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ORIGINAL ARTICLE
Measuring symptoms in gastrointestinal cancer: a systematicreview of assessment instruments
Rachelle Pullmer & Wolfgang Linden & Katerina Rnic &
Andrea Vodermaier
Received: 8 September 2013 /Accepted: 9 April 2014 /Published online: 28 May 2014# Springer-Verlag Berlin Heidelberg 2014
AbstractPurpose It is critical for gastrointestinal cancer researchers andclinicians to have access to comprehensive, sensitive andsimple-to-use symptommeasures that allow them to understandand quantify the subjective patient experience. Developmentand validation of such scales requires training in psychometricsand occasionally uses technical jargon that can be difficult topenetrate. This review evaluates existing measures of gastroin-testinal cancer symptoms, provides tool descriptions, and usespredefined, objective quality criteria to rate psychometric qual-ity and facilitate tool choices for researchers and clinicians.Methods MEDLINE, EMBASE, CINAHL, and PsycINFOdatabases were systematically reviewed for scales assessinggastrointestinal cancer and gastrointestinal cancer site-specificsymptoms. Evaluation criteria were the following: breadth ofdomain coverage (content validity), high internal consistency(α≥ .80), sensitivity to change, and extent of validation.Results In n=36 validation studies, 26 gastrointestinal cancersymptom measures were identified. Of these, n=13 tools metcriteria for recommendation, and six in particular showed
strong psychometric properties. The Functional Assessment ofCancer Therapy-Colorectal (FACT-C), European Organizationfor Research and Treatment of Cancer (EORTC) gastric cancermodule (QLQ-STO22), FACT-Hepatobiliary (FACT-Hep), andEORTC oesophagus, oesophago-gastric junction and stomachmodule (QLQ OG-25) were identified as the most comprehen-sive and best validated scales for each of the major gastrointes-tinal cancer sites. The FACT-Colorectal Symptom Index (FCSI-9) and the National Comprehensive Cancer Network(NCCN) FACT-Hepatobiliary Symptom Index (FHSI-18) werespecifically validated in patients with advanced colorectal andliver cancer and also demonstrated superior psychometricproperties.Conclusions Several comprehensive, well-validated scalesexist to adequately assess gastrointestinal cancer site-specificsymptoms. Specifically, gastrointestinal cancer submodules ofthe FACT quality of life questionnaire represent adequate toolchoices in most instances and overall, were better validatedthan the respective EORTC tools. Further improvement ofexisting, highly rated measures is recommended.
Keywords Symptoms . Gastrointestinal neoplasms .
Measures . Psychometrics . Reliability . Validity
Introduction
While incidence of several gastrointestinal (GI) cancers con-tinue to rise, mortality rates are generally declining, leading toan increase in survivors who must cope with symptoms aris-ing from the disease and its treatment [1]. Given the debilitat-ing symptoms associated with GI cancer, assessment andtracking of sequelae are pertinent to patients and care pro-viders. Self-report is typically used to tap into patients’ sub-jective illness experience and symptoms. Patients’ quality oflife (QoL), as well as decisions regarding when to seek
Electronic supplementary material The online version of this article(doi:10.1007/s00520-014-2250-z) contains supplementary material,which is available to authorized users.
R. Pullmer (*) :W. Linden :A. VodermaierDepartment of Psychology, University of British Columbia, 2136West Mall, Vancouver, BC V6T 1Z4, Canadae-mail: rpullmer@sfu.ca
W. LindenBC Cancer Agency, Vancouver, BC, Canada
K. RnicDepartment of Psychology, University of Western Ontario, London,Ontario, Canada
A. VodermaierDepartment of Obstetrics and Gynecology—Campus Grosshadern,University of Munich, Munich, Germany
Support Care Cancer (2014) 22:2941–2955DOI 10.1007/s00520-014-2250-z
professional help, are primarily driven by presence of suchsymptoms [2, 3].
Generic symptom and QoL measures may be of someuse, but given the diversity of GI cancers and relatedsymptoms, generic measures are considered inferior tothe more sensitive measurement of disease-specificchanges in symptoms [3]. A tool that measures symptomsspecific to a particular cohort of patients can provideessential information regarding patients’ QoL and theefficacy of cancer therapy [3]. Hence, it is critical thatresearchers and clinicians have access to assessment toolsthat (1) measure the symptoms that are specific to each GItumour site and (2) possess sound psychometrics [3].
Over the past two decades, several GI cancer-specificsymptom measures have been developed and validated.Currently, an abundance of QoL and symptom measuresassessing a variety of patient-reported outcomes exist. Thiscan be overwhelming for researchers and clinicians who wishto select an adequate tool with sound psychometric properties,but who are not specifically trained in psychometrics. Alimited set of GI cancer site-specific symptom measures havepreviously been reviewed. Fan and colleagues [4], as well asParameswaran and colleages [5] describe four health-relatedQoL liver and oesophageal cancer measures respectively.However, Fan and colleagues [4] do not provide informationon the psychometric properties of the liver cancer measuresincluded in the review, and neither reviews use explicit criteriato recommend certain tools for clinical use in GI cancerpatients.
