ORIGINAL RESEARCH Practice patterns and perceptions of survivorship care in Canadian genitourinary oncology: A multidisciplinary perspective Ashraf Almatar, M D f Suzanne Richter, MD M S cf Nafisha Lalani, M D f Jackie L. Bender, M D f David Wiljer, M D f Nour Alkazaz, B S cf Laura Legere, BScNf Manjula Maganti, M S cf Srikala S. Sridhar, MD, MSc, FRCPCf Pamela P. Cation, MD, MHPE, FRCPCf* Michael A.S. Jewett, MD, FRCSC '
‘ Deportments of Surgery (Urology) and Surgical Oncology, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON; fDepartment of Medical Oncology, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON; «Radiation Medicine Program, Princess Margaret Cancer Centre, University Health Network and thé University of Toronto, Toronto, ON; ’ ELLICSR: Health, Wellness and Cancer Survivorship Centre, Toronto General Hospital, University Health Network and the University of Toronto, Toronto, ON; 'Department of Biostatistics, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON
Cite as: Can t/ro //te o d 2 0 1 4 ;8 (ll-1 2 ):4 0 9 -1 7 . http://dx.doi.org/10.5489/cuai.2279 Published online December 15,2014.
Abstract Introduction: There is little knowledge of survivorship care specific to genitourinary (GU) cancers. To improve care delivery to this patient population, we need to clearly define physician perceptions of survivorship care. We therefore conducted a study to determine the challenges to GU cancer survivorship care in Canada. Methods: A web-based questionnaire was e-mailed to physicians treating GU cancers in Canada, including urologists, radiation oncologists, and medical oncologists. Five domains were assessed: demography, current post-cancer treatment care, perspectives on barriers to survivorship care, accessibility to survivorship resources, and perspectives about advocacy groups. Results: There were 306 responses, with 260 eligible for study. A total of 82% of physicians involve primary care practitioners (PCPs) at some point in survivorship care. Most physicians provide some form of written follow-up plan to PCPs. However, only 25% provided lifestyle recommendations and 53% included persistent and late effects of therapy. Lack of time or resources dedicated to survivorship care was the most commonly reported barrier. There was variation in accessibility to survivorship support programs among different subspecialties and regions. Advocacy groups generally were underutilized, particularly in testis cancer. Low response rate and the potential response bias are the main limita tions of this survey. Conclusion: To our knowledge this is the first study to address the challenges of GU cancer survivorship care in Canada. The barriers and accessibility of survivorship care quoted in this survey may be used to improve care for this group of patients. Underutilization of advocacy groups may stimulate the advocacy groups and institu tions to address its causes and solutions.
Introduction With improvements in healthcare systems, earlier cancer detection, and effective cancer treatments, the number of cancer survivors is rapidly increasing in Canada and may double by 2020.1-3 Cancer survivorship is generally felt to begin when primary treatment ends and survivorship continues until disease recurrence, second malignancy or death.2 Survivors face a range of complex medical and psychosocial issues.2 Genitourinary (GU) cancer patients constitute the largest single disease group of Canadian cancer survivors, account ing for over 50% of male cancer survivors and nearly 25% of all cancer survivors.4 However, according to a Canadian report, the proportional investment in prostate and bladder cancer survivorship research is well below what would be expected given the disease burden and there was notably no investment in kidney cancer survivorship.3 A Canadian GU survivorship meeting held in 2011 highlighted the urgent need for improved GU survivorship care. Meeting partici pants identified the value in (1) the collaboration between clinicians, researchers and cancer survivors/advocacy groups and (2) enhanced access to GU cancer survivorship resources and services.5 To date there is limited information regarding GU cancer survivorship care in Canada and worldwide. There have been many surveys assessing physician attitudes towards cancer survivorship for breast and colorectal cancer, but none for GU cancer. There have also been national stud ies in the United States and Canada to assess the attitudes of oncologists and primary care physicians (PCP) on the delivery of cancer survivorship care, but mainly for non-GU cancers.6,7 Finally, a 2008 Canadian report raised the issue that follow-up practice and services for cancer survivors are inconsistent across the country.8To address these gaps,
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w e e x a m in e d c u rre n t G U c a n c e r p h y s ic ia n s ' a ttitu d e and
v id e d fo r p a rtic ip a n ts to ch o o se th e ir p re fe rre d language.
p e rc e p tio n to w a rd can ce r s u rv iv o rs h ip care in Canada. W e
To e n h a n c e th e response rate, p o te n tia l p a rtic ip a n ts w e re
h yp o th e size d th a t there is hete ro g e n e ity in th e attitu de s and
given the o p p o rtu n ity upo n survey c o m p le tio n to enter th e ir
pe rce p tio n s o f G U ca n ce r ph ysicia n s to w a rd ca n ce r s u rv iv
names and c o n ta c t in fo rm a tio n fo r a d ra w fo r 1 o f 3 prizes
o rs h ip care and be tw e e n d iffe re n t s u b sp e cia ltie s in v o lv e d
w o rth $40 0 to $ 6 00. A n e m a il re m in d e r o f th e survey was
in the p rim a ry tre a tm e n t o f G U cancers. F urtherm ore, there
sent 2 w eeks fo llo w in g the in itia l e -m a il in v ita tio n .
m ay be g e o g ra p h ic v a ria b ility as health care is a p ro v in c ia l re s p o n s ib ility . F in a lly, fa c ilitie s at u n iv e rs ity -a ffilia te d hos
Statistical analysis
pitals m ay d iffe r fro m c o m m u n ity hospitals - th is m ay also D e s c rip tiv e statistics using SAS so ftw a re v e rsio n 9.2 w e re
c o n trib u te to the heteroge neity. F in a lly , p a rtic ip a n ts at th e 2011 C a n a d ia n G U s u rv iv
p e rfo rm e d . The c h i-s q u a re test w as used to assess associa
o rs h ip m e e tin g h ig h lig h te d th a t c lin ic ia n s and researchers
tio n betw e e n q u e stio n responses and d e m o g ra p h ic crite ria :
lacked awareness o f th e c a p a b ilitie s o f ca n ce r p a tie n t a d v o
(1) subspecia lty; (2) g e o g ra p h ica l region o f p ra ctice ; and (3)
cacy groups - w e have also addressed th is issue.5
p ra ctice base (u n ive rsity vs. c o m m u n ity hospital). A p s 0.05 was c o n sid e re d s ig n ific a n t fo r all tests. Surveys w ith d e m o g ra p h ic responses o n ly w e re ce n so re d fro m a nalysis. For
M e th o d s
c la rity , the 5 -p o in t Likert scale questions have been grouped in to 3 in th e analysis o f th e survey. Responses ne ve r and
Survey instrument development
rarely w e re gro u p e d as rarely; often and a lw a ys g ro uped as often. This p ro d u c e d 3 groups; often, som etim es and rarely.
O u r s u rv e y in s tr u m e n t w a s b a s e d o n q u e s tio n n a ir e s
The 5 -L ik e rt p o in t q u e stio n fo r th e a c c e s s ib ility o f s u rv iv o r
d e ve lo p e d at the R osw ell Park Institute in B u ffa lo 9 and the
s h ip care recourses w e re also g ro u p e d fo r a n a lysis: v e ry acce ssib le and a cce ssib le to e a s ily acce ssib le ; d iffic u lt to
E le c tro n ic L iv in g L a b o ra to ry fo r In te rd is c ip lin a ry C a n ce r S u rv iv o rs h ip Research (ELLICSR), a h e a lth , w e lln e s s and ca n ce r su rviv o rs h ip centre at Princess M a rg a re t H o sp ita l. In total, 27 questions w e re develop ed and categorized in 5 dom ains (1 ) p a rtic ip a n t d e m o g ra p h ic characteristics (8 ques tions); (2) c u rre n t post-tre a tm e n t care p ra c tic e (3 questions); (3) perspectives on barriers to p ra c tic in g s u rv iv o rs h ip care (4 questions); (4); a c c e s s ib ility to s u rv iv o rs h ip resources (7
access and v e ry d iffic u lt to access g ro u p e d to d iffic u lt to access p ro d u c in g (easily, m o d e ra te ly and d iffic u lt to access).
R e s u lts
questions); and (5) th e ir perspectives regarding G U advocacy groups (5 questions). Q u e stio n s w e re e ith e r m u ltip le c h o ic e
The survey w as d is trib u te d to 1775 ph ysicia n s: 632 u ro lo gists, 800 ra d ia tio n oncologists and 343 m ed ica l oncologists. N e a rly all urologists, 2 5 % o f C A M O m em bers and 10% o f C A R O m e m b e rs tre a t G U ca n ce rs. These la tte r n u m b e rs
o r 5 -p o in t u n ip o la r L ik e rt scale ty p e qu e stio n s (h ttp ://jo u rn a ls .s fu .c a /c u a j/in d e x .p h p /jo u rn a l/a rtic le /v ie w /2 2 7 9 /1 9 4 9 ).
w ere extrapolate d fro m the m em bership o f the a cadem ic G U o n c o lo g y societies. A to ta l o f 3 0 6 ph ysicia n s c o m p le te d the
A French language tra n s la tio n w as p ilo te d to assess c o m prehensio n and accura cy. The survey w as a p p ro ve d by the
survey o f the 8 0 0 estim ated to be e lig ib le , fo r a response rate o f 3 8 % (Fig. 1). W e ta llie d th e d e m o g ra p h ic characteristics
U n iv e rs ity H e a lth N e tw o rk Research Ethics Board.
o f p a rtic ip a tin g physicia n s (Table 1).
