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Original Article Goals of Care and End-of-Life Decision Making for Hospitalized Patients at a Canadian Tertiary Care Cancer Center David Hui, MD, MSc, FRCPC, Andrea Con, PhD, Glenda Christie, MSW, RSW, and Philippa Helen Hawley, BMed, FRCPC Department of Palliative Care & Rehabilitation Medicine (D.H.), University of Texas M.D. Anderson Cancer Center, Houston, Texas, USA; and Cancer Rehabilitation and Sociobehavioural Research Centre (A.C.), Department of Patient and Family Counseling (G.C.), and Department of Pain and Symptom Management/Palliative Care (P.H.), Vancouver Centre, British Columbia Cancer Agency, Vancouver, British Columbia, Canada Abstract Limited information is available regarding the quality of end-of-life care at cancer centers. We sought to characterize the end-of-life decision-making process for advanced cancer patients admitted to our tertiary cancer center, and to examine the association between goals of care and practice patterns. Information on patient characteristics, investigations, cancer treatments, and goals of care was collected retrospectively for consecutive patients who died at the inpatient unit of the Vancouver Cancer Center between January 1, 2005 and December 31, 2006. One hundred eighteen advanced cancer patients had a median admission duration of 10 days (range 1e64 days). A median of two tests per day was performed, with a decreasing trend over time (P < 0.001). Forty percent received cancer treatments during hospitalization, with 75% terminated prematurely. Do-not-resuscitate orders, supportive care plans, and diagnosis of dying were documented for 96%, 86%, and 76% of the patients, respectively. Early establishment of supportive care plan and diagnosis of dying were associated with timely discontinuation of cancer treatments (Spearman coefficients 0.47 and 0.60, respectively). Multivariate analysis revealed that timely diagnosis of dying was associated with early establishment of code status (P ¼ 0.042), supportive care plans (P < 0.001), and discontinuation of cancer therapy (P ¼ 0.005). Cancer patients who died at our oncology center were investigated and treated intensively during their short hospitalization. Early establishment of goals of care may be associated with changes in practice consistent with improved quality of care. J Pain Symptom Manage 2009;38:871e881. Ó 2009 U.S. Cancer Pain Relief Committee. Published by Elsevier Inc. All rights reserved. Key Words Advanced cancer, goals of care, investigations, cancer treatments, quality of care, end of life Address correspondence to: David Hui, MD, MSc, FRCPC, Department of Palliative Care & Rehabili- tation Medicine (Unit 008), University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030, USA. E-mail: dhui@ mdanderson.org Accepted for publication: May 14, 2009. Ó 2009 U.S. Cancer Pain Relief Committee Published by Elsevier Inc. All rights reserved. 0885-3924/09/$esee front matter doi:10.1016/j.jpainsymman.2009.05.017 Vol. 38 No. 6 December 2009 Journal of Pain and Symptom Management 871

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Page 1: Goals of Care and End-of-Life Decision Making for Hospitalized Patients at a Canadian Tertiary Care Cancer Center

Vol. 38 No. 6 December 2009 Journal of Pain and Symptom Management 871

Original Article

Goals of Care and End-of-Life DecisionMaking for Hospitalized Patients ata Canadian Tertiary Care Cancer CenterDavid Hui, MD, MSc, FRCPC, Andrea Con, PhD, Glenda Christie, MSW, RSW,and Philippa Helen Hawley, BMed, FRCPCDepartment of Palliative Care & Rehabilitation Medicine (D.H.), University of Texas M.D. Anderson

Cancer Center, Houston, Texas, USA; and Cancer Rehabilitation and Sociobehavioural Research

Centre (A.C.), Department of Patient and Family Counseling (G.C.), and Department of Pain and

Symptom Management/Palliative Care (P.H.), Vancouver Centre, British Columbia Cancer Agency,

Vancouver, British Columbia, Canada

Abstract

Limited information is available regarding the quality of end-of-life care at cancer centers.We sought to characterize the end-of-life decision-making process for advanced cancer patientsadmitted to our tertiary cancer center, and to examine the association between goals of care andpractice patterns. Information on patient characteristics, investigations, cancer treatments,and goals of care was collected retrospectively for consecutive patients who died at the inpatientunit of the Vancouver Cancer Center between January 1, 2005 and December 31, 2006. Onehundred eighteen advanced cancer patients had a median admission duration of 10 days(range 1e64 days). A median of two tests per day was performed, with a decreasing trend overtime (P< 0.001). Forty percent received cancer treatments during hospitalization, with 75%terminated prematurely. Do-not-resuscitate orders, supportive care plans, and diagnosisof dying were documented for 96%, 86%, and 76% of the patients, respectively. Earlyestablishment of supportive care plan and diagnosis of dying were associated with timelydiscontinuation of cancer treatments (Spearman coefficients 0.47 and 0.60, respectively).Multivariate analysis revealed that timely diagnosis of dying was associated with earlyestablishment of code status (P¼ 0.042), supportive care plans (P< 0.001), anddiscontinuation of cancer therapy (P¼ 0.005). Cancer patients who died at our oncologycenter were investigated and treated intensively during their short hospitalization. Earlyestablishment of goals of care may be associated with changes in practice consistent withimproved quality of care. J Pain Symptom Manage 2009;38:871e881. � 2009 U.S.Cancer Pain Relief Committee. Published by Elsevier Inc. All rights reserved.