To guide researchers and clinicians in their choice of as-sessment tool, we reviewed all obtainable GI cancer site-specific symptom measures, describe their domain coverage(i.e. content validity), and report on their reliability and othertypes of validity. To achieve our goal of providing a relevant,comprehensive, and detailed review, we focus primarily on GIcancers with the highest incidence rates. Measures for thesefour cancers (colorectal, stomach, liver, and oesophageal) aredescribed separately and presented below from highest tolowest according to their incidence rates. Despite high inci-dence rates, pancreatic cancer measures were not comparedhere due to the fact that only two validated symptommeasuresexist.
Methods
Study selection
The data extraction process was performed according to theguidelines for systematic reviews of diagnostic tests in cancer[6]. MEDLINE (1946 to May 2012) and EMBASE (1980 toMay 2012) databases were searched using the OVID inter-face; CINAHL (1982 to May 2012), and PsycINFO (1972 to
May 2012) databases were searched using the EBSCO inter-face for studies conducted with GI cancer patients. A searchtemplate was created inMEDLINE usingMeSH and keywordheadings (see Appendix 1) and adapted for other databases.The Cochrane Library, as well as the Patient-ReportedOutcome and QoL Instruments Database (PROQOLID) weresearched for additional publications. After eliminating dupli-cate studies, the titles, abstracts and full-length articles ofidentified studies were reviewed independently by two au-thors (R.P. and K.R.; Fig. 1). Uncertainty about whether or notstudies met inclusion criteria was resolved by seeking inputfrom another author (W.L.). Additional validation studieswere identified via hand searches of the reference section ofalready identified papers.
Study inclusion and evaluation criteria
Only studies of instruments labeled ‘validation studies’, ad-ministered by an interview or standardized self-report, anddesigned or adapted specifically for GI cancer patients wereincluded. We considered measures in all languages, obtainedfull texts and consulted native speakers when necessary toensure correct classification and interpretation of relevantstudies. We excluded translations of relevant questionnairesinto other languages unless they had been systematically re-validated following translation, as merely translating a mea-sure does not lead to new information about the psychometricproperties of a particular instrument.
Given the considerable complexity and effort required toestablish a tools’ reliability and validity, it is critical thatreviews use a transparent consensus approach in the adoptionof criteria for making value judgements and recommenda-tions. Of particular use for our review was the COSMINconsensus on tool quality for patient-reported outcomes [7,8], which offers a list of tool properties that reviewers shouldextract. The COSMIN checklist is particularly useful for thedevelopment of new tools that use item response theory (IRT).It could therefore only be partially applied for our reviewbecause none of the tools we identified are based on IRT andthe full COSMIN checklist asks for details that are available todevelopers of a new test but are not typically contained inpublished manuscripts.
To maximize the utility of this review, we applied a set ofthree clearly defined criteria to make transparent and replica-ble judgments about the perceived quality of a given scale.Using the COSMIN approach [7, 8], as well as researchconducted by Streiner and Norman as a guide [8], the threecriteria were defined as follows: (1) content validity,operationally defined as relative comprehensiveness ofsymptom coverage (i.e. a full-scale comprehensivenessscore of 4 or above; the detailed rating process isdescribed below), (2) internal consistency (the key index ofreliability, scored as poor if < 0.70; adequate if 0.70–0.79,
2942 Support Care Cancer (2014) 22:2941–2955
and excellent if ≥ 0.80) [9] and (3) extent of validation (ratedon a 1–3 scale, depending on whether one or more samples hadbeen tested and/or whether or not different validation strategieswere used). Two authors (R.P. and K.R.) independently ratedeach scale based on these criteria. Any discrepancies wereresolved by re-consulting the relevant article.
Details for each measure are offered in Tables 1, 2 and 3 [2,10–45], which are organized by GI cancer sub-type. It isimportant to note that these tables list any validation effortsand describe subsequent claimsmade by the authors regardingthe resulting validity of a particular measure. However, due to
the variability in quality of validation work performed, thesuccess of each study in adequately validating a measure isassessed in this review using the aforementioned definedcriteria, which are outlined in Table 4.