Survey administration
Practice patterns of GU physicians
T he w e b -b a s e d su rve y w as d is trib u te d b y e -m a il u sin g a secure, C anadian-based survey p la tfo rm 10 to a ll urologists, ra d ia tio n o n c o lo g is ts and m e d ic a l o n c o lo g is ts u sin g d is tr ib u tio n lists m a in ta in e d and p ro v id e d b y th e C a n a d ia n U ro lo g ic a l A sso cia tio n (C U A ), the C anadia n A sso cia tio n o f M e d ic a l O n co lo g ists (C A M O ) and the C anadian A ssociation o f R adiation O n c o lo g is ts (CARO ). W e used a non-targeted re c ru itm e n t strategy to c a p tu re b o th u n iv e rs ity - and c o m m u n ity -a ffilia te d ph ys ic ia n s . O n ly p h y s ic ia n s tre a tin g G U c a n c e r w e re in v ite d to access th e w e b -b a s e d surve y. A n
In p o st-tre a tm e n t s u rv iv o rs h ip care practices, a b o u t h a lf o f the respondents reported d is c h a rg in g patients to the PCP at som e p o in t d u rin g fo llo w - u p (Fig. 2). T here w as a s ig n ifi c a n t asso cia tio n b e tw e e n fo llo w -u p care p ra c tic e patterns a n d s u b s p e c ia lty , g e o g ra p h ic a l lo c a tio n o f p ra c tic e , and p ra c tic e base (u n iv e rs ity a ffilia te d vs. c o m m u n ity hospitals) (p < 0.05). A m o n g the ra d ia tio n o n co lo g ists (n = 90), 75% o f respondents discharged su rvivo rs at som e p o in t to the PCP c o m p a re d to m e d ic a l o n co lo g ists at 5 3 % (n = 45) o r u ro lo gists a t 4 2 % (n = 125). C o n v e rs e ly , u ro lo g is ts w e re m ost
in fo rm e d co n se n t sta te m e n t app e a re d in th e e -m a il s c rip t and c o m p le tio n o f th e su rve y in d ic a te d im p lie d co n se n t.
lik e ly to share fo llo w -u p care w ith the PCP in d e fin ite ly (37%) com pared to m ed ica l oncologists (22% ) and ra d ia tio n o n c o l
The lin k s to b o th English a n d French v e rsio n s w e re p ro
ogists (13% ). U rologists w e re m ore lik e ly to e x c lu d e the PCP
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Fig. 1. Pattern of responses from the various physician groups.
from cancer-related follow -up (18%) compared to radiation oncologists (7%) and medical oncologists (4%). There was wide geographic variation in post-treatment follow -up care (Fig. 3). Physicians working in university-affiliated hospitals were most likely to discharge survivors at some point to the Table 1. Dem ographics o f th e responders Frequency Percentage ______ ________________________________ (n = 260) (%) Subspecialty Urology
125
Medical Oncology
45
17
Radiation Oncology
90
35 12
48
Region of practice British Columbia
32
Prairie provinces
46
18
Ontario
121
47
Quebec
41
16
Atlantic Canada
19
7
0.05).
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6%
Others
Discharge follow-up care at some point to the PCP
26%
Share follow-up care with the PCP indefinitely
Continue specialist follow-up care indefinitely EXCLUDING the GP
12%
_i______ I 20
10
30
40
50
60
Fig. 2. Frequency of follow-up care patterns. GP: general practitioner; PCP: primary care practitioner.
Physician's perspective of accessibility of services to patients
There was an association between geographical location of practice and reported difficulties in accessing rehabilitation programs (p < 0.05). W hile 91% (n = 32) of physicians in British Colombia reported difficulty, participants from other areas reported lower rates of difficulty (44% [n = 18] for the Atlantic provinces, 42% [n = 41 ] for Quebec, 37% [n = 117] for Ontario and 31% [n = 45] for the Prairies). Physicians practicing in com m unity hospitals reported greater d ifficu lty in accessing survivorship care services compared to physicians at academic centres: psychosocial support (48% vs. 18%), pain management (20% vs. 12%), fe rtility (46% vs. 20%) and genetic counselling programs (48% vs. 29%), respectively (p < 0.05).
O f the respondents, 44% (n = 254) reported that cancer rehabilitation programs were most d ifficu lt to access. The other services were less frequently difficult to access: genetic counselling (38%), fertility counselling (30%), and psycho social support (30%) (Fig. 6). W e observed an association between difficulty in accessibility and the use of psycho social support and genetic counselling programs w ithin the subspecialty groups (p < 0.05). W h ile 45% (n = 123) of urologists reported difficu ltly accessing psychosocial sup port programs, only 23% (n = 43) of medical oncologists and 10% (n = 88) of radiation oncologists reported sim i lar experiences. Sim ilarly, 48% of urologists and 35% of radiation oncologists reported difficulty accessing genetic counselling, compared to only 14% of medical oncologists.
British Columbia
41%
Prairies
13%
Ontario
13%
1m
53%
3%
1
4%
78%
20%
9%
58%
Continue specialist follow-up care indefinitely EXCLUDING the GP follow-up care with the PCP □ Share indefinitely Discharge follow-up care at some point to the PCP Others
Quebec
29%
Atlantic
31%
i l l 2%
53%
I__________ i__________ i__________ i----------------1----------------1----------------1
0
20
40
60
80
100
120
Fig. 3. Post-treatment follow-up care in different regions.
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Summary of cancer status, including diagnosis and stage
87%
Summary of treatment given, including toxicities experienced
Expected persistent and late effects of therapy
Surveillance guidelines for identifying recurrent disease/second primary and/or late effects
82%
Lifestyle recommendations
100
f ig. 4. When a written care plan was provided, what components were included? (n = 230).
Referrals to patient advocacy groups
likely to refer patients to prostate cancer advocacy groups (62%) compared to radiation oncologists (42%) and medical oncologists (32%). There was an association between the frequency of refer ral to Prostate Cancer Canada and the geographical location of practice (p < 0.05). Physicians from Quebec were the least likely to refer patients to prostate cancer advocacy groups 30% (n = 40). In total, 248 respondents selected 3 initiatives to collaboratively enhance survivorship care with the advocacy groups (in order of preference): (1) create a website to describe all relevant cancer advocacy groups, community supports and their services (81%); (2) create a pamphlet to describe
Overall, referral to patient advocacy groups is low for all physicians caring for CU cancer survivors (Fig. 7). W hile there was no association between referral rates to Testicular Cancer Canada and the different subspecialties, differences were observed for bladder, prostate and kidney cancer advo cacy groups (p < 0.05). Urologists were the most likely to refer to bladder advocacy groups 26% (n = 121 ) compared to 21% (n = 43) and 2% (n = 84) for medical oncologists and radiation oncologists, respectively. Medical oncologists refer patients to kidney cancer advocacy groups more fre quently than urologists (51% vs. 27%). Urologists were most
Lack of physician knowledge of cancer survivorship issues and recomm ended surveillance practices
Lack of practice guidelines to follow
Lack of tim e or resources to support patients through this phase of the cancer experience
Lack of patient engagem ent or adherence to recomm endations
0
20
40
60
80
100
120
Fig. 5. Barriers to meeting the post-treatment care needs of survivors? (n = 254).
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Information and education about potential late effects due to cancer Opportunities to interact with other survivors Psychosocial support
| Difficult to access
Pain and symptom managementm programs
I I Moderately accessible 3 Easily accessible
Access to cancer rehabilitation programs Fertility counselling and resources Genetic counselling 0
20
40
60
80
100
120
Fig. 6. Accessibility of services to individual physician’s patients (n = 254).
all relevant cancer groups and community support services (56%); and (3) to create learning opportunities to educate healthcare professionals on the function and credibility of patient advocacy groups (38%).
Discussion This study evaluated Canadian GU cancer physician sur vivorship care attitudes, perceptions and practices. To our knowledge, this is the first study of its kind from Canada. Several models for survivorship care delivery have been proposed.2'11’13 One ideal care model is that of shared care of follow -up between the cancer specialist and the PCP.2 In our survey, only one-quarter of GU cancer specialists share survivorship care with PCPs indefinitely, w hile more than
half of them discharge patients at some point to PCP. W ith the increased number of cancer survivors that require follow up care, this may result in a decreased capacity for cancer specialists to attend to new cancer patients. A reasonable solution would be to involve PCPs in follow-up. Regardless of which approach is employed, it should fu lfil the major components of cancer survivorship care as outlined by the Institute of M edicine, including prevention of recurrence and new cancers, surveillance for recurrence and late side effects; intervention for treatment related consequences, and the coordination between the specialist and PCP to ensure all the survivors needs are met. It is critical to patient care that this transfer from specialist care to PCP care be smooth. For this to occur (1 ) PCPs need to be w illin g to assume care of survivors, (2) patients need
Fig. 7. Rates of patient referral to Canadian Genitorurinary patient advocacy groups (n = 248).
