Download Measuring symptoms in gastrointestinal cancer: a

Support Care Cancer (2014) 22:2941–2955
DOI 10.1007/s00520-014-2250-z
ORIGINAL ARTICLE
Measuring symptoms in gastrointestinal cancer: a systematic
review 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
Abstract
Purpose It is critical for gastrointestinal cancer researchers and
clinicians to have access to comprehensive, sensitive and
simple-to-use symptom measures that allow them to understand
and quantify the subjective patient experience. Development
and validation of such scales requires training in psychometrics
and occasionally uses technical jargon that can be difficult to
penetrate. This review evaluates existing measures of gastrointestinal cancer symptoms, provides tool descriptions, and uses
predefined, objective quality criteria to rate psychometric quality and facilitate tool choices for researchers and clinicians.
Methods MEDLINE, EMBASE, CINAHL, and PsycINFO
databases were systematically reviewed for scales assessing
gastrointestinal cancer and gastrointestinal cancer site-specific
symptoms. Evaluation criteria were the following: breadth of
domain coverage (content validity), high internal consistency
(α≥ .80), sensitivity to change, and extent of validation.
Results In n=36 validation studies, 26 gastrointestinal cancer
symptom measures were identified. Of these, n=13 tools met
criteria for recommendation, and six in particular showed
strong psychometric properties. The Functional Assessment of
Cancer Therapy-Colorectal (FACT-C), European Organization
for Research and Treatment of Cancer (EORTC) gastric cancer
module (QLQ-STO22), FACT-Hepatobiliary (FACT-Hep), and
EORTC oesophagus, oesophago-gastric junction and stomach
module (QLQ OG-25) were identified as the most comprehensive and best validated scales for each of the major gastrointestinal cancer sites. The FACT-Colorectal Symptom Index (FCSI9) and the National Comprehensive Cancer Network
(NCCN) FACT-Hepatobiliary Symptom Index (FHSI-18) were
specifically validated in patients with advanced colorectal and
liver cancer and also demonstrated superior psychometric
properties.
Conclusions Several comprehensive, well-validated scales
exist to adequately assess gastrointestinal cancer site-specific
symptoms. Specifically, gastrointestinal cancer submodules of
the FACT quality of life questionnaire represent adequate tool
choices in most instances and overall, were better validated
than the respective EORTC tools. Further improvement of
existing, highly rated measures is recommended.
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.
Keywords Symptoms . Gastrointestinal neoplasms .
Measures . Psychometrics . Reliability . Validity
R. Pullmer (*) : W. Linden : A. Vodermaier
Department of Psychology, University of British Columbia, 2136
West Mall, Vancouver, BC V6T 1Z4, Canada
e-mail: [email protected]
W. Linden
BC Cancer Agency, Vancouver, BC, Canada
K. Rnic
Department of Psychology, University of Western Ontario, London,
Ontario, Canada
A. Vodermaier
Department of Obstetrics and Gynecology—Campus Grosshadern,
University of Munich, Munich, Germany
Introduction
While incidence of several gastrointestinal (GI) cancers continue to rise, mortality rates are generally declining, leading to
an increase in survivors who must cope with symptoms arising from the disease and its treatment [1]. Given the debilitating symptoms associated with GI cancer, assessment and
tracking of sequelae are pertinent to patients and care providers. Self-report is typically used to tap into patients’ subjective illness experience and symptoms. Patients’ quality of
life (QoL), as well as decisions regarding when to seek
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professional help, are primarily driven by presence of such
symptoms [2, 3].
Generic symptom and QoL measures may be of some
use, but given the diversity of GI cancers and related
symptoms, generic measures are considered inferior to
the more sensitive measurement of disease-specific
changes in symptoms [3]. A tool that measures symptoms
specific to a particular cohort of patients can provide
essential information regarding patients’ QoL and the
efficacy of cancer therapy [3]. Hence, it is critical that
researchers and clinicians have access to assessment tools
that (1) measure the symptoms that are specific to each GI
tumour site and (2) possess sound psychometrics [3].
Over the past two decades, several GI cancer-specific
symptom measures have been developed and validated.
