interventions to improve care related to colorectal cancer ... · interventions to improve care...

Interventions to Improve Care Related to Colorectal CancerAmong Racial and Ethnic Minorities: A Systematic Review

Keith Naylor, MD1, James Ward, MD2, and Blase N. Polite, MD, MPP 2,3

1Section of Gastroenterology, Department of Medicine, University of Chicago, Chicago, IL, USA; 2Section of Hematology-Oncology,Department of Medicine, University of Chicago, Chicago, IL, USA; 3The University of Chicago Medical Center, Chicago, IL, USA.

OBJECTIVE: To systematically review the literature toidentify interventions that improve minority healthrelated to colorectal cancer care.DATA SOURCES: MEDLINE, PsycINFO, CINAHL, andCochrane databases, from 1950 to 2010.STUDY ELIGIBILITY CRITERIA, PARTICIPANTS, ANDINTERVENTIONS: Interventions in US populationseligible for colorectal cancer screening, and composedof ≥50 % racial/ethnic minorities (or that included aspecific sub-analysis by race/ethnicity). All includedstudies were linked to an identifiable healthcare source.The three authors independently reviewed the abstractsof all the articles and a final list was determined byconsensus. All papers were independently reviewed andquality scores were calculated and assigned using theDowns and Black checklist.RESULTS: Thirty-three studies were included in ourfinal analysis. Patient education involving phone or in-person contact combined with navigation can lead tomodest improvements, on the order of 15 percentagepoints, in colorectal cancer screening rates in minoritypopulations. Provider-directed multi-modal interventionscomposed of education sessions and reminders, as wellas pure educational interventions were found to beeffective in raising colorectal cancer screening rates, alsoon the order of 10 to 15 percentage points. No relevantinterventions focusing on post-screening follow up, treat-ment adherence and survivorship were identified.LIMITATIONS: This review excluded any interventionstudies that were not tied to an identifiable healthcaresource. The minority populations in most studiesreviewed were predominantly Hispanic and AfricanAmerican, limiting generalizability to other ethnic andminority populations.CONCLUSIONSAND IMPLICATIONSOFKEY FINDINGS:Tailored patient education combined with patient naviga-tion services, and physician training in communicatingwith patients of low health literacy, can modestly improveadherence to CRC screening. The onus is now onresearchers to continue to evaluate and refine these

interventions and begin to expand them to the entirecolon cancer care continuum.

KEY WORDS: colorectal cancer; race; ethnicity; interventions; outcomes.

J Gen Intern Med 27(8):1033–46

DOI: 10.1007/s11606-012-2044-2

© Society of General Internal Medicine 2012

INTRODUCTION

Colorectal cancer (CRC), although a preventable disease, causesthe death of more than 50,000 Americans per year.1 Given theability to detect and intervene on pre-cancerous lesions,colorectal cancer screening is associated with decreased CRCmortality.2 Because of advances in screening and treatment, theincidence of and mortality from colorectal cancer have beendeclining over the last 25 years.1 Unfortunately, this decline hasnot been shared equally by all groups, resulting in a growingracial and ethnic survival gap over that same 25-year period.1,3,4

Racial and ethnicminority patients, as well as thosewith lowerincomes and inadequate insurance, are less likely to receiveadequate screening.5–7 Once screened positive, they are lesslikely to be treated, and once treated, less likely to haveguideline recommended follow up.8–10

Avariety of physician, patient, and health systems barriers haveplayed their role in these disparities.11 Emerging in the last 10 to15 years is a body of literature that focuses on investigatinginterventions to address these barriers. The goals of this paperare: to systematically review the medical literature for inter-ventions conducted within health care systems that have thepotential to decrease racial and ethnic disparities in the care ofcolorectal cancer; to evaluate the strength of their evidence; andto recommend both public health and research strategies goingforward based on this evidence.

METHODS

In consultation with a biomedical librarian, an electronic searchwas conducted using the MEDLINE database for articlesreporting on interventions that have the potential to reducedisparities in health outcomes or health care processes in

Systematic review registration number This systematic review is notregistered.

K. Naylor and J. Ward contributed equally to the manuscript

Electronic supplementary material The online version of this article(doi:10.1007/s11606-012-2044-2) contains supplementary material,which is available to authorized users.

1033

http://dx.doi.org/10.1007/s11606-012-2044-2

colorectal cancer screening, treatment, survivorship, and end-of-life care published from 1950 to September, 2010. For the topicof colorectal cancer screening, an additional parallel search wasconducted using the PsycINFO, CINAHL, and CochraneRegister of Controlled Trials databases. In addition, a manualsearch was conducted that included topic relevant reviewarticles;12–15 reference lists obtained from the studies meetingpre-specified inclusion criteria; and unpublished abstracts pre-sented in 2009 and 2010 from selected national meetings ofprofessional societies including Digestive Diseases Week(DDW) and the American Society of Clinical Oncology(ASCO). This review conforms to the Preferred Reporting Itemsfor Systematic Reviews and Meta-Analyses (PRISMA) stand-ards.16 A summary of the review protocol may be found in theintroductory article by Chin et. al.

Search Strategy

The MEDLINE database was searched using pre-specifiedMedical Subject Headings (MeSH) terms and keywords toidentify studies evaluating interventions in colorectal cancerscreening, treatment, survivorship, and end-of-life care amongracial and ethnic minority patients. Please see Text Box 1 forthe colorectal cancer screening MEDLINE database searchstrategy. A full listing of the MeSH terms and Keywords usedin the MEDLINE database search may be found in Appendix 1(available online). A full listing of the search terms used in thePsycINFO and CINAHL database searches may be found inAppendix 2 (available online).

Inclusion and Exclusion Criteria

Articles and abstracts were assessed for inclusion based on pre-specified criteria. Study populations were required to becomposed of patient groups with greater than 50 % minority

representation (defined as >50 % racial/ethnic minority patients)or, if less than 50 %, the study must include subgroup analysisby race or ethnicity with documentation of sufficient statisticalpower. Articles must report on an experimental intervention(purely descriptive studies were excluded). Articles were notexcluded based solely on the type of experimental study designor measured outcome. Study interventions were required to takeplace within the context of a consistent source of health care(community interventions must directly integrate a system ofongoing medical care). Lastly, studies were required to beconducted in the United States and to be published in English.

