ORIGINAL ARTICLE

The oncology palliative care clinic at the Princess MargaretCancer Centre: an early intervention model for patientswith advanced cancer

Breffni Hannon & Nadia Swami & Ashley Pope & Gary Rodin & Elizabeth Dougherty &

Ernie Mak & Subrata Banerjee & John Bryson & Julia Ridley & Camilla Zimmermann

Received: 2 May 2014 /Accepted: 22 September 2014 /Published online: 4 October 2014# Springer-Verlag Berlin Heidelberg 2014

Abstract Several recently published randomized controlledtrials have demonstrated the benefits of early palliative careinvolvement for patients with advanced cancer. In the oncol-ogy outpatient setting, palliative care clinics are an ideal sitefor the provision of early, collaborative support, which can bemaintained throughout the cancer trajectory. Despite this,access to ambulatory palliative care clinics is limited, even attertiary cancer centres. Existing programs for outpatient palli-ative care are variable in scope and are not well described inthe literature. We describe the development and expansion ofan outpatient palliative care clinic at the Princess MargaretCancer Centre, Toronto, Canada, demonstrating how the clin-ic functions at a local and regional level. This clinic served asthe intervention for a recent large cluster-randomized trial ofearly palliative care. The model for this service can be adaptedby other palliative care programs that aim to provide early,integrated oncology care.

Keywords Palliative care . Advanced cancer . Earlyintervention . Outpatient clinic

Introduction

Early integration of specialized palliative care for patients withadvanced cancer leads to improved patient outcomes [1–4]and is increasingly recommended [5–7], but remains the ex-ception rather than the norm. Specialized palliative care ser-vices have traditionally been provided for inpatients, in palli-ative care units and by consultation services [8]. However,most cancer care occurs on an outpatient basis, and in order forpalliative care to be integrated early, outpatient palliative careconsultations and follow-up are necessary. Palliative careclinics provide an ideal venue for early palliative care involve-ment and for the collaborative integration of palliative careinto routine cancer care [1, 9–11]. However, many treatmentcentres still do not have outpatient palliative care clinics [9,12], and there have been few descriptions of such clinics in themedical literature [13]. One narrative review of 20 clinics hasbeen published, but this review presented summary statisticsrather than describing the detailed operational functioning ofindividual clinics [14].

Here we describe the development and structure of anoncology palliative care clinic (OPCC) in Toronto, Canada,which is integrated within a palliative care program at acomprehensive cancer centre and university hospital. Thisclinic was the main venue for an early palliative care inter-vention, which resulted in improved quality of life and in-creased satisfaction with care for patients with a wide rangeof cancer types [3]. We will describe how the clinic functionsand how it is integrated into the cancer program, both at thecancer centre and regionally, within the cancer system inToronto and Ontario.

B. Hannon : J. Bryson : C. ZimmermannDivision of Medical Oncology & Hematology, Department ofMedicine, University of Toronto, Toronto, Canada

E. Mak : S. Banerjee : J. RidleyDivision of Palliative Care, Department of Family and CommunityMedicine, University of Toronto, Toronto, Canada

G. Rodin : C. ZimmermannDepartment of Psychiatry, University of Toronto, Toronto, Canada

B. Hannon :N. Swami :A. Pope :G. Rodin : E. Dougherty :E. Mak : S. Banerjee : J. Bryson : J. Ridley :C. Zimmermann (*)Department of Psychosocial Oncology and Palliative Care, PrincessMargaret Cancer Centre, University Health Network, 610 UniversityAve., 16-712, Toronto, Ontario M5G 2 M9, Canadae-mail: camilla.zimmermann@uhn.on.ca

G. Rodin : C. ZimmermannCampbell Family Cancer Research Institute, Princess MargaretCancer Centre, University Health Network, Toronto, Canada

Support Care Cancer (2015) 23:1073–1080DOI 10.1007/s00520-014-2460-4

Palliative care in Toronto, Canada

Toronto is the capital of the province of Ontario, and thelargest city in Canada, with a population of approximately 3million (5.5 million in the Greater Toronto Area). Ontario isdivided into 14 health regions, or Local Health IntegrationNetworks (LHINs), which are responsible for health servicesin their communities, including hospitals and community careservices. The latter are provided by Community Care AccessCentres (CCACs), which organize and coordinate home careprovided by nurses, physiotherapists, social workers, dieti-tians, occupational therapists, personal support workers andothers, as well as providing home equipment and a drugbenefit program. Application for CCAC services requirescompletion of an electronic referral form, and the CCAC staffwork in close collaboration with the referring physician, whomay be a specialist or family physician, with an office- orcommunity-based practice. The range of services and maxi-mum nursing time provided are based on prognosis (estimatedby the referring physician) and on performance status, asmeasured by the Palliative Performance Scale (PPS) [15, 16].

