Barriers to Breast and Colorectal Cancer Survivorship Care: Perceptions of Primary Care Physicians and Medical Oncologists in the United States

Barriers to Breast and Colorectal Cancer Survivorship Care:Perceptions of Primary Care Physicians and MedicalOncologists in the United StatesKatherine S. Virgo, Catherine C. Lerro, Carrie N. Klabunde, Craig Earle, and Patricia A. Ganz

Katherine S. Virgo, Emory University,Atlanta, GA; Catherine C. Lerro, YaleUniversity, New Haven, CT; Carrie N.Klabunde, Division of Cancer Controland Population Sciences, NationalCancer Institute, Bethesda, MD; Patri-cia A. Ganz, Jonsson ComprehensiveCancer Center, University of CaliforniaLos Angeles, Los Angeles, CA; andCraig Earle, Institute for Clinical Evalua-tive Sciences and University of Toronto,Toronto, Ontario, Canada.

Published online ahead of print atwww.jco.org on May 20, 2013.

Supported by Grant No.HHSN261201000316C from theNational Cancer Institute and AmericanCancer Society National Home OfficeIntramural Research Department.

Presented at the 47th Annual Meetingof the American Society of ClinicalOncology, Chicago, IL, June 3-7, 2011(physician-related barriers) and theAnnual Research Meeting of Academy-Health, Seattle, WA, June 12-14, 2011(patient-related barriers).

Authors’ disclosures of potential con-flicts of interest and author contribu-tions are found at the end of thisarticle.

Corresponding author: Katherine S.Virgo, PhD, MBA, Department ofHealth Policy and Management, RSPH,Emory University, 1360 Stephens DrNE, Atlanta, GA 30329; e-mail:[email protected].

© 2013 by American Society of ClinicalOncology

0732-183X/13/3118w-2322w/$20.00

DOI: 10.1200/JCO.2012.45.6954

A B S T R A C T

PurposeHigh-quality, well-coordinated cancer survivorship care is needed yet barriers remain owing tofragmentation in the United States health care system. This article is a nationwide survey ofbarriers perceived by primary care physicians (PCPs) and medical oncologists (MOs) regardingbreast and colorectal cancer survivorship care beyond 5 years after treatment.

MethodsThe Survey of Physician Attitudes Regarding the Care of Cancer Survivors was mailed out in 2009to a nationally-representative sample (n � 3,596) of US PCPs and MOs. Ten physician-perceivedcancer survivorship care barriers/concerns were compared between the two provider types. Usingweighted multinomial logistic regression, we modeled each barrier, adjusting for physiciandemographics, reimbursement, training, and practice characteristics.

ResultsWe received responses from 2,202 physicians (1,072 PCPs; 1,130 MOs; 65.1% cooperationrate). In adjusted patient-related barriers models, MOs were more likely than PCPs to reportpatient language barriers (odds ratio, [OR], 1.72; 95% CI, 1.22 to 2.42), insurance restrictionsimpeding test/treatment use (OR, 1.42; 95% CI, 1.03 to 1.96), and patients requesting moreaggressive testing (OR, 4.08; 95% CI, 2.73 to 6.10). In adjusted physician-related barriersmodels, PCPs were more likely to report inadequate training (OR, 3.06; 95% CI, 2.03 to 4.61)and ordering additional tests/treatments because of malpractice concerns (OR, 1.87; 95% CI,1.20 to 2.93). MOs were more likely to report uncertainty regarding general preventive careresponsibility (often/always: OR, 1.97; 95% CI, 1.13 to 3.43; sometimes: OR, 2.16; 95% CI,1.60 to 2.93).

ConclusionMOs and PCPs perceive different cancer follow-up care barriers/concerns to be problematic.Resolving inadequate training, malpractice-driven test ordering, and preventive-care respon-sibility concerns may require continuing education, explicit guidelines, and survivorship careplans. Reviewing care plans with survivors may also reduce patients’ requests forunnecessary testing.