Data Collection Process

The titles and abstracts of articles obtained from theelectronic search were screened by two reviewers (KN andJW) independently to eliminate duplicates and articlesunrelated to colorectal cancer. A full text review wasperformed on the remaining articles to assess inclusionand exclusion criteria, discrepancies were resolved byconsensus among all three reviewers. A manual referencereview was performed on all articles meeting inclusioncriteria and on topic relevant reviews12–15 in order toinclude articles not identified in the electronic databasesearch. All articles not meeting inclusion criteria wereexcluded. Articles were then manually extracted for dataincluding reference citation, type of intervention, studydesign, study population, setting, outcomes assessed,results, and quality assessment measures.

Quality Assessment

To assess study quality, each article was abstracted bytwo authors and assigned a quality score using amodified Downs and Black scoring algorithm. Inter-

Text Box 1. Medline Colorectal Cancer Screening Intervention Search Strategy

1034 Naylor et al.: Colorectal Cancer Care Interventions for Minorities JGIM

rater reliability was assessed using four randomlyselected articles resulting in a weighted kappa statisticof 81.25 %. The Downs and Black checklist is avalidated instrument used to assess the methodologicalquality of studies across a variety of domains includ-ing: reporting, external validity, bias, confounding, andpower.17 For this review, we utilized a modified Downsand Black scoring checklist with a maximum achiev-able score of 29. To aid in the comparison of studyquality across articles, a qualitative categorizationgrouping articles by Downs and Black score (≥20:very good; 15-19: good; 11-14: fair; ≤10: poor) wasused.18

RESULTS

Article Selection (Figure 1)

The combined electronic database search resulted in489 articles. A manual title and abstract review wasperformed, identifying 53 articles for independent fulltext review. Fourteen articles, representing studies ofcommunity interventions, were excluded from the reviewdue to lack of a consistent source of healthcare(Appendix 3); 22 other studies also did not meet thepre-specified inclusion criteria. The combined electronicdatabase search resulted in 17 articles for data collection.A manual reference review of included studies andrelevant topic review articles resulted in an additional16 articles. Overall, the search process resulted in a total of 33articles that were included in the final systematic review.Downs and Black (DB) scores ranged from 5 to 27, with amedian score of 20. The manual review of unpublishedabstracts presented at selected national meetings resulted inthe identification of three abstracts. There was insufficientdata presented in the abstracts to perform quality assessment(Appendix 4-available online).

Demographics (Figure 2)

Figure 2 provides a breakdown of the studies by thepredominant racial or ethnic population that was ana-lyzed. Thirteen of the 33 studies included a majority ofAfrican-Americans, eight of the 33 included a majorityof Hispanics, and two of the 33 included a majority ofAsians. In seven of the 33 included studies the majorityof the subjects were composed of a mix of racial/ethnicminorities and in three of the 33 studies a majority of thesubjects was listed as “non-white”.

Intervention Type (Table 1, Figure 3)

Displayed in Table 1, are the 33 studies we included in thefinal analysis, as well as information related to study design,measured outcome(s), intervention details, setting, samplesize and ethnicity, length of follow up, major findings, and

Figure 1. Colorectal cancer screening interventions search results.

Figure 2. Breakdown of studies by race/ethnicity (# of total studies,n=33).

1035Naylor et al.: Colorectal Cancer Care Interventions for MinoritiesJGIM

Tab

le1.

Summaryof

Studies

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

Miller

et.al.

2005

21

RT

Screening

-Com

pletionof

FOBT

PL-E

Amultim

edia

compu

terprog

ram

vs.nu

rsecoun

selin

gon

FOBT

useandcollection(usual

care).

Outpt

N=20

430

dNodifference

inFOBT

completioninterventio

n62

%(58/93

)vs.u

sualcare

grou

p63

%(64/10

1);p=0.89

.Kno

wledg

emastery

(>5

correctrespon

ses)

was

similar

betweengrou

ps(p=0.09

).

26Black:72

%FOBTKno

wledg

eassessed

by6item

post-

interventio

nqu

estio

nnaire

White:28

%

Stokamer

et.al.

2005

32

RT

Screening

-Com

pletionof

FOBT

PL-E

One-on-on

eeducationsessions

plus

FOBTandbrochu

revs.

standard

educationgrou

pwith

FOBTandbrochu

re.

VA

Outpt

N=78

86m

oFOBTcompletionhigh

erin

the

interventio

ngrou

p65

.9%,vs.

standard

education51

.3%

(p<

0.00

1).Nodifference

inFOBT

completionby

race/ethnicity

(p=0.65

5)

25Black:35

%Hisp/Lat:15.9%

White:45

.6%

Basch

et.al.

2006

30

RT

Screening

-Com

pletionof

FOBT,

Sigmoido

scop

y,Colon

oscopy,or

Barium

Enema

PL-E

Tailoredteleph

oneeducation

basedon

behavioral

and

educationaltheory

vs.mailed

brochu

re.

Com

mN=45

66mo

Screening

documentedin

27.0

%of

interventio

ngrou

pvs.6

.1%

incontrol;OR4.4(95%

CI

2.6,

7.7).

24Black:63

.2%

White:16

.2%

Other:19

.7%

Walsh

et.al.

2010

29

RT

Self-repo

rted

up-to-date

screeningwith

FOBTOr

Any

CRCScreening

(FOBT,

Sigmoido

scop

y,and/or

Colon

oscopy

)

PL-E

(1)Biling

ualcultu

rally

tailo

red

brochu

rewith

FOBTor

(2)

Biling

ualcultu

rally

tailo

red

brochu

rewith

FOBTplus

teleph

onecoun

selin

gby

acommun

ityhealth

advisorvs.

(3)usualcare.

Outpt

N=17

891yr

Participantsin

brochu

re/

coun

selin

ggrou

pweremore

likelyto

repo

rtFOBT

screeningvs.usualcare.OR=

1.89

(95%

CI1.34

,2.66

),comparedto

OR=1.18

(95%

CI0.84

,1.66

)in

brochu

realon

egrou

p;In

theVietnam

ese

popu

latio

n,theadditio

nof

coun

selin

gfurtherincreased

FOBTratesOR3.02

(95%

CI

1.77

,5.14

)comparedto

brochu

reon

lyOR1.33

(95%

CI0.80

,2.20

).