Key Words

Advanced cancer, goals of care, investigations, cancer treatments, quality of care, end of life

Address correspondence to: David Hui, MD, MSc,FRCPC, Department of Palliative Care & Rehabili-tation Medicine (Unit 008), University of TexasM.D. Anderson Cancer Center, 1515 Holcombe

Blvd., Houston, TX 77030, USA. E-mail: [email protected]

Accepted for publication: May 14, 2009.

� 2009 U.S. Cancer Pain Relief CommitteePublished by Elsevier Inc. All rights reserved.

0885-3924/09/$esee front matterdoi:10.1016/j.jpainsymman.2009.05.017

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872 Vol. 38 No. 6 December 2009Hui et al.

IntroductionPatients with advanced cancer are bom-

barded with numerous decisions involvingtreatments, goals of care, and end-of-life plan-ning from the time of diagnosis until death.Many of these decisions are highly complex,emotionally charged, and have significant im-pact on how patients are managed. One ofthe key roles of the health care team is tohelp guide patients through the maze of diffi-cult choices by providing individualized rec-ommendations, taking into account thepatient’s preferences, disease state, treatmentoptions, and resources.

The role of clinical decision making is partic-ularly important for advanced cancer patientsdying in acute care settings. These patientstypically suffer from significant physical, psy-chological, and existential distress, and aresometimes too ill to engage in discussionsregarding health care decisions. This is furthercomplicated by the acute care culture of intenseinvestigations and treatments to diagnosis andtreat any potentially reversible causes.1 Theseactions often result in significant delays in deci-sion making regarding end-of-life care, leadingto aggressive interventions such as intubationand chemotherapy,1 with appropriate comfortmeasures being neglected.

A number of studies have specifically exam-ined the hospital course and end-of-lifedecision-making process for hospitalizedpatients dying in acute care settings. The land-mark SUPPORT Phase I study examined 4,301hospitalized patients with advanced diseases,and revealed multiple distressing findings.2

Less than half of the physicians knew abouttheir patients’ preferences for avoidance ofcardiopulmonary resuscitation (CPR), and46% of do-not-resuscitate (DNR) orders werewritten within only two days of death. Otherstudies focusing on patients who died in acutecare hospitals also documented aggressivemeasures and significant delays in establishinggoals of care,3e7 in contrast to patients in nurs-ing homes and palliative care units.7,8

Although it makes intuitive sense thatimproved communication and early establish-ment of goals of care can lead to improved qual-ity of care, past studies on this issue haveresulted in conflicting findings. Phase II of theSUPPORT study involved 4,804 hospitalized

patients randomized to either usual medicalcare or longitudinal interventions aimed to im-prove communication and decision making byproviding timely and reliable prognostic infor-mation. This study showed no difference in pa-tient-physician communication or in the fivetargeted outcomes, including incidence or tim-ing of written DNR orders, physicians’ knowl-edge of their patients’ preferences not to beresuscitated, number of days spent in an inten-sive care unit (ICU), comatose or receiving me-chanical ventilation before death, level ofreported pain, or hospital resource use.2 How-ever, a recent study of advanced cancer patientsdemonstrated that end-of-life discussions wereassociated with lower rates of ventilation, resus-citation, ICU admissions, and earlier hospiceenrollment.9 Of note, these studies were carriedout over weeks to months prior to patients’death, and much is still not known about the re-lationship between establishment of goals ofcare and the actual delivery of care during thelast admission. A more complete understandingof this process can help us minimize aggressiveinterventions and optimize quality of care.

We hypothesized that advanced cancer pa-tients admitted to our tertiary care cancer cen-ter were investigated and treated aggressivelyat the end of life, and that early establishmentof goals of care during the hospital stay couldhelp to minimize inappropriate interventions.The objective of this study was to characterizethe quality of care provided to cancer patientswho died at the Vancouver Cancer Center, spe-cifically related to establishment of goals ofcare milestones, investigations, and cancertreatments. We also sought to examine theassociation between goals of care milestonesand management practices.