J Clin Oncol 31:2322-2336. © 2013 by American Society of Clinical Oncology

INTRODUCTION

There are nearly 14 million cancer survivors in theUnited States today.1 Earlier detection and treat-ment, combined with recent advances in treatment,contribute to survivors living longer with cancer.The number of cancer survivors is expected to in-crease to almost 18 million with the aging of thepopulation in whom cancer incidence is highest.2

Combined with predicted shortages of primary carephysicians (PCPs) and medical oncologists (MOs),these demographic changes present unique challengesfor delivery of high-quality cancer survivorship care.3

The fragmented nature of the United Stateshealth care system presents additional challenges,highlighting the need for improved coordinationand continuity of survivorship care. Patients receivecare from many different providers (often located ingeographically diverse areas) through several phasesof illness over extended time periods.4 For patientsmore than 5 years after initial treatment, transition-ing from an oncologist’s care to follow-up care by aPCP requires care coordination that could poten-tially be improved by providing treatment summa-ries (TS) and survivorship care plans (SCP).5

Unfortunately, current physician reimbursement

JOURNAL OF CLINICAL ONCOLOGY O R I G I N A L R E P O R T

VOLUME 31 � NUMBER 18 � JUNE 20 2013

2322 © 2013 by American Society of Clinical Oncology

from 129.100.58.76Information downloaded from jco.ascopubs.org and provided by at UNIVERSITY WESTERN ONTARIO on October 28, 2014

Copyright © 2013 American Society of Clinical Oncology. All rights reserved.

mechanisms do not support oncologists developing and deliveringsuch plans. Studies have yet to demonstrate that plan use improvespatient outcomes.6-7 Further, oncologists may hesitate to dischargepatients to PCP care after monitoring patients closely over a longperiod and gaining patient trust.8 Yet with the growing number of newpatients, oncologists simply cannot follow every patient throughouthis or her remaining life span.

Insufficient communication between oncologists and PCPs canresult in uncertainty among PCPs regarding appropriate post-treatment surveillance testing.9-11 The limited evidence base to sup-port decisions regarding appropriate surveillance beyond 5 years aftertreatment presents an additional barrier to optimal care. Discrepantperceptions of MO and PCP survivorship care roles can also lead tomissed or duplicated care.12 PCP and oncologist perceptions of theirrespective roles in survivorship care are more discrepant than withpatient expectations of their roles.13 Patients may be satisfied withtheir care even if they perceive much greater participation by their PCPthan the modest participation that may actually occur.14 Receipt ofgeneral noncancer preventive care is one benefit of concurrentfollow-up by both MOs and PCPs compared with patients followed byoncologists alone.15 Other commonly cited noncancer-specific barri-ers to care, such as patient noncompliance, insurance restrictionsimpeding receipt of appropriate care, and language barriers, may alsoadversely affect patient receipt of appropriate survivorship care.11

Using nationwide survey data, we examined 10 self-reportedbarriers and concerns MOs and PCPs may encounter while caring forcancer survivors who are 5 or more years beyond completion of activetreatment and the characteristics of physicians experiencing thesebarriers and concerns. To our knowledge, this is a novel analysis,entirely distinct from the general survey overview/methodology paperpublished recently.16 We hypothesized that MOs and PCPs wouldhave different perceived barriers. The Mandelblatt et al11 adaptation ofthe behavioral model of access to care17-19 provides the conceptualframework for this analysis, as it incorporates communication be-tween PCPs and oncologists in depicting realized access to cancer care.

METHODS

The Survey of Physician Attitudes Regarding the Care of Cancer Survivors(SPARCCS), cosponsored by the National Cancer Institute and the AmericanCancer Society, is a nationally representative mailed survey of United StatesPCPs and MOs conducted in 2009. The survey sought to improve understand-ing of the knowledge, attitudes, beliefs, and practices of these two groups ofphysicians regarding post-treatment care of breast and colon cancer survivors.Breast and colon cancer were chosen for study because of their high preva-lence, long survivorship, and the availability of evidence-based guidelines forfollow-up care.20-21 SPARCCS instruments are available on request.22 Studyapproval was obtained from the National Cancer Institute’s institutional re-view board and the US Office of Management and Budget.

The complete survey methodology has been described elsewhere.16

Briefly, 2,525 PCPs (family medicine, internal medicine, obstetrics/gynecologyspecialists) and 2,750 MOs (oncology and/or hematology specialists) weresampled using a systematic stratified approach from the American MedicalAssociation Physician Masterfile.23-24 Eligible physicians (n � 3,596) wererequired to practice in a nonfederal setting, be younger than 76 years, andspend 20% or more of their time caring for patients. Furthermore, oncologistshad to provide care for breast or colon cancer patients within the previous year,and PCPs had to work in an office-based practice. Questionnaires from 1,072PCPs and 1,130 MOs were considered evaluable. The absolute weighted re-sponse rate calculated using the American Association of Public Opinion

Research RR3 method was 57.6% and the cooperation rate was 65.1%. Re-spondents did not differ significantly from nonrespondents. Survey weightswere calculated using replicate jackknife methods.16