24Hisp/Lat:52

.9%

Asian:47

.1%

Goldb

erget.

al.20

0425

RT

Screening

-Com

pletionof

FOBT

PL-O

MailedFOBTwith

appo

intm

ent

reminderletter2weeks

priorto

schedu

ledclinic

appo

intm

ent

vs.usualcare.

Outpt

N=119

1yr

Indexappo

intm

entFOBT

completionwas

35.6

%interventio

ngrou

pvs.3.3%

usualcare

grou

p,OR=16

.0(95%

CI3.5,

71.4).One

year,

FOBTcompletioninterventio

nvs.u

sualcare

OR=13

.0(95%

CI3.6,

45.5).

23Black:82

%Hisp/Lat:3%

Makou

let.

al.20

0922

PP

Viewer

ratin

gandintention

todiscussscreening

assessed

bypo

sttest

structured

interview.

Willingn

essto

consider

FOBT,

sigm

oido

scop

y,or

colono

scop

y;and

screeningkn

owledg

eassessed

pretestand

posttestby

structured

in-

terview

PL-E

Culturally

tailo

redCRC

screeningeducationalvideo

with

positiv

eintrod

uctory

appealvs.n

egativeintrod

uctory

appeal.

Outpt

N=27

0NA

Nodifference

inpo

sitiv

evs.

negativ

eintrod

uctio

nfor

view

erratin

g,kn

owledg

e,willingn

ess,or

intention(p

valueno

trepo

rted).

22

Com

positewillingnessto

considerFO

BT,

sigm

oidoscopy,

andcolonoscopyincreased

pretestv

s.posttest(p<0.001for

each).Com

posite

mean

know

ledgescores

increased

from

3.8pretestto

6.3posttest

(p<0.001).

Hisp/Lat:10

0%


Table

1.(c

ontin

ued)

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

Potteret.al.

2009

26

RT

Screening

-Com

pletionof

FOBT;or

up-to-date

screeningwith

Sigmoido

scop

y,Barium

Enema,

orColon

oscopy

PL-O

FOBTdistribu

tionandeducation

attim

eof

annu

alflushot

clinic

visitwith

reminderph

onecalls

at3and6weeks

vs.flushot

alon

ewith

usualcare.

Outpt

N=51

46mo

Interventio

ngrou

pFOBT

completionincreasedfrom

54.5%

atbaselin

eto

84.3

%at

follo

w-up(p<0.00

1)vs.52

.9%

to57

.3%

(p=0.07

1)in

the

usualcare

grou

p.68

.0%

ofinterventio

ngrou

pbecameup

-to-datewith

screeningvs.2

0.7

%forusualcare

grou

p(p<

0.00

1),OR=11.3

(95%

CI

5.8,

22.0)

22Asian:56

.1%

Hisp/Lat:25

.2%

Black:6.1%

Myerset.al.

2007

31

RT

Screening

-Com

pletionof

FOBT;or

self-reported/

documented

Sigmoido

scop

y,Colon

oscopy,or

Barium

Enema

PL-E

Participantsassign

edto

1of

4interventio

ns:Usual

care;

Stand

ardInterventio

n(SI)with

letter,inform

ationbo

oklet,and

FOBT;TailoredInterventio

n(TI),or

TailoredInterventio

nplus

reminderph

onecall(TIP).

Outpt

N=15

4624

mo

CRCscreeninguseintent-to-treat

analyses:controlgroup33

%;S

Igroup46

%(O

R=1.68,95%

CI

1.25,2.53);T

Igroup44

%(O

R=1.58,95%

CI1.18,2.12)

TIP

group48

%(O

R=1.91,95%

CI

1.42,2.56).S

creening

didnot

differacrossinterventio

ngroups

(p>0.1forall).

21Black:58

%White:38

%

Jacobs

et.

al.20

0128

Coh

ort

Screening

-Com

pletionof

annu

alFOBT

PL-O

Professionalinterpreterservices

prov

ided

at4of

14clinics

servinglim

ited-Eng

lish-

speaking

patientsvs.

comparisongrou

pof

rand

omly

selected

adultsrepresentin

g10

%of

theeligible

popu

latio

n.

Outpt

N=32

7NA

FOBTcompletioninterventio

nvs.comparisongrou

pOR=

0.66

(95%

CI0.44

,0.99

;p<

0.5)

year

one;

OR=0.86

(95%

CI0.57

,1.28

)year

two.

No

change

inFOBTcompletion

year

onevs.year

twoin

interventio

n(p=0.28

)or

comparisongrou

p(p=0.35

).

20Spanish

speaking

:79

%Portugu

ese

speaking

:21

%

Tuet.al.

2006

27

RT

Screening

-Com

pletionof

FOBT

PL-E

Trilin

gual

health

educator

plus

cultu

rally

tailo

redvideoand

printmaterialsvs.usualcare.

Outpt

N=21

06mo

FOBTcompletiongreaterin

interventio

ngrou

p69

.5%

vs.

usualcare

27.6

%;Age

adjusted

OR=5.91

(95%

CI=

3.25

,10

.75)

20Asian:10

0%

Fitzgibb

onet.al.

2007

19

RT

Screening

-Com

pletionof

FOBT,

Flexible

Sigmoido

scop

y,or

Colon

oscopy

Providerrecommendatio

nassessed

bychartabstrac-

tion

PL-E;PSL

Phy

sician

education/feedback

sessions

plus

patient

education

with

tailo

redvideo,

pamph

let,

andFOBTdistribu

tionwith

simplifiedinstructions

vs.usual

care.

VA

Outpt

N=98

66-18

mo

Providers

who

attend

edinterventio

nsessions

recommendedCRCscreening

more(64%

vs.54

%,p=

0.00

4)andtheirpatients

completed

CRCscreening

more(42.3%

vs.29

.5%,p=

0.02

)vs.prov

idersthat

attend

edno

sessions.

Patientsin

theinterventio

ngrou

pweremorelik

elyto

have

screeningrecommended

(83.7%

vs.74

.6%,p=0.00

3)vs.usualcare.Nodifference

inscreeningcompletion(39.5%

vs.41

.6%,p=0.61

).