MethodsPatients and Setting

All the patients who died on the inpatientunit of the Vancouver Cancer Center betweenJanuary 1, 2005 and December 31, 2006 wereincluded in this study. The Vancouver CancerCenter is a tertiary care oncology center serv-ing a catchment population of 4.2 million inthe province of British Columbia, Canada. Ithas an inpatient unit of 30 beds, with no ICU

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Vol. 38 No. 6 December 2009 873End-of-Life Decision Making

or palliative care beds. The patients whorequire critical care are sent to an adjacentgeneral hospital, whereas the patients who can-not return home following admission and whorequire palliative care are transferred to com-munity palliative care units or hospices asappropriate, when possible.

Information regarding patient demograph-ics, cancer and admission diagnosis, clinicalstatus on admission, frequency and appropri-ateness of investigations, active cancer treat-ments, disease trajectory, causes of death, andgoals of care was retrospectively reviewed bya medical oncologist (D. H.). A random sam-ple of 10 charts was further reviewed by a palli-ative care specialist (P. H.) to ensure accuracyof data collection. Supportive care plan, diag-nosis of dying, and appropriateness of investi-gation data were available for all but threepatients because of missing charts. TheResearch Ethics Board at the British ColumbiaCancer Agency approved this study and waivedthe requirement for informed consent.

Frequency and Appropriatenessof Investigations

Investigations performed during the finaladmission were documented under the cate-gories of blood tests, microbiology, imaging,and others (e.g., electrocardiogram and arte-rial blood gas). Procedures requiring radio-logic interventions (e.g., ultrasound-guidedparacentesis) were classified under imagingtests. Investigations were numerated based onhow they are typically ordered by physicians.For instance, complete blood count (CBC),electrolytes/urea/creatinine, calcium/magne-sium/phosphate, liver function test (LFT),troponin/creatine kinase, urinalysis, bloodculture, urine culture, chest X-ray, computedtomography chest, magnetic resonance head,bone scan, electrocardiogram (ECG), and ar-terial blood gas (ABG) were each consideredan individual test.

In addition to the frequency of investigations,we also reviewed the progress notes in detail toevaluate the proportion of tests for which therewas a clear indication (diagnosis, treatment, ormonitoring), balancing the relative invasivenessto determine whether the tests would berepeated again if the reviewers were put in thesame clinical situation. Based on this definition,we assigned investigations during hospitalization

into one of five categories of appropriateness:1¼ 0%e20%, 2¼ 21%e40%, 3¼ 41%e60%,4¼ 61%e80%, and 5¼ 81%e100%. For in-stance, a patient with 10 CBCs performed duringa two-week hospital stay may have 61%e80% oftests judged to be appropriately contributing tothe patient’s care for a clear indication (e.g., up-per gastrointestinal (GI) bleed and a need fortransfusions), whereas another patient with thesame number of tests but the majority with noclear justification may be assigned a score of21%e40%. A limitation of this measure is its sub-jectivity in interpretation of what constitutes ap-propriateness. Thus, we characterized thereliability of this measure in which a second inde-pendent observer (P. H.) determined the appro-priateness of investigations (i.e., CBCs,electrolytes, LFTs, imaging, and overall) for 10patients selected at random. The interrater reli-ability was moderate, with a Cohen’s kappa of0.70. The concordance rate (�1 category) was80%, with identical values assigned to 54% ofall cases. The discordant rate ($2 categorydifference) was 10%. No patient had a $3 cate-gory difference.

Cancer TreatmentsWe documented the start and end dates for

the last cancer treatment administered. Sys-temic therapies were classified as chemothera-peutic agents, hormones, and targetedtherapies. None of the patients were on any ex-perimental therapies or clinical trials. Externalbeam radiation was the only type of radiother-apy administered. In this study, early termina-tion of treatment was defined as less than twocycles of chemotherapy/targeted agent sincehospitalization, or unable to complete theplanned course of radiation.

Goals of Care MilestonesGoals of care were defined in this study as

(1) the presence of a DNR order in the chart,(2) whether a comfort care plan was adopted,and (3) whether a clinician considered a patientto be dying. They were assessed based on threevalidated questions previously developed forthis purpose.4 A comfort care plan was noted tobe in place if the following phrases were present:‘‘comfort care,’’ ‘‘palliative care,’’ ‘‘supportivecare,’’ ‘‘hospice,’’ or ‘‘palliative care unit.’’ Evi-dence that a patient was considered dying wasbased on documentation of the following

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874 Vol. 38 No. 6 December 2009Hui et al.

language in the progress notes: ‘‘end stage,’’ ‘‘dy-ing,’’ ‘‘terminally ill,’’ ‘‘moribund,’’ ‘‘hopeless,’’‘‘grim/grave prognosis,’’ or ‘‘days/weeks oflife.’’ The dates on whichthe milestoneswere firstdocumented were recorded.