Comprehensiveness of symptom coverage
To adequately assess comprehensiveness of symptom cover-age, four studies were identified that collected relevant datafor content validity [2, 10, 16, 28] and that pre-existedresulting publications of the measures themselves. In all of
Fig. 1 Literature review flow chart
Support Care Cancer (2014) 22:2941–2955 2943
Tab
le1
Colorectalcancersymptom
measures
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
Adelstein
Symptom
Scale[18]
23-stom
achpain/discomfort;p
ainin
andaround
anus;changein
bowel
habits;b
owelurgency;
incomplete
bowelevacuatio
n;mucus
inbowel
motions;b
lood
from
anus;fatigue;
weightloss;lumpin
stom
achor
anus;low
bloodcount
N=263patientslik
elyto
have
acolonoscopy
Not
reported
Not
reported
Not
reported
Bow
elFu
nctio
nQuestionnaire
[19]
5-bowelincontinence;b
owel
urgency;
bowelfrequency
N=961patientsrecently
undergone
lowanterior
resectionforrectal
cancer
Not
reported
Not
reported*
Incompletelyreported
EORTCColorectalQ
ualityof
Life
Questionnaire
(QLQ-CR29)[20]
29-micturitio
nproblems;abdominal
andpelvicpain;d
efecation
problems;fecalincontinence;
anxiety;
body
image;stom
a-related
problems;sexualitems;singleitems
N=120colorectalcancer
patients
Not
reported
Not
reported
Not
reported
[21]
N=351colorectalcancer
patients
Range
ofαfrom
0.69
to0.84
forrespectiv
esubscales
ICC=0.68
(7–14days)
Construct
MultitraitScalin
gAnalysis
Developed
from
previously
valid
ated
scale
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
Functio
nalA
ssessm
ento
fCancer
Therapy—ColorectalC
ancer
Subscale(FACT-C)[22]
9-stom
achpain;w
eightloss;bowel
control;digestion;
diarrhea;appetite;
physicalappearance;p
resenceof
ostomy
N=60
colorectalcancer
patients
with
advanced
diseaseN=156
EnglishandSp
anishspeaking
colorectalcancer
patientsfrom
theBilingualIntercultu
ral
OncologyQualityof
Life
project
Range
ofαfrom
0.85
to0.91
forrespectiv
esubscales
Not
reported
Construct
Correlatio
nwith
relevant
constructsof
theFL
IC,B
POMSandPO
MS-SF
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
MSKCCBow
elFu
nctio
nInstrument[23]
18-bowelfunctio
nafter
sphincter-preserving
surgery
N=127patientsundergoing
sphincter-preserving
surgery
Range
ofαfrom
0.75
to0.79
forrespectiv
esubscales
r=0.84
(7–14days)
Construct
Factoranalysis
Correlatio
nwith
relevant
constructsof
the
EORTCQLQ-C30,C
RC38
andFIQ
LCriterion
Discrim
inates
know
ngroups
ModifiedFecalIncontinence
Qualityof
LifeScale[24]
14-lifestyle;coping/behaviour;
depression/self-perceptio
n;em
barassment
N=152patientswho
hadundergone
intersphinctericresectionfor
very
lowrectalcancer
with
transanalcoloanalanastom
osis
α=0.95
Not
reported
Concurrent
Correlatio
nwith
MOSSF
36,H
ADS,and
WCG
NCCNFA
CTColorectal
CancerSym
ptom
Index
(FCSI-9)[10]
9-energy;p
ain;
weightloss;nausea;
diarrhea;swellin
gor
cram
psin
stom
ach;
appetite;ability
toenjoy
life;overallQ
oL
Nopatient
sample
Not
reported
Not
reported
Not
reported
2944 Support Care Cancer (2014) 22:2941–2955
Tab
le1
(contin
ued)
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
[25]
N=391metastatic
colorectal
cancer
patients
Range
ofαfrom
0.75
to0.84
forrespectiv
esubscales
ICC=0.76
(4weeks)
Construct
Correlatio
nwith
relevant
constructsof
theEQ-5D
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
NCCNFA
CTColorectalC
ancer
Symptom
Index(N
CCN
FACTFC
SI-19)
[2]
19-Energy;
pain;w
eightloss;nausea;
diarrhea;constipation;
swellin
gor
cram
psin
stom
ach;
numbness/
tingling;
appetite;troublemeetin
gneedsof
family;sleep;w
orry;
hairloss–bother;bowelcontrol;
ability
toenjoylife;overallQ
oL
N=50
colorectalcancer
patients
Not
reported
Not
reported
Not
reported
Patient
Generated
Index(PGI)[26]
5-self-generated
items:assess
quality
oflifeandextent
towhich
theexpectations
ofpatientssufferingfrom
rectal
cancer
arematched
byreality
N=33
rectalcancer
patients
Not
reported
Not
reported
Construct
Correlatio
nwith
relevant
constructsof
theSF
-36,QLQ-C30
andQLQ-CR38
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
Qualityof
LifeInstrumentsfor
CancerPatients:Colorectal
Cancer(Q
LICP-CR)[27]
46-basicphysiologicalfunction;
sexualfunctio
n;independence
functio
n;em
otion;
recognition;
socialsupportand
safety;effect
oflifeandeconom
ics
N=11
colorectalcancer
patient
Range
ofαfrom
0.31
to0.89
forrespectivesubscales
r=0.83
(not
specified)
Concurrent
Correlatio
nwith
Chinese
versionof
FACT-C,FACT-G
andGLICP-GM
aIndexreported
isthewrong
estim
atefortest–retestreliability
Support Care Cancer (2014) 22:2941–2955 2945
Tab
le2
Oesophagealandgastriccancer
measures
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
Dysfunctio
nafterUpper
Gastrointestin
alSu
rgery
Scale(D
AUGS20)
[12-14]
20-gastroesophagealreflux;
deglutition
dysfunction;
limited
activ
itydueto
decreasedfood;
diarrhea
symptom
s;dumping
syndromesymptom
s;transfer
dysfunction;
hypoglycem
icsymptom
s
N=662postoperative
gastriccancer
patients
N=221post-operativ
eesophagealcancer
patients
α=0.90
Not
reported
Construct
Factor
analysis
Criterion
Discrim
inates
know
ngroups
EORTCGastricCancer
Module(Q
LQ-STO22)[28]
22-dysphagia;eatingrestriction;
pain;reflux;
anxiety;
single
items
N=114gastriccancer
patients
Not
reported
Not
reported