Dependent Measures

Of the 10 specific barriers/concerns examined in the survey, six werederived from existing literature.9,25 Four were designed by the survey team.Five were categorized as patient-related barriers or concerns (language issues,nonadherence to physician-recommended care, requesting more aggressivesurveillance testing, inability to pay/lacking insurance,25 and insurance restric-tions precluding test ordering25). The remaining five were categorized asphysician-related barriers and concerns (ordering tests or treatments as mal-practice protection, uncertainty regarding which physician [MO or PCP] isproviding general preventive health care,9 concerns about duplicating care,9

missed care concerns,9 and inadequate knowledge or training to managepatient problems9). Respondents were asked how frequently they experiencedeach barrier (never, rarely, sometimes, often, always, or not applicable). Toensure an adequate number of respondents in each category to perform allanalyses, “never” and “rarely” were collapsed into a single category, as were“often” and “always,” resulting in three levels. Two crude patient- andphysician-related barrier summary variables were created by totaling all re-sponses (never, 1; always, 5) across the patient- and physician-related barrierquestions and converting the total to a dichotomous variable (� 15, low score;� 15, high score).

Independent Measures

The primary independent measure was physician type—either MO orPCP. Physician characteristics, practice and patient characteristics, salary andreimbursement information, and self-reported knowledge and training werecontrolled for in the analyses. Physician characteristics included race/ethnicity,year of medical school graduation, United States or foreign training, andteaching status.

Practice and patient characteristics included primary practice site (eg,office or hospital) and location type (eg, full- or part-owner or employee ofphysician-owned practice), number of physicians in the primary practicelocation, metropolitan statistical area, census region, electronic medical re-cords use, weekly patient volume, percent of patients categorized as “safety-net” (ie, Medicaid-insured or uninsured), and percent of patients 65 years andolder. Salary and reimbursement included whether the physician was salariedand whether salaries were productivity based. Primary reimbursement wascategorized as fee-for-service, capitation, or a mixture of both.

Several questions gauged physician confidence in cancer-related careknowledge regarding appropriate surveillance, long-term physical adverseeffects of cancer and its treatment, and psychological outcomes. Becausemany individual knowledge questions were highly correlated, a summaryvariable was created (self-ascribed knowledge of follow-up care) and de-fined as tertiles of the distribution of summed knowledge question re-sponses (high score, 17 to 18; medium, 14 to 16; low, 4 to 13). Trainingregarding late and long-term effects of cancer treatment was assessed, aswere the training methods used in the previous 5 years (eg, continuingmedical education or professional meetings).

Statistical Analyses

Analyses were performed using SAS (version 9.2; SAS Statistical Institute,Cary, NC). The surveyfreq procedure was used to apply replicate weights andconduct Rao-Scott �2 tests. Weighted multinomial logistic regression models(surveylogistic with generalized logit link) were used to examine the relation-ship between each perceived barrier and the physician and practice character-istics. This technique permitted the use of polychotomous response categories(never/rarely, sometimes, often/always) for the dependent variables with nev-er/rarely as the referent. All models included physician specialty (MO or PCP).Owing to the number of potential candidates for model inclusion, only vari-ables with a Rao-Scott �2 P value � .15 were entered into each model, reducingthe likelihood of overfitting and model noise. The Newton-Raphson methodwas specified for model fitting.

Barriers to Breast and Colorectal Cancer Survivorship Care

www.jco.org © 2013 by American Society of Clinical Oncology 2323



RESULTS

The 2,202 respondents (1,130 MOs and 1,072 PCPs) corresponded toa weighted total of 148,303 physicians (7,950 MOs and 140,353 PCPs).Physician type was significantly associated with all physician, practice,and patient characteristics; productivity-based salary; and all knowl-edge and training measures except training received from colleaguesin the past 5 years (Table 1). Physician type (MO or PCP) was alsosignificantly associated (P � .05) with all barriers to patient care inweighted-unadjusted analyses, except inability to pay/lacking insur-ance (Table 2). The average number of barriers and concerns physi-cians reported (often/always or sometimes) was 4.8 overall (standarddeviation [SD], 2.2), 4.9 for MOs (SD, 2.2), and 4.7 for PCPs (SD, 2.3).

Patient-Related Barriers

For all respondents combined, the most common patient-related barrier was patient inability to pay/lacking insurance cov-erage (64.6%). Compared with PCPs in weighted-unadjustedanalyses, MOs were significantly more likely to report that patientsoften/always request more aggressive surveillance testing than thephysician would recommend (28.9% v 10.0%; P � .05), often/always/sometimes have language barriers that interfere with com-munication (25.7% v 20.3%), and sometimes have insurancerestrictions that preclude obtaining necessary tests or treatments(43.2% v 37.3%). MOs were also significantly more likely to reportthat patients sometimes are noncompliant with recommendedcare (55.2% v 47.5%; P � .01; Table 2).

