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Caring Advanced Cancer Patients at Home During COVID-19 Outbreak: Burnout and Psychological Morbidity Among Palliative Care Professionals in Italy

      Abstract

      Context

      Providing palliative care (PC) at home for patients with advanced cancer has become essential during the COVID-19 emergency. Nevertheless, the home PC professionals (PCPs) faced a challenging situation because of increased number of discharged patients, reduced availability of health-care facilities, and physical/relational barriers between them and patients.

      Objectives

      This study aimed to investigate the impact of COVID-19 pandemic on burnout and psychological morbidity among home PCPs in Italy.

      Methods

      One hundred and ninety-eight PC physicians and nurses working in home assistance in Italy were invited to participate. The results obtained by the investigation conducted during the COVID-19 emergency (COVID2020) were compared with data collected in 2016 in the same setting (BURNOUT2016). The questionnaires (socio-demographics, Maslach Burnout Inventory and General Health Questionnaire-12) were the same for both the surveys. The PCPs participating in COVID2020 survey (n = 145) were mostly the same (70%) who participated in the BURNOUT2016 study (n = 179).

      Results

      One hundred and forty-five PCPs participated in the study (response rate 73.2%). During the COVID-19 emergency, home PCPs presented a lower burnout frequency (P < .001) and higher level of personal accomplishment than in 2016 (P = .047). Conversely, the risk for psychological morbidity was significantly higher during the pandemic (P < .001).

      Conclusions

      In the age of COVID-19, the awareness of being at the forefront of containing the pandemic along with the sense of responsibility toward their high-risk patients may arouse PCPs' psychological distress, but, on the other hand, this condition may improve their sense of professional satisfaction and personal accomplishment.

      Key Words

      Key message

      This article investigates burnout and psychological morbidity among Italian palliative care professionals during the COVID-19 pandemic. Results indicate being at the forefront of containing the pandemic may arouse palliative care professionals' psychological distress, but, on the other hand, this condition may improve their sense of professional satisfaction and personal accomplishment.

      Introduction

      COVID-19, caused by novel coronavirus severe acute respiratory syndrome coronavirus-2, emerged in Wuhan, China, in December 2019. On March 11th, it was declared a pandemic by the World Health Organization.
      General’s opening remarks at the media briefing on COVID-19 [Internet]. World Health Organization.
      The Italian outbreak began on February 21st in the Lombardy region (northern Italy) and rapidly diffused across the country, tragically overwhelming the National Health Care System capacity.
      Coronavirus disease 2019 (COVID-19) situation report [Internet]. World Health Organization.
      ,
      Confermato caso italiano: a Milano situazione simile a quella della Germania
      Adottate le misure tra più restrittive previste in caso di focolaio epidemico. [Internet]. Istituto Superiore di Sanità.
      During the pandemic, home supportive and palliative care (PC) for patients with advanced cancer have been even more essential to limit the extent of the disease, reducing admissions to hospitals, maintaining symptom control, and ensuring psychological support for patients and family.
      • Nouvet E.
      • Sivaram M.
      • Bezanson K.
      • et al.
      Palliative care in humanitarian crises: a review of the literature. J Int Humanit Action [Internet].
      No less significant, PC professionals (PCPs) used their communication skills to talk appropriately with patients and their family, where the fear and the anxiety due to this period might worsen symptoms.
      HOW TO COMMUNICATE WITH FAMILIES LIVING IN COMPLETE ISOLATION [Internet]. SIAARTI - Aniarti - SICP - SIMEU.
      With the spread of the pandemic and the lockdown in Italy, home PCPs had to face with a challenging situation because of increased number of discharged patients and, at the same time, reduced availability of health-care facilities.
      • Porzio G.
      • Cortellini A.
      • Bruera E.
      • et al.
      Home care for cancer patients during COVID-19 pandemic: the Double triage protocol.
      • Boccia S.
      • Ricciardi W.
      • Ioannidis J.P.A.
      What other Countries can Learn from Italy during the COVID-19 pandemic.
      • Costantini M.
      • Rabitti E.
      • Beccaro M.
      • et al.
      Validity, reliability and responsiveness to change of the Italian palliative care outcome scale: a multicenter study of advanced cancer patients Cancer palliative care.
      In addition, the poor knowledge about the virus, the lack of personal protective equipment, and the procedures to reduce the risk of infection have created physical and relational barriers between PCPs and patients.
      • Indolfi C.
      • Spaccarotella C.
      The outbreak of COVID-19 in Italy.
      ,
      • Nacoti M.
      • Ciocca A.
      • Giupponi A.
      • et al.
      At the Epicenter of the Covid-19 pandemic and humanitarian crises in Italy: Changing Perspectives on Preparation and Mitigation.
      Consequently, the PCP's daily work routine became slower, more complex, and more demanding. Anxiety, overwork, and isolation can cause worrying consequences that negatively impact on their physical and psychological well-being, leading to burnout syndrome and other mental health concerns.
      • Pappa S.
      • Ntella V.
      • Giannakas T.
      • Giannakoulis V.G.
      • Papoutsi E.
      • Katsaounou P.
      Prevalence of depression, anxiety, and insomnia among healthcare workers during the COVID-19 pandemic: a systematic review and meta-analysis.
      Stressful events might otherwise result in individual growth, involving individual resources and fostering personal accomplishment (PA).
      Burnout syndrome is defined as a state of mental and/or physical exhaustion caused by prolonged exposure to excessive and prolonged work-related stress and has become a relevant and widely described psychosocial problem among PCPs.
      • Dunwoodie D.A.
      • Auret K.
      Psychological morbidity and burnout in palliative care doctors in Western Australia.
      • Martins Pereira S.
      • Fonseca A.M.
      • Sofia Carvalho A.
      Burnout in palliative care: a systematic review.
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.
      • Koh M.Y.H.
      • Chong P.H.
      • Neo P.S.H.
      • et al.
      Burnout, psychological morbidity and use of coping mechanisms among palliative care practitioners: a multi-centre cross-sectional study.
      Burnout in health-care professionals has been frequently associated to psychological morbidity, a dimension that may early indicate the onset of major depressive, anxiety, and somatization disorders.
      • Dunwoodie D.A.
      • Auret K.
      Psychological morbidity and burnout in palliative care doctors in Western Australia.
      ,
      • Koh M.Y.H.
      • Chong P.H.
      • Neo P.S.H.
      • et al.
      Burnout, psychological morbidity and use of coping mechanisms among palliative care practitioners: a multi-centre cross-sectional study.
      • Mampuya W.A.
      • Matsuo Y.
      • Nakamura A.
      • Hiraoka M.
      Evaluation of the prevalence of burnout and psychological morbidity among radiation oncologist members of the Kyoto Radiation Oncology Study Group (KROSG).
      • Grassi L.
      • Magnani K.
      Psychiatric morbidity and burnout in the medical profession: an Italian study of general practitioners and hospital physicians.
      The aim of the present study was to investigate the impact of COVID-19 pandemic on burnout and psychological morbidity in home PCPs in Italy. Physicians and nurses working in PC setting from high- and low-impact areas of COVID-19 infections were enrolled in this survey to provide a comprehensive picture of the Italian situation. To describe the variation due to the COVID-19 emergency, we have compared these results with our previous survey,
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.
      carried out four years ago on a similar sample of PCPs.