Not
reported
[39]
N=219gastriccancer
patients
Range
ofαfrom
0.72
to0.80
forrespectiv
esubscales
ICC=0.60
to>0.70
(3–5
days)
Construct
MultitraitScalingAnalysis:
refinedmodule
Correlations
with
QLQ-C30
Criterion
Discrim
inates
know
ngroups;
responsiveness
tochange
EORTCOesophagealCancer
Module(Q
LQ-O
ES1
8)[16-17]
18-dysphagia;deglutition;
eatin
grelateditems;reflux;
pain;anxiety
N=491esophageal
cancer
patients
Not
reported
Not
reported
Construct
Multitraitscalinganalysis:
repeated
item
deletio
nDeveloped
from
EORTC
QLQ-O
ES2
4Correlationanalysiswith
core
questio
nnaire
(QLQ-C30)
Criterion
Discrim
inates
know
ngroups
EORTCOesophagus,
Oesophago-G
astric
Junctio
nandStom
ach
Module(Q
LQ-O
G25)[30]
25-dysphagia;eatingrestrictions;
reflux;o
dynophagia;p
ain;
anxiety
N=300esophageal,gastric,
andesophago-gastric
junctio
ncancer
patients
Range
ofαfrom
0.67
to0.87
forrespectiv
esubscales
Not
reported
Construct
Developed
from
EORTC
QLQ-O
ES1
8andEORTC
QLQ-STO22
Correlationanalysiswith
core
questio
nnaire
(QLQ-C30)
Criterion
Discrim
inates
know
ngroups
EsophagealQ
ualityof
Life
Questionnaire(EQOL)[31]
15-physicalfunctio
n;activ
ities
ofdaily
living;
emotional
functio
n;socialfunctio
n;symptom
s
N=65
oesophagus
and
oesophago-gastric
junctio
ncancer
patients
Not
reported
r=0.73
to0.89
(1week)
Construct
Based
onEORTCQLQ-C30
Concurrent
Correlateswith
MOSSF
-36
Criterion
Responsivenessto
clinical
change
2946 Support Care Cancer (2014) 22:2941–2955
Tab
le2
(contin
ued)
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
FACTEsophagealC
ancer
Subscale(FACT-E)[32]
17-eating;
appetite;sw
allowing;
pain;talking/com
municating;
mouth
dryness;breathing
difficulty;coughing;
weightloss
N=83
Oesophagealcancer
patients
α>0.80
Not
reported
Construct
Correlatio
nwith
relevant
EORTCQLQ-30subscales
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinical
change
FACTGastriccancer
subscale(FACT-Ga)
[33]
19-physical,functional,
emotionaland
social
well-being,andadditio
nal
concerns
(gastric-cancer
specific)
Not
reported
Not
reported
Not
reported
Not
reported
[34]
N=82
gastriccancer
patients
α=0.86
ICC=0.88
(2weeks)
Construct
Correlations
with
anxietyand
depression
measures
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinical
change
Gastrointestin
alQuality
ofLifeIndex(C-G
IQLI)[35]
17-physicalwell-being;
mental
well-being;
digestion;
defecatio
n
N=140
Postoperativegastric
cancer
patients
α=0.89
ICC=0.88
(2weeks)
Constructa
Factor
analysis
Correlations
with
WHOQOL-BREF-HK
Qualityof
LifeInstrument
forPatientswith
Stom
ach
Cancer(Q
LICP-ST
)[36]
39-disease-specificquality
oflife
N=86
stom
achcancer
patients
α=0.91
r=0.98
(2–3
days)
Construct
Factor
analysis
Item
-owncorrelation
Criterion
Responsivenessto
clinical
change
aAttempted
butp
oorvalid
ationwork
Support Care Cancer (2014) 22:2941–2955 2947
Tab
le3
Liver
cancer
symptom
measures
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
EORTCLiver
MetastasesColorectal
Module(Q
LQ-LMC21)[37]
21-eatin
g;pain;fatigue;relationships;
psychosocial;singleitems
N=102colorectalcancer
patients
with
hepatic
metastases
Not
reported
Not
reported
Not
reported
[38]
N=356colorectalcancer
patients
with
hepatic
metastases
Range
ofαfrom
0.69
to0.93
forrespectiv
esubscales
Not
reported
Construct
MultitraitScalingAnalysis
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
EORTCHepatocellularCarcinoma
Module(Q
LQ-H
CC18)[39]
18-fatig
ue;b
odyim
age;jaundice;
nutrition;p
ain;
fevers;sexualinterest;
abdominalsw
ellin
gandbody
image
N=158hepatocellu
larcancer
patients
Not
reported
Not
reported
Not
reported
[40]
N=272hepatocellu
larcancer
patients
Range
ofαfrom
0.34
to0.72
forrespectiv
esubscales
ICC=0.64
to0.87
(1week)
Construct
MultitraitScalingAnalysis
Correlatio
nwith
relevant
subscales
ofQLQ-C30
Criterion
a
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
FACT—Hepatobiliary(FACT-Hep)
[41]
18-abdominaldiscom
fort;w
eightloss;
bowelcontrol;digestion;
diarrhea;
appetite;physicalappearance;b
ack
pain;fatigue;constipation;
daily
activ
ities;jaundice–bother;fevers;
itching;changein
food
taste;
chills;drymouth
N=51
hepatobiliary
cancer
patients
α=0.85
ICC=0.82
(3–7
days)
Construct
Strong
negativ
ecorrelations
with
POMS,
correlationwith
relevant
subscaleof
ISEL,divergedwith
MCSD
SCriterion
Discrim
inates
know
ngroups
[42]
N=158hepatobiliary
cancer
patients
Range
ofαfrom
0.76
to0.97
forrespectiv
esubscales
Not
reported
Criterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
LiverDisease
Qualityof
Life
Questionnaire(LDQOL1.0)
[43]
75-symptom
sof
liver
disease;effects
ofliv
erdisease;concentration;
mem
ory;
quality
ofsocialinteraction;
health
distress;sleep;loneliness;
hopelessness;stig
ma;sexual
functio
ning/problem
s
N=200patientsaw
aitin
gliv
ertransplantation
Range
ofαfrom
0.63
to0.91
forrespectiv
esubscales
Not
reported
Construct
Relevantscalescorrelated
with
PCSandMCSof
SF-36
Criterion
Discrim
inates
know
ngroups
NCCNFA
CTHepatobiliarySy
mptom
Index(N
CCNFA
CTFH
SI-8)
[44]
8-Hepatobiliaryspecificsymptom
sand
issues
(pain;
fatig
ue;n
ausea;
weightloss;jaundice)
N=51
hepatobiliary
cancer
patients
α=0.79
r=0.77–0.86
(3–7
days)
Construct
Significant,negativecorrelations
with
POMS.