Statistical AnalysisThe Statistical Package for the Social Sciences

(SPSS) software was used for statistical analysis(version 14.0, SPSS Inc., Chicago, IL). Compar-isons were made using the Student’s t-test andANOVA for independent samples for continu-ous outcomes, and Pearson’s Chi-square testfor categorical outcomes. We applied both lin-ear and Poisson regression modeling to deter-mine the trends regarding frequency ofinvestigations over the admission. The Spear-man’s correlation test was used to examine therelationship between nonparametric variables.

To identify factors that were independentlyassociated with the timing of establishment ofgoals of care milestones, appropriateness ofclinical investigations, and the timing of

Table 1Characteristics of Cancer Patients Who Die

Clinical CharacteristicsMedical

Oncologist (n¼ 80)R

Oncol

Median age 61Female gender 45Symptoms

Dyspnea 23Confusion 14Pain 42Nausea and vomiting 22Anorexia/cachexia 26Bleeding 7ECOG 3e4 69

Reason for admissionSymptom management 80Palliative anticancer tx 27Diagnostic workup 5

Cancer diagnosisGastrointestinal 29Lung 10Breast 13Hematologic 11Gynecological 1Genitourinary 6Primary unknown 6Head and neck 3Others 1

StageSolid tumordmetastatic 63Solid tumordlocally advanced 6Hematologicdadvanced 11

ECOG¼ Eastern Cooperative Oncology Group; NS¼ not significant; tx¼ treaP-values were based on comparisons among the three specialties.

discontinuation of cancer treatments, we per-formed nonparametric multivariate linear re-gression using backward elimination. Eachmodel incorporated age, gender, attendingservice, cancer stage, Eastern Cooperative On-cology Group (ECOG) performance status,frequency of investigation, appropriateness ofinvestigation, length of hospital stay, and theduration between admission and establish-ment of milestones (excluding the dependentvariable). A two-tailed P-value of less than 0.05was considered to be statistically significant.

ResultsBaseline Characteristics on Admission

During the two-year study period, 118(4.7%) patients died out of a total of 2,533 ad-missions. The characteristics of the 118 pa-tients who died in hospital are shown inTable 1. Nine percent were diagnosed with he-matologic malignancies and 91% had solid tu-mors, of whom 84% had metastatic disease.

d in Hospital, by Medical Specialty

adiationogist (n¼ 28)

Gynecologist(n¼ 10) P-valuea

Total(n¼ 118)

70 57 0.012 62 (19e89)14 10 NS 69 (58.5%)

7 4 NS 34 (29.8%)7 0 NS 21 (18.4%)

22 6 0.037 70 (61.4%)6 5 NS 33 (28.9%)7 2 NS 35 (30.7%)3 0 NS 11 (9%)

25 9 NS 108 (91%)

28 10 NS 118 (100%)17 4 0.016 48 (40.7%)1 1 NS 7 (5.9%)

7 0 d 36 (30.5%)11 0 d 21 (17.8%)1 0 d 14 (11.9%)0 0 d 11 (9.3%)1 8 d 10 (8.5%)3 0 d 9 (7.6%)0 2 d 8 (6.8%)4 0 d 7 (5.9%)1 0 d 2 (1.7%)

18 9 d 90 (76.3%)10 1 d 17 (14.4%)0 0 d 11 (9.3%)

atment.

Page 5: Goals of Care and End-of-Life Decision Making for Hospitalized Patients at a Canadian Tertiary Care Cancer Center

Table 2Frequency of Investigations in 115 Cancer Patients Who Died in Hospitala

InvestigationsNumber of Tests

(% of Total)Number of Tests

per DayMedian (Range)per Admission

Blood work 2418 (75.1%) 1.54 12.5 (0e153)CBC 787 (24.5%) 0.50 4 (0e60)Electrolytes 803 (25.0%) 0.51 4 (0e62)Liver function tests 368 (11.4%) 0.23 1 (0e22)INR 236 (7.3%) 0.15 1 (0e15)Others 224 (7.0%) 0.14 1 (0e18)

Microbiology 339 (10.5%) 0.22 1 (0e20)Imaging 307 (9.5%) 0.20 2 (0e10)

CXR 142 (4.4%) 0.09 1 (0e7)Others 165 (5.1%) 0.11 1 (0e9)

Others 154 (4.8%) 0.10 1 (0e11)Total 3218 (100%) 2.05 17 (0e179)

CBC¼ complete blood count; CXR¼ chest X-ray; INR¼ international normalized ratio.aInformation regarding investigation was not available for three patients.

