had never heard of spiritual care [254]. Another study investigating the cultural mourning ritual, the ‘First Feast’, found this tradi tion helped to ease the grief response of relatives and might be a useful auxiliary method for PC teams to help grieving families [255]. There are other studies that focus on the psychosocial and spiritual issues on caregivers [256258].

A study also found that 80% of the caregivers had inadequate health literacy regarding general health [259]. Barriers for PC development were discussed in some studies [20, 24, 34]. The major barriers reported by Turkish MoH, 2nd Turkish Medical General Assembly Clinical Oncology Study Group were lack of public and professional awareness, failure of PC planning and disconnection from anticancer treatment, hurdles in the accessibility of opioid analgesics, financial issues and the lack of trained PC providers [260].


Discussion

The population is ageing in Turkey, the proportion of people over 65 years of age comprised 9.5% of the population in 2020 [8]. The need for PC in Turkey has increased in parallel to the burden of NCDs and cancer. The estimated annual deaths due to NCDs in Turkey was 407,300, it makes 89% of total deaths in 2016 [261]. Cancer is listed as the second most common cause of mortality which accounts for 18.4% of all deaths in Turkey during 2019 [262]. There were very limited services mainly provided during the routine care in tertiary care hospitals before 2000. Indeed, the situation was not much different at a global level – it was reported that globally over 56.8 million people are in need of PC each year. Most of them are living in developing countries [5]. The EAPC published that the number of PC beds per million inhabitants was 45–75 in advanced European countries, the rest had few beds [133]. Both professionals (mainly oncologists and anaesthesiologists) and government have contributed on the progress of PC after 2010 significantly in Turkey. The partnership between oncology societies and cancer control department at MoH became a successful model for the planning and implementation of PC services in Turkey. MoH actions in PC boosted the involvement of other stakeholders, regional/international organisation. The PC activity was scaled up to group 3b in 2011. After the implementation of Palliaturk project in 2011, various PC related legal regulations were enacted [6, 12, 3335]. During the same period, the demand for PC due to changing demographic patterns (ageing, decrease in household size) and burden of cancer/NCDs was also increasing.

Many studies showed that awareness and knowledge about PC among medical professionals was very limited. PC is still not a recognised speciality in Turkey. Only a few universities include PC education in the under and postgraduate curriculum. National and international meetings were the main source of PC training. There is still a large variation in palliative medicine (PM); education even in Europe. In the WHO Europe region, PM courses were included in all medical schools of 13 out of 43 countries, PM was not taught within medical curricula in 14 countries [263]. Major oncology associations like the American Society of Clinical Oncology (ASCO) & ESMO are also investing in the integration of PC services in oncology [264]. During the last 10 years, PC medicine is gaining more investment from all stakeholders. Sedhom et al [265] commented that PC is still not integrated into cancer care with such a priority focus of oncology training on treatment and research. There is still a strong need for an advanced education and structured human resource policies. An early literature review in Turkey showed the limited PC publications before 2005 [266]. The number of scientific publications and presentations started to increase after 2015; however, most of the studies were either surveys or descriptive studies. More focus on evidence-based research in PC is still needed. A bibliometric analysis on PC during 2000–2016 showed that the publications increased after 2006, the USA and UK were pioneering the scientific work [267].

The use of opioids is being recommended for the control of the pain and improving quality of life [5, 229], and it is used as an indicator for the PC service availability [268]. There were strong critics to Turkey for underuse of opioids for pain management, although Turkey was one of the leading opioid producing countries [34, 43, 121]. The situation improved after the investments on PC starting from 2010, however, it is still much lower than the global average [34, 43]. Consumption in defined daily doses for statistical purposes (S-DDD) per million inhabitants per day is within the scale of 201–1,000 during 2014–16 which was less than North America and Europe but higher than most Asian and African countries [269]. Based on our literature review, we can classify the barriers to opioid use into three groups: first is the lack of awareness and opiophobia among the health care professionals and public; second the complexity in prescription of the opioids due to legal procedures and thirdly the lack of organised PC structure until 2010. There is still a need for investments in the infrastructure, training and human resource management on PC under the concept of ‘health system strengthening’.

