Article Text

Early referral to a palliative team improves end-of-life care among gynecological cancer patients: a retrospective, population-based study
  1. Torbjørn Paulsen1,2,
  2. Heidi Liland1,
  3. Tor Åge Myklebust2,3 and
  4. Kristina Lindemann1,4
  1. 1 Department of Gynecological Oncology, Division of Cancer Medicine, Oslo University Hospital, Oslo, Norway
  2. 2 Department of Registration, Cancer Registry of Norway, Oslo, Norway
  3. 3 Department of Research and Innovation, Møre og Romsdal Hospital Trust, Ålesund, Norway
  4. 4 Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway
  1. Correspondence to Dr Torbjørn Paulsen, Department of Gynecological Oncology, Division of Cancer Medicine, Oslo, Oslo University Hospital, Oslo, Norway; tpa{at}


Objective To assess end-of-life care among patients with gynecological cancer, and to describe the association between timing of palliative care referral and patterns of care.

Methods All women with residence in Oslo, Norway, who died of gynecological cancer between January 1, 2015 and December 30, 2017 (36 months), were identified. Patients were primarily treated at the Norwegian Radium Hospital and clinical data on end-of-life care were retrospectively extracted from the medical records.

Results We identified 163 patients with median age 70.1 years at death (range 26–100) with the following diagnoses: ovarian (n=100), uterine (n=40), cervical (n=21), and vulvar cancer (n=2). 53 (33%) of patients died in a palliative care unit, 34 patients (21%) died in nursing homes without palliative care, and 48 (29%) patients died in hospital. Only 15 (9%) patients died at home. 25 (15%) patients received chemotherapy in the last 30 days before death, especially ovarian cancer patients (n=21, 21%). 103 patients (61%) were referred to a palliative team prior to death. Referral to a palliative team was associated with a significantly reduced risk of intensive care unit admission (OR 0.11, 95% CI 0.02 to 0.62) and higher likelihood of a structured end-of-life discussion (OR 2.91, 95% CI 1.03 to 8.25). Palliative care referral also seemed to be associated with other quality indicators of end-of-life care (less chemotherapy use, more home deaths).

Conclusions End-of-life care in patients with gynecological cancer suffers from underuse of palliative care. Chemotherapy is still commonly used towards end-of-life. Early palliative care referral in the disease trajectory may be an important step towards improved end-of-life care.

  • palliative care
  • ovarian neoplasms
  • uterine cervical neoplasms
  • uterine neoplasms

Data availability statement

Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information. On request an anonymous data file might be available by contacting the main author.

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  • Early referral to palliative care reduced the risk of intensive care unit admission and increased the likelihood of a structured end-of-life conversation.

  • Early referral was also associated with less chemotherapy use.

  • The findings emphasize the importance of early referral to a palliative care team.


Many gynecological cancer patients will experience recurrence and die despite optimal anticancer treatment.1 In particular, patients with ovarian cancer have a high and complex symptom burden with almost 70% presenting nine or more symptoms.2 The ultimate goal of cancer-directed treatment in recurrent disease is, therefore, palliation. However, only half of patients report symptom improvement on palliative chemotherapy, and deterioration in the quality of life is common.3 Careful evaluation of the expected benefits and trade-offs for quality of life must be considered when offering palliative chemotherapy towards the end-of-life. A consensus statement of the American Society of Clinical Oncology advocates against the use of cancer-directed therapy in patients with low performance status and without strong evidence that further anticancer treatment provides clinical benefit. Among oncologists and gynecologic oncologists, there is a growing concern about chemotherapy use at the end-of-life.4 5 Retrospective series have reported that 12–29% of gynecological cancer patients receive chemotherapy towards the end-of-life,6 7 and we need further awareness on when to stop chemotherapy.8 The extensive use of chemotherapy and other treatments resulting in emergency admissions and hospitalizations, as well as the underuse of palliative and hospice services, have been identified as important areas for improvement of end-of-life care. Early integration of palliative care has not only been reported to reduce aggressiveness of care, improve quality of life, and increase the likelihood of patients receiving care in line with their preferences,9 in some studies it has also been associated with prolonged survival.10 End-of-life care should further take patients’ preferences into account. The most important factors for quality end-of-life care includes trust in the treating physician, avoidance of unwanted life support, effective communication, and continuity of care.11 Place of death also seems to be an important factor for patients, with the majority of patients preferring to die at home.12

In our study, we aimed to assess patterns of care towards the end-of-life in a population-based series of patients who died of gynecological cancer in Oslo, Norway. We focused on chemotherapy use, as well as palliative care involvement in end-of-life care between different cancer sites. We also aimed to study how involvement of a palliative care team influences these patterns.