      Methods

      Study Design and Sample

      The participants were PCPs (physicians and nurses) working for the National Tumor Assistance (ANT) in 11 Italian regions. ANT is a nonprofit organization, which has been providing since 1978 free-of-charge specialized PC at home to patients with advanced cancer. The results obtained by the investigation conducted on the PCPs during the COVID-19 emergency (COVID2020) have been compared with data collected on the PCPs working in the same organization in 2016 (BURNOUT2016) and partially published in 2019.
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.
      The questionnaires were the same for both the studies. Based on the changes in the composition of the ANT staff during the last four years, we can assume that the PCPs participating in COVID2020 survey were mostly the same (70%) who participated in the BURNOUT2016 study. No specific exclusion criteria were set, with the exception of the PCPs who declined participation. The research was carried out in full accordance with the Declaration of Helsinki and the Good Clinical Practice. Participants provided the informed consent to the investigation, data analysis, and publication.

      COVID2020

      The survey was conducted during the phase II of the lockdown for the COVID-19 outbreak in Italy, and data were collected from May 11th to June 2nd, 2020. All the PCPs (n = 198) working in ANT were invited to participate by an email explaining the aim and the method of the research and reporting the link to the questionnaires. The data were anonymously collected on a web-based platform (www.survio.com), and the answers were analyzed using the Survio analyzing tool. The investigation was approved by the Ethical Committee of the Central Area of Emilia Romagna (619–2020-OSS-AUSLBO).

      BURNOUT2016
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.

      The survey was performed between May and June 2016. All the PCPs working in ANT (n = 212) were invited to participate by the ANT psychologists during the ordinary meetings of the teams. The data were anonymously collected on paper questionnaires. The investigation was approved by the Ethical Committee Interaziendale Bologna-Imola-CE-BI (16028; Prot. N.504/CE).

      Measures

      Socio-demographic and Professionals Data

      Data about gender, age, marital status, offspring, profession, years of experience in PC, and geographical area of work were collected.

      Maslach Burnout Inventory
      • Maslach C.
      • Jackson S.E.
      The measurement of experienced burnout.

      Burnout was measured by the Italian version of the Maslach Burnout Inventory (MBI). The questionnaire consists of 22 items investigating different aspects of burnout syndrome ascribable to 3 specific dimensions: emotional exhaustion (EE, 9 items), depersonalization (DP, 5 items), and PA (8 items). EE refers to an excessive emotional engagement that leads to a feeling of draining and loss of personal resources and energy, DP describes a negative attitude of detachment from work and patients, and a low level of PA is defined as a sense of failure and incompetence and is characterized by a decrease in own desire of success. The answers are graded on a 7-point scale from 0 (never) to 6 (everyday). The results of the MBI were analyzed using 3 different methods: 1) The score obtained in each subscale was considered as continuous variable (i.e., mean score); 2) the frequency of PCPs showing burnout symptoms as high level for EE and DP and low level of PA was assessed according the cutoff (EE ≥ 24, DP ≥ 9, PA ≤ 29) reported by the Italian Maslach Manual
      • Sirigatti S.
      • Stefanile C.
      MBI Maslach Burnout Inventory: adattamento e taratura per l’Italia.
      ; 3) the frequency of PCPs showing burnout was defined as high level of EE (>27) and/or high level of DP (>10). The frequency of PCPs with a low sense of PA (<31) was separately considered.
      • Shanafelt T.D.
      • Boone S.
      • Tan L.
      • et al.
      Burnout and satisfaction with work-life Balance among US physicians relative to the general US Population.
      The latter is the most commonly used method.
      • Reddy S.K.
      • Yennu S.
      • Tanco K.
      • et al.
      Frequency of burnout among palliative care physicians participating in a continuing medical education Course.

      General Health Questionnaire-12 Items
      • Endicott J.
      • Nee J.
      • Harrison W.
      • Blumenthal R.
      Quality of life Enjoyment and satisfaction questionnaire: a new measure.
      ,
      • Politi P.L.
      • Piccinelli M.
      • Wilkinson G.
      Reliability, validity and factor structure of the 12-item General Health Questionnaire among young males in Italy.

      General Health Questionnaire 12 (GHQ-12) is a self-report questionnaire whose aim is to identify the risk of developing psychological morbidity in general population. Items are rated on 4-point Likert scale from 0 to 3. The results of GHQ-12 were analyzed both as a continuous variable (i.e., mean total score) and as a dichotomous variable considering the PCPs with a total score higher than 19 as showing psychological morbidity.

      Statistical Methods

      According the normality test Shapiro-Wilk, the scores obtained from the MBI and GHQ-12 questionnaires were not normally distributed; thus, nonparametric tests were applied. The comparison of the MBI subscale scores and GHQ-12 total score between PCPs participating in the two studies was analyzed by Mann-Whitney U test, the distribution of PCPs showing burnout symptoms (MBI), and psychological morbidity (GHQ-12) as well as the overlap between the two conditions were compared between the studies by Chi square test.
      The potential predictors (socio-demographics [marital status, offspring]; professional data [profession, years of experience in PC, and geographical area of work]; psychological morbidity [GHQ-12 score]) for burnout symptoms (EE, DP, and PA subscale scores) were investigated by linear regression models adjusted for age and gender. The P values of the association analysis were adjusted by the Benjamini-Hockberg correction for multiple testing with a false discovery rate of .05.
      The significance threshold was set at .05. A statistical analysis was executed by the English version of SPSS 25 for Windows.