Palliative care in Toronto is provided by hospital-basedpalliative care services, in acute and community palliativecare units, in hospices and at home. Home palliative care,including 24-h on-call coverage, is provided mainly bycommunity-based groups of physicians dedicated to provid-ing palliative care for patients in their community. Thesephysicians work closely with the CCAC and family physi-cians in their area and provide either primary palliative care orconsultative care. Because most family physicians in Torontohave office-based practices and rarely do house calls, special-ized home palliative care physicians provide most of the homepalliative care in Toronto. However, Cancer Care Ontario, theprovincial cancer control agency, has recently undertakenseveral initiatives to increase the palliative care involvementof primary care physicians [17].

Structure of the palliative care program at the PrincessMargaret Cancer Centre

The Princess Margaret Cancer Centre (PM) is the largestcentre in Canada for cancer care and research and is a partof the University Health Network (UHN). The UHN alsoincludes three other academic hospitals: Toronto GeneralHospital (TGH), Toronto Western Hospital (TWH) andToronto Rehabilitation Institute (TRI), all of which are affili-ated with the University of Toronto. PM is located in theToronto Central LHIN, which serves approximately 1.15 mil-lion residents. However, because PM is a tertiary cancercentre, the majority of patients attending the cancer centrereside in neighbouring Toronto LHINs or elsewhere in theprovince.

The palliative care program at PM is housed within theDepartment of Psychosocial Oncology and Palliative Care. Inaddition to daily palliative care clinics, the palliative careprogram also has a 12-bed acute palliative care unit (theLederman Palliative Care Centre) [18] and a 10-bed residen-tial hospice (Kensington Hospice). It is also part of the largerUHN palliative care program that includes inpatient consulta-tion services at all sites [19]. This represents one of the mostcomprehensive programs available in a North American can-cer centre and encompasses all of the key operational featuresfor hospital palliative care programs as outlined by the Centerto Advance Palliative Care [8].

Philosophy and evolution of the oncology palliative careclinic

The OPCC provides a venue for specialized early palliativecare of ambulatory patients with cancer. The emphasis is ontimely, collaborative care, and on fluid communication withthe various individuals and programs involved in the patient’songoing care; mainly, these are the patient and family, thereferring oncology team, CCAC care providers and the pa-tient’s family physician (Fig. 1). For this reason, care isprovided longitudinally, rather than in a single consultation,and telephone follow-up with patients and care providers is acrucial component of care.

The OPCCwas established in 2002, with a single physicianproviding consultations and follow-up in a once-weekly clin-ic. At that time, clinic space and a receptionist were shared

Fig. 1 Main providers of longitudinal care for ambulatory patients withadvanced cancer. OPCC Oncology Palliative Care Clinic, CCAC Com-munity Care Access Centre

1074 Support Care Cancer (2015) 23:1073–1080

with an oncology clinic.With a yearly increase in referrals, theclinic quickly grew in size. Currently, there are 22 half-dayclinics, including daily “stat” clinics for urgent referrals, toaccommodate the increased demand for both scheduled andurgent same-day consultations. There are now six palliativecare physicians, four palliative care nurses, one social workerand three to five residents and fellows who work in the OPCC.Physicians and nurses follow their own patients longitudinal-ly, to ensure consistency and continuity of care.

The referral process

Over the past decade, there has been a progressive acceptancewithin PM of the philosophy of early palliative care.Currently, approximately 75 % of the 1,300 new referralsyearly to the PM palliative care program are first seen in theOPCC. Referral criteria are broad: Any patient with advancedand progressive cancer in the UHN cancer program may bereferred, with no limitation on prognosis. Referrals are madeby a physician (generally the patient’s primary oncologist),using a standardized form. All consult requests are screenedand triaged daily by a palliative care physician prior to book-ing the appointment. For routine consultations, the mediantime from referral to consultation is approximately 2 weeks.Same-day referrals are accommodated in daily “stat” clinics.

The initial palliative care consultation

At the initial consultation, a palliative care physician and nurseconduct a thorough assessment and physical exam, taking 60to 90 minutes. The philosophy of palliative care is outlined atthe initial clinic visit, including the multidisciplinary approachto pain and symptom management, with an emphasis onimproving quality of life and providing continuity of care.Reassurance of close collaboration and ongoing communica-tion with the patient’s oncology team is reinforced.

