Current status of integrating oncology and palliative care in Japan: a nationwide survey

Background Palliative care (PC) is increasingly recognized as essential for oncology care, and several academic societies strongly recommend integrating oncology and palliative care (IOP) in daily practice. Similarly, the Japanese government encouraged the implementation of IOP through the Cancer Control Act of 2007; however, its detailed progress remains unclear. Therefore, this cross-sectional nationwide survey was conducted to investigate the current status and hospital executive physicians’ perception of IOP. Methods The questionnaire was developed based on IOP indicators with international consensus. It was distributed to executive physicians at all government-designated cancer hospitals (DCHs, n = 399) and matched non-DCHs (n = 478) in November 2017 and the results were compared. Results In total, 269 (67.4%) DCHs and 259 (54.2%) non-DCHs responded. The number of PC resources in DCHs was significantly higher than those in non-DCHs (e.g., full-time PC physicians and nurses, 52.8% vs. 14.0%, p < 0.001; availability of outpatient PC service ≥3 days per week, 47.6% vs. 20.7%, p < 0.001). Routine symptom screening was more frequently performed in DCHs than in non-DCHs (65.1% vs. 34.7%, p < 0.001). Automatic trigger for PC referral availability was limited (e.g., referral using time trigger, 14.9% vs. 15.3%, p = 0.700). Education and research opportunities were seriously limited in both types of hospitals. Most executive physicians regarded IOP as beneficial for their patients (95.9% vs. 94.7%, p = 0.163) and were willing to facilitate an early referral to PC services (54.7% vs. 60.0%, p < 0.569); however, the majority faced challenges to increase the number of full-time PC staff, and < 30% were planning to increase the staff members. Conclusions This survey highlighted a considerable number of IOP indicators met, particularly in DCHs probably due to the government policy. Further efforts are needed to address the serious research/educational gaps.


Background
In the last decades, palliative care (PC) is widely recognized as an emerging clinical expertise and an essential part of oncology care [1,2]. Recent cumulative evidence revealed that early integration of PC is effective for patients with advanced cancer undergoing cancer treatment [3][4][5]. Several academic societies, including the European Society for Medical Oncology and American Society of Clinical Oncology, strongly support and recommend integrating oncology and palliative care (IOP) in daily oncology practice [6,7].
Similarly, the Ministry of Health, Labor, and Welfare in Japan has been enhancing the early and continuous delivery of quality care for patients with cancer (both early and advanced stage) from the time point of cancer diagnosis via the Cancer Control Act since 2007 [8,9]. The policy promotion includes comprehensive strategies including PC training for all physicians working at all governmentdesignated cancer hospitals (DCHs), implementation of PC services and routine screening, the establishment of referral criteria to PC services, and public education [8,[10][11][12][13]. However, detailed progress and dissemination of IOP remain unclear. Therefore, this cross-sectional nationwide survey aimed to investigate the current status and executive physicians' perception of IOP.

Methods
This cross-sectional nationwide survey in Japan was conducted targeting executive physicians at hospitals providing cancer treatments as respondents. The survey form was distributed in November 2017, and nonresponding institutions were reminded 3 weeks after the first mailing. Responses to the survey in written format were considered consent to participate. Based on the national ethical guideline of epidemiological studies in Japan, this study was exempted from review by the Ethics Committee at the Kyoto University Graduate School and Faculty of Medicine, Kyoto University Hospital.

Target samples
Two target samplings were identified: one was 399 DCHs, where the Ministry of Health, Labor, and Welfare-authorized high-quality cancer treatment was provided, and the other sample was non-DCHs that potentially manage patients with cancer because a considerable number of patients could receive cancer treatment at non-DCHs. Non-DCHs were randomly sampled and then stratified based on regions and inpatient bed numbers.
The sampling strategy is summarized in Fig. 1. To identify DCHs, the list of DCHs was obtained from the Ministry website as of April 2017. To identify non-DCHs, all hospital data were acquired from Japan Medical Press, Inc., in October 2017. To identify non-DCHs that offer cancer treatment, we excluded the following hospitals: (i) hospitals with < 100 general ward beds (this was because there were no DCHs with < 100 inpatients beds), (ii) national sanatorium, (iii) hospitals not delivering cancer treatment based on the hospital name and clinical departments (e.g., rehabilitation hospitals or no cancer treatment departments), and (iv) others (e.g., breast cancer-specified hospitals). To ensure representativeness and comparability between DCHs and non-DCHs at each region, stratified random sampling was performed based on the region and inpatient bed number. Regional strata were divided into nine categories: Hokkaido, Tohoku, Tokyo, Kanto other than Tokyo, Chubu, Kansai, Chugoku, Shikoku, and Kyushu- Okinawa. Inpatient bed number strata were divided into four categories based on the actual distribution of DCHs: < 299 beds, 300-499 beds, 500-699 beds, and > 700 beds. Considering the possibility that the response rate from non-DCHs may be low, three times more non-DCHs were extracted in each stratum. Moreover, responding hospitals that did not provide three cancer treatment modalities (surgery, systemic chemotherapy, and radiation therapy) at their own hospitals were excluded from the analysis in order to ensure comparability according to predefined exclusion criteria.