Vol. 38 No. 6 December 2009 875End-of-Life Decision Making

Notably, none of the patients who died in hos-pital had early stage disease. Gastrointestinal(31%), lung (18%), and breast (12%) malig-nancies accounted for the top 60% of all ad-missions in this cohort. All the patients weresymptomatic on admission and required sup-portive care, with 41% admitted for palliativeanticancer therapy and 6% admitted forworkup of malignancy, as a cancer diagnosishad not been established at the time of admis-sion. Pain (61%), anorexia and cachexia(31%), dyspnea (30%), and nausea and vomit-ing (29%) were common symptoms on admis-sion. Ninety-one percent had an ECOGperformance status of three or greater.

The median duration from diagnosis to ad-mission was 10 months (range �0.1 to 204.2months). However, 14% had the diagnosis ofcancer made less than one month prior tothe final admission and 6% during the last hos-pitalization, suggesting a highly aggressivecourse of disease for these individuals. Themedian duration of admission was 10 days(range 1e64 days), with 14% of the patientsadmitted for three days or less before theirdeaths. Ten percent of the patients had a pro-longed course in hospital lasting more thanfour weeks.

Frequency and Appropriatenessof Investigations

In total, 3,218 investigations were per-formed during a combined 1,568 hospitaldays, with an average of two tests per day for ev-ery admitted day (Table 2). Blood work (75%)

constituted most of the investigations, withCBC (25%) and electrolytes (25%) orderedmost frequently.

The number of tests per day inverselycorrelated with the duration of admission(Spearman’s correlation coefficient �0.31,P¼ 0.001). Using two different regressionmodels, there was a decreasing trend of the fre-quency of investigations (Poisson regressionslope �0.137, standard error (SE)¼ 0.017,P< 0.001, Fig. 1) over the hospital course.However, investigations were done in 91%and 28% of the patients during the last weekand last day of life, respectively.

We also evaluated the appropriateness of in-vestigations, based on the proportion of testsfor which there was a clear indication(Fig. 2). In 41% of the patients, >80% of inves-tigations were considered appropriate,whereas in 75% of the patients, >60% of thetests were justified. LFTs and imaging investi-gations were more frequently performed ap-propriately, whereas CBC and electrolytestended to be ordered with less discretion(P< 0.001, Chi-square test).

Cancer TreatmentsAmong the 118 patients who died in hospi-

tal, 17 (14.4%) never received any cancer treat-ments. Forty-two (36%) patients receivedactive treatments within the last two weeks oftheir lives, including 21 (18%) treated withchemotherapy (Table 3).

During the last admission, 25 (21%) and 24(20%) patients were treated with systemic

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Fig. 1. Regression models of investigation frequency during hospitalization. The number of investigations perweek was plotted for 118 patients over the hospital course. Both linear regression and Poisson regression modelsrevealed a significant trend of decreasing frequency of investigations over time.

876 Vol. 38 No. 6 December 2009Hui et al.

therapy and radiation, respectively. All chemo-therapy treatments given during admissionwere terminated prematurely, whereas 48% ofthe patients who received radiation duringthe last admission were able to complete theplanned course. Among patients who receivedcancer therapy in hospital, the median dura-tion between last chemotherapy and deathwas 7.5 days, and the median time betweenlast radiation and death was five days (Fig. 3).Among patients who completed the course ofpalliative radiation during admission, the

Fig. 2. Appropriateness of investigations based on the type owas a measure of the proportion of tests for which there wasing). Imaging investigations and liver function tests were ahigher appropriateness scores compared to CBC and electro

median duration between last radiotherapyfraction and death was 12.5 days (interquartilerange [Q1eQ3] 6e18 days), with only one pa-tient living four weeks post-treatment. Giventhe short interval between radiation anddeath, few patients in our cohort likelybenefited from this treatment.

Goals of Care MilestonesDNR orders, supportive care plans, and di-

agnosis of dying were documented for 94%,86%, and 76% of the patients, respectively

f investigation. The appropriateness of investigationsa clear indication (diagnosis, treatment, or monitor-ssociated with a higher percentage of patients withlytes.

Page 7: Goals of Care and End-of-Life Decision Making for Hospitalized Patients at a Canadian Tertiary Care Cancer Center

Table 3Cancer Treatments Given to 118 Cancer Patients

Who Died in Hospital

Anticancer TherapyNumber of

Patients (%)

Last active cancer treatment before or during admissionChemotherapy 61 (51.7%)Radiation therapy 33 (28.0%)Hormonal therapy 3 (2.5%)Biological therapy (Phase I trial) 1 (0.8%)Chemoradiation 1 (0.8%)Chemoembolization 1 (0.8%)Surgery (laparotomy) 1 (0.8%)None 17 (14.4%)

Active cancer treatment during admissionPalliative radiation 23 (19.5%)Palliative chemotherapy 22 (18.6%)Hormonal therapy 2 (1.7%)Palliative chemoradiation 1 (0.8%)None 70 (59.3%)

Active cancer treatment within 14 days of deatha

Palliative radiation 19 (14.4%)Palliative chemotherapy 21 (17.8%)Hormonal therapy 1 (0.8%)Palliative chemoradiation 1 (0.8%)None 76 (64.4%)

Early termination of treatments during admissionRadiation 13 of 23 (56.5%)Chemotherapy 22 of 22 (100%)Chemoradiation 1 of 1 (100%)Hormonal therapy 0 of 2 (0%)

aPatients treated prior to admission were also included in thisanalysis.