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to be satisfied w ith PCP fo llo w -u p , and m ost im p o rta n tly (3)
P ro v id in g PCPs w ith g u id e lin e s and m o re in fo rm a tio n on
th e re sh o u ld be c o m m u n ic a tio n b e tw e e n th e ca n c e r spe
the m anagem e nt o f tre a tm e n t side effects m ay im p ro v e th e ir c o n fid e n c e in ca rin g fo r G U ca n ce r survivors.
c ia lis t and the PCP. C anadia n PCPs are w illin g to take part in th e m ana g e m e n t o f ca n ce r s u rvivo rs and even ta ke fu ll
M a n y b a rrie rs to c a n c e r s u rv iv o rs h ip ca re h a ve been
re s p o n sib ility after c o m p le tio n o f a ctive tre a tm e n t if they are p ro v id e d w ith th e a p p ro p ria te in fo rm a tio n and g u id e lin e s
re p o rte d and these w e re c le a rly su m m a riz e d in th e re p o rt b y th e In s titu te o f M e d ic in e .2 From a C a n a d ia n re p o rt in
fo r f o llo w u p .14' 17 A su rve y o f breast c a n c e r s u rv iv o rs by G ru n fe ld and colleagu es in 2 0 0 6 noted th a t m ost patients acce pt th e ir PCP ta kin g re sp o n s ib ility o f th e ir ca n ce r fo llo w
2 0 0 8 , a la ck o f fin a n c ia l resources w as th e m ost c o m m o n b a rrie r in ca n c e r s u rv iv o rs h ip care, fo llo w e d b y a la ck o f
up, a lth o u g h 4 5 % w e re u n w illin g to be tra n s fe rre d .18 To o v e rco m e this issue it has been suggested th a t PCPs b ecom e
In o u r survey, ph ysicia n s u n iv e rs a lly rep o rte d a la c k o f tim e and resources regardless o f su b sp e cia lty, p ra c tic e lo c a tio n
in v o lv e d e a rly in th e s u rv iv o r's e x p e rie n c e using a shared
o r p ra c tic e base. These are im p o rta n t barriers th a t sh o uld be studied fu rth e r. To im p ro v e care, it appears th a t th e p h ys
care m odel th a t encourages c o n tin u e d c o m m u n ic a tio n and c o o rd in a tio n betw een the PCP and ca n ce r s p e c ia lis t.19 This m ay encourage the p a tie n t to d e v e lo p trust in th e care p ro v id e d by th e ir PCP so th a t w h e n the tra n s itio n happens they
m odels fo r fo llo w -u p care and e vidence -b ased g u id e lin e s .8
ic ia n needs to d e vo te tim e to understand the p a tie n t's sup p o rtiv e care needs (such as p s y c h o so cia l and o th e r issues related to s u rv iv o rs h ip care) w h ic h w o u ld re q u ire a d d itio n a l
are co m fo rta b le . The A m erica n Society o f C lin ic a l O n c o lo g y strongly recom m ends effective c o m m u n ic a tio n betw een the
re im b u rse m e n t to p h y s ic ia n s .28 A lack o f p ra c tic e g u id e lin e s w as th e second m ost c o m
s p e c ia list and th e PCP to ensure a c o n tin u u m o f care in to p rim a ry p ra c tic e .20 M o st o f the G U physicia n s w h o p a rtic i
m o n ly c ite d b a rrie r to th e p ro v is io n o f s u rv iv o rs h ip care. C urrent guidelin es fo r G U cancer care focus on the detection
pated in this survey w o u ld p ro v id e w ritte n plans to PCPs, a lth o u g h these plans tend to lack im p o rta n t details, such as re co m m e n d a tio n s fo r the m anagem e nt o f persistent and late
o f n e w o r re cu rre n t cancers. These g u id e lin e s la ck in fo rm a tio n on o th e r im p o rta n t aspects o f s u rv iv o rs h ip care, such as life style re co m m e n d a tio n s and psychosocia l d y s fu n ctio n .
effects o f tre a tm e n t and life s ty le re c o m m e n d a tio n s .21-22 To enhance c o m m u n ic a tio n , im p le m e n ta tio n o f a standardized te m p la te fo r d ic ta tio n to th e PCP w as s h o w n to im p ro v e PCP satisfaction regarding the in fo rm a tio n p ro v id e d 23 - this m ay im p ro v e p a tie n t c o n fid e n c e in th e PCP p ro v is io n o f fo llo w -u p care.
M o st g u id e lin e s also lack in fo rm a tio n on h o w to assess and m anage persistent and late effects o f ca n ce r tre a tm e n t. The d e v e lo p m e n t and d is s e m in a tio n o f s ta n d a rd iz e d s u rv iv o r
C ancer survivors are at an increased risk o f d e v e lo p in g a se cond c a n ce r, c a rd io v a s c u la r disease, d ia b e te s m e llitus, osteoporosis and o th e r c h ro n ic illnesses. These can be caused by th e ir cancer treatm ent o r lifestyle factors o r predis positions. Lifestyle factors are m o d ifia b le , and re co m m e n d a tio n s are supported by the Institute o f M e d ic in e re p o rt and th e A m e ric a n C ancer S ociety (ACS).2-24-25 M o st respondents p ro vid e d a w ritte n plan; how ever, lifestyle recom m endatio ns w e re often no t in c lu d e d . This m ay be due to the sp ecialist's e xp e ctatio n th a t th e PCP w ill e x p lo re th is w ith the p a tie n t or th a t the specialist provides this in fo rm a tio n v e rb a lly . W e d id n o t s p e c ific a lly ask if the specialist's p ro v id e life style re co m m e n d a tio n s, b u t in a survey c o n d u c te d by K id n e y C ancer C anada (KCC) to assess the types o f in fo rm a tio n p ro v id e d to p a tie n ts b e fo re and afte r surgery, o n ly 5 0 % o f pa tie n ts rece ived life style re co m m e n d a tio n s fro m th e ir u ro lo g is t.26 It is n o t c le a r w h a t percentag e receive th is re c o m m e n d a tio n e ither from the specialists o r PCP, thus w e reco m m e n d better c o m m u n ic a tio n w ith th e PCP. In terestingly o n ly h a lf o f G U physicia n s w h o p a rtic ip a te d in th e survey p ro v id e d in fo rm a tio n and g u id e lin e s fo r the m a n a g e m e n t o f p e rsiste n t and late effects o f tre a tm e n t in th e ir w ritte n p la n to th e PCP. T he lite ra tu re suggests th a t PCPs are less c o n fid e n t in m a n a g in g late s id e e ffe c ts .27
s h ip care g u id e lin e s and assessm ent to o ls fo r G U c a n c e r is an im p o rta n t goal. To fu rth e r adva n ce s u rv iv o rs h ip care, in n o va tive m odels th a t reduce cost and im p ro ve e ffic ie n c y o f care are needed. T heir d e v e lo p m e n t w ill depend on research fu n d in g , s c ie n tific rigor, kn o w le d g e tra n sla tio n o p p o rtu n itie s at early stages o f tra in in g and focus on patient-cen tered q u a l ity o f care. The differences in p ra ctice patterns betw een aca d e m ic and c o m m u n ity o n co lo g ists also in d ic a te th a t m odels and g u id e lin e s m ust also be re le va n t to the setting in w h ic h the p a tie n t is b e in g treated. A lth o u g h re h a b ilita tio n is im p o rta n t fo r c a n c e r s u rv iv o rs ,2-29'33 a b o u t o n e h a lf o f G U p h y s ic ia n s in o u r s tu d y re p o rte d d if fic u ltly in acce ssin g re h a b ilita tio n p ro g ram s. Little v a ria tio n was fo u n d betw een regions, except fo r British C o lu m b ia w h e re m o re (91% ) G U p h y s ic ia n s re p o rte d d if fic u lty . It is n o t k n o w n , h o w e ve r, w h e th e r these lo w levels o f a c c e ssib ility re fle ct a lack o f a v a ila b le program s o r m erely a lack o f k n o w le d g e o f th e ir existence and, co n s e q u e n tia lly, underuse. U ro lo g ists are the least lik e ly to refer patients fo r p s ych o social su p p o rt and g enetic c o u n s e llin g , w ith a b o u t 5 0 % of urologists re p o rtin g d iffic u lty w ith access. Since these servi ces appeared to be easily accessible by o th e r subspecialties, the observed u n d e ru tiliz a tio n m ay be due to lo w levels o f aw areness o f these services o r o f sp e c ific p a tie n t needs. W e also fo u n d th a t G U c a n c e r a d v o c a c y gro u p s w e re u n d e ru tiliz e d . The m ost c o m m o n ly used a d v o c a c y g ro u p
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was for prostate cancer. This may be because it is the most established in Canada and prostate cancer is the most com mon GU cancer. To explore means to enhance collaboration between advocacy groups and GU cancer physicians, we asked respondents to rank initiatives proposed by the GU cancer survivorship conference consensus. 5 Respondents felt that written information, electronic information and learning opportunities provided by the advocacy groups were most likely to improve collaboration. Limitations of this study include our inability to verify that respondents in fact treated GU cancer and which respond ents were trainees. The survey was directed to GU cancer physicians and may not be applicable to other cancer site groups. Close-ended questions may have limited the strength of the responses. Answers assessing the accessibility of ser vices may be biased toward the awareness of the physician, rather than represent a true lack of services. We acknow ledge that the practice patterns may differ according to the stage of the disease, which is not covered in this survey. We did not include it for the sake of brevity - a long survey may have affected our response rate. This issue may need to be covered in a future survey. The response rate appears low, but it is comparable to other web-based surveys of health providers. W e chose a web-based survey to appeal to the busy physician responders, w h ile recognizing the poten tial lower response rate. Other survey methods by mail or telephone w ould have enhanced the rate. The results may also be subject to bias because respondents may have been more interested in cancer survivorship. This is an exploratory study, and stratification was done to better understand the associations among the variables. Proportions and p values may be specific to the study population, but may not be generalizable. Future studies w ould be helpful in further validating our results.