In weighted, adjusted, multinomial models, MOs were morelikely than PCPs to report patients requesting more aggressive testingas a barrier (often/always: odds ratio [OR], 4.08; 95% CI, 2.73 to 6.10;sometimes: OR, 1.99; 95% CI, 1.53 to 2.58; Table 3). Compared withsolo practitioners, physicians in small- to medium-sized practices(two to five and six to 15 physicians, respectively) were more likely toreport patients sometimes requesting unnecessary testing. Physicianstreating a higher percentage of safety-net patients (6% or more) wereless likely to report patients sometimes requesting unnecessary testingas a barrier than were physicians treating few safety-net patients.

MOs were more likely to report patient language as a barrier tosurvivorship care compared with PCPs (often/always/sometimes: OR,1.72; 95% CI, 1.22 to 2.42). Language was also a significant barrier tocare among physicians (MOs and PCPs combined) in the northeastand west, those practicing at community health centers, in large prac-tices (� 16 physicians) or in metropolitan statistical areas, and thosereimbursed by capitation.

MOs were significantly more likely than PCPs to report insur-ance restrictions precluding the ordering of tests/treatments as abarrier (sometimes: OR, 1.42; 95% CI, 1.03 to 1.96). Insurance restric-tions were also problematic for Hispanic physicians and those withproductivity-based salaries. Conversely, respondents in medium-to-large practices (� six physicians), in the west, physicians trained in theUnited States, and those who were not paid by salary or whose salarieswere not based on productivity were less likely to report insurancerestrictions as a barrier to test ordering.

PCPs and MOs did not differ in reporting the remaining twopatient-related barriers (patient inability to pay/lacking insurance orrefusing recommended care) in adjusted analyses (results not shown).Although MOs had high patient-related barrier scores overall com-

pared with PCPs in unadjusted analyses (P � .001), this associationwas no longer significant in adjusted analyses (P � .1132).

Physician-Related Barriers

For all respondents combined, the most common physician-related barrier was concern about missed care (55.7%). Comparedwith MOs in weighted-unadjusted analyses, PCPs were significantlymore likely (P � .001) to often/always/sometimes report lacking ade-quate training (46.4% v 10.5%) and order tests/treatments as malprac-tice protection (51.1% v 40.2%). PCPs were also significantly morelikely to often/always voice concerns about missed care (15.1% v11.7%; P � .01). MOs were more likely (P � .01) to often/always/sometimes report concerns about duplicated care (56.0% v 47.7%)and general preventive health care responsibility (42.3% v 33.1%).

In weighted-adjusted multinomial models, inadequate knowl-edge or training to manage patient problems was significantly morelikely to be reported as a barrier by PCPs compared with MOs (often/always/sometimes: OR, 3.06; 95% CI, 2.03 to 4.61; Table 4). Physiciancharacteristics associated with a lower likelihood of reporting inade-quate knowledge or training included black race, being in the mid-range of the listed medical school graduation years (1980 to 1996),having high or moderate self-ascribed knowledge regarding follow-upcare, and being trained in late- and long-term effects.

MOs were more likely than PCPs to report uncertainty regardinggeneral preventive health care responsibility (often/always: OR, 1.97;95% CI, 1.13 to 3.43; sometimes: OR, 2.16; 95% CI, 1.60 to 2.93; Table4). Uncertainty was also more likely to be a concern for physicians(MOs and PCPs combined) in the west and those in practices thatwere transitioning to a full electronic medical record system. Physi-cians with high self-ascribed knowledge of cancer-related follow-upcare and those physicians whose practice was 26% to 50% elderlypatients were less likely to express uncertainty.

PCPs were more likely than MOs to report often or always order-ing extra tests/treatments as malpractice protection (often/always:OR, 1.87; 95% CI, 1.20 to 2.93). Ordering extra tests or treatments wasalso more common among physicians who were reimbursed via cap-itation, were of Asian/Pacific Islander descent, saw more than 100patients per week, and had only some late-effects training. Physiciancharacteristics associated with a lower likelihood of ordering tests/treatments as malpractice protection included high self-ascribedknowledge of cancer-related follow-up care, detailed late-effects train-ing, receipt of late-effects training from colleagues, being in the mid-range of listed medical school graduation years (1980 to 1996), andhaving a salary not based on productivity.

PCPs and MOs did not differ in reporting the final two physician-related barriers (concerns regarding duplicated or missed care) inadjusted analyses (results not shown). Although PCPs had highphysician-related barrier scores overall compared with MOs in unad-justed analyses (P � .0166), this association was no longer significantafter adjustment (P � .9986).