      Results

      The present study considered the sample of PCPs responding to the BURNOUT2016 survey (179 out of 212 PCPs, response rate 84.4%) and the sample of PCPs responding to the COVID2020 survey (145 out of 198, response rate 73.2%). All the participants have been working in the home PC program for patients with advanced cancer over the Italian territory.
      Table 1 presents a summary of the demographic and professional characteristics of the enrolled PCPs. The BURNOUT2016 sample consisted of 104 physicians (58%) and 75 nurses (42%) while the COVID2020 sample included 77 physicians (53%) and 68 nurses (47%). For both the surveys, most of the participants were female (67% and 68%, respectively), married or cohabitant (65% and 53%, respectively), with children (55% and 52%, respectively), and the average age was 42 years. The distribution according the experience in PC and the geographical area of work is quite similar between the participants of BURNOUT2016 and COVID2020 surveys (Table 1).
      Table 1Socio-demographic and Professional Characteristics of PCPs Working in ANT Participating in BURNOUT2016 and COVID2020 Surveys
      StudyBURNOUT2016COVID2020BURNOUT2016COVID2020BURNOUT2016COVID2020
      ProfessionPCPs, n = 179PCPs, n = 145Physicians, n = 104Physicians, n = 77Nurses, n = 75Nurses, n = 68
      Gender
       Men59 (33%)47 (32%)38 (36%)28 (36%)21 (28%)19 (28%)
       Women120 (67%)98 (68%)66 (64%)49 (64%)54 (72%)49 (72%)
      Age, mean (±St.Dev)42 (±11)42 (±12)45 (±10)48 (±10)37 (±11)36 (±10)
      Marital status
       Unmarried50 (28%)59 (41%)20 (19%)19 (25%)30 (40%)40 (59%)
       Married/cohabitant117 (65%)77 (53%)77 (74%)51 (66%)40 (53%)26 (38%)
       Separated/divorced10 (6%)9 (6%)6 (6%)7 (9%)4 (5%)2 (3%)
       Widowed2 (1%)1 (1%)1 (1%)
      With children
       Yes98 (55%)75 (52%)62 (60%)48 (62%)36 (48%)27 (40%)
       No81 (45%)70 (48%)42 (40%)29 (38%)39 (52%)41 (60%)
      Years of work in palliative care
       <2 years49 (27%)27 (19%)25 (24%)10 (13%)24 (32%)17 (25%)
       2-5 years47 (26%)40 (28%)22 (21%)18 (23%)25 (33%)22 (32%)
       6-10 years27 (15%)23 (16%)16 (15%)11 (14%)11 (15%)12 (18%)
       >10 years56 (31%)55 (38%)41 (39%)38 (49%)15 (20%)17 (25%)
      Geographical area of work
      Northern Italy (Emilia-Romagna and Lombardia); Central Italy (Tuscany, Umbria, Marche, Lazio); Southern Italy (Campania, Basilicata and Puglia).
       Northern Italy70 (39%)49 (34%)41 (39%)28 (36%)29 (39%)21 (31%)
       Central Italy32 (18%)32 (22%)21 (20%)17 (22%)11 (15%)15 (22%)
       Southern Italy77 (43%)64 (44%)42 (40%)32 (42%)35 (47%)32 (47%)
      ANT = National Tumor Assistance; PCPs = palliative care professionals.
      a Northern Italy (Emilia-Romagna and Lombardia); Central Italy (Tuscany, Umbria, Marche, Lazio); Southern Italy (Campania, Basilicata and Puglia).
      Table 2 showed the comparison of the level of burnout of the PCPs between the two studies according three different methods: 1) Considering the MBI subscale scores as continuous variables, the PCPs of COVID2020 showed lower level of DP (P < .001) and higher level of PA (P < .001) than BURNOUT2016. These results were confirmed also dividing physicians and nurses (P < .001 for both professions). 2) Analyzing the frequency of burnout according the cutoff from the Italian Maslach Manual,
      • Sirigatti S.
      • Stefanile C.
      MBI Maslach Burnout Inventory: adattamento e taratura per l’Italia.
      PCPs showing burnout symptoms on DP and PA dimension were less numerous in COVID2020 than in the BURNOUT2016 (for DP: 26.1% vs. 65.9%, P < .001; for PA 11.9% vs. 22.3%, P = .018). The lower frequency of DP in COVID2020 study was confirmed also considering physicians and nurses separately (P < .001 for both professions). 3) According to the definition criteria described by Shanafelt et al.,
      • Shanafelt T.D.
      • Boone S.
      • Tan L.
      • et al.
      Burnout and satisfaction with work-life Balance among US physicians relative to the general US Population.
      31 PCPs (22.0%) participating in COVID2020 showed burnout compared with the 82 PCPs involved in BURNOUT2016 (45.8%) (P < .001). The separate analysis of physicians and nurses confirmed the lower burnout frequency in the COVID2020 than that in the BURNOUT2016 (P < .001 for physicians, P = .008 for nurses). The frequency of PCPs with a low sense of PA was lower in COVID2020 (25 PCPs, 17.2%) than that in BURNOUT2016 (48 PCPs, 26.8%) (P = .047).
      Table 2MBI Subscale Scores and Frequency of Burnout Among PCPs Working in ANT Participating in BURNOUT2016 and COVID2020 Surveys
      StudyBURNOUT2016COVID2020BURNOUT2016COVID2020BURNOUT2016COVID2020
      ProfessionPCPs, n = 179PCPs, n = 145Physicians, n = 104Physicians, n = 75Nurses, n = 75Nurses, n = 68
      MBI subscale scores, mean (±St.Dev.)P
      Statistical analysis compared the MBI subscale scores between PCPs participating to the two studies by Mann-Whitney U Test.
      P
      Statistical analysis compared the MBI subscale scores between PCPs participating to the two studies by Mann-Whitney U Test.
      P
      Statistical analysis compared the MBI subscale scores between PCPs participating to the two studies by Mann-Whitney U Test.
       Emotional exhaustion (EE)13.7 (±8.1)12.7 (±7.2).20014.5 (±8.7)13.3 (±7.6).47012.7 (±7.0)11.8 (±6.5).306
       Depersonalization (DP)10.2 (±4.5)7.1 (±4.6)<.00110.4 (±4.7)7.0 (±4.6)<.0019.9 (±4.2)7.1 (±4.7)<.001
       Personal accomplishment (PA)33.3 (±5.5)36.4 (±6.1)<.00133.2 (±5.3)36.5 (±6.2)<.00133.4 (±5.7)36.4 (±6.1)<.001
      PCPs showing burnout symptoms, n (%)
      Cutoff from the Italian Maslach manual by Sirigatti and Stefanile, 1993(19).
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
       High level of EE (≥24)20 (11.2%)12 (8.4%).40715 (14.4%)7 (9.2%).3605 (6.7%)5 (7.5%).853
       High level of DP (≥9)118 (65.9%)37 (26.1%)<.00169 (66.3%)15 (19.5%)<.00149 (65.3%)22 (33.8%)<.001