19Black:50

%White:45

%


Table

1.(c

ontin

ued)

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

Friedman

et.al.

2001

24

RT

Screening

-Com

pletionof

FOBT

PL-E

Culturally

tailo

redvideo

featuringpeer

educatorsand

health

profession

alsvs.

standard

printeducation.

Outpt

N=16

03mo

FOBTcompletiondidno

tdiffer

betweenthevideo43

.6%

vs.

standard

education36

%(p=

0.84

7).Kno

wledg

e,self

efficacy,andintent

scores

were

high

erin

thevideovs.stand

ard

education(F-stastistics,p<

0.00

1foreach).

19Black:87

.5%

CRCkn

owledg

eassessed

by16

-item

measure

Hisp/Lat:5%

Selfefficacy

andintent

assessed

bysing

leitem

measure

Hoffm

anet.

al.19

9123

Coh

ort

Stage

ofCRCat

timeof

diagno

sis

PL-E,PSL

Edu

catio

nalpamph

let;

distribu

tionof

free

FOBTkits;

nurseFOBTdemon

stratio

n;and

multid

isciplinaryprotocol

for

diagno

stic

evaluatio

nand

treatm

entof

FOBTpo

sitiv

epatientsvs.usualcare

Outpt

N=81

9265

mo

There

were0%

mod

ified

Duk

es’stageD

and35

%(6/

16)stageA

intheinterventio

ngrou

pcomparedto

33%

(114

/34

6)Duk

es’stageD

and0%

stageA

forusualcare.

Interventio

ncoho

rtwere

diagno

sedat

anearlierDuk

e’s

stagevs.usualcare

(p=0.00

3).

10Black:95

%

Dietrichet

al20

0634

RT

Screening

adherence

accordingto

USPSTF

guidelines

PL-N

Frequ

ent(m

ean4)

phon

ecall

follo

wup

from

apreventio

ncare

manager

versus

usualcare.

Outpt

N=1,41

318

mo

24%

ininterventio

ngrou

pvs.

11%

incontrolgrou

pwere

screened;a13

%difference

(95

%CI:0.07

-0.19),p<0.00

1.

27Race/Ethnicity

not

prov

ided;

however,6

4%

ofpatientslisted

Spanish

asprim

arylang

uage

Percac-

Lim

aet

al.

2008

36

RT

Screening

with

colono

scop

y,sigm

oido

scop

y,barium

enem

a,or

FOBTdu

ring

stud

yperiod

PL-N

Culturally

tailo

redpatient

navigatorprog

ram

Outpt

Com

mN=1,22

39mo

27.4

%of

interventio

nvs.11.9

%of

controlgrou

pwere

screened

with

inthefollo

w-up

interval

(p<0.00

1).

24Hisp/Lat:40

.1%

Black:6.4%

Asian:1.5%

Jand

orfet.

al.20

0538

RT

Screening

with

FOBT,

flexiblesigm

oido

scop

y,or

colono

scop

y

PL-N

Patient

navigator(PN)

interventio

n(including

written

reminders,teleph

onecalls,and

schedu

lingassistance)

Outpt

N=78

6mo

23.7

%of

PNgrou

pvs.5

.0%

ofcontrolgrou

preceived

screeningendo

scop

yin

the

follo

w-upinterval

(p=0.01

9).

23Hisp/Lat:82

.1%

Fordet.al.

2006

35

RT

Screening

with

sigm

oido

scop

yat

3years

afterbaselin

escreening

PL-N

Casemanagem

entinterventio

nwith

outreach

(atleast

mon

thly),serviceplanning

,servicelin

kage,m

onito

ring

,and

advo

cacy

vs.usualcare.

Outpt

N=70

33yr

Flexiblesigm

oido

scop

ywas

completed

by68

.9%

oflow-

incomepatientsin

the

interventio

ngrou

pand51

.3%

inthecontrolgrou

p(p=0.10

).In

themod

erate-to-highincome

grou

p,53

.8%

ofpatientsin

the

interventio

narm

vs.62

.5%

ofpatientsin

thecontrolarm

completed

flexible

sigm

oido

scop

y(p=0.22

).

22Black

men:10

0%

enrolledin

the

Prostate,

Lun

g,Colorectal,and

Ovarian

(PLCO)

cancer

screening

trial


Table

1.(c

ontin

ued)

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

Nashet.al.

2006

39

PP

Screening

-Receipt

ofcolono

scop

ypermon

thin

preversus

post

interventio

nperiod

.Provider/System-Broken

appo

intm

entrate

preand

postinterventio

n

PL-N

DirectEnd

oscopicReferral

System

andpatient

navigator

system

atan

urbanpu

blic

hospital..

Outpt

N=1,06

011

mo

The

averagenu

mberof

Medicaidpatientsun

dergoing

screeningcolono

scop

yper

mon

thincreasedfrom

17.0

pre

to48

.4po

st-intervention(p<

0.00

1).Brokenappo

intm

ent

ratesforcolono

scop

ydecreasedfrom

67%

preto

5%

post-intervention.

The

authorsno

tedaRRof

2.6(95

%CI2.2-3.0)

ofkeepinga

colono

scop

yappo

intm

entin

thepo

st-interventioncompared

tothepre-interventio

nsetting

.

20PSL

Hisp/Lat:

69%-79%

Black:6%-17%

Chenet.al.

2008

33

Coh

ort

Screening

-Com

pletionof

colono

scop

yov

er30

mon

threview

period

.

PL-N

open-accessendo

scop

yschedu

lingandpatient

navigator

services

(providing

education,

reminderph

onecalls,

transportatio

nassistance,and

face

toface

meetin

gs)

Outpt

N=53

2NA

353(66%)of

navigatedpatients

completed

colono

scop

y(Com

paredto

43%

inEast

Harlem

Area).

16PSL

Hisp/Lat:55

%Black:30

%at

EastHarlem

Hospital

Provider/System-N

oSho

wRate

Hispanics

morelik

elyto

completethan

AA

(OR

1.67

;95%CI1.1-2.5)

Noshow

rate

drop

pedfrom

40%

to9.8%.

Christie

et.

al.20

0837

RT

Screening

-Com

pletionof

Colon

oscopy

PL-N

patient

navigatorinterventio

nvs.

usualcare.screening

colono

scop

yratesdu

ring

follo

w-upinterval.