Before the implementation of the Palliaturk project, few hospitals and universities started to invest on PC services, there were no specialised PC centres in those years [20, 21, 23, 26, 43, 133]. The government Palliaturk project, the PC Directive and the Home Care Regulations contributed to the progress made during recent years [12, 20, 39, 41]. Currently, there is a PC section within MoH at top management level and MoH was able to invest in the dissemination of PC capacity in Turkey [137]. Our findings show that integration for PC services with oncology services is an area for further research and investment. There are a number of cultural barriers and opportunities for the utilisation of PC centres in Turkey. Talking about death is a cultural taboo. Doctors, patients and care givers are reluctant to talk about end of life care. This results in delayed referral to PC centres by professionals. Moreover, the concept of PC centres is not clear in the minds of the public. Therefore, referral to PC centres was sometimes perceived as an abandonment of oncological care. Due to this, patients and caregivers want to be under the care of the primary oncology team instead of PC centres. The integration of PC care into oncology practice will help to overcome these cultural barriers. Traditionally, terminally ill patients were cared for in their homes by family members. However, with social and economic changes, care givers now more commonly prefer their patients to be cared for in the hospital. This could be an opportunity for the utilisation of PC centres more widely. ASCO as a leading professional cancer organisation also strongly advocates the integration of PC into oncology practice to disseminate and implement it more effectively [270].

Currently, there is no DNR Law in Turkey [20, 217]. Moreover, the Turkish society is not ready to implement DNR policies due to several reasons such as health literacy, taboo of discussing death and lack of legal framework. Therefore, DNR is not a priority issue either for the public or government. End of life care and DNR policies must be brought in to the discussion at the public, professional and government level. It is also a time for Turkey to invest in hospice care. The Turkish Society of Internal Medicine also declared that they support Choosing Wisely®, a health initiative campaign with recommendations to advance a national dialogue on avoiding unnecessary medical tests, treatments and procedures and ‘Do not delay the palliative care’ is among the recommendations by this campaign [271]. A recent article by Currow et al [272] discusses the need for transition of hospice care and integration of cancer services with hospices care. It seems the hospice concept will be evolved through the changes in the cancer care in future years.

Now, monitoring the global situation of PC is highly essential. The burden of chronic diseases was in the agenda of UN General Assembly in 2011 and the international organisations/NGO’s started to speak more about the need for PC. Due to the increased burden of NCDs including cancers, Turkey must scale up its PC services. One important issue is the effect of the COVID-19 pandemic on cancer care including PC [273, 274]. An NCD pandemic is a high possibility in the post-COVID-19 period and a greater need of PC is expected.

The International Association for Hospice and Palliative Care re-defined PC as ‘Palliative care is the active holistic care of individuals across all ages with serious health-related suffering due to severe illness and especially of those near the end of life. It aims to improve the quality of life of patients, their families and their caregivers’ [275].


Conclusion

In conclusion, this review presents evidence of the significant progress made in Turkey during the last 20 years but also presents the opportunities for further improvement. Bridging the gaps in human resources and training, including PC care as a priority area in the national health agenda, the commitment of all stakeholders, and investing in public and professional awareness should be the focus of the next steps and also shaping the integration of PC in cancer care in Turkey. The inequity in PC must be a priority action for decision makers not only for Turkey but also globally. The stakeholders and decision makers should not neglect the need for PC improvement under the current pressure of the COVID-19 pandemic on health and the economy at a national and global level.


Conflicts of interest

The authors declare that there are no conflicts of interest.


Authors’ contributions

TK, FA, MC and MK contributed to the (I) Conception and design, (II) Administrative support, (III) Provision of study materials, (IV) Collection and assembly of data, (V) Data analysis and interpretation, (VI) Manuscript writing: All authors and (VII) Final approval of manuscript.

BA, MŞ and SY contributed to the (I) Conception and design, (III) Provision of study materials, (IV) Collection and assembly of data, (V) Data analysis and interpretation, (VI) Manuscript writing and (VII) Final approval of manuscript.