The palliative care nurse administers the EdmontonSymptom Assessment System (ESAS) scale [20, 21] andtakes a brief history; the physician undertakes a complete chartreview, medical and psychosocial history. The patient’s per-formance status is recorded, using both the PPS [15, 16] andthe Eastern Cooperative Oncology Group (ECOG) [22] mea-sures. Nursing and medical recommendations for treatment,education and counselling are then discussed with the patientand family. These may include changes to medications, refer-ral to community services, and equipment and lifestyle tech-niques to help with symptom control. In general, the initialvisit tends to focus on introducing the palliative care team andaddressing physical and psychological symptoms, and discus-sions around advance care planning are deferred to subsequentvisits. Involvement of the palliative care social worker is

sought if there are specific social issues to address, such asfacilitating financial and advance care planning, or providingcounselling for families with young children.

Referrals are made, as needed, to services such as palliativeradiation oncology, psychosocial oncology and interventionalradiology, amongst others (Fig. 2). Most patients referred tothe clinic require some form of home assistance, which mayinvolve wound care, personal care, supervision of medica-tions, and symptom assessment. This is arranged through areferral to the patient’s local CCAC service. Patients areprovided with a resource binder that contains contact detailsfor the palliative care team; information on palliative care,spiritual care, community resources and advance care plan-ning; and the Canadian Cancer Society booklet, “Living withAdvanced Cancer” [23]. A complete note is dictated for thepatient’s electronic medical record and a copy is sent to thepatient’s oncologist and family physician.

Follow-up in the OPCC

After the initial consultation, patients who are still receivingchemotherapy or radiation at the PM are followed in theOPCC, generally at intervals of 1–3 months. Follow-up iscarried out in the OPCC, by telephone, and at times in theoncologist’s office or chemotherapy day care centre, if this ismore convenient for the patient. The PM palliative care teamcommunicates regularly with the CCAC home care nurses.All clinic patients have access to a 24-h on-call service staffedby palliative care physicians, so that urgent symptom issuescan be readily addressed.

Advance care planning is carried out according to the needsand readiness of the individual patient and family. This mayinclude discussion of resuscitation and completion of a “noCPR” form, assignment of a power of attorney for medicalcare, and completion of paperwork for local community pal-liative care units. Although most patients express a desire todie at home if possible, this paperwork is done as a “backup”for the possibility of eventual transfer to an inpatient setting.Patients work with the social worker to choose up to threecommunity units, based on factors such as location and prox-imity to family or friends, the level of care required, andestimated prognosis [24].

Transition of care at the end of life

Figure 3 shows typical pathways of care, culminating in end-of-life care either at home or at a palliative care unit orhospice. While early palliative care involves integrated,shared care by the palliative care team with oncologists,family physicians and community services, patients eventual-ly require transfer of care from the outpatient clinic setting to

Support Care Cancer (2015) 23:1073–1080 1075

Fig. 2 Typical referrals madefrom the OPCC. 1CommunityCare Access Centre servicesinclude nursing, personal support,physical therapy, occupationaltherapy and equipment such ashospital bed, walker andwheelchair. 2Medical/surgicalspecialists may includeneurosurgery, ophthalmology anddentistry. 3Other supportive careservices at the cancer centreinclude spiritual care, wound care,dietitian, music therapy, andoccupational or physical therapy.OPCC Oncology Palliative CareClinic, CCAC Community CareAccess Centre

Referral to Pallia�ve Care

Clinic

Home Pallia�ve Care

Lederman Pallia�ve Care

Centre

Community PCU/

Residen�al Hospice

Early Pallia�ve

Care

Transi�onaland end of

life care

Fig. 3 Pathways of palliativecare upon referral to OncologyPalliative Care Clinic. Note thatreferrals to other services byOncology Palliative Care Clinicstaff are not included in thisfigure. Longitudinal follow-up isusually weeks to months, but maybe days to years. Transfers of careto community palliative careunits, hospices or home palliativecare are for transitional and end-of-life care; transfers to theLederman Center may be for end-of-life care or symptom control

1076 Support Care Cancer (2015) 23:1073–1080

either the home setting or a hospice or palliative care unit. If apatient is able to manage at home, but not well enough tocome back and forth to the clinic, an enquiry is made whetherthe patient’s family physician is willing to make home visitsand provide 24-h on-call care. If not, patients are referred to aspecialized home palliative care physician providing care intheir community (either shared with the family physician or asthe most responsible physician). Some patients are quite ill atthe initial OPCC consultation and are transferred directly tothe Lederman Palliative Care Centre [18].