Outpt

N=21

patients

3mo

53.8

%of

thenavigatedpatients

completed

colono

scop

yversus

13%

ofno

n-navigatedpatients

(p=0.08

5).63

%of

patientsin

theno

n-navigatedgrou

prefusedcolono

scop

ycompared

to23

%in

thenavigatedgrou

p.

16Hisp/Lat:71

%White:22

%

Dietrichet

al19

9847

RT

Screening

-Com

pletionof

FOBTor

sigm

oido

scop

yPSL

Multi-modalintervention

(workshops,rem

inders,clinic

flow

sheets)designed

toincrease

recommendations

andscheduling

ofCRCscreeningtests.

Outpt

N=26

4824

mo

There

wereno

statistically

sign

ificantdifferences(p>

0.05

)betweentheinterventio

nandcontrolclinicsin

term

sof

FOBTor

sigm

oido

scop

yuse

from

baselin

eto

24mon

thfollo

wup

.

25Black:30

%Hisp/Lat:22

%White:22

%Unk

nown:

20%

Ferreiraet

al.20

0548

RT

Screening

-Com

pletionof

FOBT,

sigm

oido

scop

y,or

colono

scop

y

PSL

Multi-mod

alinterventio

ninclud

ingeducationalsessions

oncommun

icatingwith

patientswith

low

literacyskills

aswellas

feedback

sessions

atwhich

individu

alandgrou

plevelcoloncancer

screening

data

werepresented.

Outpt

N=1,97

818

mo

Phy

siciansin

theinterventio

ngrou

pweremorelik

elyto

recommendscreening,

asmeasuredby

chartauditwith

in6-18

mon

thsof

thefirstvisit

(76%

vs.6

9.4%,p

=0.02

),and

theirpatientsweremorelik

ely

tocompletescreening(41.3%

vs.32

.4%,p=0.00

3).Results

weremostimpressive

forapre-

plannedsubset

ofanalysisof

patientswith

low

literacyskills

(55.7%

vs.39

.0%,p=0.00

2).

23Black:50

%

Process-Phy

sician

recommendatio

nof

CRC

screening

Pre-plann

edsubset

analysis

amon

glow

health

literacy

patients


Table

1.(c

ontin

ued)

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

Khank

ariet.

al.20

0746

PP

Screening

-Com

pletionof

FOBT,

sigm

oido

scop

y,or

colono

scop

y

PSL

Manualtracking

ofpatients;

physicianandpatient

education;

andestablishm

ento

famon

itoring

“feedb

ackloop”.

The

outcom

esof

interestwere

ratesof

physicianCRC

screeningrecommendatio

n(m

easuredby

prov

ider

chart

auditat

12mon

thspo

st-

interventio

n)andpatient

completionof

CRCscreening.

Outpt

N=17

412

mo

Phy

sician

recommendatio

nof

CRCscreeningincreasedfrom

31.6

pre-

to92

.9%

(p<0.00

1)po

st-intervention.

Com

pletion

ofCRCscreeningat12

mon

ths

increasedfrom

11.5

%pre-

to27

.9%

(p<0.00

1)po

st-

interventio

n.

21PL-O

Black:51

.7%

Hisp/Lat:44

.8%

Process-Phy

sician

recommendatio

nof

CRC

screening

Sheinfeld-

Gorin

et.

al.20

0045

PP

Kno

wledg

e-survey

questio

nnairesof

CRC

barriers,preventio

nand

screeningkn

owledg

e

PSL

Primarycare

physicians

received

individu

alized

inform

ationon

currentcancer

preventio

nand

screeningrecommendatio

nsvs.

acontrolgrou

pwith

nointerventio

n.

Outpt

N=12

218

mo

Nosign

ificantdifference

betweengrou

psin

self-

repo

rted

cancer

preventio

nand

screeningpractices

(survey

score9.82

vs.9.63

,p=0.42

).Interventio

ngrou

pph

ysicians

identifiedsign

ificantly

fewer

barriers

topracticepo

st-

interventio

ncomparedto

controlph

ysicians

(survey

scores

4.73

vs.5.35

,p<0.05

).

20Black:32

%Hisp/Lat:24

%

Laneet

al.

2008

44

RT

Screening

-Com

pletionof

FOBT,

sigm

oido

scop

y,or

colono

scop

y

PSL

CMEapprov

eddidactic

sessions.

Outpt

N=2,22

412

mo

16%

increase

inCRCscreening

amon

gstpatientsseen

byph

ysicians

intheinterventio

ngrou

p(post-interventio

n)comparedto

a4%

increase

inCRCscreeningin

thecontrol

grou

p(m

easuredby

chart

auditin

the1year

period

before

andafterinterventio

n),

OR2.25

(95%

CI:1.67

,3.04

).

19“N

on-W

hite”:78

%

Process-Phy

sician

recommendatio

nof

orreferralforCRCscreening

Roetzheim

etal.

2004

49

RT

Screening

-com

pletionof

FOBT

PSL

Multi-mod

alinterventio

nconsistin

gof

checklists,chart

reminders,andfeedback

ofscreeningratesto

clinic

staff.

Rates

ofcompletionof

FOBT

atbaselin

eandfollo

w-upwere

assessed

in15

0charts

rand

omly

selected

from

each

clinic.

Outpt

N=1,19

612

mo

There

was

a14

%absolute

improv

ementin

FOBT

completion(O

R2.56

,95

%CI

[1.65-4.01

],p<0.00

1)forthe

interventio

nclinicsversus

controlclinics,as

measuredby

chartauditat

1,2,

and3

mon

thspo

st-intervention.

19Black:29

%White:48

%Hisp/Lat:23

%

Struewing

et.al.

1991

43

PP

Screening

-com

pletionof

rectal

exam

,FOBT,

orsigm

oido

scop

y

PSL

Amulti-levelinterventio

nthat

includ

ed:system

atic

distribu

tionof

FOBTkits,

housestaffandnu

rsing

education,

andph

ysician

screeningremindercards.