       Low level of PA (≤29)40 (22.3%)17 (11.9%).01820 (19.2%)8 (10.5%).14520 (26.7%)9 (13.4%).062
      PCPs showing burnout, n (%)
      Criteria used by Shanafelt et al., 2012(20).
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
      P
      Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
       EE > 27 and/or DP > 1082 (45.8%)31 (22.0%)<.00146 (44.2%)14 (18.4%)<.00136 (48.0%)17 (26.2%).008
       Low level of PA (<31)48 (26.8%)25 (17.2%).04725 (24%)12 (15.6%).17623 (30.7%)13 (19.1%).124
      ANT = National Tumor Assistance; MBI = Maslach Burnout Inventory; PCPs = palliative care professionals.
      a Statistical analysis compared the MBI subscale scores between PCPs participating to the two studies by Mann-Whitney U Test.
      b Statistical analysis compared the distribution of PCPs showing burnout symptoms between PCPs participating to the two studies by Chi square test.
      c Cutoff from the Italian Maslach manual by Sirigatti and Stefanile, 1993(19).
      d Criteria used by Shanafelt et al., 2012(20).
      Table 3 reported the evaluation of psychological morbidity of the PCPs participating to the two surveys. Analyzing the GHQ-12 score as a continuous variable, psychological morbidity was significantly higher in PCPs of the COVID2020 than in BURNOUT2016 (P < .001), and this result was confirmed considering physicians and nurses separately (P = .004 for physicians and P < .001 for nurses). Sixty-eight PCPs (45.1%) participating in COVID2020 showed psychological morbidity comparable to the 28 PCPs (15.6%) of BURNOUT2016 (P < .001). The higher frequency of psychological morbidity among COVID2020 participants was confirmed by the separate analysis of physicians and nurses (P < .001 for both professions).
      Table 3GHQ-12 Score and Frequency of Psychological Morbidity Among PCPs Working in ANT Participating to BURNOUT2016 and COVID2020 Surveys
      StudyBURNOUT2016COVID2020PBURNOUT2016COVID2020PBURNOUT2016COVID2020P
      PCPs, n = 179PCPs, n = 145Physicians, n = 104Physicians, n = 75Nurses, n = 75Nurses, n = 68
      GHQ-12 score, mean (±St.Dev.)15.9 (±3.9)18.2 (±4.5)<.001
      Statistical analysis compared the GHQ-12 score between PCPs participating to the two studies by Mann-Whitney U Test.
      16.4 (±3.7)18.2 (±4.9).004
      Statistical analysis compared the GHQ-12 score between PCPs participating to the two studies by Mann-Whitney U Test.
      15.1 (±3.9)18.3 (±4.1)<.001
      Statistical analysis compared the GHQ-12 score between PCPs participating to the two studies by Mann-Whitney U Test.
      PCPs showing psychological morbidity, n (%)28 (15.6%)64 (45.1%)<.001
      Statistical analysis compared the distribution of PCPs showing psychological morbidity (GHQ-12 score > 19) between PCPs participating to the two studies by Chi square test.
      19 (18.3)34 (45.9%)<.001
      Statistical analysis compared the distribution of PCPs showing psychological morbidity (GHQ-12 score > 19) between PCPs participating to the two studies by Chi square test.
      9 (12.0%)30 (45.9%)<.001
      Statistical analysis compared the distribution of PCPs showing psychological morbidity (GHQ-12 score > 19) between PCPs participating to the two studies by Chi square test.
      ANT = National Tumor Assistance; GHQ-12 = General Health Questionnaire 12; PCPs = palliative care professionals.
      a Statistical analysis compared the GHQ-12 score between PCPs participating to the two studies by Mann-Whitney U Test.
      b Statistical analysis compared the distribution of PCPs showing psychological morbidity (GHQ-12 score > 19) between PCPs participating to the two studies by Chi square test.
      The linear regression models failed to identify potential predictors of burnout among the socio-demographic and professional variables (age, gender, marital status, offspring, profession, years of experience in PC, geographical area of work) both for COVID2020 and BURNOUT2016 surveys (data not shown).
      Table 4 displayed the linear regression models showing the association between psychological morbidity (GHQ-12 score) and burnout dimensions (EE, DP, and PA subscale scores) adjusted for age and gender in PCPs participating in COVID2020 and BURNOUT2016 studies. The level of psychological morbidity was significantly associated with the burnout dimensions in both the surveys with very similar coefficient (for EE: β coefficient = .403, P < .001 in BURNOUT2016 and β coefficient = .417, P < .001 in COVID2020; for DP: β coefficient = .372, P < .001 in BURNOUT2016 and β coefficient = .253, P < .001 in COVID2020; for PA: β coefficient = −.206, P = .006 in BURNOUT2016 and β coefficient = −219, P = .009 in COVID2020). Among COVID2020 participants, 23 out of the 31 PCPs (74.2%) showing burnout displayed also psychological morbidity, while in the BURNOUT2016 study, this percentage was significantly lower (19 out of 82 PCPs [23.2%] showed both burnout and psychological morbidity; P < .001). Among COVID2020 participants, all the PCPs with EE (n = 12) showed psychological morbidity, while in the BURNOUT2016 study, only 8 out of the 20 (20%) PCPs with EE showed also psychological morbidity (P < .001).
      Table 4Linear Regression Models Showing the Association Between Psychological Morbidity (GHQ-12 Score, Independent Variable) and Burnout Dimensions (EE, DP, and PA Subscale Scores, Dependent Variables) Adjusted for Age and Gender in PCPs Participating in BURNOUT2016 and COVID2020 Surveys
      MBI DimensionBURNOUT2016COVID2020
      β Coeff. (95% CI)Pβ Coeff. (95% CI)P
      EE.403 (.550/1.125)<.001.417 (.4200/.902)<.001
      DP.372 (.267/.593)<.001.253 (.095/.428)<.001
      PA−.206 (−.499/ −.083).006−.219 (−.522/ −.077).009
      DP = depersonalization; EE = emotional exhaustion; MBI = Maslach Burnout Inventory; PA = personal accomplishment; PCPs = palliative care professionals.