Waiting lists for home palliative care physicians can rangefrom 2 to 6 weeks, or longer. The OPCC palliative care teamcontinues to follow patients until they have been seen by thehome palliative care physician, at which time there is anofficial sign-over of care. However, patients are often referredback to the PM palliative care service for admission to theLederman Palliative Care Centre, either for urgent symptomcontrol or for terminal care. The OPCC palliative care teamcontinues to follow patients living in areas without access to ahome palliative care physician, either in person or by tele-phone in conjunction with community-based nurse practi-tioners, until their death or the time of admission to an inpa-tient facility.

Characteristics of patients referred to the OPCC

Table 1 shows the demographic characteristics and perfor-mance status of the patients referred to the OPCC in 2012.Most patients were referred for general symptommanagement(57 %) or more specifically, for pain control (32 %). Smallernumbers were referred for advance care planning (9 %) or forterminal care (2 %). Forty-nine percent were female, themedian age was 65 years (range 18–96), and the majoritywere from the gastrointestinal (26 %), lung (19 %) andgynaecological (12 %) disease sites. In terms of performancestatus, the majority of patients had an ECOG score of 1 or 2(39 and 42 %, respectively), or a PPS score of 60–70 % (70 %of patients). Most patients were referred by medical oncology(61 %) or radiation oncology (24 %). Table 2 shows the ESASscores of patients before their first consultation. The medianESAS Distress Score was 37 (range 0–86) with the worstsymptoms out of 10 being tiredness (median 7), and a medianof 5 each for pain, drowsiness, appetite, well-being and sleep.Most patients (97 %) had moderate to severe symptom ratings(i.e. rated greater than 4 on the ESAS scale) [25] and twopatients were asymptomatic (i.e. rated “0” for all symptoms).

Academic activities in the OPCC

The OPCC is not only a clinical service but also a site for theeducation of physicians, nurses and other health professionals

who desire training in outpatient palliative care. Residentsundertaking clinical electives may come from diverse disci-plines including medical, surgical or radiation oncology, in-ternal medicine, family medicine, anaesthesia and psychiatry.Fellows enrolled in 2-year research fellowships also followpatients in the OPCC on a longitudinal basis several days aweek, with supervision. The outpatient setting provides avenue for education in aspects that are less available in tradi-tional rotations in the palliative care unit or inpatient consul-tation services, such as monitoring and titrating pain andsymptom medications on an outpatient basis; advance careplanning; and early and ongoing communication with thepatient, family and other health care providers regarding thechanging goals of care. The clinic is also an important venuefor research, including for clinical trials, prospective, retro-spective and descriptive studies, and the validation or devel-opment of measures [26–33].

Discussion

There is increasing evidence for the effectiveness of introduc-ing palliative care early in the disease trajectory for patientswith advanced cancer. OPCCs are the obvious site for suchcare to be initiated and provided in a complementary fashionwith concurrent anticancer treatment. We have described themodel of care for the OPCC at our centre. This model has beenshown to improve quality of life, satisfaction with care, andsymptom control, both in a phase II trial and in a recentcluster-randomized controlled trial of early palliative careversus standard oncology care [3, 10].

Reported barriers to early palliative care referral include alack of available palliative care services, and the requirementby some of these services that patients have stopped chemo-therapy [34, 35]. Ongoing anticancer treatment should notpreclude referral to palliative care services [5], particularlybecause increasing numbers of patients continue to receivetreatment up until the last weeks to months of life [36]. Thistrend is likely to continue, given the advent of targetedtreatments that are effective later in the disease trajectory[37]. A Canadian survey confirmed that a higher referralfrequency was seen when palliative care services acceptedpatients receiving ongoing chemotherapy [34]. We encourageearly referral of patients receiving chemotherapy, and ourservice has grown to accommodate increased and earlierreferrals.

There is ongoing debate about the wisdom of renamingthe specialty or individual palliative care services “sup-portive care”. In a recent national survey of Canadianoncologists, one third stated that they would refer to palli-ative care earlier if it were renamed “supportive care” [34].Similarly, a recently published randomized trial reportedthat the term “supportive care” was viewed more

Support Care Cancer (2015) 23:1073–1080 1077

favourably than “palliative care” by patients with advancedcancer [38]. The palliative care service at MD AndersonCancer Center has observed earlier outpatient referralssince changing its name from palliative care to supportivecare in 2007 [39], although oncologists at that centre didnot think that the name change had influenced their referralpractices [40]. Other services have taken the stance thateducation, rather than a name change, is the way forward[41]. We have taken the latter approach, in that we explic-itly call our clinic the Oncology Palliative Care Clinic, butalso encourage early referrals and promote the message