Vol. 38 No. 6 December 2009 877End-of-Life Decision Making

(Table 4). The median time from establish-ment of these key indicators to death waseight, seven, and four days (Fig. 3). The diag-nosis of dying was consistently documented

Fig. 3. Decision milestones from date of death. Box plot displast chemotherapy treatment (only for patients who receivedation (only for patients who received radiation during admisscare including DNR, supportive care plan, and diagnosis of ddays from each of the respective decision points to the date

later and in fewer patients than the other twomilestones (Table 4).

Code status was addressed in 112 (94%) pa-tients, with DNR orders written for 111 ofthem, and one patient requesting full code de-spite repeated discussions. One of the patientswith a DNR order in place mistakenly receivedCPR. Among the six patients without docu-mentation of code status discussion, five re-ceived some form of resuscitation, with CPRperformed on three of them.

Correlation Between Goals of Care Milestonesand Clinical Management

The timing of establishment of the threegoals of care milestones (DNR orders, support-ive care plans, and diagnosis of dying) corre-lated with each other, with a particularlystrong association between diagnosis of dyingand establishment of supportive care plan(Table 5). Early establishment of goals ofcare correlated with more appropriate order-ing of investigations. The timing of establish-ment of supportive care plans and diagnosisof dying also were associated with discontinua-tion of cancer treatments (Table 5). Thesemilestones also correlated with length of stay.The patients with longer hospitalizationswere more likely to have had goals of careestablished later in admission.

In multivariate analysis, the timely establish-ment of both code status and supportive careplans were associated with early diagnosis of

laying the number of days from death to admission,chemotherapy during admission), last dose of radi-

ion), last investigation, and establishment of goals ofying. The numbers indicate the median number ofof death.

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Table 4Number of Patients with Goals of Care Milestones Established, by Discipline and Duration of Admission

Admission Milestones Medical Oncologist Radiation Oncologist Gynecologic Oncologist All

All DNR established 76 (95%) 25 (89%) 10 (100%) 111 (94%)Care plan established 67 (86%) 24 (89%) 6 (60%) 99 (86%)Dying established 62 (80%) 16 (59%) 8 (80%) 87 (76%)

<Four-day stay DNR established 9 (82%) 4 (80%) d 13 (81%)Care plan established 8 (73%) 4 (80%) d 12 (75%)Dying established 7 (64%) 3 (60%) d 10 (63%)

$Four-day stay DNR established 67 (97%) 21 (91%) 10 (100%) 98 (96%)Care plan established 59 (88%) 20 (91%) 6 (60%) 85 (86%)Dying established 55 (82%) 13 (59%) 8 (80%) 77 (78%)

878 Vol. 38 No. 6 December 2009Hui et al.

dying (Table 6). The diagnosis of dying, inturn, was associated with early discontinuationof cancer therapy. Furthermore, the appropri-ateness of clinical investigations improved withboth early discontinuation of cancer treat-ments and decreased frequency of investiga-tions (Table 6).

Practice Pattern Differences by DisciplineWe compared the admission characteristics,

investigations, treatments, and goals of caremilestones among medical, radiation, and gy-necologic oncologists. The patients admittedunder radiation oncology tended to be older(P¼ 0.01), required pain control (P¼ 0.04),and were admitted for palliative cancer treat-ments (P¼ 0.02, Table 1). Medical oncologypatients had more investigations on averagethan those under radiation and gynecologiconcology (2.6� 1.8 vs. 1.8� 0.8 and 1.8� 1.0investigations per day, respectively); however,the appropriateness of investigations did not

Table 5Univariate Analysis for Timing of Establish

Timing of Goals of Care MilestonesTimin

Statu

Timing of code status (days from admission)

Timing of care plan (days from admission)P<

Timing of dying diagnosis (days from admission)P<

Length of admission (days)P¼

Appropriateness of investigations �P¼

Timing of stopping treatment (days from admission)P¼

d¼ not applicable.aSpearman correlation coefficients were shown.

differ among the teams, suggesting that medi-cal oncology patients may inherently requiremore testing because of the nature of their dis-eases. No significant differences were detectedamong the three disciplines regarding cancertreatments and establishment of goals of caremilestones.