DISCUSSION

Our article examined 10 self-reported barriers and concerns MOs andPCPs face regarding the care of breast and colon cancer survivors whoare 5 years or more beyond completion of active treatment. To ourknowledge, this is the first nationwide study of its kind. Our primary

Virgo et al

2324 © 2013 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY



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ng4,

622

3.1

501

6.3

4,12

22.

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eim

burs

emen

t.5

265

Prim

arily

fee

for

serv

ice

58,1

9939

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320

41.8

54,8

7939

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ixtu

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for

serv

ice

and

capi

tatio

n10

,151

6.8

457

5.8

9,69

36.

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rimar

ilyca

pita

tion

8,78

05.

945

45.

78,

327

5.9

Do

not

know

,in

appl

icab

le,

mis

sing

71,1

7348

.03,

719

46.8

67,4

5448

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ontin

ued

onfo

llow

ing

page

)

Virgo et al




Tabl

e1.

Des

crip

tive

Cha

ract

eris

tics

byP

hysi

cian

Type

,W

eigh

ted

Com

paris

ons

(con

tinue

d)

Cha

ract

eris

tic

Tota

l(N

�14

8,30

3)�†

Onc

olog

ist

(n�

7,95

0)�†

PC

P(n

�14

0,35

3)�†

P‡

No.

%N

o.%

No.

%

Kno

wle

dge

and

trai

ning

Sel

f-as

crib

edkn

owle

dge

ofca

ncer

-rel

ated

follo

w-u

pca

refo

rbr

east

and

colo

nca

ncer

surv

ivor

s�

.001

Low

know

ledg

e;sc

ore,

4-13

§66

,815

45.1

919

11.6

65,8

9647

.0M

ediu

mkn

owle

dge;

scor

e,14

-16

53,7

9536

.33,

314

41.7

50,4

8136

.0H

igh

know

ledg

e;sc

ore,

17-1

827

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18.5

3,70

546

.623

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16.9

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sing

214

0.1

120.

120

20.

1R

ecei

ved

trai

ning

rega

rdin

glo

ng-t

erm

effe

cts

ofca

ncer

trea

tmen

tth

atsu

rviv

ors

mig

htex

perie

nce

�.0

01

No

50,7

4934

.256

37.

150

,185

35.8

Yes

,so

me

87,3

7458

.94,

505

56.7

82,8

6859

.0Y

es,

inde

tail

8,45

75.

72,

856

35.9

5,60

24.

0M

issi

ng1,

723

1.2

250.

31,

697

1.2

Inth

epa

st5

year

s,ho

wdi

dyo

ure

ceiv

eth

istr

aini

ng?

Con

tinui

ngm

edic

aled

ucat

ion

.010

8N

o48

,461

33.4

2,25

528

.546

,206

33.7

Yes

96,5

0866

.65,

662

71.5

90,8

4766

.3P

rofe

ssio

nalm

eetin

gsor

conf

eren

ces

�.0

01N

o88

,838

61.3

1,92

124

.386

,917

63.4

Yes

56,1

3138

.75,

996

75.7

50,1

3536

.6M

edic

alsc

hool

.034

6N

o13

4,93

193

.17,

557

95.5

127,

374

92.9

Yes

10,0

386.

936

04.

59,

678

7.1

Med

ical

jour

nals

�.0

01N

o65

,408

45.1

2,09

026

.463

,317

46.2

Yes

79,5

6154

.95,

827

73.6

73,7

3553

.8C

olle

ague

s.3

970

No

89,2

9161

.64,

748

60.0

84,5

4261

.7Y

es55

,678

38.4

3,16

940

.052

,510

38.3

Abb

revi

atio

ns:

EM

R,

elec

tron

icm

edic

alre

cord

s;H

MO

,he

alth

mai

nten

ance

orga

niza

tion;

MS

A,

met

ropo

litan

stat

istic

alar

ea;

PC

P,

prim

ary

care

phys

icia

n;P

I,P

acifi

cIs

land

er.

�P

erce

ntag

esm

ayno

tad

dup

toto

taln

umbe

rbe

caus

eof

roun

ding

.†U

nwei

ghte

dnu

mbe

rsar

eas

follo

ws:

tota

l,2,

202;

onco

logi

st,

1,13

0;P

CP

,1,

072.

‡Rao

-Sco

tt�

2te

st.

§Sco

res

of4

or5

wer

eat

trib

utab

leto

mis

sing

resp

onse

s.





Tabl

e2.