Table 1 Characteristics of patients attending the Oncology PalliativeCare Clinic (N=849)

Patient characteristics Number (%),Mean [SD]

Sex

Male 437 (51)

Female 412 (49)

Age, in years 64 [13]

Cancer type

Gastrointestinal 217 (26)

Lung 163 (19)

Gynaecologic 105 (12)

Genitourinary 84 (10)

Head and neck 59 (7)

Breast 56 (7)

Hematologic 45 (5)

Central nervous system 44 (5)

Skin 26 (3)

Sarcoma 22 (3)

Unknown primary 18 (2)

Neuroendocrine 10 (1)

Primary reasons for referral

General symptom management 484 (57)

Pain control 276 (32)

Palliative care planning 76 (9)

Terminal care 13 (2)

Referring service

Medical oncology 518 (61)

Radiation oncology 201 (24)

Surgical oncology 64 (7)

Haematology 44 (5)

Othera 22 (3)

ECOG performance status (N=698)b

0 6 (1)

1 273 (39)

2 292 (42)

3 119 (17)

4 8 (1)

Palliative Performance Scale (N=699)c

80–100 56 (8)

Table 1 (continued)

Patient characteristics Number (%),Mean [SD]

60–70 492 (70)

40–50 148 (21)

10–30 3 (<1)

Data are for the year 2012. Performance status scores are those reportedon the first visit

SD standard deviationa Other includes palliative care physician from another University HealthNetwork (UHN) hospital site (N=9), psychosocial oncology department(6), other UHN physician (3), family physician (2) or unknown (2)b ECOG=EasternCooperativeOncologyGroup.AnECOGscore of 0=fullyactive at pre-disease performance, 1=ambulatory but restricted in physicallystrenuous activity, 2=not fully ambulatory and lying/sitting <50%of the day,3=capable of limited self-care and lying/sitting >50 % of the day, 4=completely disabled, unable to self-care and confined to lying/sitting [20]c Palliative Performance Scale (PPS) score of 80–100=fully ambulatory,60–70=reduced ambulation, 40–50=mainly lying/sitting and 10–30=bedbound [30]

Table 2 Self-reported symptoms by patients attending the OncologyPalliative Care Clinic (N=806)

Mean (SD) Median(range)

Number (%)of patientsrating ≥4

Symptom

Pain 5.23 (3.24) 5 (0–10) 541 (67)

Tiredness 6.28 (2.58) 7 (0–10) 685 (85)

Nausea 2.24 (2.83) 1 (0–10) 220 (27)

Depression 3.22 (2.97) 3 (0–10) 342 (42)

Anxiety 3.58 (2.99) 3 (0–10) 388 (48)

Drowsiness 4.28 (2.93) 5 (0–10) 486 (60)

Appetite problems 5.00 (3.12) 5 (0–10) 542 (67)

Well-being 5.19 (2.65) 5 (0–10) 593 (74)

Shortness of breath 3.25 (3.09) 3 (0–10) 345 (43)

Constipation 3.30 (3.34) 3 (0–10) 340 (42)

Sleep difficulties 4.50 (3.27) 5 (0–10) 456 (57)

Number (%) of patientswith at least onesymptom ≥4

- 783 (97)

Number (%) of patientswho are asymptomatic(all “0” scores)

- 2 (<1)

ESAS Distress Scorea

Median (range) 37 (0–86) -

Mean (SD) 38.24 (16.63) -

Data are for the year 2012; symptoms are those reported on the first visit

SD standard deviation, ESAS Edmonton SymptomAssessment System scalea ESAS Distress Score (EDS) is calculated by summing all items exceptconstipation and sleep difficulties, multiplying by the total number ofitems (9), and dividing by the total number of items answered, as long as>50 % of items are answered. EDS range is 0–90, with higher numbersrepresenting worse symptom severity. Three patients who answered<50 % of items were excluded from the EDS calculation

1078 Support Care Cancer (2015) 23:1073–1080

that palliative care is relevant throughout the illnesstrajectory.

The palliative care model at our institution is not neces-sarily reflective of service availability elsewhere. Access todaily OPCCs as well as an inpatient consultation team, anacute PCU and a residential hospice facilitates referral tothe palliative care program at all stages of disease and isresponsive to the needs of patients, their families andreferring oncologists. However, our OPCC began as asingle day clinic with one physician and expanded overtime, based on demand and advocacy for additional re-sources [19, 42]. A model of a weekly half-day clinicmay be more easily reproducible for smaller or newlyestablished programs [43].