Outpt

N=36

56wks

Nochange

inrectal

exam

orsigm

oido

scop

ywas

seen

inanygrou

pat

sixweeks

post-

interventio

n.The

prop

ortio

nof

patientscompliant

with

three-

dayFOBTincreasedfrom

1.3

%preto

56.8

%po

st-

interventio

n(p<0.00

1)

19Black:51

.2%

White:48

.8%


Table

1.(c

ontin

ued)

Reference

Design

Outcom

eTyp

eIntervention

Typ

eIntervention

(s)

Setting

Sam

pleSizeRace/

Ethnicity

Follow

up

Results

DB

Score

McPheeet

al.19

8950

RT

Screening

-com

pletionof

rectal

exam

,FOBT,

orsigm

oido

scop

y

PSL

Providerreminders,chartaudit

with

feedback,or

nointerventio

n.

Outpt

N=3,90

59mo

Com

paredto

controls,acancer

screeningremindersystem

aimed

atinternal

medicine

residentsincreasedFOBTrates

by19

%(P=0.00

2),increased

rectal

exam

ratesby

23%

(p<

0.00

1),andincreased

sigm

oido

scop

yratesby

31%

(p=0.00

2).

17Black:25

%Hisp/Lat:17

%Asian:14

%

Arm

ouret

al.20

0440

Coh

ort

Screening

-com

pletionof

FOBT,

sigm

oido

scop

y,colono

scop

y,or

doub

le-

contrastbarium

enem

a

PSL

Financial

bonu

sesas

incentives

toim

prov

eCRCscreening

rates.

Outpt

HP

N=6,74

9NA

CRCscreeninguseincreased

from

23%

to26

%of

eligible

patients(p<0.01

)in

theyear

afterfinancialincentives

were

added.

16Black:28

%

Parikhet

al.

2001

41

Cohort

Other-com

parisonof

endo

scop

yresults

follo

wing3-dayat

home

FOBTvs.1-dayin-office

FOBT

PSL

One-tim

e,in-officeFOBTwas

comparedto

3-dayho

meFOBT

asascreeningmechanism

for

CRC.

Outpt

N=35

0NA

There

was

good

correlation

betweenin-officeFOBTand

the3-dayFOBTtestresults

(k=0.63

16).

15PL-O

Black:52

%Hisp/Lat:19

%

Friedman

et.al.

2007

20

PP

Screening

-com

pletionof

FOBT,

rectal

exam

,sigm

oido

scop

y,or

colono

scop

y

PSL

Edu

catio

nalinterventio

nwith

pre

andpo

st-intervention

mon

itoring

ofcancer

screening

documentatio

nin

themedical

record.

Outpt

N=16

66mo

The

prop

ortio

nof

orders

for

endo

scop

icCRCscreening

increasedfrom

26.7

%preto

59.1

%po

st-intervention(p<

0.00

01).Perform

ance

ofFOBT

didno

tsign

ificantly

change

follo

wingtheinterventio

n.

14Black:10

0%

Zub

arik

etal.200

042

PP

Screening

-com

pletionof

flexible

sigm

oido

scop

yPSL

Provider-directed

educational

materialsstressingthe

impo

rtance

ofCRCscreening

andtheavailabilityof

flexible

sigm

oido

scop

y.

Outpt

N=12

15mo

useof

flexible

sigm

oido

scop

yincreasedby

42%

(from

xpre

toypo

st-intervention,

p=xx

x).

12Inpt

Com

mBlack:97

%

Lloyd

et.al.

2007

51

PP

Screening

-com

pletionof

colono

scop

yPSL

Trainingprim

arycare

physician

toperform

screening

colono

scop

y.

Outpt

Com

mN=50

NA

The

prop

ortio

nof

prim

arycare

patientsscreened

bycolono

scop

yincreasedfrom

20%

pre-

to80

%po

st-

interventio

n(p-value

not

prov

ided).

5Nopatient

race/

ethn

icity

data

repo

rted.

Listof

abbreviatio

nsforTable1

CRC,ColorectalCan

cer;

FOBT,

Fecal

OccultBlood

Test;Outpt,Outpa

tient;Inpt,Inpa

tient/Hospital;Com

m,Com

mun

ity;HP,

Health

Plan/Health

Insurance;

RT,

Ran

domized

Trial;PP,

Pre/Post;

Hisp/Lat,Hispa

nic/Latino;

CI,Con

fidence

Interval;PL-E,Patient-level

Edu

catio

n;PL-N,Patient-level

Navigation;

PL-O

,Patient-level

Other;PSL

,Provider/system

level.


DB score. For the purpose of further discussion and dataanalysis, the articles were grouped into one of three majorintervention types: patient-level interventions (includingeducation and other interventions), patient-level navigation,and provider/system-level interventions based on the pre-dominant intervention evaluated in the study. Sixteen of 33(48.5 %) articles included interventions that targeted CRCdisparities across multiple levels (patient, provider, and/orsystem). Figure 3 provides a graphic description of thisinformation, including a breakdown of the studies by thepredominant intervention type, as well as the number ofmulti-level intervention studies.

Patient-Level Interventions (Table 1),n=13 (39.4 %)Intervention. Of the thirteen articles evaluating non-navigationrelated patient-level interventions, ten studies assessededucational interventions; Five evaluated educationadministered by trained professionals (telephone, one-on-one,and/or group presentation),19–23 and five assessed self-administered media interventions (computer, brochure, and/orvideo).19,21–24 Two studies evaluated FOBT distributioninterventions, one through the mailing of FOBT kits25 andthe other through a point of care intervention at the time ofinfluenza vaccination.26 Three studies27–29 evaluatedmultilingual interventions consisting of community healthadvisors, tailored bilingual educational materials, or interpreterservices.

Quality. Ten of the 13 patient-level intervention articles wererandomized controlled trials,19,21,24–27,29–32 two were cohortstudies,23,28 and one was a pre-test/post-test design.22 DBscores ranged from 10–26 with a median score of 22.