      Discussion

      Until now, very few studies have explored the psychological status of PCPs during COVID-19 pandemic,
      • Reddy S.K.
      • Yennu S.
      • Tanco K.
      • et al.
      Frequency of burnout among palliative care physicians participating in a continuing medical education Course.
      and no studies have compared the burnout level during the age of COVID-19 with the psychological conditions of PC staff in a period before the pandemic. The available literature reported a lower burnout levels for PCPs than for other medical discipline.
      • Dunwoodie D.A.
      • Auret K.
      Psychological morbidity and burnout in palliative care doctors in Western Australia.
      ,
      • Shanafelt T.D.
      • West C.P.
      • Sinsky C.
      • et al.
      Changes in burnout and satisfaction with work-life integration in physicians and the general US working Population between 2011 and 2017.
      • Ramirez A.
      • Graham J.
      • Richards M.
      • et al.
      Burnout and psychiatric disorder among cancer clinicians.
      • Lepnurm R.
      • Lockhart W.S.
      • Keegan D.
      A measure of daily distress in Practising medicine.
      • Asai M.
      • Morita T.
      • Akechi T.
      • et al.
      Burnout and psychiatric morbidity among physicians engaged in end-of-life care for cancer patients: a cross-sectional nationwide survey in Japan.
      Two recent studies
      • Reddy S.K.
      • Yennu S.
      • Tanco K.
      • et al.
      Frequency of burnout among palliative care physicians participating in a continuing medical education Course.
      ,
      • Kamal A.H.
      • Bull J.H.
      • Wolf S.P.
      • et al.
      Prevalence and predictors of burnout among hospice and palliative care clinicians in the U.S.
      reported a burnout frequency among PCPs of about 38%, while the prevalence of burnout widely ranged in the previous literature, based on work context, characteristics of the health-care professionals, and coping strategies.
      • Martins Pereira S.
      • Fonseca A.M.
      • Sofia Carvalho A.
      Burnout in palliative care: a systematic review.
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.
      • Koh M.Y.H.
      • Chong P.H.
      • Neo P.S.H.
      • et al.
      Burnout, psychological morbidity and use of coping mechanisms among palliative care practitioners: a multi-centre cross-sectional study.
      In their study, Koh et al.
      • Koh M.Y.H.
      • Chong P.H.
      • Neo P.S.H.
      • et al.
      Burnout, psychological morbidity and use of coping mechanisms among palliative care practitioners: a multi-centre cross-sectional study.
      found a higher risk of burnout (36.9%) for PCPs who worked in home care setting than in other setting (hospice or hospital). In a health emergency situation, the psychological stress level of health workers is expected to increase, thus facilitating the onset of burnout and other distress-related syndromes.
      • Pappa S.
      • Ntella V.
      • Giannakas T.
      • Giannakoulis V.G.
      • Papoutsi E.
      • Katsaounou P.
      Prevalence of depression, anxiety, and insomnia among healthcare workers during the COVID-19 pandemic: a systematic review and meta-analysis.
      ,
      • Adibe B.
      • Perticone K.
      • Hebert C.
      Creating Wellness in a pandemic: a Practical Framework for health systems responding to Covid-19.
      During COVID-19 pandemic, health-care workers have faced many difficulties such as the risk of infection, excessive workload, relationship constraints, and lack of medical guidelines and available protocols.
      • Adams J.G.
      • Walls R.M.
      Supporting the health care Workforce during the COVID-19 global Epidemic.
      • Lai J.
      • Ma S.
      • Wang Y.
      • et al.
      Factors associated with mental health Outcomes among health care workers exposed to coronavirus disease 2019.
      • Costantini M.
      • Sleeman K.E.
      • Peruselli C.
      • Higginson I.J.
      Response and role of palliative care during the COVID-19 pandemic: a national telephone survey of hospices in Italy.
      Considering that the data about the burnout prevalence in PC are not univocal and strictly dependent on different settings, inferring the burden of the pandemic on the PCPs' psychological status results in a very demanding challenge. For this reason, the present study for the first time aimed to compare burnout level during COVID-19 emergency with MBI scores of a similar sample collected four years ago
      • Ercolani G.
      • Varani S.
      • Peghetti B.
      • et al.
      Burnout in home palliative care: what is the role of coping strategies?.
      in the same home PC service.
      Surprisingly, providing home PC in the age of COVID-19 seemed to lead to a lower burnout level than before the pandemic. In particular, the DP score was significantly lower during outbreak than that four years ago. Consistently, PA score was higher in the sample forced to face the COVID-19. Similar unexpected findings have been recently attained in a study where most of the health-care professionals interviewed strongly disagree that they feel more burnout during COVID-19 than before the outbreak.
      • Wu Y.
      • Wang J.
      • Luo C.
      • et al.
      A comparison of burnout frequency among oncology physicians and nurses working on the Frontline and Usual Wards during the COVID-19 Epidemic in Wuhan, China.
      On the contrary, psychological morbidity, as measured by the GHQ-12 questionnaire, was worse during the pandemic than in routine work under standard conditions. Psychological morbidity was significantly associated with the three dimensions of burnout, confirming data from previous studies.
      • Dunwoodie D.A.
      • Auret K.
      Psychological morbidity and burnout in palliative care doctors in Western Australia.
      ,
      • Mampuya W.A.
      • Matsuo Y.
      • Nakamura A.
      • Hiraoka M.
      Evaluation of the prevalence of burnout and psychological morbidity among radiation oncologist members of the Kyoto Radiation Oncology Study Group (KROSG).
      ,
      • Grassi L.
      • Magnani K.
      Psychiatric morbidity and burnout in the medical profession: an Italian study of general practitioners and hospital physicians.
      ,
      • Koh S.J.
      • Keam B.
      • Hyun M.K.
      • et al.
      Cancer pain management education rectifies patients’ misconceptions of cancer pain, reduces pain, and improves quality of life.
      In the COVID2020 survey, we found a strong overlap between burnout, particularly for the EE dimension, and psychological morbidity.
      Some considerations may explain the results of this study. During the pandemic, the frequency of burnout decreased, and we can suppose that the crucial social role played by PCPs could have fostered their professional satisfaction. On the other hand, the few cases of burnout among PCPs facing with the COVID-19 showed also psychological morbidity, and this finding could be ascribed mainly to individual factors of emotional distress. Accordingly, our data have shown that during the global crisis, PCPs have maintained their capacity to find gratification from their work, and they have increased their sense of vocation promoting greater professional fulfilment.
      • Launer J.
      Burnout in the age of COVID-19.
      ,
      • Barello S.
      • Palamenghi L.
      • Graffigna G.
      Stressors and resources for healthcare professionals during the Covid-19 pandemic: Lesson Learned from Italy.
      In particular, recent studies reported a key role of PC in pandemics both for previously healthy people who had been severely infected by the virus and for patients with preceding life-threatening conditions.
      • Nouvet E.
      • Sivaram M.
      • Bezanson K.
      • et al.
      Palliative care in humanitarian crises: a review of the literature. J Int Humanit Action [Internet].
      ,
      • Costantini M.
      • Sleeman K.E.
      • Peruselli C.
      • Higginson I.J.
      Response and role of palliative care during the COVID-19 pandemic: a national telephone survey of hospices in Italy.
      ,
      • Radbruch L.
      • Knaul F.M.
      • de Lima L.
      • de Joncheere C.
      • Bhadelia A.
      The key role of palliative care in response to the COVID-19 tsunami of suffering.
      PC is critical for improving symptom control, facilitating triage and difficult decision-making, and advancing communication with patients and families.
      • Nouvet E.
      • Sivaram M.
      • Bezanson K.
      • et al.
      Palliative care in humanitarian crises: a review of the literature. J Int Humanit Action [Internet].
      In order to guarantee, during the pandemic, the care of the seriously ill patients, many studies highlighted the particular need to enhance PC at home to prevent hospitalizations and to ensure continuity of care.
      • Costantini M.
      • Sleeman K.E.
      • Peruselli C.
      • Higginson I.J.
      Response and role of palliative care during the COVID-19 pandemic: a national telephone survey of hospices in Italy.
      ,
      • Chen T.-J.
      • Lin M.-H.
      • Chou L.-F.
      • Hwang S.-J.
      Hospice utilization during the SARS outbreak in Taiwan.
      ,
      • Etkind S.N.
      • Bone A.E.
      • Lovell N.
      • et al.
      The role and response of palliative care and hospice services in Epidemics and pandemics: a Rapid review to Inform Practice during the COVID-19 pandemic.