Other centres have adopted different approaches to deliv-ering palliative care in the ambulatory setting. For example,in a model described at the MD Anderson Cancer Center,newly referred patients are seen sequentially over 4 to 5 h byvarious members of the multidisciplinary team. This processculminates in a team meeting and subsequent relaying of upto 13 different recommendations to patients and caregivers[42][13]. At our centre, while a variety of disciplines isavailable for patient support in the OPCC, individual patientneeds are assessed at each visit by a nurse and physician,and referrals are made to other palliative care specialists asrequired. Irrespective of the precise model of care, it isimportant that palliative care services are amenable to earlyreferral, do not have prohibitive policies such as lack ofacceptance of patients on chemotherapy, and are fully inte-grated within their parent institution as well as within thelocal community.

Early palliative care referral, and the opportunities thisaffords for earlier, phased discussions about end-of-life carepreferences, may help to improve symptom control, increasesatisfaction with care, clarify goals of care, reduce aggressive-ness of care at the end of life and help more patients to die in aplace of their preference. The model we have described isappropriate for cancer centres or hospitals with large outpa-tient cancer programs, and illustrates that a model of earlyoutpatient palliative care is feasible and effective. This modelcan be modified for smaller centres, or to include patients withnon-malignant diagnoses.

Acknowledgments We extend our thanks to all the interdisciplinarypalliative care team members who made the functioning of this clinicpossible. Special thanks to Catherine Purcell, Christine Cameron, MalkaBerman and Pat Cotman for their commitment to clinical and academicexcellence in developing our outpatient palliative care service. Thisresearch was funded by the Canadian Cancer Society (grant #700862;CZ), and the Ontario Ministry of Health and Long Term Care. Dr.Zimmermann is supported by the Rose Family Chair in Supportive Care,Faculty of Medicine, University of Toronto.

Conflict of interest There are no financial disclosures from any ofthe authors.

References

1. Temel JS, Greer JA, Muzikansky A, Gallagher ER, Admane S,Jackson VA, Dahlin CM, Blinderman CD, Jacobsen J, Pirl WF,Billings JA, Lynch TJ (2010) Early palliative care for patients withmetastatic non-small-cell lung cancer. N Engl J Med 363(8):733–742. doi:10.1056/NEJMoa1000678

2. Bakitas M, Lyons KD, Hegel MT, Balan S, Brokaw FC, Seville J,Hull JG, Li Z, Tosteson TD, Byock IR, Ahles TA (2009) Effects of apalliative care intervention on clinical outcomes in patients withadvanced cancer: the Project ENABLE II randomized controlledtrial. JAMA 302(7):741–749. doi:10.1001/jama.2009.1198

3. Zimmermann C, Swami N, Krzyzanowska M, Hannon B, Leighl N,Oza A, Moore M, Rydall A, Rodin G, Tannock I, Donner A (2014)Lo C (2014) Early palliative care for patients with advanced cancer: acluster-randomised controlled trial. Lancet 383(9930):1721–30. doi:10.1016/S0140-6736(13)62416-2

4. Mack JW, Cronin A, Keating NL, Taback N, Huskamp HA, MalinJL, Earle CC, Weeks JC (2012) Associations between end-of-lifediscussion characteristics and care received near death: a prospectivecohort trial. J Clin Oncol 30(35):4387–95. doi:10.1200/JCO.2012.43.6055

5. World Health Organisation (2010) WHO definition of palliative care.http://www.who.int/cancer/palliative/definition Accessed 17December 2013

6. Smith TJ, Temin S, Alesi ER, Abernethy AP, Balboni TA, Basch EM,Ferrell BR, Loscalzo M, Meier DE, Paice JA, Peppercorn JM,Somerfield M, Stovall E, Von Roenn JH (2012) American Societyof Clinical Oncology Provisional Clinical Opinion: the integration ofpalliative care into standard oncology care. J Clin Oncol 30(8):880–887. doi:10.1200/JCO.2011.38.5161

7. Foley K, Gelband H (eds) (2001) Improving palliative care forcancer: summary and recommendations. National Academies Press,Washington DC

8. Weissman DE, Meier DE (2008) Operational features for hospitalpalliative care programs: consensus recommendations. J Palliat Med11(9):1189–1194. doi:10.1089/jpm.2008.0149

9. Meier DE, Beresford L (2008) Outpatient clinics are a new frontierfor palliative care. J Palliat Med 11(6):823–828. doi:10.1089/jpm.2008.9886