Conclusion and practice implications Canada has well-developed patient advocacy groups and other organizations that provide survivorship support. Most GU cancer physicians discharge survivors to PCPs at some point after treatment. There is variability in practice between different GU subspecialties, geographical areas of practice and practice bases (university affiliated vs. community hospi tals). GU specialists do not appear to provide sufficient infor mation to the PCP. Lack of physician time and the limited availability of other resources are key barriers to providing survivorship care and may lim it physician cooperation. GU physicians lack knowledge about available cancer survivor ship care facilities. Advocacy groups are underutilized with variation between subspecialties and geographical location of practice. The findings from our survey highlight several areas that require further investigation.
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We recommend that a standardized dictation template. This tem plate w ould include inform ation on diagnosis, treatment received, record of side effects experienced dur ing and after treatment, expected short- and long-term side effects with management options, guidelines for follow-up, including screening for recurrence of disease, proposed caregiver responsibilities, and a list of available services and programs including relevant advocacy groups. Lack of physician knowledge about survivorship care appears to be an important barrier. The inclusion of cancer survivorship issues in the curricula of Canadian medical schools and in rotations for PCP residency programs would improve phy sician awareness. Developing and supporting standardized programs and services for patients, as w ell as inform ing physicians about survivorship care programs and facilities, may increase awareness and positively affect access. We recommend involving advocacy groups to help educate physicians about their services to increase the utilization of these groups. Competing interests: Dr. Almatar, Dr. Richter, Dr. Lalani, Dr. Bender, Dr. Wiljer, Dr. Alkazaz, Dr. Legere, Dr. Maganti, Dr. Sridhar and Dr. Catton have no competing financial or personal interests. Dr. Jewett is a member of the Advisory Board for Pfizer. He has also received grants from Novartis, GSK and Pfizer. Lostly, he has participated in clinical trials with Novartis, GSK and Pfizer.
This paper has been peer-reviewed.
References 1. Canadien Cancer Society's Steering Committee on Cancer Statistics. Canadian Cancer Statistics 2012. Toronto, ON: Canadian Cancer Society; 2012. http://bit.ly/lybPhD6. Accessed November 26, 2014. 2. Hewitt M, Greenfield S, Stovall E. From cancer patient to cancer survivor: Lost in transition. Washington: The National Academies Press; 2006. http://www.nap.edu/openbook.php?record_id=l 1468. Accessed November 26, 2014. 3. Canadian Cancer Research Alliance. Investment in Research on Survivorship and Palliative and Fnd-of-Life Care, 20 05 -200 S : A Special Report from the Canadian Cancer Research Alliance’s Survey of Government Voluntary Sector Investment in Cancer Research. Toronto: CCRA; 2011. http://www.partnershipagainstconcer.co/wp-content/uploods/Survivorship_E.pdf. Accessed November 26, 2014. 4. Gilbert SM, Miller DC, Hollenbeck BK, et ol. Cancer survivorship: Challenges ond changing paradigms. 1 (to /2008;179:431-8. http://dx.doi.org/! 0.1016/j.juro.2007.09.029 5. Bender JL, Wiljer D, Matthew A, et al. Fostering partnerships in survivorship care: Report of the 2011 Canadian genitourinary cancers survivorship conference. J CancerSurviv2012;6:296-304. http://dx.doi. org/10.10 0 7 /s l 1764-012-0220-3 6. Cheung WY, Aziz N, Noone AM, et ol. Physician preferences and attitudes regarding different models of cancer survivorship care: A comparison of primary care providers and oncologists, i Cancer Surviv 2013;7:343-54. http://dx.doi.org/10.1007/sll764-013-0281-y 7. Potosky AL, Han PK, Rowland J, ef ol. Differences between primary care physicians' and oncologists' knowledge, attitudes and practices regarding the core of cancer survivors. J Gen Intern Med 2011 ;26:140310. http://dx.d 0i.0rg /l 0.10 0 7 /s l 1606-011-1808-4 8. Ristovski-Slijepcevic S. Environmental Scan of Cancer Survivorship in Canada: Conceptualization, Practice and Research. British Columbia Cancer Agency: Vancouver, British Columbia; 2008. 9. Goge EA, Pailler M, Zevon MA, et ol. Structuring survivorship care: Discipline-specific clinician perspectives. J Cancer Surviv 2011;5:217-25. http://dx.doi.org/10.1007/sll764-011-0174-x 10. FluidSurveys. www.fluidsurveys.com. Accessed November 26, 2014.
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11. Aziz NM, Oeffinger KC, Brooks S, et ni. Comprehensive long-term follow-up programs for pediatric cancer survivors. Cancer 2006;107:841-8. http://dx.doi.org/10.1002/cncr.22096 12. MacBride SK, Whyte F. Survivorship ond the cancer follow-up clinic. Cur J Cancer Care (Engl) 1998;7:4755. http://dx.doi.O rg/10.1046/j.1365-2354.1998.00065.x 13. Oeffinger KC, McCabe MS. Models for delivering survivorship care. J Clin Oncol 2006;24:5117-24. http://dx.doi.org/10.1200/JCO .2006.07.0474 14. Worster A, Bass M l, Wood ML. Willingness to follow breast cancer. Survey of family physicians. Can Earn Physician 1996;42:263-8. 15. Norman A, Sisler J, Hack T, et ol. Family physicians and cancer care. Palliative care patients' perspectives. Can Fam Physician 2001;47:2009-12, 2015-6. 16. Songster JF, Gerace TM, Hoddinott SN. Family physicians' perspective of patient care at the London regional concer clinic. Can Fam Physician 1987;33:71-4. 17. Del Giudice ME, Grunfeld E, Harvey BJ, et al. Primary care physicians' views of routine follow-up care of cancer survivors. J Clin Oncol 2009;27:3338-45. http://dx.doi.O rg/l 0.1200/JC0.2008.20.4883 18. Grunfeld E, Levine MN, Julian JA, et al. Randomized trial of long-term follow-up for early-stage breast cancer: A comparison of family physician versus specialist care. J Clin Oncol 2006;24:848-55. h ttp :// dx.doi.org/10.1200/JC 0.2005.03.2235 19. Maiedema B, Tatemichi S, MacDonald I. Cancer follow-up care in New Brunswick: cancer surveillance, support issues and fear of recurrence. Can J Rural Med 2004;9:101-7. 20. McCabe MS, Bhatia S, Oeffinger KC, et ol. American Society of Clinical Oncology statement: Achieving high-quality cancer survivorship care. J Clin Oncol 2013;31:631-40. h ttp ://d x .d o i.o rg /1 0 .1 2 0 0 / JC0.2012.46.6854 21. Dworkind M, Towers A, Murnaghan D, et al. Communication between family physicians and oncologists: Qualitative results of an exploratory study. Cancer Prev Control 1999;3:137-44. 22. Barnes EA, Hanson J, Neumann CM, et al. Communication between primary care physicians and radiation oncologists regarding patients with cancer treated with palliative radiotherapy. J Clin Oncol2000;18:2902-7. 23. Braun TC, Hagen NA, Smith C, et al. Oncologists and family physicians. Using a standardized letter to improve communication. Can Fam Physician 2003;49:882-6.
24. Rock CL, Doyle C, Demark-Wahnefried W, et al. Nutrition and physical activity guidelines for cancer survivors. C4 Cancer J Clin 2012;62:243-74. http://dx.doi.org/10.3322/caac.21142 25. Demark-Wahnefried W, Jones LW. Promoting a healthy lifestyle among cancer survivors. Hematol Oncol Clin North Am 2008,22:319-42, viii. http://dx.doi.org/10-l 016/|.hoc.2008.01.012 26. A Survey of Canadian Kidney Cancer Patients/Caregivers and Urologists Their Views on Survivorship Care, http://www.kidneycancercanada.ca/media/94560/412.pdf. Accessed November 26, 2014. 27. Skolorus TA, Holmes-Rovner M, Northouse LL, et al. Primary core perspectives on prostate concer survivorship: Implications for improving quality of care. Urol Oncol 2013;31:727-32. http ://d x.d o i. org/10.1016/j.urolonc.2011.06.002 28. Irwin M, Klemp JR, Glennon C, et al. Oncology nurses' perspectives on the state of cancer survivorship care: Current practice and barriers to implementation. Oncol Nuts Forum 2011;38:E11-9. http://dx.doi. org/10 .1 1 8 8 /1 1.0NF.E11-El 9 29. Cheville AL, Beck LA, Petersen TL, et al. The detection and treatment of concer-related functional prob lems in an outpatient setting. Supportive Care Cancer 2009;17:61-7. h ttp ://d x.d o i.o rg /1 0 .1 0 0 7 / S00520-008-0461-X 30. Guo V, Shin KY, Hainley S, et ol. Inpatient rehabilitation improved functional status in asthenic patients with solid ond hematologic malignancies. Am J Phys Med Rehabil 2 011;90:265-71. h ttp ://d x.d o i. org/10.1097/PHM .0b013e3182063ba6 31. Thorsen L, Gjersef GM, Loge JH, et al. Cancer patients' needs for rehabilitation services. Acta Oncol 2011;50:212-22. http://dx.d 0i.0r g /l 0 .3109/0284 186X.2010.531050 32. Silver JK. Strategies to overcome cancer survivorship care barriers. PM R 2011;3:503-6. http://dx.doi. org/10.1016/j.pmrj.201 1.04.014 33. Alfano CM, Ganz PA, Rowland JH, et al. Cancer survivorship and cancer rehabilitation: Revitalizing the link. J Clin Oncol 2012;30:904-6. http://dx.doi.org/10.1200/JCO .2011.37.1674
Correspondence: Dr. Michael A.S. Jewett, Division of Urology, Departments of Surgical and Medical Oncology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, 610 University Ave., Suite 3-130, Toronto, ON M5G 2M9; [email protected]
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Copyright of Canadian Urological Association Journal is the property of Canadian Urological Association and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
‘ Deportments of Surgery (Urology) and Surgical Oncology, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON; fDepartment of Medical Oncology, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON; «Radiation Medicine Program, Princess Margaret Cancer Centre, University Health Network and thé University of Toronto, Toronto, ON; ’ ELLICSR: Health, Wellness and Cancer Survivorship Centre, Toronto General Hospital, University Health Network and the University of Toronto, Toronto, ON; 'Department of Biostatistics, Princess Margaret Cancer Centre, University Health Network and the University of Toronto, Toronto, ON
Cite as: Can t/ro //te o d 2 0 1 4 ;8 (ll-1 2 ):4 0 9 -1 7 . http://dx.doi.org/10.5489/cuai.2279 Published online December 15,2014.