Sample size calculation
We did not define a primary outcome owning to the explanatory nature of the survey. However, to compute the confidence interval of the point estimate within 10%, responses were needed from at least 96 hospitals. Therefore, at least 40% of responses were estimated to be obtained, consisting of 240 hospitals from both types of hospital.

Survey development
The questionnaire was created after a comprehensive literature search. A pilot test was performed on three physicians with positions equivalent to that of executives in cancer hospitals to ensure face and content validity.

i) Current status of IOP
To clarify the current status of IOP, the international consensus was used as the IOP indicator [14], consisting of five sections: clinical structure, clinical process, clinical outcomes, education, and research, which were categorized as major or minor indicators. Clinical outcome indicators were excluded because the target respondents were experiencing difficulties in answering these questions due to the heterogeneity among specialties within the same hospitals based on the pilot test results. Thus, a total of 25 questions (Tables 2, 3, 4) were primarily used based on the categorical answer format from no (0%), limited (1-24%), approximately half (25-74%), mostly (75-99%), and all (100%) departments.

ii) Executive physicians' perception toward IOP
To investigate executive physicians' perceptions of the oncology department toward IOP, 16 questions were used based on the literature search [6,[15][16][17][18][19][20][21]. Each question was rated on a 5-point Likert-type scale, from 1 (strongly disagree) to 5 (strongly agree). In addition, a free text query was prepared by asking opinions regarding IOP.

Analysis
Descriptive statistics was performed to summarize the data. To adjust the biased distribution of inpatient bed number between the responding DCHs and non-DCHs, each stratum of non-DCHs was weighted according to DCH distributions in inpatient bed number (< 299 beds, 300-499 beds, 500-699 beds, and > 700 beds). Missing data was not imputed. The t-test or Cochrane-Armitage trend test was used to compute differences in the proportion, as appropriate. A P-value of < 0.05 was considered statistically significant. Owning to the exploratory nature of this survey, the adjustment of multiple testing was not performed. The GNU R software (version 3.2.0; R Project for Statistical Computing, Vienna, Austria) was used for all statistical analyses.
Free comment responses were qualitatively analyzed using inductive content analysis method [22,23]. Two independent investigators (M.N. and S.I.) reviewed and generated the codes. Then, emerging codes were compared and discussed with an expert PC physician (Y.U.) to achieve agreement of the codes labeled from the data. To ensure rigor and trustworthiness, an experienced investigator (T.M) supervised and examined the consistency of results.

Response rates and demographic data
Among the 399 DCHs and 478 non-DCHs surveyed, a total of 269 (67.4%) and 259 (54.2%) responded, respectively. Among the latter, 150 non-DCHs (31.4%) were included for analyses where surgery, chemotherapy, and radiation therapy were performed within the same hospitals to ensure comparability. The hospital's demographic data are summarized in Table 1.

Major IOP indicators (Table 2)
More than 90% of the DCHs had full-time PC staff (91.5% vs. 42.0%), interdisciplinary PC team (a team of two or more occupations) (98.5% vs. 90.0%), and outpatient clinics (95.2% vs. 58.0%), and the rates were significantly higher than that in non-DCHs. Routine symptom screening was performed in more than half of the DCHs (65.1% vs. 34.7%); however, routine documentation of advanced care planning was performed in < 40% in both types of hospitals (39.0% vs. 28.7%). Automatic trigger for PC referral was also employed in < 40% of surveyed hospitals (time trigger, 14.9% vs. 15.3%; needs trigger, 37.5% vs. 27.3%).