Currently, an abundance of QoL and symptom measures
assessing a variety of patient-reported outcomes exist. This
can be overwhelming for researchers and clinicians who wish
to select an adequate tool with sound psychometric properties,
but who are not specifically trained in psychometrics. A
limited set of GI cancer site-specific symptom measures have
previously been reviewed. Fan and colleagues [4], as well as
Parameswaran and colleages [5] describe four health-related
QoL liver and oesophageal cancer measures respectively.
However, Fan and colleagues [4] do not provide information
on the psychometric properties of the liver cancer measures
included in the review, and neither reviews use explicit criteria
to recommend certain tools for clinical use in GI cancer
patients.
To guide researchers and clinicians in their choice of assessment tool, we reviewed all obtainable GI cancer sitespecific symptom measures, describe their domain coverage
(i.e. content validity), and report on their reliability and other
types of validity. To achieve our goal of providing a relevant,
comprehensive, and detailed review, we focus primarily on GI
cancers with the highest incidence rates. Measures for these
four cancers (colorectal, stomach, liver, and oesophageal) are
described separately and presented below from highest to
lowest according to their incidence rates. Despite high incidence rates, pancreatic cancer measures were not compared
here due to the fact that only two validated symptom measures
exist.
Methods
Study selection
The data extraction process was performed according to the
guidelines for systematic reviews of diagnostic tests in cancer
[6]. MEDLINE (1946 to May 2012) and EMBASE (1980 to
May 2012) databases were searched using the OVID interface; CINAHL (1982 to May 2012), and PsycINFO (1972 to
Support Care Cancer (2014) 22:2941–2955
May 2012) databases were searched using the EBSCO interface for studies conducted with GI cancer patients. A search
template was created in MEDLINE using MeSH and keyword
headings (see Appendix 1) and adapted for other databases.
The Cochrane Library, as well as the Patient-Reported
Outcome and QoL Instruments Database (PROQOLID) were
searched for additional publications. After eliminating duplicate studies, the titles, abstracts and full-length articles of
identified studies were reviewed independently by two authors (R.P. and K.R.; Fig. 1). Uncertainty about whether or not
studies met inclusion criteria was resolved by seeking input
from another author (W.L.). Additional validation studies
were identified via hand searches of the reference section of
already identified papers.
Study inclusion and evaluation criteria
Only studies of instruments labeled ‘validation studies’, administered by an interview or standardized self-report, and
designed or adapted specifically for GI cancer patients were
included. We considered measures in all languages, obtained
full texts and consulted native speakers when necessary to
ensure correct classification and interpretation of relevant
studies. We excluded translations of relevant questionnaires
into other languages unless they had been systematically revalidated following translation, as merely translating a measure does not lead to new information about the psychometric
properties of a particular instrument.
Given the considerable complexity and effort required to
establish a tools’ reliability and validity, it is critical that
reviews use a transparent consensus approach in the adoption
of criteria for making value judgements and recommendations. Of particular use for our review was the COSMIN
consensus on tool quality for patient-reported outcomes [7,
8], which offers a list of tool properties that reviewers should
extract. The COSMIN checklist is particularly useful for the
development of new tools that use item response theory (IRT).
It could therefore only be partially applied for our review
because none of the tools we identified are based on IRT and
the full COSMIN checklist asks for details that are available to
developers of a new test but are not typically contained in
published manuscripts.
To maximize the utility of this review, we applied a set of
three clearly defined criteria to make transparent and replicable judgments about the perceived quality of a given scale.
Using the COSMIN approach [7, 8], as well as research
conducted by Streiner and Norman as a guide [8], the three
criteria were defined as follows: (1) content validity,
operationally defined as relative comprehensiveness of
symptom coverage (i.e. a full-scale comprehensiveness
score of 4 or above; the detailed rating process is
described below), (2) internal consistency (the key index of
reliability, scored as poor if < 0.70; adequate if 0.70–0.79,
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Fig. 1 Literature review flow chart
and excellent if ≥ 0.80) [9] and (3) extent of validation (rated
on a 1–3 scale, depending on whether one or more samples had
been tested and/or whether or not different validation strategies
were used). Two authors (R.P. and K.R.) independently rated
each scale based on these criteria. Any discrepancies were
resolved 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 is
important to note that these tables list any validation efforts
and describe subsequent claims made by the authors regarding
the resulting validity of a particular measure. However, due to
the variability in quality of validation work performed, the
success of each study in adequately validating a measure is
assessed in this review using the aforementioned defined
criteria, which are outlined in Table 4.