Abstract Introduction: There is little knowledge of survivorship care specific to genitourinary (GU) cancers. To improve care delivery to this patient population, we need to clearly define physician perceptions of survivorship care. We therefore conducted a study to determine the challenges to GU cancer survivorship care in Canada. Methods: A web-based questionnaire was e-mailed to physicians treating GU cancers in Canada, including urologists, radiation oncologists, and medical oncologists. Five domains were assessed: demography, current post-cancer treatment care, perspectives on barriers to survivorship care, accessibility to survivorship resources, and perspectives about advocacy groups. Results: There were 306 responses, with 260 eligible for study. A total of 82% of physicians involve primary care practitioners (PCPs) at some point in survivorship care. Most physicians provide some form of written follow-up plan to PCPs. However, only 25% provided lifestyle recommendations and 53% included persistent and late effects of therapy. Lack of time or resources dedicated to survivorship care was the most commonly reported barrier. There was variation in accessibility to survivorship support programs among different subspecialties and regions. Advocacy groups generally were underutilized, particularly in testis cancer. Low response rate and the potential response bias are the main limita tions of this survey. Conclusion: To our knowledge this is the first study to address the challenges of GU cancer survivorship care in Canada. The barriers and accessibility of survivorship care quoted in this survey may be used to improve care for this group of patients. Underutilization of advocacy groups may stimulate the advocacy groups and institu tions to address its causes and solutions.
Introduction With improvements in healthcare systems, earlier cancer detection, and effective cancer treatments, the number of cancer survivors is rapidly increasing in Canada and may double by 2020.1-3 Cancer survivorship is generally felt to begin when primary treatment ends and survivorship continues until disease recurrence, second malignancy or death.2 Survivors face a range of complex medical and psychosocial issues.2 Genitourinary (GU) cancer patients constitute the largest single disease group of Canadian cancer survivors, account ing for over 50% of male cancer survivors and nearly 25% of all cancer survivors.4 However, according to a Canadian report, the proportional investment in prostate and bladder cancer survivorship research is well below what would be expected given the disease burden and there was notably no investment in kidney cancer survivorship.3 A Canadian GU survivorship meeting held in 2011 highlighted the urgent need for improved GU survivorship care. Meeting partici pants identified the value in (1) the collaboration between clinicians, researchers and cancer survivors/advocacy groups and (2) enhanced access to GU cancer survivorship resources and services.5 To date there is limited information regarding GU cancer survivorship care in Canada and worldwide. There have been many surveys assessing physician attitudes towards cancer survivorship for breast and colorectal cancer, but none for GU cancer. There have also been national stud ies in the United States and Canada to assess the attitudes of oncologists and primary care physicians (PCP) on the delivery of cancer survivorship care, but mainly for non-GU cancers.6,7 Finally, a 2008 Canadian report raised the issue that follow-up practice and services for cancer survivors are inconsistent across the country.8To address these gaps,
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w e e x a m in e d c u rre n t G U c a n c e r p h y s ic ia n s ' a ttitu d e and
v id e d fo r p a rtic ip a n ts to ch o o se th e ir p re fe rre d language.
p e rc e p tio n to w a rd can ce r s u rv iv o rs h ip care in Canada. W e
To e n h a n c e th e response rate, p o te n tia l p a rtic ip a n ts w e re
h yp o th e size d th a t there is hete ro g e n e ity in th e attitu de s and
given the o p p o rtu n ity upo n survey c o m p le tio n to enter th e ir
pe rce p tio n s o f G U ca n ce r ph ysicia n s to w a rd ca n ce r s u rv iv
names and c o n ta c t in fo rm a tio n fo r a d ra w fo r 1 o f 3 prizes
o rs h ip care and be tw e e n d iffe re n t s u b sp e cia ltie s in v o lv e d
w o rth $40 0 to $ 6 00. A n e m a il re m in d e r o f th e survey was
in the p rim a ry tre a tm e n t o f G U cancers. F urtherm ore, there
sent 2 w eeks fo llo w in g the in itia l e -m a il in v ita tio n .
m ay be g e o g ra p h ic v a ria b ility as health care is a p ro v in c ia l re s p o n s ib ility . F in a lly, fa c ilitie s at u n iv e rs ity -a ffilia te d hos
Statistical analysis
pitals m ay d iffe r fro m c o m m u n ity hospitals - th is m ay also D e s c rip tiv e statistics using SAS so ftw a re v e rsio n 9.2 w e re
c o n trib u te to the heteroge neity. F in a lly , p a rtic ip a n ts at th e 2011 C a n a d ia n G U s u rv iv
p e rfo rm e d . The c h i-s q u a re test w as used to assess associa
o rs h ip m e e tin g h ig h lig h te d th a t c lin ic ia n s and researchers
tio n betw e e n q u e stio n responses and d e m o g ra p h ic crite ria :
lacked awareness o f th e c a p a b ilitie s o f ca n ce r p a tie n t a d v o
(1) subspecia lty; (2) g e o g ra p h ica l region o f p ra ctice ; and (3)
cacy groups - w e have also addressed th is issue.5
p ra ctice base (u n ive rsity vs. c o m m u n ity hospital). A p s 0.05 was c o n sid e re d s ig n ific a n t fo r all tests. Surveys w ith d e m o g ra p h ic responses o n ly w e re ce n so re d fro m a nalysis. For
M e th o d s
c la rity , the 5 -p o in t Likert scale questions have been grouped in to 3 in th e analysis o f th e survey. Responses ne ve r and
Survey instrument development
rarely w e re gro u p e d as rarely; often and a lw a ys g ro uped as often. This p ro d u c e d 3 groups; often, som etim es and rarely.
O u r s u rv e y in s tr u m e n t w a s b a s e d o n q u e s tio n n a ir e s
The 5 -L ik e rt p o in t q u e stio n fo r th e a c c e s s ib ility o f s u rv iv o r
d e ve lo p e d at the R osw ell Park Institute in B u ffa lo 9 and the
s h ip care recourses w e re also g ro u p e d fo r a n a lysis: v e ry acce ssib le and a cce ssib le to e a s ily acce ssib le ; d iffic u lt to
E le c tro n ic L iv in g L a b o ra to ry fo r In te rd is c ip lin a ry C a n ce r S u rv iv o rs h ip Research (ELLICSR), a h e a lth , w e lln e s s and ca n ce r su rviv o rs h ip centre at Princess M a rg a re t H o sp ita l. In total, 27 questions w e re develop ed and categorized in 5 dom ains (1 ) p a rtic ip a n t d e m o g ra p h ic characteristics (8 ques tions); (2) c u rre n t post-tre a tm e n t care p ra c tic e (3 questions); (3) perspectives on barriers to p ra c tic in g s u rv iv o rs h ip care (4 questions); (4); a c c e s s ib ility to s u rv iv o rs h ip resources (7
access and v e ry d iffic u lt to access g ro u p e d to d iffic u lt to access p ro d u c in g (easily, m o d e ra te ly and d iffic u lt to access).
R e s u lts
questions); and (5) th e ir perspectives regarding G U advocacy groups (5 questions). Q u e stio n s w e re e ith e r m u ltip le c h o ic e
The survey w as d is trib u te d to 1775 ph ysicia n s: 632 u ro lo gists, 800 ra d ia tio n oncologists and 343 m ed ica l oncologists. N e a rly all urologists, 2 5 % o f C A M O m em bers and 10% o f C A R O m e m b e rs tre a t G U ca n ce rs. These la tte r n u m b e rs
o r 5 -p o in t u n ip o la r L ik e rt scale ty p e qu e stio n s (h ttp ://jo u rn a ls .s fu .c a /c u a j/in d e x .p h p /jo u rn a l/a rtic le /v ie w /2 2 7 9 /1 9 4 9 ).
w ere extrapolate d fro m the m em bership o f the a cadem ic G U o n c o lo g y societies. A to ta l o f 3 0 6 ph ysicia n s c o m p le te d the
A French language tra n s la tio n w as p ilo te d to assess c o m prehensio n and accura cy. The survey w as a p p ro ve d by the
survey o f the 8 0 0 estim ated to be e lig ib le , fo r a response rate o f 3 8 % (Fig. 1). W e ta llie d th e d e m o g ra p h ic characteristics
U n iv e rs ity H e a lth N e tw o rk Research Ethics Board.
o f p a rtic ip a tin g physicia n s (Table 1).