DiscussionWe found that cancer patients who died at

our oncology center were investigated andtreated intensively during their short hospital-izations. Our results suggest that there is a lotof room for improvement in the delivery ofquality end-of-life care on our unit. Quality ofcare for advanced cancer patients is depen-dent on a number of factors, including the es-tablishment of goals of care, the intensity ofinvestigations and cancer treatments, painand symptom management, and psychosocial

ment of Goals of Care Milestonesa

Goals of Care Milestones

g of Codes (Days)

Timing of CarePlan (Days)

Timing of DyingDiagnosis (Days)

d 0.39 0.49P< 0.001 P< 0.001

0.39 d 0.700.001 P< 0.001

0.49 0.70 d0.001 P< 0.001

0.30 0.49 0.650.001 P< 0.001 P< 0.0010.25 �0.20 �0.260.008 P¼ 0.048 P¼ 0.014

0.10 0.47 0.600.52 P¼ 0.002 P< 0.001

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Table 6Multivariate Analysis for Timing of

Establishment of Goals of Care Milestones andPractice Patternsa

Variables

Multivariate Analysis

P-valuea

Early establishment of code statusTiming of diagnosis of dying 0.042

Early establishment of care planTiming of diagnosis of dying <0.001Length of admission 0.037

Early diagnosis of dyingTiming of care plan <0.001Timing of discontinuation

of cancer treatment0.045

Appropriateness of investigationsFrequency of investigations <0.001Timing of discontinuation

of cancer treatment0.015

Early discontinuation of cancer treatmentsTiming of diagnosis of dying 0.005Length of admission 0.028

aNonparametric multivariate linear regression was performed us-ing stepwise elimination to determine factors associated with goalsof care milestones, appropriateness of investigations, and timing ofdiscontinuation of cancer treatments. Each model incorporatedage, gender, attending service, cancer stage, ECOG performancestatus, frequency of investigation, appropriateness of investigation,length of hospital stay, and the duration between admission and es-tablishment of milestones (excluding the dependent variable).Only the significant factors are shown above.

Vol. 38 No. 6 December 2009 879End-of-Life Decision Making

support, including advance care planning,communication, and availability of palliativecare resources, such as hospices.10 Althougha number of studies have examined the qualityof care for dying patients in generalhospitals,2e7,11 our study represents one ofthe few to specifically examine the uniquechallenges for advanced cancer patients admit-ted to a tertiary care oncology center. The bal-ance between quality-of-life measures and life-prolonging treatments presents a logistic andphilosophical dilemma for patients who are dy-ing while admitted to a cancer center and forthose caring for them, especially when thegoals of care have not been clearly established.

This is the most comprehensive study todate examining both the frequency and appro-priateness of investigations in cancer patients.We observed an overall decreasing trend inthe number of investigations over the courseof hospitalization; however, 28% of the pa-tients still had tests performed on the verylast day of life, despite the fact that 78% ofthe patients had the diagnosis of dying madea median of four days prior to death. Although

some of these tests might be justified as physi-cians searched for reversible causes of clinicaldeterioration, it was clear that many did notcontribute to the patient’s care and were thusunnecessary.12 Although there will inevitablybe an occasional patient who dies unexpect-edly, for example, of pulmonary embolus ormyocardial infarction, improving the abilityof clinicians to recognize patients who areactively dying and to differentiate them frompatients who may recover would help tominimize unnecessary investigations andtreatments.

We also introduced the concept of appropri-ateness of investigation in this study as an attemptto quantify this by the nature of subjective mea-sure. The inter-rater reliability between two inde-pendent observers was moderate. This outcomemeasure has face validity. For instance, imaginginvestigations and LFTs were more often orderedappropriately than CBCs and electrolytes, whichis consistent with clinical practice. In multivariateanalysis, the appropriateness of investigation wasassociated with both the frequency of testing andearly discontinuation of cancer therapy, whichhighlights the link between treatment and theneed for frequent monitoring. Further studiesare required to determine the validity and reli-ability of this measure.

A somewhat distressing finding is thatamong patients with far advanced cancer,38% received aggressive treatments withinthe last two weeks of life and 41% during thelast hospitalization. Given the fact that thegreat majority of these patients had poor per-formance status (ECOG $ 3), treatment wasprobably contraindicated in many. Indeed,therapy had to be terminated prematurely forabout half of all the patients on radiation,and for all the patients on chemotherapy. Al-though it is not unusual for patients to be ad-mitted or transferred to cancer centers withthe intention of starting antineoplastic treat-ments, oncologists carry the important respon-sibility of deciding whether therapy iswarranted and/or contraindicated, after as-sessing the patients. For the particular cohortin this study, therapy was not only futile, butcould be potentially harmful. Indeed, the liter-ature is filled with studies documenting theincreasing trends of chemotherapy use closeto the end of life,13,14 with hope beinga key reason behind both patients’15,16 and

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880 Vol. 38 No. 6 December 2009Hui et al.

oncologists’17 decision to pursue aggressivetherapies. Improved prognostication toolsthat help clinicians to identify patients whoare ‘‘actively dying,’’ coupled with treatmentdecision tools, can help limit the inappropri-ate use of potentially harmful therapies.