      Owing to their fragile condition, patients with cancer have to receive an overprotection from the risk of contracting COVID-19, both to guarantee their safety and to avoid additional burden of the health system.
      • Porzio G.
      • Cortellini A.
      • Bruera E.
      • et al.
      Home care for cancer patients during COVID-19 pandemic: the Double triage protocol.
      In this scenario, PCPs enrolled in our study may have felt at the forefront of containing the pandemic and keeping safe the vulnerable patients they care.
      • Wu Y.
      • Wang J.
      • Luo C.
      • et al.
      A comparison of burnout frequency among oncology physicians and nurses working on the Frontline and Usual Wards during the COVID-19 Epidemic in Wuhan, China.
      The awareness of being responsible for the safety of such high-risk patients may, on the one hand, had arouse PCPs' concerns and stress, but on the other hand, it could have strengthened their sense of professional satisfaction and PA. We can assume that in such a situation, they may have felt more emotionally close and involved with their patients, who had become even more frail, isolated, and suffering from the pandemic.
      • Radbruch L.
      • Knaul F.M.
      • de Lima L.
      • de Joncheere C.
      • Bhadelia A.
      The key role of palliative care in response to the COVID-19 tsunami of suffering.
      COVID-19 pandemic increased PCPs' distress because of work overload, fear of contagion, and difficulty in delivering effective PC despite isolation and necessary barrier precautions.
      • Adams J.G.
      • Walls R.M.
      Supporting the health care Workforce during the COVID-19 global Epidemic.
      ,
      • Lai J.
      • Ma S.
      • Wang Y.
      • et al.
      Factors associated with mental health Outcomes among health care workers exposed to coronavirus disease 2019.
      ,
      • Schwartz J.
      • King C.-C.
      • Yen M.-Y.
      Protecting healthcare workers during the coronavirus disease 2019 (COVID-19) outbreak: Lessons from Taiwan’s Severe Acute Respiratory syndrome response.
      On the other hand, the PCPs, playing a strategic role in the management of the health emergency, may acquire a pride that prevents DP and overcome the risk of burnout. It is possible that psychological distress might happen earlier and lead later to burnout. More research with longitudinal follow-up might be needed in future studies. When the emergency ceases, a further survey will be necessary to give a complete and exhaustive view of the long-term consequences of the COVID-19 pandemic on the PCPs. Our results highlighted the importance of acknowledging the key role of PC within the public health system, especially in an emergency context such as pandemics.
      • Nouvet E.
      • Sivaram M.
      • Bezanson K.
      • et al.
      Palliative care in humanitarian crises: a review of the literature. J Int Humanit Action [Internet].
      ,
      • Costantini M.
      • Sleeman K.E.
      • Peruselli C.
      • Higginson I.J.
      Response and role of palliative care during the COVID-19 pandemic: a national telephone survey of hospices in Italy.
      ,
      • Radbruch L.
      • Knaul F.M.
      • de Lima L.
      • de Joncheere C.
      • Bhadelia A.
      The key role of palliative care in response to the COVID-19 tsunami of suffering.
      ,
      • Powell V.D.
      • Silveira M.J.
      What should palliative Care’s response Be to the COVID-19 pandemic?.
      Nowadays it became evident that PC competence and skills, such as symptom control, psychological support for patients and families, breaking bad news, and end-of-life decision-making are essential in the public health context and not only in PC setting.
      • Costantini M.
      • Rabitti E.
      • Beccaro M.
      • et al.
      Validity, reliability and responsiveness to change of the Italian palliative care outcome scale: a multicenter study of advanced cancer patients Cancer palliative care.
      Working on a deeper PC integration in a broader community health-care context could improve PCPs' PA and professional satisfaction.
      • Tanzi S.
      • Alquati S.
      • Martucci G.
      • De Panfilis L.
      Learning a palliative care approach during the COVID-19 pandemic: a case study in an Infectious Diseases Unit.
      • Osman H.
      • Shrestha S.
      • Temin S.
      • et al.
      Palliative care in the global setting: ASCO Resource-Stratified Practice guideline.
      • Centeno C.
      • Sitte T.
      • de Lima L.
      • et al.
      White paper for global palliative care Advocacy: Recommendations from a PAL-LIFE expert Advisory Group of the Pontifical Academy for life, Vatican City.
      • Hui D.
      • Bruera E.
      Models of palliative care delivery for patients with cancer.
      • Radbruch L.
      • De Lima L.
      • Knaul F.
      • et al.
      Redefining palliative care—a new Consensus-based definition.
      • Tziraki C.
      • Grimes C.
      • Ventura F.
      • et al.
      Rethinking palliative care in a public health context: addressing the needs of persons with non-communicable chronic diseases.
      There is a wide range of literature on the relationship between health-care professionals' psychological health and quality of care.
      • Welp A.
      • Meier L.L.
      • Manser T.
      Emotional exhaustion and workload predict clinician-rated and objective patient safety.
      • Tawfik D.S.
      • Scheid A.
      • Profit J.
      • et al.
      Evidence relating health care provider burnout and quality of care a systematic review and meta-analysis.
      • Chen K.Y.
      • Yang C.M.
      • Lien C.H.
      • et al.
      Burnout, job satisfaction, and medical malpractice among physicians.
      • Williams E.S.
      • Manwell L.B.
      • Konrad T.R.
      • Linzer M.
      The relationship of organizational culture, stress, satisfaction, and burnout with physician-reported error and suboptimal patient care.
      DP, intended as an attitude of emotional disengagement from one's work, could increase the risk of medical errors and render difficult the adaptivity to change.
      • Welp A.
      • Meier L.L.
      • Manser T.
      Emotional exhaustion and workload predict clinician-rated and objective patient safety.
      ,
      • Demerouti E.
      • Bakker A.B.
      • Leiter M.
      Burnout and job performance: the moderating role of selection, optimization, and compensation strategies.
      Other studies reported an association between burnout and worst indicators of patient safety increasing the risk of adverse events.
      • Shanafelt T.D.
      • Boone S.
      • Tan L.
      • et al.
      Burnout and satisfaction with work-life Balance among US physicians relative to the general US Population.
      ,
      • Welp A.
      • Meier L.L.
      • Manser T.
      Emotional exhaustion and workload predict clinician-rated and objective patient safety.
      ,
      • Tawfik D.S.
      • Profit J.
      • Morgenthaler T.I.
      • et al.
      Physician burnout, well-being, and work Unit safety Grades in relationship to reported medical errors.
      ,
      • Chen Z.
      • Leng J.
      • Pang Y.
      • He Y.
      • Heng F.
      • Tang L.
      Demographic, occupational, and societal features associated with burnout among medical oncology staff members: cross-sectional results of a Cancer Center in Beijing, China.
      On the contrary, a greater PA makes PCPs feeling more self-efficacious in coping with patients' needs, encouraging them to take in charge challenging clinical tasks.
      • Welp A.
      • Meier L.L.
      • Manser T.
      Emotional exhaustion and workload predict clinician-rated and objective patient safety.
      Although the majority of evidence suggested a negative impact of burnout on the professional performance, the available literature did not provide clear evidence on the relationship between specific burnout dimensions and quality of care outcomes.
      • Tawfik D.S.
      • Scheid A.
      • Profit J.
      • et al.
      Evidence relating health care provider burnout and quality of care a systematic review and meta-analysis.
      ,
      • Dewa C.S.
      • Loong D.
      • Bonato S.
      • Trojanowski L.
      The relationship between physician burnout and quality of healthcare in terms of safety and acceptability: a systematic review.
      ,
      • Loerbroks A.
      • Glaser J.
      • Vu-Eickmann P.
      • Angerer P.
      Physician burnout, work engagement and the quality of patient care.
      Starting from these observations, it could be interesting to investigate if home PCPs may have provided a similar, or even better, quality of care during COVID-19 pandemic than in nonemergency situations.
      During the pandemic, the home PC organization did not improve the psychological support for the PCPs. The ordinary measures of support, such as the monthly supervision with an external expert psychologist and multidisciplinary weekly staff e-meeting with cases discussions, have been maintained during emergency period. A systematic regular monitoring of burnout and psychological morbidity among the PC staff could become a suitable strategy to identify early signal of distress and to develop additional intervention aimed at the maintenance of the PCPs' well-being. Further studies should be devoted to this issue.