Screening Completion Outcomes. Eleven of the patient-level intervention articles measured completion of CRC

screening as a primary outcome. Six of the studies assessedCRC screening through fecal occult blood test (FOBT)exclusively.20,21,25,27,28,32 The five remaining studies assessedcompletion of any CRC screening test modality.19,26,29–31

Three RCT studies19,21,24 assessing educational mediainterventions did not achieve significant increases in theirCRC screening outcomes. Conversely, all five27,29–32

articles assessing educational interventions administeredthrough direct contact by trained professionals achievedsignificant improvements in CRC screening completion,with an absolute improvement ranging from 11 % to 41.9 %(median improvement of 15 %).Two articles examined interventions related to FOBT

distribution. Goldberg et al.25 found that in a sample ofpredominately African American patients, mailing FOBTkits along with a standard clinic appointment reminder lettertwo weeks prior to the scheduled appointment, resulted in16-fold (95 % CI 3.5, 71.4) greater odds of FOBT return atthe index appointment and 13-fold (95 % CI 3.6, 45.5)greater odds of FOBT return by one year compared to usualcare. Potter et al. found that in a sample of predominatelyAsian and Hispanic/Latino patients, providing FOBT kitsand education during annual influenza vaccination appoint-ments increased FOBT completion rates by 29.8 %(p<0.001) compared to a 4.4 % (p=0.07) increase in theusual care group.26

Two of the three articles evaluating multilingual interven-tions reported increases in CRC screening outcomes. In thestudy by Jacobs et al., providing professional interpreterservices to selected outpatient clinics in a Spanish andPortuguese speaking population did not significantly increasethe rates of FOBT completion over a two year interval, p=0.28.28 Conversely, Tu et al. found that the odds of FOBTcompletion were 5.9 (95 % CI 3.25, 10.75) fold greater inChinese Americans who received an educational interventionprovided by a trilingual health educator.27 While, Walsh et al.reported that addition of a bilingual brochure with counselingby community health advisors increased the odds of self-reported FOBT screening by 3.02 (95 % CI 1.77, 5.14)compared to usual care in a predominately Hispanic/Latinoand Asian patient sample.

Patient Navigator Interventions (Table 1) n=7(21.2 %)Intervention. All of the navigator models included, at theminimum: repeat phone calls to patients to aid withscheduling, bowel preparation instructions, and appointmentreminders. Four of the studies included more expansiveservices such as assistance with transportation, translationservices, and referral to other social services if needed,33–36

and two included face-to-face meetings with participants,including accompanying to endoscopy visits if needed.33,36

One trial provided assistance to facilitate patient-physiciancommunication34 through the use of patient activation cards.

Figure 3. Breakdown of studies by intervention type (# of totalstudies, n=33).


Quality. Five of the seven studies were randomizedcontrolled trials (RCT),34–38 one was a pre-test/post-testdesign39 and one was an observational cohort study.33 TheDB scores ranged from 16-27 with a median of 22. Five hadDB scores in the very good range and the remaining twohad scores in the good range.

Screening CompletionOutcomes. Excluding the observationalcohort study, four studies achieved significant screeningcompletion results with the intervention,34,36,38,39 and twodid not.35,37 In those studies with a comparator arm,34,36,38

absolute improvement in endoscopy screening completionamong the navigated group ranged from 7 % to 40 % with amedian improvement of 16 %.One study provided pre-planned subgroup analyses.33 In

the cohort study by Chen, et al., Hispanic patients weremore likely to complete screening compared to AfricanAmerican patients (HR 1.67;95 %CI:1.1–2.5).

Process Outcomes. Four studies specifically reported patientwillingness to participate in a navigator intervention and inthese studies, 44 % to 74 % agreed to navigation serviceswith a median of 72 % agreeing to participate.33,34,36,38

Patient navigation also reduced the rates of brokenappointments anywhere from 12 % to 62 %.33,37,39 In termsof types of services provided by navigators, in the study byPercac-Lima and colleagues, logistical barriers wereidentified for 60 % of patients (scheduling, bowelpreparation, transportation, etc) and an intervention wasperformed for 65 % of these barriers.36

Other Outcomes. In the study by Chen et al., 66 % of patientsreported they definitely or probably would not havecompleted their colonoscopy without the navigator.33 In therandomized trial by Christie and colleagues, 63 % of non-navigated patients refused colonoscopy compared to 23 % innavigated group and 77 % of navigated patients reported theywould refer family or friends for colonoscopy.

Provider/ System Level Interventions (Table 1),n=13 (39.4 %)Intervention. The interventions tested in these studies werepredominantly multi-modal, however, all but two includedan educational component.40,41 Seven of the studiesincluded an educational component that focused ondidactic sessions stressing standard national guidelines forCRC screening and the importance of screening.20,42–47 Thesessions varied widely in style, number and length. Twostudies focused on training providers in communicationskills targeting low-income/low-literacy patients.46,48 Threestudies utilized individual and/or group feedback sessions.48–50

Four studies used a provider reminder intervention.43,47,49,50

Two studies evaluated interventions that aimed to improveclinic flow.47,49

Quality. Of these 13 studies, six utilized a pre-test/post-testdesign,20,42,43,45,46,50,51 five were randomized controlledtrials,47,48 and two were cohort studies.40,41 The DBscores ranged from 5–25 with a median of 19. Ten of thestudies had DB scores within the good or very goodrange,40,41,43–50 two were fair,20,42 and one was poor.51

Screening Completion Outcomes Measures. The primaryendpoint for 11 of the 13 included studies was completion ofCRC screening. Six of the studies with DB scores in the “verygood” or “good” range achieved a significant increase inscreening completion results with the intervention43,44,46,48–50

and two did not.40,47 In those studies with a comparator arm(n=4), absolute improvement in CRC screening completionamong the intervention group ranged from 4.2 % to 16 %(median 8.9 %).44,48,49 In those studies with a pre-test/post-testdesign (n=6), the absolute improvement in CRC screeningcompletion in the post-intervention setting ranged from12.3 % to 55.8 % (median 17.7 %).20,42,43,46,50,51 In therandomized study by Ferreira and colleagues48 whichmeasured the effect of didactic educational sessions (aimedat communicating with patients with low literacy) on CRCscreening completion, the effect was particularly pronouncedin patients with health literacy skills less than the ninth gradelevel (55.7 % FOBT completion in the intervention arm vs.30 % of the controls, p<0.01). Similarly in the pre-test/post-test study by Khankari et al.,46 which focused oncommunication strategies for physicians of patients withlower health literacy as well as physician feedback andreminder systems, the CRC screening rate increased from11.5 % to 27.9 % (p<0.001).