Significantpositivecorrelations
with
FACTG,and
FACT-Hep
Criterion
Discrim
inates
know
ngroups
[10]
Nopatient
sample
Not
reported
Not
reported
Not
reported
NCCNFA
CT
HepatobiliaryCancer
Sym
ptom
Index(N
CCNFA
CT
FHSI-18)
[2]
18-energy;p
ain;
weightloss;fatigue;
jaundice– bother;ill
feelings;n
ausea;
abdominaldiscom
fort;m
eetin
gfamilialneeds;appetite;sleepquality
;worry;sadness;treatmentside
effects–bother;abilityto
dousual
activ
ities;o
verallQoL
N=50
hepatobiliary
cancer
patients
Not
reported
Not
reported
Not
reported
2948 Support Care Cancer (2014) 22:2941–2955
these studies, systematic and comprehensive literature reviewswere conducted on symptom prevalence. Further, since rat-ings of symptom severity and prevalence often vary depend-ing on the source, both patients and health care professionalswere consulted [10].
The most important symptoms for each GI cancer subtypewere extracted from these studies, and placed into broadsymptom classes (Table 5). Given that it is important for ameasure to include an adequate amount of broad symptomclasses in addition to more specific items, these two criteriawere rated separately. When rating broad symptom classes, ascore of 3 was given to measures that included ≥ 80% ofclasses, a score of 2 was given to those that included > 50%(but less than 80%), and a score of 1 was given to those thatincluded ≤ 50%. The same criteria were applied when ratingspecific items (i.e. a score of 3 to measures that included ≥ 80%of items, a score of 2 to those that included > 50% and a scoreof 1 to those that included ≤ 50%). After rating eachmeasure onthese two criteria, the two scores were aggregated to create atotal comprehensiveness score ranging from limited (aggregatescore of 3 or less) to extensive (aggregate score of 6) (Table 4).To rate measures that assessed gastric and oesophageal can-cer symptoms simultaneously [15, 30], the relevant broadsymptom classes and specific items for both of these cancerswere amalgamated due to their high overlap.
Reliability
Reliability was defined as internal consistency, and is reported asCronbach’s alpha for the full scale and the subscales (wheneverpossible). Test–retest reliability is also reported to revealwhether a given scale is sensitive to change in longitudinalresearch and clinical trials. Additionally, two searches wereconducted on Health Canada and the US National Institutes ofHealth clinical trial databases to fully consider data on sensi-tivity to clinical change of relevant measures that may havebeen embedded in clinical trials.T
able3
(contin
ued)
Scale
Num
berof
items-domains
covered
Sample
Internalconsistency
Test–retestreliability
Validity
[11]
N=50
hepatobiliary
cancer
patients(stage
IIIandIV
)α=0.89
Not
reported
Concurrent
Correlatio
nwith
FACT-GandFA
CT-Hep
Criterion
Discrim
inates
know
ngroups
Qualityof
LifeforPatientswith
LiverCancer(Q
OL-LC)[45]
22-physicalfunction;
psychological
function;
socialfunction;
symptom
s/side
effects
N=105liv
ercancer
patients
Range
ofσfrom
0.68
to0.81
forrespectiv
esubscales
r=0.71–0.86
(1–2
days)
Construct
Item
swith
ineach
domainconverged
with
oneanother,anddiverged
with
itemsof
otherdomains
Correlatio
nwith
relevant
domains
oftheFL
ICCriterion
Discrim
inates
know
ngroups;
responsiveness
toclinicalchange
aAttempted
butpoorvalidationwork
Table 4 Objectively defined quality criteria
Criteria Labels Definition
Comprehensiveness Limited Total comprehensiveness scoreof 3 or below
Moderate Total comprehensiveness scoreof 4 or 5
Extensive Total comprehensiveness score of 6
Internal consistency Poor α<0.70
Acceptable α between 0.70 and 0.80
High α>0.80
Validity Limited One sample, one type of validity
Moderate One sample, multiple validities
Extensive Multiple samples, multiple validities
Support Care Cancer (2014) 22:2941–2955 2949
Validity
Given the purpose and environment in which symptom mea-sures are typically developed, the assumption was made thatall symptom measures included in this review would haveface validity and at least some content validity. Thus, inaddition to describing domain coverage, we focused on thedescription and evaluation of construct, concurrent, and crite-rion validity for each respective measure.