      Study Limitation

      Our study has a number of limitations. This study is designed to describe the variation due to the COVID-19 emergency in the burnout frequency and psychological status of PCPs working at home in Italy. To this aim, the data obtained during a “normal” period of work have been used as reference. The PCPs participating in COVID2020 survey were mostly the same who participated to the BURNOUT2016 study, but it is worth noting that the composition of the ANT staff has undergone some inevitable changes in the last four years, especially concerning the nursing team. Regarding the physician staff, which has remained more stable, four more years of age and experience in home PC must be considered. It is also possible that improvement in other aspects of the working conditions might have resulted in the observed improvement in burnout rate. In addition, owing to the emergency period, the data-collection methods of the two surveys were different. In the BURNOUT2016, the questionnaires were filled on paper forms, while in the COVID2020 survey, the data were collected through an online platform. In both cases, the interviews were anonymous rendering impossible the execution of a paired data analysis.

      Conclusion

      The frequency of burnout among PCPs during the pandemic was significantly lower than 4 years before, while the severity of psychological distress was significantly worse. More research is needed to better characterize the impact of pandemics on health-care professionals.

      Disclosures and Acknowledgments

      The authors declare that they have no conflicts of interest.
      The authors received no financial support for the research, author-ship, and/or publication of this article.

      References

      1. General’s opening remarks at the media briefing on COVID-19 [Internet]. World Health Organization.
        (Available from)
      2. Coronavirus disease 2019 (COVID-19) situation report [Internet]. World Health Organization.
        (Available from)
        • Confermato caso italiano: a Milano situazione simile a quella della Germania
        Adottate le misure tra più restrittive previste in caso di focolaio epidemico. [Internet]. Istituto Superiore di Sanità.
        (Available from)
        https://bit.ly/2VRVasN
        Date: 2020
        Date accessed: October 10, 2020
        • Nouvet E.
        • Sivaram M.
        • Bezanson K.
        • et al.
        Palliative care in humanitarian crises: a review of the literature. J Int Humanit Action [Internet].
        (Available from)
      3. HOW TO COMMUNICATE WITH FAMILIES LIVING IN COMPLETE ISOLATION [Internet]. SIAARTI - Aniarti - SICP - SIMEU.
        ([cited 2020 Apr 18]. Available from)
        • Porzio G.
        • Cortellini A.
        • Bruera E.
        • et al.
        Home care for cancer patients during COVID-19 pandemic: the Double triage protocol.
        J Pain Symptom Manage. 2020; 60: e5-e7
        • Boccia S.
        • Ricciardi W.
        • Ioannidis J.P.A.
        What other Countries can Learn from Italy during the COVID-19 pandemic.
        JAMA Intern Med. 2020; 180: 927-928
        • Costantini M.
        • Rabitti E.
        • Beccaro M.
        • et al.
        Validity, reliability and responsiveness to change of the Italian palliative care outcome scale: a multicenter study of advanced cancer patients Cancer palliative care.
        BMC Palliat Care. 2016; 15: 1-12
        • Indolfi C.
        • Spaccarotella C.
        The outbreak of COVID-19 in Italy.
        JACC Case Rep. 2020; 2: 1414-1418
        • Nacoti M.
        • Ciocca A.
        • Giupponi A.
        • et al.
        At the Epicenter of the Covid-19 pandemic and humanitarian crises in Italy: Changing Perspectives on Preparation and Mitigation.
        Catal Innov Care Deliv. 2020;
        • Pappa S.
        • Ntella V.
        • Giannakas T.
        • Giannakoulis V.G.
        • Papoutsi E.
        • Katsaounou P.
        Prevalence of depression, anxiety, and insomnia among healthcare workers during the COVID-19 pandemic: a systematic review and meta-analysis.
        Brain Behav Immun. 2020; 88: 901-907
        • Dunwoodie D.A.
        • Auret K.
        Psychological morbidity and burnout in palliative care doctors in Western Australia.
        Intern Med J. 2007; 37: 693-698
        • Martins Pereira S.
        • Fonseca A.M.
        • Sofia Carvalho A.
        Burnout in palliative care: a systematic review.
        Nurs Ethics. 2011; 18: 317-326
        • Ercolani G.
        • Varani S.
        • Peghetti B.
        • et al.
        Burnout in home palliative care: what is the role of coping strategies?.
        J Palliat Care. 2020; 35: 46-52
        • Koh M.Y.H.
        • Chong P.H.
        • Neo P.S.H.
        • et al.
        Burnout, psychological morbidity and use of coping mechanisms among palliative care practitioners: a multi-centre cross-sectional study.
        Palliat Med. 2015; 29: 633-642
        • Mampuya W.A.
        • Matsuo Y.
        • Nakamura A.
        • Hiraoka M.
        Evaluation of the prevalence of burnout and psychological morbidity among radiation oncologist members of the Kyoto Radiation Oncology Study Group (KROSG).
        J Radiat Res. 2017; 58: 217-224
        • Grassi L.
        • Magnani K.
        Psychiatric morbidity and burnout in the medical profession: an Italian study of general practitioners and hospital physicians.
        Psychother Psychosom. 2000; 69: 329-334
        • Maslach C.
        • Jackson S.E.
        The measurement of experienced burnout.
        J Organ Behav. 1981; 2: 99-113
        • Sirigatti S.
        • Stefanile C.
        MBI Maslach Burnout Inventory: adattamento e taratura per l’Italia.
        in: MBI Maslach Burnout Inventory Manuale. OS Organizzazioni Speciali, Florence, Italy1993: 33-42
        • Shanafelt T.D.
        • Boone S.
        • Tan L.
        • et al.
        Burnout and satisfaction with work-life Balance among US physicians relative to the general US Population.
        Arch Intern Med. 2012; 172: 1377-1385
        • Reddy S.K.
        • Yennu S.
        • Tanco K.
        • et al.
        Frequency of burnout among palliative care physicians participating in a continuing medical education Course.
        J Pain Symptom Manage. 2020; 60: 80-86.e2
        • Endicott J.
        • Nee J.
        • Harrison W.
        • Blumenthal R.
        Quality of life Enjoyment and satisfaction questionnaire: a new measure.
        Psychopharmacol Bull. 1993; 29: 321-326
        • Politi P.L.
        • Piccinelli M.
        • Wilkinson G.
        Reliability, validity and factor structure of the 12-item General Health Questionnaire among young males in Italy.
        Acta Psychiatr Scand. 1994; 90: 432-437
        • Shanafelt T.D.
        • West C.P.
        • Sinsky C.
        • et al.
        Changes in burnout and satisfaction with work-life integration in physicians and the general US working Population between 2011 and 2017.
        Mayo Clin Proc. 2019; 94: 1681-1694
        • Ramirez A.
        • Graham J.
        • Richards M.