Survey administration
Practice patterns of GU physicians
T he w e b -b a s e d su rve y w as d is trib u te d b y e -m a il u sin g a secure, C anadian-based survey p la tfo rm 10 to a ll urologists, ra d ia tio n o n c o lo g is ts and m e d ic a l o n c o lo g is ts u sin g d is tr ib u tio n lists m a in ta in e d and p ro v id e d b y th e C a n a d ia n U ro lo g ic a l A sso cia tio n (C U A ), the C anadia n A sso cia tio n o f M e d ic a l O n co lo g ists (C A M O ) and the C anadian A ssociation o f R adiation O n c o lo g is ts (CARO ). W e used a non-targeted re c ru itm e n t strategy to c a p tu re b o th u n iv e rs ity - and c o m m u n ity -a ffilia te d ph ys ic ia n s . O n ly p h y s ic ia n s tre a tin g G U c a n c e r w e re in v ite d to access th e w e b -b a s e d surve y. A n
In p o st-tre a tm e n t s u rv iv o rs h ip care practices, a b o u t h a lf o f the respondents reported d is c h a rg in g patients to the PCP at som e p o in t d u rin g fo llo w - u p (Fig. 2). T here w as a s ig n ifi c a n t asso cia tio n b e tw e e n fo llo w -u p care p ra c tic e patterns a n d s u b s p e c ia lty , g e o g ra p h ic a l lo c a tio n o f p ra c tic e , and p ra c tic e base (u n iv e rs ity a ffilia te d vs. c o m m u n ity hospitals) (p < 0.05). A m o n g the ra d ia tio n o n co lo g ists (n = 90), 75% o f respondents discharged su rvivo rs at som e p o in t to the PCP c o m p a re d to m e d ic a l o n co lo g ists at 5 3 % (n = 45) o r u ro lo gists a t 4 2 % (n = 125). C o n v e rs e ly , u ro lo g is ts w e re m ost
in fo rm e d co n se n t sta te m e n t app e a re d in th e e -m a il s c rip t and c o m p le tio n o f th e su rve y in d ic a te d im p lie d co n se n t.
lik e ly to share fo llo w -u p care w ith the PCP in d e fin ite ly (37%) com pared to m ed ica l oncologists (22% ) and ra d ia tio n o n c o l
The lin k s to b o th English a n d French v e rsio n s w e re p ro
ogists (13% ). U rologists w e re m ore lik e ly to e x c lu d e the PCP
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Survivorship care in Canadian G U oncology
Fig. 1. Pattern of responses from the various physician groups.
from cancer-related follow -up (18%) compared to radiation oncologists (7%) and medical oncologists (4%). There was wide geographic variation in post-treatment follow -up care (Fig. 3). Physicians working in university-affiliated hospitals were most likely to discharge survivors at some point to the Table 1. Dem ographics o f th e responders Frequency Percentage ______ ________________________________ (n = 260) (%) Subspecialty Urology
125
Medical Oncology
45
17
Radiation Oncology
90
35 12
48
Region of practice British Columbia
32
Prairie provinces
46
18
Ontario
121
47
Quebec
41
16
Atlantic Canada
19
7
0.05).
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6%
Others
Discharge follow-up care at some point to the PCP
26%
Share follow-up care with the PCP indefinitely
Continue specialist follow-up care indefinitely EXCLUDING the GP
12%
_i______ I 20
10
30
40
50
60
Fig. 2. Frequency of follow-up care patterns. GP: general practitioner; PCP: primary care practitioner.
Physician's perspective of accessibility of services to patients
There was an association between geographical location of practice and reported difficulties in accessing rehabilitation programs (p < 0.05). W hile 91% (n = 32) of physicians in British Colombia reported difficulty, participants from other areas reported lower rates of difficulty (44% [n = 18] for the Atlantic provinces, 42% [n = 41 ] for Quebec, 37% [n = 117] for Ontario and 31% [n = 45] for the Prairies). Physicians practicing in com m unity hospitals reported greater d ifficu lty in accessing survivorship care services compared to physicians at academic centres: psychosocial support (48% vs. 18%), pain management (20% vs. 12%), fe rtility (46% vs. 20%) and genetic counselling programs (48% vs. 29%), respectively (p < 0.05).
O f the respondents, 44% (n = 254) reported that cancer rehabilitation programs were most d ifficu lt to access. The other services were less frequently difficult to access: genetic counselling (38%), fertility counselling (30%), and psycho social support (30%) (Fig. 6). W e observed an association between difficulty in accessibility and the use of psycho social support and genetic counselling programs w ithin the subspecialty groups (p < 0.05). W h ile 45% (n = 123) of urologists reported difficu ltly accessing psychosocial sup port programs, only 23% (n = 43) of medical oncologists and 10% (n = 88) of radiation oncologists reported sim i lar experiences. Sim ilarly, 48% of urologists and 35% of radiation oncologists reported difficulty accessing genetic counselling, compared to only 14% of medical oncologists.
British Columbia
41%
Prairies
13%
Ontario
13%
1m
53%
3%
1
4%
78%
20%
9%
58%
Continue specialist follow-up care indefinitely EXCLUDING the GP follow-up care with the PCP □ Share indefinitely Discharge follow-up care at some point to the PCP Others
Quebec
29%
Atlantic
31%
i l l 2%
53%
I__________ i__________ i__________ i----------------1----------------1----------------1
0
20
40
60
80
100
120
Fig. 3. Post-treatment follow-up care in different regions.
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Summary of cancer status, including diagnosis and stage
87%
Summary of treatment given, including toxicities experienced
Expected persistent and late effects of therapy
Surveillance guidelines for identifying recurrent disease/second primary and/or late effects
82%
Lifestyle recommendations
100
f ig. 4. When a written care plan was provided, what components were included? (n = 230).
Referrals to patient advocacy groups
likely to refer patients to prostate cancer advocacy groups (62%) compared to radiation oncologists (42%) and medical oncologists (32%). There was an association between the frequency of refer ral to Prostate Cancer Canada and the geographical location of practice (p < 0.05). Physicians from Quebec were the least likely to refer patients to prostate cancer advocacy groups 30% (n = 40). In total, 248 respondents selected 3 initiatives to collaboratively enhance survivorship care with the advocacy groups (in order of preference): (1) create a website to describe all relevant cancer advocacy groups, community supports and their services (81%); (2) create a pamphlet to describe
Overall, referral to patient advocacy groups is low for all physicians caring for CU cancer survivors (Fig. 7). W hile there was no association between referral rates to Testicular Cancer Canada and the different subspecialties, differences were observed for bladder, prostate and kidney cancer advo cacy groups (p < 0.05). Urologists were the most likely to refer to bladder advocacy groups 26% (n = 121 ) compared to 21% (n = 43) and 2% (n = 84) for medical oncologists and radiation oncologists, respectively. Medical oncologists refer patients to kidney cancer advocacy groups more fre quently than urologists (51% vs. 27%). Urologists were most
Lack of physician knowledge of cancer survivorship issues and recomm ended surveillance practices
Lack of practice guidelines to follow
Lack of tim e or resources to support patients through this phase of the cancer experience
Lack of patient engagem ent or adherence to recomm endations
0
20
40
60
80
100
120
Fig. 5. Barriers to meeting the post-treatment care needs of survivors? (n = 254).
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Information and education about potential late effects due to cancer Opportunities to interact with other survivors Psychosocial support
| Difficult to access
Pain and symptom managementm programs
I I Moderately accessible 3 Easily accessible
Access to cancer rehabilitation programs Fertility counselling and resources Genetic counselling 0
20
40
60
80
100
120
Fig. 6. Accessibility of services to individual physician’s patients (n = 254).
all relevant cancer groups and community support services (56%); and (3) to create learning opportunities to educate healthcare professionals on the function and credibility of patient advocacy groups (38%).
Discussion This study evaluated Canadian GU cancer physician sur vivorship care attitudes, perceptions and practices. To our knowledge, this is the first study of its kind from Canada. Several models for survivorship care delivery have been proposed.2'11’13 One ideal care model is that of shared care of follow -up between the cancer specialist and the PCP.2 In our survey, only one-quarter of GU cancer specialists share survivorship care with PCPs indefinitely, w hile more than
half of them discharge patients at some point to PCP. W ith the increased number of cancer survivors that require follow up care, this may result in a decreased capacity for cancer specialists to attend to new cancer patients. A reasonable solution would be to involve PCPs in follow-up. Regardless of which approach is employed, it should fu lfil the major components of cancer survivorship care as outlined by the Institute of M edicine, including prevention of recurrence and new cancers, surveillance for recurrence and late side effects; intervention for treatment related consequences, and the coordination between the specialist and PCP to ensure all the survivors needs are met. It is critical to patient care that this transfer from specialist care to PCP care be smooth. For this to occur (1 ) PCPs need to be w illin g to assume care of survivors, (2) patients need
Fig. 7. Rates of patient referral to Canadian Genitorurinary patient advocacy groups (n = 248).