Sur

vivo

rshi

pC

are

Bar

riers

and

Con

cern

sby

Phy

sici

anTy

pe,

Wei

ghte

dC

ompa

rison

s

Cha

ract

eris

tic

Tota

l(N

�14

8,30

3)�

Onc

olog

ist

(n�

7,95

0)�

PC

P(n

�14

0,35

3)�

P†

No.

%N

o.%

No.

%

Pat

ient

-rel

ated

barr

iers

/con

cern

sP

atie

nts

refu

seor

dono

tad

here

tore

com

men

ded

care

.000

2O

ften

/alw

ays

16,3

7411

.963

48.

115

,741

12.1

Som

etim

es65

,962

47.9

4,32

055

.261

,642

47.5

Nev

er/r

arel

y55

,272

40.2

2,87

836

.852

,394

40.4

Iam

not

able

toor

der

appr

opria

tete

sts

ortr

eatm

ents

beca

use

ofhe

alth

insu

ranc

epl

anre

stric

tions

.032

9O

ften

/alw

ays

17,1

1612

.697

112

.516

,145

12.6

Som

etim

es51

,205

37.6

3,34

543

.247

,860

37.3

Nev

er/r

arel

y67

,764

49.8

3,42

244

.264

,342

50.1

Pat

ient

sha

vela

ngua

geba

rrie

rsth

atin

terf

ere

with

com

mun

icat

ion‡

.023

5O

ften

/alw

ays

3,44

62.

526

73.

43,

179

2.5

Som

etim

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,637

18.0

1,73

522

.322

,902

17.8

Nev

er/r

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y10

8,64

279

.55,

783

74.4

102,

859

79.8

Pat

ient

sre

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tm

ore

aggr

essi

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ncer

surv

eilla

nce

test

ing

than

wha

tI

wou

ldre

com

men

d�

.001

Oft

en/a

lway

s14

,898

11.1

2,26

828

.912

,630

10.0

Som

etim

es58

,526

43.5

3,64

746

.554

,879

43.3

Nev

er/r

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y61

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45.5

1,93

524

.659

,312

46.8

Pat

ient

sar

eun

able

topa

y(o

rla

ckin

sura

nce

cove

rage

for

follo

w-u

pca

re)

.918

6O

ften

/alw

ays

17,3

8912

.798

212

.716

,407

12.7

Som

etim

es70

,779

51.9

4,08

652

.866

,693

51.8

Nev

er/r

arel

y48

,298

35.4

2,67

534

.645

,622

35.4

Tota

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ient

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.001

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;�

1511

3,94

081

.65,

753

72.8

108,

187

82.1

Hig

h;�

1525

,674

18.4

2,15

227

.223

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17.9

Phy

sici

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once

rns

Ior

der

test

sor

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mys

elf

agai

nst

mal

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litig

atio

n�

.001

Oft

en/a

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9.7

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imes

46,4

7934

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374

30.5

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66,5

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59.8

61,8

5448

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abou

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hich

phys

icia

n(o

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ogy

spec

ialis

tor

PC

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ispr

ovid

ing

patie

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gene

ral

prev

entiv

ehe

alth

care

.000

7

Oft

en/a

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s8,

675

6.3

724

9.3

7,95

16.

1S

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37,4

9627

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568

33.0

34,9

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6066

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644

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Virgo et al




Tabl

e2.

Sur

vivo

rshi

pC

are

Bar

riers

and

Con

cern

sby

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%

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erne

dab

out

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sed

care

byth

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CP

and

onco

logy

spec

ialis

t.0

047

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en/a

lway

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14.9

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56,1

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749

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52,4

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102

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lem

s‡�

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Oft

en/a

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s4,

921

3.7

961.

34,

825

3.8

Som

etim

es54

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40.7

702

9.2

54,0

5842

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ever

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74,7

8755

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89.5

67,9

6453

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-rel

ated

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ier

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5,69

982

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836

86.5

108,

863

82.7

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ian.

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ach

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over

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patie

nts

(N�

148,

303)

inal

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nly

non-

mis

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uded

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em

ultiv

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ble

anal

ysis

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nwei

ghte

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mbe

rsar

eas

follo

ws:

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l,2,

202;

onco

logi

st,

1,13

0;P

CP

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072.

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-Sco

tt�

2te

st.

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ause

ofsm

alls

ampl

esi

zes,

“som

etim

es”

was

com

bine

dw

ith“o

ften

/alw

ays”

for

purp

oses

ofal

lana

lyse

s.§C

rude

tota

lbar

rier

scor

esw

ere

calc

ulat

edby

addi

ngal

lres

pons

es(n

ever

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s,5)

acro

ssth

epa

tient

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late

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ange

s,1-

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d1-

24,r

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ctiv

ely)

and

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tal

toa

dich

otom

ous

varia

ble

(�15

,lo

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ore;

�15

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ghsc

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.