Results
Thirty-six articles reporting on 26 instruments met inclusioncriteria (Fig. 1). All identified instruments were self-report;none were based on interview. No disagreements on studyinclusion emerged among reviewers. Detailed descriptions ofinstruments and validation information are listed in alphabet-ical order in Tables 1, 2 and 3 [2, 10–45]. Based on criteriamade explicit in Table 4, we decided to recommend thosescales that (1) were rated as at least moderately comprehen-sive, (2) had a mean internal consistency score of ≥ 0.70 and(3) had been rated as at least moderately well validated. As isapparent in Tables 1, 2 and 3, 22 measures were designedspecifically for use in GI cancer patients, whereas 4 [24, 26,35, 43] were originally developed in non-GI cancer popula-tions, but subsequently validated for GI cancer.
It is important to note that all EORTC and FACT question-naires described below are designed to be administered along-side a more generic QoL questionnaire (EORTC QLQ-C30and FACT-G, respectively) [46, 47]. Therefore, the compre-hensiveness of EORTC and FACT questionnaires were ratedaccordingly.
The following scales met all criteria for scale recom-mendation: EORTC colorectal module (QLQ-CR29) [20,21], FACT-C [22], FCSI-9 [10, 25], FHSI-8 [2, 44],FHSI-18, [11, 12], FACT-Hep [41, 42], EORTC livermodule (QLQ-LMC21) [37, 38], QoL Instrument forPatients with Liver Cancer (QOL-LC) [45], EORTCQLQ-STO22 [28, 29], FACT-Gastric (FACT-Ga) [33,34], Dysfunction After Upper Gastrointestinal Surgery(DAUGS-20) [15], FACT-esophageal (FACT-E) [32] andthe EORTC QLQ-OG25 [30]. Among these recommendedscales, five stood out as having particularly strong psy-chometric properties, namely, the FACT-C, FCSI-9, FHSI-18, FACT-Hep and the EORTC QLQ-STO22. No furtherdata on sensitivity to change were found through ourliterature search of Health Canada and the US NationalInstitutes of Health clinical trial databases on GI cancerclinical trials.
Below, unique characteristics and applications for someof the scales are described to reveal idiosyncratic strengthsweaknesses that are not contained in a quantitative evalu-ation alone.
Colorectal cancer
Ten symptom measures validated in 13 studies have beencreated for use amongst colorectal cancer patients.
Measures relevant for all colorectal cancer patients
Five measures (Table 1) have been validated in colorectalcancer patients, regardless of disease stage or treatment. The
Table 5 Relevant broad symptom classes and specific symptoms
Colorectalcancer
Livercancer
Oesophagealcancer
Gastriccancer
Bowel-related items
Control of bowels X
Diarrhea X
Pain
Abdominal pain/discomfort X X X
Abdominal swelling/cramps X X X
Back pain X
Pain/discomfort when eating X X
Chest pain X
General pain X X
Eating-/taste-related items
Appetite X X
Blockage when eating X
Troublesome eating X X
Trouble/change in taste X X
Feeling full too quickly X X
Trouble with digestion
Belching X X
Reflux X
Heartburn X
Trouble with acid/bile X X
Fatigue
Lack of energy X X
Feeling fatigued X X X X
Physical appearance
Jaundice X
Deglutition
Being able to swallow saliva X
Choking when swallowing X
Dysphagia
Eating solid foods X X
Eating soft foods X X
Drinking liquids X X
Other symptoms
Itching X
Nausea X X
Weight loss X X X X
2950 Support Care Cancer (2014) 22:2941–2955
EORTC QLQ-CR29 [20, 21] and FACT-C [22] are two of themost widely used symptom measures because of their modu-lar approach.
Although more comprehensive than the revised scale, theoriginal version of the EORTC QLQ-CR29 was not includedin the present review because it is no longer in use [48, 49].The most recent version of the EORTC QLQ-CR29 is avail-able in 16 languages.
The FACT-C was designed for use in clinical trials andclinical practice evaluation and is available in 36 languages.
Adelstein’s symptom scale [18] is a self-administered ques-tionnaire developed to assess the presence, severity and typeof lower bowel symptoms that may be indicative of colorectalcancer. This scale is designed for use in both research andclinical settings.
While the Patient Generated Index (PGI), a generalQoL measure, was not developed specifically for colorec-tal cancer patients, it has been validated in pre-operativepatients with rectal cancer [26]. The PGI is unique in thatit assesses patient symptomatology and QoL in threestages. In the first stage, patients are asked to list up tofive areas of their lives that have been affected by cancer.In the second stage, patients are asked to rate how currenthealth reality meets their expectations. In the third stage,patients assign a total of 14 imaginary points to areas oftheir life they wish they could improve. Due to the self-generated nature of the questionnaire, an objective assess-ment of its comprehensiveness could not be completed.However, comprehensiveness based on the content areasincluded are comparable to those of the FCSI-19 [2].