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to be satisfied w ith PCP fo llo w -u p , and m ost im p o rta n tly (3)
P ro v id in g PCPs w ith g u id e lin e s and m o re in fo rm a tio n on
th e re sh o u ld be c o m m u n ic a tio n b e tw e e n th e ca n c e r spe
the m anagem e nt o f tre a tm e n t side effects m ay im p ro v e th e ir c o n fid e n c e in ca rin g fo r G U ca n ce r survivors.
c ia lis t and the PCP. C anadia n PCPs are w illin g to take part in th e m ana g e m e n t o f ca n ce r s u rvivo rs and even ta ke fu ll
M a n y b a rrie rs to c a n c e r s u rv iv o rs h ip ca re h a ve been
re s p o n sib ility after c o m p le tio n o f a ctive tre a tm e n t if they are p ro v id e d w ith th e a p p ro p ria te in fo rm a tio n and g u id e lin e s
re p o rte d and these w e re c le a rly su m m a riz e d in th e re p o rt b y th e In s titu te o f M e d ic in e .2 From a C a n a d ia n re p o rt in
fo r f o llo w u p .14' 17 A su rve y o f breast c a n c e r s u rv iv o rs by G ru n fe ld and colleagu es in 2 0 0 6 noted th a t m ost patients acce pt th e ir PCP ta kin g re sp o n s ib ility o f th e ir ca n ce r fo llo w
2 0 0 8 , a la ck o f fin a n c ia l resources w as th e m ost c o m m o n b a rrie r in ca n c e r s u rv iv o rs h ip care, fo llo w e d b y a la ck o f
up, a lth o u g h 4 5 % w e re u n w illin g to be tra n s fe rre d .18 To o v e rco m e this issue it has been suggested th a t PCPs b ecom e
In o u r survey, ph ysicia n s u n iv e rs a lly rep o rte d a la c k o f tim e and resources regardless o f su b sp e cia lty, p ra c tic e lo c a tio n
in v o lv e d e a rly in th e s u rv iv o r's e x p e rie n c e using a shared
o r p ra c tic e base. These are im p o rta n t barriers th a t sh o uld be studied fu rth e r. To im p ro v e care, it appears th a t th e p h ys
care m odel th a t encourages c o n tin u e d c o m m u n ic a tio n and c o o rd in a tio n betw een the PCP and ca n ce r s p e c ia lis t.19 This m ay encourage the p a tie n t to d e v e lo p trust in th e care p ro v id e d by th e ir PCP so th a t w h e n the tra n s itio n happens they
m odels fo r fo llo w -u p care and e vidence -b ased g u id e lin e s .8
ic ia n needs to d e vo te tim e to understand the p a tie n t's sup p o rtiv e care needs (such as p s y c h o so cia l and o th e r issues related to s u rv iv o rs h ip care) w h ic h w o u ld re q u ire a d d itio n a l
are co m fo rta b le . The A m erica n Society o f C lin ic a l O n c o lo g y strongly recom m ends effective c o m m u n ic a tio n betw een the
re im b u rse m e n t to p h y s ic ia n s .28 A lack o f p ra c tic e g u id e lin e s w as th e second m ost c o m
s p e c ia list and th e PCP to ensure a c o n tin u u m o f care in to p rim a ry p ra c tic e .20 M o st o f the G U physicia n s w h o p a rtic i
m o n ly c ite d b a rrie r to th e p ro v is io n o f s u rv iv o rs h ip care. C urrent guidelin es fo r G U cancer care focus on the detection
pated in this survey w o u ld p ro v id e w ritte n plans to PCPs, a lth o u g h these plans tend to lack im p o rta n t details, such as re co m m e n d a tio n s fo r the m anagem e nt o f persistent and late
o f n e w o r re cu rre n t cancers. These g u id e lin e s la ck in fo rm a tio n on o th e r im p o rta n t aspects o f s u rv iv o rs h ip care, such as life style re co m m e n d a tio n s and psychosocia l d y s fu n ctio n .
effects o f tre a tm e n t and life s ty le re c o m m e n d a tio n s .21-22 To enhance c o m m u n ic a tio n , im p le m e n ta tio n o f a standardized te m p la te fo r d ic ta tio n to th e PCP w as s h o w n to im p ro v e PCP satisfaction regarding the in fo rm a tio n p ro v id e d 23 - this m ay im p ro v e p a tie n t c o n fid e n c e in th e PCP p ro v is io n o f fo llo w -u p care.
M o st g u id e lin e s also lack in fo rm a tio n on h o w to assess and m anage persistent and late effects o f ca n ce r tre a tm e n t. The d e v e lo p m e n t and d is s e m in a tio n o f s ta n d a rd iz e d s u rv iv o r
C ancer survivors are at an increased risk o f d e v e lo p in g a se cond c a n ce r, c a rd io v a s c u la r disease, d ia b e te s m e llitus, osteoporosis and o th e r c h ro n ic illnesses. These can be caused by th e ir cancer treatm ent o r lifestyle factors o r predis positions. Lifestyle factors are m o d ifia b le , and re co m m e n d a tio n s are supported by the Institute o f M e d ic in e re p o rt and th e A m e ric a n C ancer S ociety (ACS).2-24-25 M o st respondents p ro vid e d a w ritte n plan; how ever, lifestyle recom m endatio ns w e re often no t in c lu d e d . This m ay be due to the sp ecialist's e xp e ctatio n th a t th e PCP w ill e x p lo re th is w ith the p a tie n t or th a t the specialist provides this in fo rm a tio n v e rb a lly . W e d id n o t s p e c ific a lly ask if the specialist's p ro v id e life style re co m m e n d a tio n s, b u t in a survey c o n d u c te d by K id n e y C ancer C anada (KCC) to assess the types o f in fo rm a tio n p ro v id e d to p a tie n ts b e fo re and afte r surgery, o n ly 5 0 % o f pa tie n ts rece ived life style re co m m e n d a tio n s fro m th e ir u ro lo g is t.26 It is n o t c le a r w h a t percentag e receive th is re c o m m e n d a tio n e ither from the specialists o r PCP, thus w e reco m m e n d better c o m m u n ic a tio n w ith th e PCP. In terestingly o n ly h a lf o f G U physicia n s w h o p a rtic ip a te d in th e survey p ro v id e d in fo rm a tio n and g u id e lin e s fo r the m a n a g e m e n t o f p e rsiste n t and late effects o f tre a tm e n t in th e ir w ritte n p la n to th e PCP. T he lite ra tu re suggests th a t PCPs are less c o n fid e n t in m a n a g in g late s id e e ffe c ts .27
s h ip care g u id e lin e s and assessm ent to o ls fo r G U c a n c e r is an im p o rta n t goal. To fu rth e r adva n ce s u rv iv o rs h ip care, in n o va tive m odels th a t reduce cost and im p ro ve e ffic ie n c y o f care are needed. T heir d e v e lo p m e n t w ill depend on research fu n d in g , s c ie n tific rigor, kn o w le d g e tra n sla tio n o p p o rtu n itie s at early stages o f tra in in g and focus on patient-cen tered q u a l ity o f care. The differences in p ra ctice patterns betw een aca d e m ic and c o m m u n ity o n co lo g ists also in d ic a te th a t m odels and g u id e lin e s m ust also be re le va n t to the setting in w h ic h the p a tie n t is b e in g treated. A lth o u g h re h a b ilita tio n is im p o rta n t fo r c a n c e r s u rv iv o rs ,2-29'33 a b o u t o n e h a lf o f G U p h y s ic ia n s in o u r s tu d y re p o rte d d if fic u ltly in acce ssin g re h a b ilita tio n p ro g ram s. Little v a ria tio n was fo u n d betw een regions, except fo r British C o lu m b ia w h e re m o re (91% ) G U p h y s ic ia n s re p o rte d d if fic u lty . It is n o t k n o w n , h o w e ve r, w h e th e r these lo w levels o f a c c e ssib ility re fle ct a lack o f a v a ila b le program s o r m erely a lack o f k n o w le d g e o f th e ir existence and, co n s e q u e n tia lly, underuse. U ro lo g ists are the least lik e ly to refer patients fo r p s ych o social su p p o rt and g enetic c o u n s e llin g , w ith a b o u t 5 0 % of urologists re p o rtin g d iffic u lty w ith access. Since these servi ces appeared to be easily accessible by o th e r subspecialties, the observed u n d e ru tiliz a tio n m ay be due to lo w levels o f aw areness o f these services o r o f sp e c ific p a tie n t needs. W e also fo u n d th a t G U c a n c e r a d v o c a c y gro u p s w e re u n d e ru tiliz e d . The m ost c o m m o n ly used a d v o c a c y g ro u p
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was for prostate cancer. This may be because it is the most established in Canada and prostate cancer is the most com mon GU cancer. To explore means to enhance collaboration between advocacy groups and GU cancer physicians, we asked respondents to rank initiatives proposed by the GU cancer survivorship conference consensus. 5 Respondents felt that written information, electronic information and learning opportunities provided by the advocacy groups were most likely to improve collaboration. Limitations of this study include our inability to verify that respondents in fact treated GU cancer and which respond ents were trainees. The survey was directed to GU cancer physicians and may not be applicable to other cancer site groups. Close-ended questions may have limited the strength of the responses. Answers assessing the accessibility of ser vices may be biased toward the awareness of the physician, rather than represent a true lack of services. We acknow ledge that the practice patterns may differ according to the stage of the disease, which is not covered in this survey. We did not include it for the sake of brevity - a long survey may have affected our response rate. This issue may need to be covered in a future survey. The response rate appears low, but it is comparable to other web-based surveys of health providers. W e chose a web-based survey to appeal to the busy physician responders, w h ile recognizing the poten tial lower response rate. Other survey methods by mail or telephone w ould have enhanced the rate. The results may also be subject to bias because respondents may have been more interested in cancer survivorship. This is an exploratory study, and stratification was done to better understand the associations among the variables. Proportions and p values may be specific to the study population, but may not be generalizable. Future studies w ould be helpful in further validating our results.
Conclusion and practice implications Canada has well-developed patient advocacy groups and other organizations that provide survivorship support. Most GU cancer physicians discharge survivors to PCPs at some point after treatment. There is variability in practice between different GU subspecialties, geographical areas of practice and practice bases (university affiliated vs. community hospi tals). GU specialists do not appear to provide sufficient infor mation to the PCP. Lack of physician time and the limited availability of other resources are key barriers to providing survivorship care and may lim it physician cooperation. GU physicians lack knowledge about available cancer survivor ship care facilities. Advocacy groups are underutilized with variation between subspecialties and geographical location of practice. The findings from our survey highlight several areas that require further investigation.