Tabl

e3.

Pat

ient

-Rel

ated

Bar

riers

and

Con

cern

sto

Can

cer

Sur

vivo

rshi

pC

are:

Wei

ghte

dA

djus

ted

Mul

tinom

ialL

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ticR

egre

ssio

nM

odel

s

Var

iabl

e

Insu

ranc

eP

lan

Res

tric

tions

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ngua

geB

arrie

rs†

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uest

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eA

ggre

ssiv

eC

are‡

Res

pons

e(v

R/N

)O

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IR

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(vR

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CI

Res

pons

e(v

R/N

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R95

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Phy

sici

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CP

1.00

Ref

1.00

Ref

1.00

Ref

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olog

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O/A

0.93

0.59

to1.

46O

/A/S

1.7

21

.22

to2

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O/A

4.0

82

.73

to6

.10

S1.4

21.0

3to

1.9

6S

1.9

91

.53

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No.

ofph

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ians

inpr

imar

ypr

actic

elo

catio

n1

1.00

Ref

1.00

Ref

1.00

Ref

2-5

O/A

0.84

0.47

to1.

49O

/A/S

1.27

0.81

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00O

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210.

64to

2.29

2-5

S0.

900.

60to

1.34

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1.6

01

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to2

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6-15

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7to

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1.32

0.80

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95to

3.66

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6to

0.9

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0.7

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mun

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1.24

0.64

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0.94

0.62

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1.44

0.80

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58O

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1.63

0.98

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est

O/A

1.28

0.63

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60O

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2.3

51

.40

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tS

0.5

40.3

6to

0.8

1

MS

A Non

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O/A

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71

.13

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1.00

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940.

45to

1.96

6-10

%sa

fety

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0.3

5to

0.9

9

11-2

0%sa

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O/A

0.65

0.33

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2711

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safe

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tS

0.4

90

.31

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0.59

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0.6

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730.

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4

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paid

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O/A

0.61

0.37

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sala

ryS

0.5

80.4

0to

0.8

4

(con

tinue

don

follo

win

gpa

ge)

Virgo et al




Tabl

e3.

Pat

ient

-Rel

ated

Bar

riers

and

Con

cern

sto

Can

cer

Sur

vivo

rshi

pC

are:

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ted

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tinom

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nM

odel

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iabl

e

Insu

ranc

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lan

Res

tric

tions

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ngua

geB

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rs†

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uest

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pons

e(v

R/N

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ent

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tion/

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680.

91to

3.10

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itatio

nO

/A/S

2.0

01

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to3

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hite

1.00

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1.00

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Asi

an/P

IO

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860.

48to

1.54

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1.28

0.74

to2.

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sian

/PI

S1.

100.

73to

1.64

S1.

080.

77to

1.52

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pani

c¶O

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21.1

3to

5.1

7O

/A0.

980.

47to

2.06

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pani

cS

1.08

0.56

to2.

09S

1.22

0.66

to2.

24B

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O/A

1.06

0.45

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49O

/A0.

960.

27to

3.38

Bla

ckS

0.62

0.31

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0.52

0.25

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ther

/mis

sing

O/A

0.56

0.17

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89O

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670.

20to

2.21

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Virgo et al




finding was that MOs and PCPs perceived different barriers and con-cerns as problematic, though the actual number of perceived barriersdid not differ between MOs and PCPs (4.9 and 4.7, respectively).MOs were more likely to report concerns about language barrierswhen communicating with patients, insurance restrictions imped-ing ordering tests/treatments, patients requesting unnecessary test-ing, and general preventive-care responsibility. PCPs were moreconcerned with feeling inadequately trained and ordering extratests/treatments as malpractice protection. Guidelines regardingcancer survivor follow-up care tend to be more explicit for theinitial 5 years after treatment, but less so beyond 5 years.26-27 PCPsseem aware that there are additional services they should be pro-viding for cancer survivors but may be unclear what those servicesshould include.

Our findings regarding PCPs feeling inadequately trained in sur-vivorship care and ordering excess tests/treatments suggest the needfor improved physician education and training in survivorship care,particularly considering the growing population of long-term cancersurvivors. Oncology and primary care professional societies shouldpartner with cancer research organizations to develop improvedguidelines and webinars for clinicians that address clinical knowledgegaps identified by provider studies such as SPARCCS and the unmetmedical and psychosocial patient needs as reported by cancer survivorsurveys.28-29 Guidelines should be expanded to include the periodbeyond 5 years after primary treatment and clearly differentiateamong guideline-recommended care, care that may be considered butis not explicitly guideline-recommended, and care that is clearlynot indicated.