10. Follwell M, Burman D, Le LW,Wakimoto K, Seccareccia D, BrysonJ, Rodin G, Zimmermann C (2009) Phase II study of an outpatientpalliative care intervention in patients with metastatic cancer. J ClinOncol 27(2):206–213. doi:10.1200/JCO.2008.17.7568

11. Rabow M, Kvale E, Barbour L, Cassel JB, Cohen S, Jackson V,Luhrs C, Nguyen V, Rinaldi S, Stevens D, Spragens L, Weissman D(2013) Moving upstream: a review of the evidence of the impact ofoutpatient palliative care. J Palliat Med 16(12):1540–9. doi:10.1089/jpm.2013.0153

12. Hui D, Elsayem A, De la Cruz M, Berger A, Zhukovsky DS, Palla S,Evans A, Fadul N, Palmer JL, Bruera E (2010) Availability andintegration of palliative care at US cancer centres. JAMA 303:1054–61. doi:10.1001/jama.2010.258

13. Strasser F, Sweeney C, Willey J, Benisch-Tolley S, Palmer JL,Bruera E (2010) Impact of a half-day multidisciplinary symptomcontrol and palliative care outpatient clinic in a comprehensivecancer centre on recommendations, symptom intensity, and patientsatisfaction: a retrospective descriptive study. J Pain SymptomManag 27(6):481–91

14. Smith AK, Thai JN, Bakitas MA, Meier DE, Spragens LH, TemelJS, Weissman DE, Rabow MW (2013) The diverse landscape ofpalliative care clinics. J Palliat Med 16(6):661–8. doi:10.1089/jpm.2012.0469

15. Anderson F, Downing GM (1996) Palliative Performance Scale(PPS): a new tool. J Palliat Care 12(1):5–11

Support Care Cancer (2015) 23:1073–1080 1079

16. Ho F, Lau F, Downing MG, Lesperance M (2008) A reliability andvalidity study of the Palliative Performance Scale. BMC Palliat Care7:10. doi:10.1186/1472-684X-7-10

17. Cancer Care Ontario (2013) Palliative Care Collaborative Care Plans(CCPs) End-of-Life Stage. Cancer Care Ontario. https://www.cancercare.on.ca/common/pages/UserFile.aspx?fileId=13620Accessed 17 December 2013

18. Bryson J, Coe G, Swami N, Murphy-Kane P, Seccareccia D, Le LW,Rodin G, Zimmermann C (2010) Administrative outcomes five yearsafter opening an acute palliative care unit at a comprehensive cancercentre. J Palliat Med 13(5):559–65. doi:10.1089/jpm.2009.0373

19. Zimmermann C, Seccareccia D, Clarke A, Warr D, Rodin G (2006)Bringing palliative care to a Canadian cancer centre: the palliativecare program at Princess Margaret Hospital. Support Care Cancer14(10):982–987

20. Bruera E (1991) The Edmonton Symptom Assessment System(ESAS): a simple method for the assessment of palliative care pa-tients. J Palliat Care 7:6–9

21. Chang VT, Hwang SS, Feuerman M (2000) Validation of theEdmonton Symptom Assessment Scale. Cancer 88(9):2164–2171

22. OkenMM, Creech RH, Tormey DC, Horton J, Davis TE, McFaddenET, Carbone PP (1982) Toxicity and response criteria of the EasternCooperative Oncology Group. Am J Clin Oncol 5:649–55

23. Canadian Cancer Society (2010) Living with Advanced Cancer.http://www.cancer.ca/en/support-and-services/resources/publications/?region=on Accessed 09 March 2014

24. Towns K, Dougherty E, Kevork N, Wiljer D, Seccareccia D, RodinG, Le LW, Zimmermann C (2012) Availability of services in Ontariohospices and hospitals providing inpatient palliative care. J PalliatMed 15(5):527–34. doi:10.1089/jpm.2011.0453

25. Selby D, Cascella A, Gardiner K, Do R, Morovan V, Myers J, ChowE (2010) A single set of numerical cutpoints to define moderate andsevere symptoms for the Edmonton Symptom Assessment System. JPain Symptom Manag 39(2):241–9. doi:10.1016/j.jpainsymman.2009.06.010

26. Cheung WY, Le LW, Zimmermann C (2009) Symptom clusters inpatients with advanced cancers. Support Care Cancer 17(9):1223–30.doi:10.1007/s00520-009-0577-7

27. Lo C, Burman D, Rodin G, Zimmermann C (2009) Measuringpatient satisfaction in oncology palliative care: psychometric proper-ties of the FAMCARE-Patient scale. Qual Life Res 16(6):747–52.doi:10.1007/s11136-009-9494-y