Compared to previously published studies ofhospitalized patients in general hospitals,4e6

goals of care milestones were establishedmore frequently at our institution, althoughstill suboptimally. Documentation of the diag-nosis of dying is arguably the most importantof the three, as it signals to the health careteam that the patient is close to the end oflife, yet it was established later and less fre-quently compared to DNR and supportivecare plans in our cohort. In some cases, itmay be clear in the clinician’s mind that thepatient is dying, but it has not been writtenin the chart; we argue that documentation isessential for establishment of this importantdiagnosis and for communication amongteam members. The delay in diagnosis of dyingis probably related to the technical difficultyand emotional hesitancy in establishing a ‘‘ter-minal’’ diagnosis. Indeed, no clear definitionfor ‘‘dying’’ exists. Nevertheless, symptomssuch as poor performance status, anorexia-cachexia, inability to swallow, dyspnea, anddelirium are suggestive of this diagnosis inpatients with advanced cancer. It is importantto recognize that the diagnosis of dying canbe made knowing that there is still a smallchance of recovery in some patients.18,19 In-deed, a frank discussion with patients and theirfamilies would provide an important opportu-nity to plan ahead, with the potential for im-proving the quality of end-of-life care.20

To our knowledge, this is the first study todemonstrate that early establishment of goalsof care milestones, particularly diagnosis ofdying, was associated with changes in clinicalpractice consistent with improved quality ofcare. However, the strength of correlationwas only mild to moderate overall, suggestingthe multifactorial nature and complexity ofclinical decision making. Importantly, thegoals of care milestones remained significantafter accounting for length of stay and otherclinical factors with multivariate analysis.Our finding is supported by a recent studythat demonstrated that the end-of-life discus-sions were associated with less aggressive

medical care near death and earlier hospicereferrals.9

We further analyzed the differences in prac-tice patterns between medical oncologists,radiation oncologists, and gynecologic oncolo-gists. The patients admitted under medical on-cology had more investigations, although nodifference in appropriateness of investigationwas found. This finding may suggest that med-ical oncology patients required more testingbecause of the intrinsic nature of their dis-eases, such as acute renal failure, liver dysfunc-tion, and infections. Importantly, it alsodistinguishes appropriateness of investigationas a measure that is distinct from frequencyof investigation. We found no significant dif-ferences among the three disciplines in regardto treatments or goals of care milestones,although this would need to be interpretedwith caution given the small sample size.

Limitations of this study include its retro-spective nature and the small sample sizefrom a single institution. First, the patientswho were transferred to other hospitals or hos-pices and died shortly after were not includedin this study; nevertheless, the proportion ofpatients who fit this profile is estimated to below, as oncologists in our institution generallyavoid transferring patients who are deemedto be imminently dying. For instance, therewere only 18 transfers to inpatient hospicesover the two-year study period. Second, weonly collected data from the last admission,and did not include prior information ongoals of care milestones or treatments. Likemany other institutions, however, our centerrequires a revisit of goals of care on each ad-mission, recognizing that the patient’s clinicalstatus and preferences evolve rapidly overtime. Thus, the information from the last ad-mission would be most representative for thepurpose of this study. Third, other importantaspects of quality of end-of-life care, such assymptom assessment and psychosocial inter-ventions, were not included in this study.Fourth, the use of ‘‘appropriateness of investi-gation’’ as an indicator of quality of care war-rants further validation. Finally, comparisonwith a group of advanced cancer patientswho were discharged alive from our cancercenter would be informative.

Findings from this study have important im-plications for the management of cancer

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Vol. 38 No. 6 December 2009 881End-of-Life Decision Making

patients at the end of life. On the basis of ourdata, we conclude that the cancer patients whodied at our tertiary care cancer center were in-vestigated and treated intensively during theirshort hospitalizations, suggesting that there re-mains much room for improvement in opti-mizing the quality of care. Importantly, thisstudy demonstrated that early recognition ofthe dying process may help to limit aggressivemeasures. To help patients and families navi-gate through times of uncertainties, cliniciansneed to be skilled at prognostication and com-munication, providing realistic expectations tofacilitate discussions surrounding goals of careand end-of-life issues. Further developments inthe areas of prognostication models, treatmentdecision tools for clinicians, decision-makingaids for patients, and integrated care pathwayscan help enhance the quality of care for ad-vanced cancer patients.

AcknowledgmentsWe would like to thank Mr. Ryan Wood for

his assistance in statistical analysis.

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