MOs’ concerns regarding requests from patients for unnecessarytesting suggest a need for patient education. Patient navigators aretrained to address education and two other concerns of MOs: lan-guage barriers when communicating with patients and insurance re-strictions impeding necessary test/treatment ordering. Navigators canidentify translators and link patients with support groups providingboth educational and psychological structure. Navigators are alsotrained to assist patients in finding affordable care, often aided bysocial workers.30-31 The new standards for American College of Sur-geons Commission on Cancer–accredited hospitals requiring thatpatient navigation be available either on site or by referral should helpreduce oncologists’ concerns.32

In addition, our findings regarding MOs’ uncertainty about gen-eral preventive care responsibility suggest the need for increased coor-dination among clinicians in cancer survivorship care delivery.Survivorship care can be difficult to navigate. A team effort is neededto facilitate the patient-to-survivor transition.11 Improved care plan-ning is needed beyond 5 years after primary treatment, despite the lackof survivorship care standards. For patients transitioning back to PCPsfor continued care, TS and SCP are promising tools for improvingcontinuity and coordination of care and for improving survivors’knowledge of optimal tests.33 Increased coordination among clini-cians may also improve PCPs’ confidence in their ability to managepatient problems. We found that PCPs who more frequently reported

receiving a TS or SCP from the patient’s oncology specialist were lesslikely to indicate having inadequate knowledge or training to managepatient problems (TS: often/always, 42.6%; sometimes, 41.9%; v rare-ly/never, 57.3%; SCP: often/always, 37.6%; sometimes, 44.5%; v rare-ly/never, 51.3%).

Potential study limitations include the focus on breast and coloncancer survivorship care barriers. Though the barriers included werefairly generic, it is possible that barriers encountered in providingfollow-up care for children who are cancer survivors, for example,may differ from the barriers reported in this article. Similarly, as ouranalysis was comparative in nature, some barriers perceived solely byPCPs or solely by medical oncologists may have been overlooked insurvey design. In addition, the self-reported nature of the data is apotential limitation. Over- or under-reporting is possible because ofsocial desirability bias. For example, the number of physicians whoreported ordering extra tests/treatments as malpractice protectionmay be an undercount of the actual number of respondents orderingmore tests/treatments than necessary.

The importance of long-term follow-up care for cancer survivorsshould not be underestimated. Years ago, post-treatment survival forcancer patients was relatively short and surveillance was focused pri-marily on detecting recurrences and new primary cancers. With ad-vances in diagnosis and treatment, patients are living longer andconcerns about late effects of cancer and its treatment have come tothe forefront, as have heightened concerns regarding psychosocialissues. The current study is important in highlighting potential chal-lenges in transitioning survivors’ care from MOs to PCPs and isunique in identifying MO- and PCP-specific concerns. High priorityshould be given to developing more efficient methods of communi-cation among providers and between providers and patients,11 design-ing new models of survivorship care such as oncology medicalhomes,34-35 and establishing educational programs tailored to thespecific concerns of PCPs regarding appropriate surveillance testingand late- and long-term effects of cancer and its treatment. Nationallyrepresentative physician surveys, such as SPARCCS, have been andwill continue to remain crucial for systematic evaluation of the impactof such changes on cancer survivorship care.

AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTSOF INTEREST

The author(s) indicated no potential conflicts of interest.

AUTHOR CONTRIBUTIONS

Conception and design: All authorsCollection and assembly of data: Katherine S. Virgo, Catherine C. Lerro,Carrie N. KlabundeData analysis and interpretation: Katherine S. Virgo, Catherine C.Lerro, Carrie N. KlabundeManuscript writing: All authorsFinal approval of manuscript: All authors

REFERENCES

1. American Cancer Society: Cancer Treatmentand Survivorship Facts & Figures, 2012-2013. At-lanta, GA, American Cancer Society, 2012

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Virgo et al




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http://ncccp.cancer.gov/files/NCCCP_SurvPalliativeCare.pdf

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http://healthservices.cancer.gov/surveys/sparccs/

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http://www.nccn.org/professionals/physicians_gls/pdf/breast.pdf

http://www.nccn.org/professionals/physician_gls/pdf/colon.pdf

http://www.nccn.org/professionals/physician_gls/pdf/colon.pdf

http://patientnavigatortraining.org/website/courses.htm

http://patientnavigatortraining.org/website/courses.htm

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http://www.hpfreemanpni.org/the-program/

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http://facs.org/cancer/coc/cocprogramstandards2012.pdf

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