28. Zimmermann C, Burman D, Bandukwala S, Seecareccia D, Kaya E,Bryson J, Rodin G, Lo C (2010) Nurse and physician inter-rateragreement of three performance status measures in palliative careoutpatients. Support Care Cancer 18(5):609–16. doi:10.1007/s00520-009-0700-9

29. Riechelmann R, Burman D, Rodin G, Tannock I, Zimmermann C(2010) Phase II trial of mirtazapine for cancer-related cachexia. Am JHosp Palliat Med 27(2):106–10. doi:10.1177/1049909109345685

30. Zimmermann C, Burman D, Follwell M, Wakimoto K, SeccarecciaD, Bryson J, Le L, Rodin G (2010) Predictors of symptom severityand response in patients with metastatic cancer. Am J Hosp PalliatMed 27(3):175–81. doi:10.1177/1049909109346307

31. Ma C, Bandukwala S, Burman D, Bryson J, Seccareccia D, BanerjeeS, Myers J, Rodin G, Dudgeon D, Zimmermann C (2010)Interconversion of three measures of performance status: an empiricalanalysis. Eur J Cancer 46(18):3175–3183

32. Jang RW, Burman D, Swami N, Kotler J, Banerjee S, Ridley J, MakE, Bryson J, Rodin G, Le LW, Zimmermann C (2013) Impact of anoncology palliative care clinic on access to home care services. Am JHosp Palliat Med 30(5):425–31. doi:10.1177/1049909112452469

33. Jang RW, Caraiscos V, Swami N, Banerjee S, Mak E, Kaya E, RodinG, Bryson J, Ridley J, Le LW, Zimmermann C A simple prognosticmodel for patients with advanced cancer based on performancestatus. J Oncol Pract (in press)

34. Wentlandt K, Krzyzanowska M, Swami N, Rodin G, Le L,Zimmermann C (2012) Referral practices of oncologists to special-ized palliative care. J Clin Oncol 30(35):4380–6. doi:10.1200/JCO.2012.44.0248

35. Schenker Y, Crowley-Matoka M, Dohan D, Rabow MW, Smith CB,White DB, Chu E, Tiver GA, Einhorn S, Arnold RM (2013)Oncologist factors that influence referrals to subspecialty palliativecare clinics. J Oncol Practice [epub ahead of print]

36. Earle CC, LandrumMB, Souza JM, Neville BA, Weeks JC, AyanianJZ (2008) Aggressiveness of cancer care near the end of life: is it aquality of care issue? J Clin Oncol 26(23):3860–3866. doi:10.1200/JCO.2007.15.8253

37. Ho TH, Barbera L, Saskin R, Lu H, Neville BA, Earle CC (2011)Trends in the aggressiveness of end-of-life cancer care in the univer-sal health care system of Ontario, Canada. J Clin Oncol 29(12):1587–91. doi:10.1200/JCO.2010.31.9897

38. Maciasz RM, Arnold RM, Chu E, Park SY, White DB, Vater LB,Schenker Y (2013) Does it matter what you call it? A randomizedtrial of language used to describe palliative care services. SupportCare Cancer 21:3411–3419. doi:10.1007/s00520-013-1919-z

39. Dalal S, Palla S, Hui D, Nguyen L, Chacko R, Li Z, Fadul N,Scott C, Thornton V, Coldman B, Amin Y, Bruera E (2011)Association between a name change from palliative to supportivecare and the timing of patient referrals at a comprehensive cancercentre. Oncologist 16(1):105–11. doi:10.1634/theoncologist.2010-0161

40. Rhondali W, Burt S, Wittenberg-Lyles E, Bruera E, Dalal S(2013) Medical oncologists’ perception of palliative care pro-grams and the impact of name change to supportive care oncommunication with patients during the referral process. A qual-itative study. Palliat Support Care 11(5):397–404. doi:10.1017/S1478951512000685

41. Milne D, Jefford M, Schofield P, Aranda S (2013) Appropriate,timely referral to palliative care services: a name change will nothelp. J Clin Oncol 31(16):2055. doi:10.1200/JCO.2012.48.4493

42. Bruera E, Sweeney C (2001) The development of palliative care atthe University of Texas M.D. Anderson Cancer Centre. Support CareCancer 9(5):330–4

43. Muir JC, Daly F, Davis MS, Weinberg R, Heintz JS, Paivanas TA,Beveridge R (2010) Integrating palliative care into the outpatient,private practice oncology setting. J Pain SymptomManag 40(1):126–35. doi:10.1016/j.jpainsymman.2009.12.017

1080 Support Care Cancer (2015) 23:1073–1080