This population-based, retrospective, single-center study includes patients with residence in Oslo who died between January 1, 2015 and December 31, 2017. All patients were primarily treated at the Norwegian Radium Hospital, a tertiary referral center for all patients with gynecological cancer in the South East Health Region. The Norwegian Radium Hospital also serves as a primary hospital for Oslo County. To analyze a population-based sample, we included only patients from Oslo County. Patients were identified in a prospectively maintained institutional quality assurance database (Medinsight Version From the database we obtained information on baseline characteristics and previous treatment. From the medical electronic records we obtained administered end-of-life treatment and serious toxicity assessed asCommon Terminology Criteria for Adverse Events (CTCAE) grade 4 (Online supplemental file 1).13 Individual survival data were available through linkage to the Norwegian Cause of Death Registry.

Supplemental material

The Charlson Comorbidity Index was used to categorize comorbidity. The selected conditions are rated from 1 to 6, with a score of 6 being the most severe morbidity. The comorbidity scores result in a summary score which was categorized as low (0–2), moderate (3–5), and high score (≥6).14 15

We defined surgical procedures as all invasive procedures performed by radiologists, anesthesiologists, surgeons or gynecologists.


The present study was approved on May 15, 2018 by the Data Protection Office at Oslo University Hospital (No. 18/09560). As all patients included in this study had deceased, informed signed consent was waived.

Statistical Analysis

Standard descriptive statistics were used, including means, medians, and range for continuous variables and absolute and relative frequencies for categorical variables. Pearson χ2 test was used to test associations between categorical variables. Median overall survival was defined from the date of the primary diagnosis until the date of death, and estimated using the Kaplan-Meier estimator. To identify outcomes potentially associated with referral patterns to palliative care, odds ratios were estimated from a multivariate logistic regression model controlled for age for each of the following covariates: use of chemotherapy within the last 30 days (yes/no), parenteral nutrition (yes/no), hospital admissions (yes/no), intensive care unit (ICU) admissions (yes/no), structured conversation at the end-of-life (yes/no), and home death. We categorized patients into early (> 30 days before death) and late referral to palliative care (≤ 30 days before death). A two-sided p value <0.05 was considered statistically significant. All analyses were performed with International Business Machines Corporation (IBM) Statistical Package for the Social Sciences (SPSS) for Windows version 25.0 and Stata V 16.0.


Study Sample

We identified 215 women diagnosed with gynecological cancer. Median age at primary diagnosis was 66 years (range 24–98). Of these, 163 women died of gynecological cancer and were included in the analyses (Table 1). Median age at the time of death was 70.1 years (range 26–100). Median duration of disease was 4.1 years for all patients.

Table 1

Basic characteristics of all patients who died of gynecological cancer 2015–17 (n=163)

Sixty-one percent (n=100) of patients had ovarian cancer, 25% (n=40) had uterine, 13% (n=21) cervical, and 1% (n=2) vulvar cancer. The baseline characteristics of patients according to primary diagnosis are shown in Table 1. The median age at death was 67.8 years for ovarian cancer patients, 75 years for uterine cancer patients, and 64.5 years for cervical cancer patients. The majority of ovarian cancer patients scored low (score 0–2) (n=27, 27%) or moderate (score 3–5) (n=53, 53%) on the Charlson Comorbidity Index. Significantly more uterine cancer patients had a high (score ≥6) Charlson Comorbidity Index (n=16, 40%) compared with ovarian and cervical cancer patients (20% and 19%, respectively, p=0.03, between disease sites).

End-of-Life Treatment Patterns

Sixty-seven of the patients were admitted to hospital in the last 30 days of life. The median stay in hospital towards end-of-life was 4 days (range 0–30 days) (Table 2). Fifteen patients (9%) were treated in the intensive care unit in the last 30 days of life.

Forty-eight (29%) patients died in hospital, 53 (33%) in a nursing home with a palliative unit, and 34 (21%) in a nursing home without a palliative unit. Thirteen out of 34 patients (21%) dying in a nursing home without a palliative care unit were referred to the palliative team. Only 15 patients (9%) died at home.

Overall, 25 of the 163 patients (15%) received systemic chemotherapy within 30 days of death (Table 3); another eight patients had locally administered chemotherapy (mitoxantrone) in pleura or peritoneum (Figure 1). Totally 48 patients had other non-chemotherapy cancer treatment and nine patients had palliative radiation therapy 30 days before death (Online supplemental file 2). Twenty-one (21%) of the ovarian cancer patients received systemic chemotherapy within 30 days before death, while only four (10%) of the uterine cancer patients had chemotherapy during this time period. None of the cervical and vulvar cancer patients had systemic chemotherapy in their last weeks of life. There were no statistically significant differences across gynecological cancer diagnoses (p=0.06). Details of the administered regimen are given in Figure 1. Three patients had serious (CTCAE grade 4) side effects: bone marrow depression, sepsis, and gastrointestinal bleeding (Online supplemental file 1). Toxicity of lower grade was neither systematically recorded nor collected.