416
We recommend that a standardized dictation template. This tem plate w ould include inform ation on diagnosis, treatment received, record of side effects experienced dur ing and after treatment, expected short- and long-term side effects with management options, guidelines for follow-up, including screening for recurrence of disease, proposed caregiver responsibilities, and a list of available services and programs including relevant advocacy groups. Lack of physician knowledge about survivorship care appears to be an important barrier. The inclusion of cancer survivorship issues in the curricula of Canadian medical schools and in rotations for PCP residency programs would improve phy sician awareness. Developing and supporting standardized programs and services for patients, as w ell as inform ing physicians about survivorship care programs and facilities, may increase awareness and positively affect access. We recommend involving advocacy groups to help educate physicians about their services to increase the utilization of these groups. Competing interests: Dr. Almatar, Dr. Richter, Dr. Lalani, Dr. Bender, Dr. Wiljer, Dr. Alkazaz, Dr. Legere, Dr. Maganti, Dr. Sridhar and Dr. Catton have no competing financial or personal interests. Dr. Jewett is a member of the Advisory Board for Pfizer. He has also received grants from Novartis, GSK and Pfizer. Lostly, he has participated in clinical trials with Novartis, GSK and Pfizer.
This paper has been peer-reviewed.
References 1. Canadien Cancer Society's Steering Committee on Cancer Statistics. Canadian Cancer Statistics 2012. Toronto, ON: Canadian Cancer Society; 2012. http://bit.ly/lybPhD6. Accessed November 26, 2014. 2. Hewitt M, Greenfield S, Stovall E. From cancer patient to cancer survivor: Lost in transition. Washington: The National Academies Press; 2006. http://www.nap.edu/openbook.php?record_id=l 1468. Accessed November 26, 2014. 3. Canadian Cancer Research Alliance. Investment in Research on Survivorship and Palliative and Fnd-of-Life Care, 20 05 -200 S : A Special Report from the Canadian Cancer Research Alliance’s Survey of Government Voluntary Sector Investment in Cancer Research. Toronto: CCRA; 2011. http://www.partnershipagainstconcer.co/wp-content/uploods/Survivorship_E.pdf. Accessed November 26, 2014. 4. Gilbert SM, Miller DC, Hollenbeck BK, et ol. Cancer survivorship: Challenges ond changing paradigms. 1 (to /2008;179:431-8. http://dx.doi.org/! 0.1016/j.juro.2007.09.029 5. Bender JL, Wiljer D, Matthew A, et al. Fostering partnerships in survivorship care: Report of the 2011 Canadian genitourinary cancers survivorship conference. J CancerSurviv2012;6:296-304. http://dx.doi. org/10.10 0 7 /s l 1764-012-0220-3 6. Cheung WY, Aziz N, Noone AM, et ol. Physician preferences and attitudes regarding different models of cancer survivorship care: A comparison of primary care providers and oncologists, i Cancer Surviv 2013;7:343-54. http://dx.doi.org/10.1007/sll764-013-0281-y 7. Potosky AL, Han PK, Rowland J, ef ol. Differences between primary care physicians' and oncologists' knowledge, attitudes and practices regarding the core of cancer survivors. J Gen Intern Med 2011 ;26:140310. http://dx.d 0i.0rg /l 0.10 0 7 /s l 1606-011-1808-4 8. Ristovski-Slijepcevic S. Environmental Scan of Cancer Survivorship in Canada: Conceptualization, Practice and Research. British Columbia Cancer Agency: Vancouver, British Columbia; 2008. 9. Goge EA, Pailler M, Zevon MA, et ol. Structuring survivorship care: Discipline-specific clinician perspectives. J Cancer Surviv 2011;5:217-25. http://dx.doi.org/10.1007/sll764-011-0174-x 10. FluidSurveys. www.fluidsurveys.com. Accessed November 26, 2014.
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11. Aziz NM, Oeffinger KC, Brooks S, et ni. Comprehensive long-term follow-up programs for pediatric cancer survivors. Cancer 2006;107:841-8. http://dx.doi.org/10.1002/cncr.22096 12. MacBride SK, Whyte F. Survivorship ond the cancer follow-up clinic. Cur J Cancer Care (Engl) 1998;7:4755. http://dx.doi.O rg/10.1046/j.1365-2354.1998.00065.x 13. Oeffinger KC, McCabe MS. Models for delivering survivorship care. J Clin Oncol 2006;24:5117-24. http://dx.doi.org/10.1200/JCO .2006.07.0474 14. Worster A, Bass M l, Wood ML. Willingness to follow breast cancer. Survey of family physicians. Can Earn Physician 1996;42:263-8. 15. Norman A, Sisler J, Hack T, et ol. Family physicians and cancer care. Palliative care patients' perspectives. Can Fam Physician 2001;47:2009-12, 2015-6. 16. Songster JF, Gerace TM, Hoddinott SN. Family physicians' perspective of patient care at the London regional concer clinic. Can Fam Physician 1987;33:71-4. 17. Del Giudice ME, Grunfeld E, Harvey BJ, et al. Primary care physicians' views of routine follow-up care of cancer survivors. J Clin Oncol 2009;27:3338-45. http://dx.doi.O rg/l 0.1200/JC0.2008.20.4883 18. Grunfeld E, Levine MN, Julian JA, et al. Randomized trial of long-term follow-up for early-stage breast cancer: A comparison of family physician versus specialist care. J Clin Oncol 2006;24:848-55. h ttp :// dx.doi.org/10.1200/JC 0.2005.03.2235 19. Maiedema B, Tatemichi S, MacDonald I. Cancer follow-up care in New Brunswick: cancer surveillance, support issues and fear of recurrence. Can J Rural Med 2004;9:101-7. 20. McCabe MS, Bhatia S, Oeffinger KC, et ol. American Society of Clinical Oncology statement: Achieving high-quality cancer survivorship care. J Clin Oncol 2013;31:631-40. h ttp ://d x .d o i.o rg /1 0 .1 2 0 0 / JC0.2012.46.6854 21. Dworkind M, Towers A, Murnaghan D, et al. Communication between family physicians and oncologists: Qualitative results of an exploratory study. Cancer Prev Control 1999;3:137-44. 22. Barnes EA, Hanson J, Neumann CM, et al. Communication between primary care physicians and radiation oncologists regarding patients with cancer treated with palliative radiotherapy. J Clin Oncol2000;18:2902-7. 23. Braun TC, Hagen NA, Smith C, et al. Oncologists and family physicians. Using a standardized letter to improve communication. Can Fam Physician 2003;49:882-6.
24. Rock CL, Doyle C, Demark-Wahnefried W, et al. Nutrition and physical activity guidelines for cancer survivors. C4 Cancer J Clin 2012;62:243-74. http://dx.doi.org/10.3322/caac.21142 25. Demark-Wahnefried W, Jones LW. Promoting a healthy lifestyle among cancer survivors. Hematol Oncol Clin North Am 2008,22:319-42, viii. http://dx.doi.org/10-l 016/|.hoc.2008.01.012 26. A Survey of Canadian Kidney Cancer Patients/Caregivers and Urologists Their Views on Survivorship Care, http://www.kidneycancercanada.ca/media/94560/412.pdf. Accessed November 26, 2014. 27. Skolorus TA, Holmes-Rovner M, Northouse LL, et al. Primary core perspectives on prostate concer survivorship: Implications for improving quality of care. Urol Oncol 2013;31:727-32. http ://d x.d o i. org/10.1016/j.urolonc.2011.06.002 28. Irwin M, Klemp JR, Glennon C, et al. Oncology nurses' perspectives on the state of cancer survivorship care: Current practice and barriers to implementation. Oncol Nuts Forum 2011;38:E11-9. http://dx.doi. org/10 .1 1 8 8 /1 1.0NF.E11-El 9 29. Cheville AL, Beck LA, Petersen TL, et al. The detection and treatment of concer-related functional prob lems in an outpatient setting. Supportive Care Cancer 2009;17:61-7. h ttp ://d x.d o i.o rg /1 0 .1 0 0 7 / S00520-008-0461-X 30. Guo V, Shin KY, Hainley S, et ol. Inpatient rehabilitation improved functional status in asthenic patients with solid ond hematologic malignancies. Am J Phys Med Rehabil 2 011;90:265-71. h ttp ://d x.d o i. org/10.1097/PHM .0b013e3182063ba6 31. Thorsen L, Gjersef GM, Loge JH, et al. Cancer patients' needs for rehabilitation services. Acta Oncol 2011;50:212-22. http://dx.d 0i.0r g /l 0 .3109/0284 186X.2010.531050 32. Silver JK. Strategies to overcome cancer survivorship care barriers. PM R 2011;3:503-6. http://dx.doi. org/10.1016/j.pmrj.201 1.04.014 33. Alfano CM, Ganz PA, Rowland JH, et al. Cancer survivorship and cancer rehabilitation: Revitalizing the link. J Clin Oncol 2012;30:904-6. http://dx.doi.org/10.1200/JCO .2011.37.1674
Correspondence: Dr. Michael A.S. Jewett, Division of Urology, Departments of Surgical and Medical Oncology, Princess Margaret Cancer Centre, University Health Network, University of Toronto, 610 University Ave., Suite 3-130, Toronto, ON M5G 2M9; [email protected]
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