Process Outcomes Measures. Two studies included processoutcomes: physician recommendation of CRC screening.46,48

Ferreira reports that the recommendation rate was 76 % in theintervention arm compared to 69.4 % in the control arm (p=0.02)48 and Khankari reports that physician recommendationincreased from 31.6 % in the pre-intervention setting to92.9 % in the post-intervention setting (p<0.001).46

Knowledge Outcomes Measures. The study by Sheinfeld–Gorin45 measured the effect of repeated one on onephysician education didactic sessions. Following theeducational sessions, the physicians in the intervention armcompleted a questionnaire and were able to correctly identifymore barriers to CRC screening (5.35 vs. 4.73, p<0.05) andan increased knowledge of cancer screening guidelines (2.26vs. 5.9, p<0.0001) compared to the pre-test setting.

DISCUSSION

Our systematic review resulted in the identification of 33articles that reported on interventions to improve CRCscreening in minority populations. We were unable to identify


any articles that tested interventions to reduce disparities inpost-screening follow-up, CRC treatment, survivorship, orend-of-life care. Therefore, a significant portion of the cancercare continuum remains neglected in the published literatureon how to improve colorectal cancer care for racial and ethnicminorities. The absence of studies aimed at increasinginitiation and adherence to treatment or follow up aftertreatment is unfortunate given that prior work has shown thatthere are clear racial and ethnic differences in stage-specificcolorectal cancer survival and in treatment and follow up aftertreatment.3,4,8,9 Moreover, there is evidence from both clinicaltrials and equal access systems such as the Department ofDefense that when treatment and follow up are equal, racialand ethnic disparities in survival disappear.52,53

The dominant CRC screening promotion interventions testedto date are patient education and navigation. The heterogene-ity across the targeted population, intervention, and measuredoutcome makes the identification of essential interventioncharacteristics difficult. However, a common theme related tothe intensity of patient contact did emerge. Patient educationinterventions that did not successfully increase screening ratesincluded an 8-minute video and pamphlet, computer-assistedinstruction, and a video instrument that due to “poor videoquality” and “technical difficulties” was rendered ineffectualin its objective. Comparatively, in a study that used telephoneoutreach and education, CRC screening increased by morethan four-fold.30 In patient education studies without directpatient contact, the use of culturally tailored printed materialsappeared superior to standard materials.31 For patient naviga-tion services, even the most basic model appeared to besuccessful in improving completion of colorectal cancerscreening rates on the order of 15 %.In short, the data suggests that patient education involving

phone or in-person contact combined with navigation throughat least the basic steps of the colon cancer screening process(appointment set up, bowel preparation, appointment remind-er) can lead to modest improvements in colorectal cancerscreening rates among the minority populations tested. Themore difficult question is how to implement these intensiveinterventions on a system-wide scale. In two studies whichreported the time resources involved, approximately 3–5phone calls were required for each patient and initial phonecalls lasted roughly 20 minutes with subsequent calls lastingabout 15 minutes; thus, roughly 1-1.5 hours of staff time werespent per patient.30,34 In another study involving 352 patients,two case managers made 14,978 calls over 3 years of the trialand responded to 780 requests for services.35 Hiring thepersonnel to do this in every clinical setting will likely be cost-prohibitive and some type of centralization of services will beneeded to achieve economies of scale. In addition, it isimperative that this type of service be reimbursed if it is evergoing to take hold. We believe the next generation of studiesshould focus on implementation logistics of such an approachin a system-wide setting.

The results of studies targeting providers or clinic systemssuggest that provider-directed educational interventions areeffective in increasing CRC screening rates on the order of10-15 percentage points. The strongest evidence from thesestudies involved the training of physicians to communicatewith patients of low health literacy.46,48 System processimprovements such as physician reminder systems and checklists were also successful; however, an important caveat isthat most of these studies were performed in a singleinstitution or clinic. The use of these systems in a largecommunity health center network was less successful.47 Thenext generation of studies need to focus on both theimplementation logistics of this type of approach in largehealth care systems rather than in the controlled setting ofsmall clinics and must include long-term follow to determinethe durability and sustainability of this type of approach.There are several limitations inherent in this type of

systematic review of the literature. Certainly publication biasof positive results remains foremost. Because our review andsearch terms were limited to interventions targeting under-served racial and ethnic minority patients, we found thatmany articles, (subsequently discovered during referencereviews), included these populations but were not soclassified in the MESH headings or key word searches. Wehave taken all efforts to ensure that all relevant articles areincluded in this review, but cannot exclude the possibility ofmissing articles. Since many of the studies focused only onminority patients rather than on comparisons with whitepatients, we cannot conclude that these interventions wouldtruly reduce the growing disparity gap in colon cancer care.The minority populations in these studies were predominant-ly Hispanic and African American, thereby limiting general-izing findings across other minorities, such as Asian andPacific Islander populations. Finally, the specified criteria forthis review excluded purely public health campaigns such astargeted advertising to at-risk populations and community-based interventions, such as education provided in churchesor at health fairs, if there was no documented link to aspecific health care clinic or system (see Appendix 3 for alisting of these studies-available online).The field of cancer health disparities has matured over the

last decade, and we can now point to well designed andimplemented studies that are not satisfied with simplypointing out disparities, but rather have focused on ways toeliminate them. The studies included in this systematicreview provide a good foundation of evidence that tailoredpatient education ideally involving personal contact com-bined with patient navigation services to overcome logisticalbarriers to screening, and physician training in moreeffectively communicating with patients of low healthliteracy, can modestly improve adherence to CRC screening.The onus is now on researchers to continue to evaluate andrefine these interventions and begin to expand them to theentire colon cancer care continuum.


Acknowledgments: We thank Toni Cipriano for her careful reviewof this manuscript.

Funding Source: Support for this publication was provided by agrant from the Robert Wood Johnson Foundation’s Finding Answers:Disparities Research for Change Program.

Prior Presentations: None.

Conflict of Interest: Keith Naylor and James Ward declare thatthey do not have a conflict of interest.

Blase Polite provides consulting to Quintiles Consulting Groupand, Roche-Genentech

Corresponding Author: Blase N. Polite, MD, MPP; The University ofChicago Medical Center, 5841 South Maryland Avenue, MC 2115,Chicago, IL 60637-1470, USA (e-mail: [email protected]).

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