Supplemental material

Table 3

Treatments and interventions 30 days before death (n=163)

Table 4

Effect of early referral to a palliative team on chemotherapy, parenteral nutrition, hospitalization, ICU admission, structured conversations, and place of death

Figure 1

Systemic and intrapleural or peritoneal chemotherapy 30 days before death (n=33).

Parenteral nutrition was administered in 23 (14%) of all patients; 76% of the patients required per oral opioid treatment. Other supportive treatment such as saline hydration, antibiotic use, and blood transfusions are listed in Table 3.

Fifty-seven (35%) patients received one or multiple surgical/invasive procedures during their last 30 days (Table 3). The most commonly performed procedures were drainage of ascites (n=24), pleural effusions (n=16), and intraperitoneal/pleural installation of mitoxantrone (n=17). Eight patients underwent percutaneous nephrostomy and one had surgery for an ileostomy. All surgical procedures 30 days before death are summarized in the Online supplemental file 3.

Supplemental material

Table 2

Table 2

Referral, structured conversations and place of death 30 days before death (n=163)

Palliative Care Referral and End-of-Life Conversation

One hundred and three (61%) patients were treated by a palliative care team prior to death, 43 (26%) of those within 30 days prior to death (Table 2). A structured conversation at the end-of-life (including change of treatment goals and termination of tumour-directed treatment) was documented in 89 (55%) of the patients.

Impact of Palliative Care Referral on Patterns at End-of-Life Care

We categorized patients in early and late referral to palliative care (Table 4). The numerically lower risk of chemotherapy in patients referred early did not reach statistical significance (OR 0.26, 95% CI 0.07 to 1.01). Patients referred late had a higher risk of receiving parenteral nutrition (OR 6.88, 95% CI 1.39 to 33.93) and had a significantly higher risk of being admitted to hospital in the last 30 days (OR 6.98, 95% CI 1.78 to 27.27).

Patients referred to the palliative team had a significantly lower risk of admission to ICU (OR 0.11, 95% CI 0.02 to 0.64 for early referrals; OR 0.30, 95% CI 0.07 to 1.24 for late referrals). Referral to palliative care, in particular early referral, was associated with a higher likelihood for a structured end-of-life conversation (OR 2.91, 95% CI 1.03 to 8.25 for early referrals; OR 2.33, 95% CI 0.78 to 6.98 for late referrals). OR for death at home also increased with timing of palliative referral but did not reach statistical significance (OR 7.85, 95% CI 0.9 to 68.22 for early referrals; OR 4.02, 95% CI 0.41 to 39.60 for late referrals).


Summary of Main Results

Only 61% of the patients were referred to palliative care prior to death. Chemotherapy use towards end-of-life, especially in ovarian cancer patients, is still common. There is a significant decrease in ICU admission and an increase in the use of structured conversation at end-of-life by early referral to a palliative team. We observed a significant increase in hospitalization and use of parenteral nutrition with late referral. Other quality indicators for end-of-life care (less chemotherapy use, home death) are associated with early palliative care referral.

Results in the Context of Published Literature

Our study is consistent with other patients’ series where up to 29% of the patients were given chemotherapy at end-of-life.7 8 16 In our study, up to 13% of the patients were admitted to ICU during their last 30 days. This is lower than for other studies. In a US study, 8% of the patients with metastatic cancer from all primary sites died in ICU while 32.9% of the patients were admitted to ICU at end-of-life.17 Lee and co-workers demonstrated that a statement on not giving life-sustaining treatment was associated with lower ICU admission compared with patients who were recommended full life-sustaining treatment.18 The increased likelihood of a structured end-of-life conversation associated with palliative care referral in our study may therefore in part explain the reduced risk of ICU admission in these patients. A considerable number of patients were admitted to hospital during their final 30 days and few patients (9%) died at home compared with the percentage of home deaths for many other countries.19 In a study by Higginson and Sen-Gupta, more than half of patients expressed a wish to die at home and preference seem to change little towards the end-of-life.20 Between 1986 and 2012, the number of home deaths fell in Norway from 17.9% to 14.5% for both women and men according to Statistics of Norway 2020. Lately, the authorities have increased the focus on home deaths by strengthening home services delivered by both public and private institutions in line with the fact that the limited availability of specialized home care may prevent patients from dying at home.