RS and RH contributed to the (I) Conception and design, (V) Data analysis and interpretation, (VI) Manuscript writing and (VII) Final approval of manuscript.


Funding

This work was supported by The UK Research and Innovation Global Challenges Research Fund (GCRF) Research for Health in Conflict in the Middle East and North Africa (R4HC-MENA) project; developing capability, partnerships and research in the Middle East and North Africa [ES/P010962/1].


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339. Kado A (2017) Palliative Care Needs Cancer Patients and their Proximity Questions and Solution Suggestions [Dissertation] (Istanbul: Yeni Yüzyıl University)

340. Güney H (2017) Determination of Patients with Applied Emergency Service and Palliative Care with a New Screening Method, Investigation of Needs and Symptoms by Speed, Edmonton and Karnofsky Scales [Dissertation] (Tokat: Tokat Gaziosmanpaşa University)

341. Filiz S (2017) Determination of Nursing Care Satisfaction Levels and Effective Factors in Patients with Patient Care [Dissertation] (Istanbul: Üsküdar University)

342. Saygılı M (2016) An Evaluation of Three Different Palliative Care Service Models in Terms of Patients with Cancer Diagnosis-their Family Caregivers and Cost-Effectiveness Analysis [Dissertation] (Ankara: Hacettepe University)

343. Gürakan G (2016) Effect of Aromatherapy Massage on Pain and Plasma Beta-Endorphine Levels in Palliative Cancer Patients [Dissertation] (İzmir: Ege University)

344. Akyüz S (2014) Examination of Palliative Care Offered to Cancer Patients [Dissertation] (Ankara: Gazi University)

345. Uslu F (2013) Determination of the Palliative Care Practices of the Midwives and Nurses in the Gynecological Oncology Units in the Centrum of Ankara [Dissertation] (Ankara: Hacettepe University)

346. Özçelik H (2011) Examining the Effect of Case Management Model on Patient Results in Palliative Care of Cancer Patients [Dissertation] (İzmir: Ege University)

347. Turgay G (2010) Healthcare Professionals’ Views on Palliative Care [Dissertation] (Ankara: Başkent University)

348. Ekici Kocakafa G (2019) Determination of the Caregiving Burden of Family Members Caring for the Inpatients in Palliative Care Unit [Dissertation] (Istanbul: Marmara University)

349. Karabuğa H (2009) Evaluation of Quality of Life Among Caregivers of Patients with Cancer [Dissertation] (Istanbul: Marmara University)

350. Çalışkan T (2012) Inadequacy and Differences about the Attitudes in Pain Control of Cancer Patients: Assessment of Algology Department [Dissertation] (Ankara: Hacettepe University)

351. Elevli E (2012) Home Care Services in an Investigation that Determined You Need [Dissertation] (Istanbul: Beykent University)

352. Kılınç G (2015) Evaluation of the Prognosis of Cancer Patients Treated in Intensive Care Units [Dissertation] (Denizli: Pamukkale University)

353. Uzunkaya P (2016) Determining Attitudes of Nurses Working in Oncology Clinics Towards Care of Dying Patients and Principles about Death with Dignity and their Opinions Regarding Good Death [Dissertation] (Ankara: Hacettepe University)

354. Terzi K (2018) End of Life Care from the Perspectives of Patients with Cancer and Nurses [Dissertation] (Ankara: Hacettepe University)

355. Yalçın S (2018) Process Evaluati̇on of End Stage İntensi̇ve Care Pati̇ents [Dissertation] (Denizli: Pamukkale University)

356. Özyalçın D (2019) Opinions of Cancer Patients, Nears and Nurses Related to Death and Good Death [Dissertation] (Ankara: Başkent University)

357. Şipal G (2019) Supportive Care Needs and the Disease Acceptance Level of Hematological Cancer Patients [Dissertation] (Konya: Selçuk University)


Supplementary appendix

The supplementary tables are also available online at https://doi.org/10.6084/m9.figshare.17057009.v1.

Supplementary Table 1. Details of the included studies.

Supplementary Table 2. Scales used as assessment tool in PC for cancer research in Turkey.

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