        • et al.
        Burnout and psychiatric disorder among cancer clinicians.
        Br J Cancer. 1995; 71: 1263-1269
        • Lepnurm R.
        • Lockhart W.S.
        • Keegan D.
        A measure of daily distress in Practising medicine.
        Can J Psychiatry. 2009; 54: 170-180
        • Asai M.
        • Morita T.
        • Akechi T.
        • et al.
        Burnout and psychiatric morbidity among physicians engaged in end-of-life care for cancer patients: a cross-sectional nationwide survey in Japan.
        Psychooncology. 2007; 16: 421-428
        • Kamal A.H.
        • Bull J.H.
        • Wolf S.P.
        • et al.
        Prevalence and predictors of burnout among hospice and palliative care clinicians in the U.S.
        J Pain Symptom Manage. 2020; 59: e6-e13
        • Adibe B.
        • Perticone K.
        • Hebert C.
        Creating Wellness in a pandemic: a Practical Framework for health systems responding to Covid-19.
        NEJM Catal. 2020;
        • Adams J.G.
        • Walls R.M.
        Supporting the health care Workforce during the COVID-19 global Epidemic.
        JAMA. 2020; 323: 1439
        • Lai J.
        • Ma S.
        • Wang Y.
        • et al.
        Factors associated with mental health Outcomes among health care workers exposed to coronavirus disease 2019.
        JAMA Netw Open. 2020; 3: e203976
        • Costantini M.
        • Sleeman K.E.
        • Peruselli C.
        • Higginson I.J.
        Response and role of palliative care during the COVID-19 pandemic: a national telephone survey of hospices in Italy.
        Palliat Med. 2020; 34: 889-895
        • Wu Y.
        • Wang J.
        • Luo C.
        • et al.
        A comparison of burnout frequency among oncology physicians and nurses working on the Frontline and Usual Wards during the COVID-19 Epidemic in Wuhan, China.
        J Pain Symptom Manage. 2020; 60: e60-e65
        • Koh S.J.
        • Keam B.
        • Hyun M.K.
        • et al.
        Cancer pain management education rectifies patients’ misconceptions of cancer pain, reduces pain, and improves quality of life.
        Pain Med (United States. 2018; 19: 2546-2555
        • Launer J.
        Burnout in the age of COVID-19.
        Postgrad Med J. 2020; 96: 367-368
        • Barello S.
        • Palamenghi L.
        • Graffigna G.
        Stressors and resources for healthcare professionals during the Covid-19 pandemic: Lesson Learned from Italy.
        Front Psychol. 2020; 11
        • Radbruch L.
        • Knaul F.M.
        • de Lima L.
        • de Joncheere C.
        • Bhadelia A.
        The key role of palliative care in response to the COVID-19 tsunami of suffering.
        Lancet. 2020; 395: 1467-1469
        • Chen T.-J.
        • Lin M.-H.
        • Chou L.-F.
        • Hwang S.-J.
        Hospice utilization during the SARS outbreak in Taiwan.
        BMC Health Serv Res. 2006; 6: 94
        • Etkind S.N.
        • Bone A.E.
        • Lovell N.
        • et al.
        The role and response of palliative care and hospice services in Epidemics and pandemics: a Rapid review to Inform Practice during the COVID-19 pandemic.
        J Pain Symptom Manage. 2020; 60: e31-e40
        • Schwartz J.
        • King C.-C.
        • Yen M.-Y.
        Protecting healthcare workers during the coronavirus disease 2019 (COVID-19) outbreak: Lessons from Taiwan’s Severe Acute Respiratory syndrome response.
        Clin Infect Dis. 2020; 71: 858-860
        • Powell V.D.
        • Silveira M.J.
        What should palliative Care’s response Be to the COVID-19 pandemic?.
        J Pain Symptom Manage. 2020; 60: e1-e3
        • Tanzi S.
        • Alquati S.
        • Martucci G.
        • De Panfilis L.
        Learning a palliative care approach during the COVID-19 pandemic: a case study in an Infectious Diseases Unit.
        Palliat Med. 2020; 34: 1220-1227
        • Osman H.
        • Shrestha S.
        • Temin S.
        • et al.
        Palliative care in the global setting: ASCO Resource-Stratified Practice guideline.
        J Glob Oncol. 2018; 4: 1-24
        • Centeno C.
        • Sitte T.
        • de Lima L.
        • et al.
        White paper for global palliative care Advocacy: Recommendations from a PAL-LIFE expert Advisory Group of the Pontifical Academy for life, Vatican City.
        J Palliat Med. 2018; 21: 1389-1397
        • Hui D.
        • Bruera E.
        Models of palliative care delivery for patients with cancer.
        J Clin Oncol. 2020; 38: 852-865
        • Radbruch L.
        • De Lima L.
        • Knaul F.
        • et al.
        Redefining palliative care—a new Consensus-based definition.
        J Pain Symptom Manage. 2020; 60: 754-764
        • Tziraki C.
        • Grimes C.
        • Ventura F.
        • et al.
        Rethinking palliative care in a public health context: addressing the needs of persons with non-communicable chronic diseases.
        Prim Health Care Res Dev. 2020; 21: e32
        • Welp A.
        • Meier L.L.
        • Manser T.
        Emotional exhaustion and workload predict clinician-rated and objective patient safety.
        Front Psychol. 2015; 5
        • Tawfik D.S.
        • Scheid A.
        • Profit J.
        • et al.
        Evidence relating health care provider burnout and quality of care a systematic review and meta-analysis.
        Ann Intern Med. 2019; 171: 555-567
        • Chen K.Y.
        • Yang C.M.
        • Lien C.H.
        • et al.
        Burnout, job satisfaction, and medical malpractice among physicians.
        Int J Med Sci. 2013; 10: 1471-1478
        • Williams E.S.
        • Manwell L.B.
        • Konrad T.R.
        • Linzer M.
        The relationship of organizational culture, stress, satisfaction, and burnout with physician-reported error and suboptimal patient care.
        Health Care Manage Rev. 2007; 32: 203-212
        • Demerouti E.
        • Bakker A.B.
        • Leiter M.
        Burnout and job performance: the moderating role of selection, optimization, and compensation strategies.
        J Occup Health Psychol. 2014; 19: 96-107
        • Tawfik D.S.
        • Profit J.
        • Morgenthaler T.I.
        • et al.
        Physician burnout, well-being, and work Unit safety Grades in relationship to reported medical errors.
        Mayo Clin Proc. 2018; 93: 1571-1580
        • Chen Z.
        • Leng J.
        • Pang Y.
        • He Y.
        • Heng F.
        • Tang L.
        Demographic, occupational, and societal features associated with burnout among medical oncology staff members: cross-sectional results of a Cancer Center in Beijing, China.
        Psychooncology. 2019; 28: 2365-2373
        • Dewa C.S.
        • Loong D.
        • Bonato S.
        • Trojanowski L.
        The relationship between physician burnout and quality of healthcare in terms of safety and acceptability: a systematic review.
        BMJ Open. 2017; 7: e015141
        • Loerbroks A.
        • Glaser J.
        • Vu-Eickmann P.
        • Angerer P.
        Physician burnout, work engagement and the quality of patient care.
        Occup Med (Lond). 2017; 67: 356-362