Education and research IOP indicators (Table 4)
Education opportunity of PC for oncologists was limited in both types of hospitals (e.g., routine rotation in PC, 8.2% vs. 2.0%); and education opportunity on oncology for PC physicians was also limited (e.g., routine rotation in oncology, 9.7% vs. 1.3%). Research opportunity was more frequent in DCHs, but still far limited in both types of hospitals (e.g., tenured faculty in PC, 3.3% vs. 1.3%).

Executive physicians' perspectives toward IOP (Additional file 1)
A total of ≥70% executive physicians in both types of hospitals did not regard their primary PC (PC services which was provided by the primary physicians and nurses) as good enough (74.7% vs. 75.3%). They also indicated that IOP encouragement would be beneficial for their patients (95.9% vs. 94.7%) and not be costly for their hospitals (29.4% vs. 33.3%). However, many hospitals were facing challenges to allocate more staff to provide PC services (75.5% vs. 86.7%). More than half of hospitals were planning to facilitate early referral to PC services (54.6% vs. 60.0%).

Qualitative analysis of free text query
In total, 106 (26.6%) DCHs and 68 (14.2%) non-DCHs responded to the free text query. Summarized data is presented in Additional files 2, 3 and 4. Three major categories were generated: perception toward IOP, challenges to encourage IOP, and solutions to encourage IOP. The typical perception was that enhancing the primary PC service is vital due to the large estimated number of patients with PC needs as compared with the available specialized PC service, although the importance of IOP, in general, was recognized.

Discussion
This nationwide survey comprehensively investigated the current status and executive physicians' perspectives of IOP in Japan. From 2007, the Ministry of Health, Labor, and Welfare has presented several mandatory requirements for DCH certification, such as referral criteria for PC services, institutionally accepted symptom management guidelines, and routine PC screening, and many of these requirements overlapped with the surveyed IOP indicators. Thus, the current IOP status at DCHs was found to be highly satisfied with respect to the clinical structure and process indicators even as compared with the previous literature in the European and North American countries [6,15,[17][18][19][20]. For instance, outpatient PC service availability was equivalent to European Society for Medical Oncology (ESMO)-designated centers (DCs) (e.g., Japan DCHs vs. ESMO DCs: outpatient clinic available 95% vs. 89%; same-day outpatient consultation available, 79% vs. 82%) [6]. This supported the promising role of the government to disseminate quality care nationwide.
Our survey also found that research and education opportunities were seriously limited at the vast majority of cancer hospitals. Continuing education for attending physicians was held in more than half of the facilities in ESMO DCs, whereas more than half of Japanese hospitals did not have opportunities for continuing education [6]. Mutual rotation training opportunities for fellows were also limited between oncology and PC departments. Research infrastructure was also extremely limited, with  levels similar to those in the USA in 2010 [15] (e.g., institutional funding for palliative oncology research, 19% in Japan vs. 13% in the USA). As education and research activities across the specialty can promote smooth coordination among healthcare professionals [24][25][26], further efforts to develop education and research infrastructures (e.g. employing tenured or full-time PC faculty who engages the education and research) are valuable. Most leaders in cancer hospitals recognized IOP as beneficial and reasonable for their cancer patients. They also planned to facilitate early referral of cancer patients to PC services. Meanwhile, they were facing challenges  in recruiting specialized PC staff and less likely planned to employ more PC staff. Accordingly, the current specialized PC staff seemed to be overwhelmed by the routine clinical practice and had actual difficulties to implement more IOPs. Lack of PC resources is a wellknown barrier for IOP, and our qualitative analysis also supported this situation [27][28][29]. Given that enrichment of PC resources is unrealistic, enhancing the primary PC provided by oncologists to effectively optimize existing resources such as standardized care pathway may be valuable [1].
This study had several limitations. First, as target respondents were executive physicians in oncology departments, it was not evident whether several IOP indicators actually work in routine practice. Detailed analysis of how those indicators work in practice would help determine the optimal clinical IOP models. Second, as the target hospitals were restricted to those providing three cancer treatment modalities (i.e., surgery, radiation therapy, and chemotherapy), the results in these analyses cannot be generalized in smaller hospitals. Third, owning to the exploratory