The Quality of Life Instruments for Cancer Patients-Colorectal Cancer (QLICP-CR) [27] was designed toassess various aspects of QoL related to colorectal can-cer. We were unable to access the full copy of theoriginal Chinese questionnaire, which precluded ade-quate assessment of the scale’s comprehensiveness.However, the journal article was translated by a bilin-gual Chinese individual, who helped extract importantinformation regarding relevant psychometric propertiesof the tool.
Stage and treatment-specific measures
Five measures (Table 1) have been validated in eitherpatients with advanced disease stage or patients receivingsurgery or chemotherapy for colorectal cancer. Both theNCCN FACT FCSI-9 [10, 25] and the NCCN FACTFCSI-19 [2] were designed for advanced stage colorectalpatients receiving chemotherapy. The FCSI-9 is a short,very comprehensive and internally consistent scale. Themore recent version of the FCSI-9, the FCSI-19, is evenmore comprehensive, yet no information on the scale’sinternal consistency and extent of validation is currently
available. In contrast to one translation of the FCSI-19,the FCSI-9 exists in 28 languages.
Three measures have been developed in postoperative pa-tients who have undergone surgery for colorectal cancer(Table 1). Among these, the Memorial Sloan–KetteringCancer Center Bowel Function Instrument (MSKCC-BFI)[23] was designed for use in colorectal cancer patients whounderwent sphincter-preserving surgery. Due, in part, to itsspecific application, this measure is limited with respect tocomprehensiveness.
Similar to the MSKCC-BFI, the Modified FecalIncontinence Quality of Life Scale [24] was developed foruse in postoperative patients who underwent intersphinctericresection.
The Bowel Function Questionnaire [19] was developedto assess bowel dysfunction after surgery for rectal cancer.The scale has several weaknesses including lack of com-prehensiveness, no reported internal consistency and lim-ited validation no reported internal consistency and limit-ed validation efforts.
Gastric cancer
Five symptom measures (Table 2) have been created for useamongst gastric cancer patients.
Measures relevant for all gastric cancer types
Three measures (Table 2) have been created for use. As withcolorectal cancer measures, the EORTCQLQ-STO22 [28, 29]and the FACT-Ga [33, 34] are the most widely used measures.Both the FACT-Ga (available in 28 languages) and theEORTC QLQ-STO22 (available in 38 languages) are com-prehensive measures. While the FACT-Ga has a higher overallinternal consistency and includes questions about functionaland social/family well-being, the EORTC QLQ-STO22 con-tains more specific symptom-related items.
The Quality of Life Instrument-Stomach Cancer (QLICP-ST) [36] was developed to assess aspects of QoL related tostomach cancer. Given that the original Chinese questionnairewas not retrievable, we were unable to assess the scale’scomprehensiveness.
Treatment-specific measures
Two measures (Table 2) were developed for patients receivingparticular treatments for gastric cancer.
The Chinese Gastrointestinal Quality of Life Index (C-GIQLI) [35] is a culturally adapted version of theGastrointestinal Quality of Life Index. The original scalewas developed for use in patients with gastrointestinal prob-lems; however, Yeung and colleagues [35] validated the scalein postoperative gastric cancer patients. While the measure’s
Support Care Cancer (2014) 22:2941–2955 2951
internal consistency is adequate, its extent of validation andcomprehensiveness is limited.
The DAUGS-20 [15] was developed to assess postopera-tive QoL in gastric and oesophageal cancer patients who havepreviously undergone upper GI tract surgery. The older ver-sion of the DAUGS-20 [12–14] was not included here be-cause it is a precursor to the current version and no longer inuse. The DAUGS-20 is a comprehensive measure with highinternal consistency.
Liver cancer
Seven symptom measures (Table 3) have been created for useamongst liver cancer patients. Both the EORTC QLQ-HCC18[39, 40] and FACT-Hep [41, 42] are widely used measures.However, despite its use in research and clinical trials, theEORTC QLQ-HCC18 (available in 23 languages) is not com-prehensive, and no extant data is available on sensitivity tochange.
The FACT-Hep is available in 40 languages. It is morecomprehensive than the EORTC QLQ-HCC18, has ex-cellent internal consistency and has been extensivelyvalidated.
The EORTC QLQ-LMC21 [38] is the only scale specifi-cally developed for patients with liver metastases from colo-rectal cancer and is available in five languages.
Both the NCCN FACT FHSI-8 [2, 45] and FHSI-18[11, 12] evaluate response to chemotherapy for patientswith advanced disease. Despite the limited validationefforts for the FHSI-8, the scale is concise, comprehen-sive and internally consistent. The more recent versionof the FHSI-8 (the FHSI-18) has a higher internalconsistency and underwent careful development. Itemsendorsed at a greater frequency by both experts andpatients were retained to create a very comprehensivesymptom index. Although the FHSI-18 has not beentranslated, the FHSI-8 is available in 31 languages.
The QOL-LC [45] is a Chinese-specific measure that takescultural background into account.
The Liver Disease Quality of Life Questionnaire(LDQOL 1.0) [43] was originally developed for use inpatients with several types of liver disease. Recently, aSpanish version has been validated in patients awaitingliver transplantation. The LDQOL 1.0 has several limi-tations including length (mean completion time of36 min precludes use in many settings), modest validityand poor comprehensiveness.
Oesophageal cancer
Four symptom measures (Table 2) have been developed foruse amongst oesophageal cancer patients.