Giving critically-ill patients chemotherapy provides little benefit on symptom control, quality of life, or survival.5 21 22 Ovarian cancer patients are at particular risk of receiving multiple lines of treatment. An often detrimental effect of chemotherapy on quality of life has been reported earlier,3 and only about half of the patients on palliative chemotherapy report improvement of symptoms.23 This is important when we counsel patients for the expected benefit of chemotherapy. Hence, patients who experience a discrepancy between perceived and expected symptom benefit are at higher risk of developing depression and anxiety.24 Therefore, we need to address these gaps in communication, especially regarding treatment goals, preferences, and prognosis. In our study, 22% of the patients did not have a conversation recorded about ending tumor-directed treatment and end-of-life care shortly before death. The majority of gynecological cancer patients prefer to be informed about end-of-life care when their disease progresses or if tumor directed treatment no longer is an option.25 However, we still fail to communicate prognosis and trade-offs adequately, and ovarian cancer patients in particular remain at high risk of chemotherapy use towards end-of-life.

Despite the high symptom burden in gynecological cancer patients and the doubtful benefit of continued chemotherapy for quality of life, 26% of patients were not seen by a palliative team prior to death, and 54 patients were referred late, within 30 days of death. Early referral to the palliative team seems important when we aim for less aggressive treatment towards the end-of-life. The availability of palliative care services are rather good in our region; however, the referral of patients occurs late in the cancer course when the patient experiences increased symptom burden and disease progression. Referred patients are more likely to have structured end-of-life conversations, but it is equally important to strengthen the communication of gyne-oncologists to facilitate these discussions early in the disease trajectory as this may prevent aggressive end-of-life care.

The importance of good communication about prognosis, adverse effects, and symptom management to facilitate the decision process has also been highlighted by the Ovarian Oncology Guidelines Group in Canada. Recurrences treated with chemotherapy should be managed individually, taking into consideration the expected medical benefit and toxicities and the patients’ preferences.26

The most common surgical interventions are those that are associated with the highest impact on symptom relief, such as ascites, pleural, and abscess drainage. However, interventions such as stoma operation or percutaneous nephrostomy may have doubtful palliative benefit when performed in the last month of life and should be avoided for patients with short life expectancy.

We could not find any literature demonstrating the benefit of early referral to the palliative care team among gynecological cancer patients.

Strengths and Weaknesses

The strengths of this study include its population-based design, including all patients who died of gynecological cancer with residence in Oslo County. We have valid and complete data on diagnosis, cause of death, and use of chemotherapy. The retrospective design is a weakness of the study and explains in part missing data on some end-of-life treatment and the lack of information on detailed toxicity from chemotherapy. Individual discussions with the patient about treatment goals may have taken place but have not been documented in the patient’s records, causing us to underestimate the prevalence of end-of-life discussions. The limited number of cases included may have prevented definite conclusion for some of the associations studied with palliative care referral. When estimating associations between referral to the palliative team and related outcomes we only controlled for patients’ age at death. There are arguably other potentially confounding factors that may influence these associations which we left out either because we lacked information or because the proportion missing was high. The results presented should therefore be interpreted with caution.

Implications for Practice and Future Research

This study has led to increased attention on early referral to the palliative care team and chemotherapy use towards end-of-life among gynecological cancer patients. Structured training in communication has been implemented in collaboration with the European Palliative Care Research Center at Oslo University Hospital.

We recommend planning these structured conversations at end-of-life earlier in the trajectory of cancer treatment4 to allow for shared decision-making, and to increase the involvement of patients and their carers. Assessing patients’ and carers’ expectations and satisfaction with end-of-life care is a prerequisite when we aim for patient centered care. The planned Gynecologic Cancer InterGroup/Nordic Society of Gynecologic Oncology/Australia New Zealand Gynecological Oncology Group collaborative trial PEACE (Palliation in gyne-oncology: patients’ expectations and assessment) will help us to understand the patients’ and carers’ perspectives in end-of-life care. Identification of gaps in care will guide the development of targeted interventions to improve patient-centered care and shared decision making.27–29


Chemotherapy and other invasive treatments towards the end-of-life are common in gynecological cancer, especially for patients with ovarian cancer. We believe it should be less than 10% of the last 30 days of life. Early referral to palliative care and structured communication seem crucial when we aim for less aggressive end-of-life care, in line with patients’ preferences. Multidisciplinary collaborative efforts to drive palliative research in gyne-oncology patients are needed to improve patient centered care.

Data availability statement

Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information. On request an anonymous data file might be available by contacting the main author.

Ethics statements

Patient consent for publication


We want to thank Bård Kloppen, Marthe Sylten Engh for their contribution to collecting the data, and Martin Turzer for his contribution to the research idea. Some of these data were previously published at IGCS in Rio de Janeiro and at ESGO in Athens, 2019.


Supplementary materials


  • Collaborators Bård Kloppen, Marthe Sylten Engh, Martin Turzer.

  • Contributors The authors TP, HL, and KL have contributed with data collection from the medical records and writing the manuscript. TP, TÅM, and KL have contributed to the statistical analyses. All authors read and commented on the manuscript and approved the final version. TP is acting as guarantor and accepts full responsibility for the work and the conduct of the study. TP had access to the data, and controlled the decision to publish.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.