The EORTC oesophageal module (QLQ-OES18) [16,17] EORTC QLQ-OG25 [30] and FACT-E [32] areall widely used measures. The EORTC QLQ-OES18(available in 23 languages) is very comprehensive, butinternal consistency and validity are insufficient. TheEORTC QLQ-OG25 was developed for use amongst gas-tric, oesophageal and esophago-gastric junction patients,a n d c omb i n e s t h e EORTC QLQ-OES18 an dEORTC QLQ-STO22 [28 , 29 ] . A l t hough t h eEORTC QLQ-OG25 (available in 11 languages) is verysimilar to the EORTC QLQ-OES18, it covers more keycontent than other oesophageal cancer measures [5]. It isinternally consistent, and more extensively validated thanthe EORTC QLQ-OES18.
The FACT-E (available in 16 languages) assesses symp-toms of oesophageal cancer for use in clinical trials andclinical practice. While the FACT-E is slightly less compre-hensive than the EORTC QLQ-OES18, its internal consisten-cy is excellent.
The Esophageal Quality of Life Questionnaire (EQOL)[31] determines QoL associated with curative treatment mo-dalities in oesophageal cancer patients, and is meant to be usedin conjunction with the EORTC QLQ-C30 [46]. Despiteestablished validity of the scale, it is limited with respect tocomprehensiveness, and no data exists on internal consistency.
Other measures
Another six measures validated in six studies [3, 50–54] werenot extensively analyzed because the focus of this review is GIcancer subtypes with high incidence rates. Two of these mea-sures were designed as general GI cancer symptom measures(scale name not specified [3] and the MDAnderson SymptomInventory [51]).
One measure was developed to assess health-relatedQoL amongst patients with cholangiocarcinoma and gall-bladder cancer (EORTC QLQ-BIL21) [53]. Anothermeasure assesses health-related QoL in patients with GIneuroendocrine tumours (EORTC QLQ-GINET21) [52].A further two measures have been validated in pancreaticcancer patients (i.e., the EORTC QLQ-PAN26 and theGIQLI [50, 54]).
Promising tools and further recommendations
This systematic review identified 26 scales that met inclusioncriteria. Thirteen of these scales were considered to havesufficiently good psychometric properties to permit recom-mendation for use, and five stood out as having the strongestpsychometric properties. The respective modules of the FACTand EORTCQoL scales, (i.e., the FACT-C [22], EORTCQLQSTO-22 [28, 29], FACT-Hep [41, 42] and EORTC QLQ OG-
2952 Support Care Cancer (2014) 22:2941–2955
25 [30]), were rated as best for the major GI cancer sitesinvestigated. Furthermore, for symptom assessment with ad-vanced colorectal or liver cancer, the FCSI-9 [10, 25] andFHSI-18 [11, 12] are adequate tool options. All of the recom-mended tools were developed within the last 13 years andseveral represent revisions of earlier versions.
With respect to colorectal cancer measures, it is importantto note that both the PGI [26] and the QLICP-CR [27] wereonly validated in very small samples (n=33 and n=11, re-spectively). Thus, these measures may benefit from furthervalidation in larger samples. With respect to hepatologicalcancer measures, note that despite the modular approachadopted by the EORTC QoL group, the EORTC QLQ-HCC18 [39, 40] should be revised and re-validated. Whilethe C-GIQLI [35] is comprehensive, further validation isrecommended in other populations due to its culturally sensi-tive nature. Similarly, the DAUGS-20 [15], a gastric cancer-specific questionnaire with sound psychometrics, is in need offurther cross-cultural validation, as its use is currently limitedto Japanese patients. In terms of oesophageal cancer measures,our conclusions are not significantly different fromParameswaran and colleagues [5], but additional recommen-dations and more detailed analysis of psychometric propertiesare added to the literature here.
When it comes to clinical practice recommendations, thefocus of this review on symptom measures should not preventresearchers from adding generic measures of QoL, distress,pain, sleep problems, etc., to their study, depending on theresearch and/or clinical question. There is no singular goldstandard with which to rate multidimensional tools; in eachcase, choosing a tool requires checking whether it has beenvalidated for the intended sample and context.
Several weaknesses were apparent across multiple instrumentsincluded in this review. Repeatedly, we observed that new toolswere developed and applied to a clinical study with minimal, ifany, validation work. Some questionnaires contained subscaleswith low internal consistency but no effort was made to improveon these measures with additional test development work. Thiscriticism does not apply to the recommended measures.
Importantly, 10 out of 26measures (Tables 1, 2 and 3) werenot determined as sensitive to clinical change. Thus, an area ofscale improvement represents the analysis of sensitivity tochange with longitudinal data. This criticism applies to threerecommended measures (EORTCQLQOG-25 [30], FHSI-18[11, 12] and FCSI-19 [2]). However, it is likely due to therecency of tool development that no extant data on sensitivityto change is currently available for the FHSI-18 and FCSI-19.
Conclusion
In summary, a considerable number of GI cancer site-specificsymptom measures with good psychometric properties have
been identified, with submodules of the FACT being the besttool choice for most cancer types. Further improvement ofalready existing, promising measures is recommended.
Disclosures and acknowledgments No funding was received for thismanuscript. None of the authors are in any financial or personal conflictof interest regarding this work. We are very grateful for the feedback ofDr. Jessica McAlpine on an earlier draft of this manuscript.
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