Comprehensiveness of symptom coverage
To adequately assess comprehensiveness of symptom coverage, four studies were identified that collected relevant data
for content validity [2, 10, 16, 28] and that pre-existed
resulting publications of the measures themselves. In all of
9 - stomach pain; weight loss; bowel
control; digestion; diarrhea; appetite;
physical appearance; presence of
ostomy
18 - bowel function after
sphincter-preserving surgery
14 - lifestyle; coping/behaviour;
depression/self-perception;
embarassment
9 - energy; pain; weight loss; nausea;
diarrhea; swelling or cramps in
stomach; appetite; ability to enjoy
life; overall QoL
Functional Assessment of Cancer
Therapy—Colorectal Cancer
Subscale (FACT-C) [22]
MSKCC Bowel Function
Instrument [23]
Modified Fecal Incontinence
Quality of Life Scale [24]
NCCN FACT Colorectal
Cancer Symptom Index
(FCSI-9) [10]
[21]
EORTC Colorectal Quality of Life
Questionnaire (QLQ-CR29) [20]
29 - micturition problems; abdominal
and pelvic pain; defecation
problems; fecal incontinence;
anxiety; body image; stoma-related
problems; sexual items; single items
23 - stomach pain/discomfort; pain in
and around anus; change in bowel
habits; bowel urgency; incomplete
bowel evacuation; mucus in bowel
motions; blood from anus; fatigue;
weight loss; lump in stomach or
anus; low blood count
5 - bowel incontinence; bowel
urgency; bowel frequency
Adelstein Symptom Scale [18]
Bowel Function Questionnaire [19]
Number of items - domains
covered
Scale
Table 1 Colorectal cancer symptom measures
N=152 patients who had undergone
intersphincteric resection for
very low rectal cancer with
transanal coloanal anastomosis
No patient sample
N=60 colorectal cancer patients
with advanced disease N=156
English and Spanish speaking
colorectal cancer patients from
the Bilingual Intercultural
Oncology Quality of Life
project
N=127 patients undergoing
sphincter-preserving surgery
N=351 colorectal cancer patients
ICC=0.68
(7–14 days)
Not reported
r=0.84
(7–14 days)
Not reported
Range of α from 0.69 to
0.84 for respective
subscales
Range of α from 0.85 to
0.91 for respective
subscales
Range of α from 0.75 to 0.79
for respective subscales
α=0.95
Not reported
Not reported
Not reported
Not reported
Not reported*
Not reported
Test–retest reliability
Not reported
Not reported
N=263 patients likely to have a
colonoscopy
N=961 patients recently undergone
low anterior resection for rectal
cancer
N=120 colorectal cancer patients
Internal consistency
Sample
Not reported
Concurrent
Correlation with MOS SF36, HADS, and
WCG
Construct
Factor analysis
Correlation with relevant constructs of the
EORTC QLQ-C30, CRC38 and FIQL
Criterion
Discriminates known groups
Construct
Correlation with relevant constructs of
the FLIC, BPOMS and POMS-SF
Criterion
Discriminates known groups;
responsiveness to clinical change
Construct
Multitrait Scaling Analysis
Developed from previously validated scale
Criterion
Discriminates known groups;
responsiveness to clinical change
Not reported
Incompletely reported
Not reported
Validity
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a
46 - basic physiological function;
sexual function; independence
function; emotion; recognition;
social support and safety; effect
of life and economics
19 - Energy; pain; weight loss; nausea;
diarrhea; constipation; swelling
or cramps in stomach; numbness/
tingling; appetite; trouble meeting
needs of family; sleep; worry;
hair loss–bother; bowel control;
ability to enjoy life; overall QoL
5 - self-generated items: assess
quality of life and extent to
which the expectations of
patients suffering from rectal
cancer are matched by reality
Number of items - domains
covered
Index reported is the wrong estimate for test–retest reliability
Quality of Life Instruments for
Cancer Patients: Colorectal
Cancer (QLICP-CR) [27]
Patient Generated Index (PGI) [26]
NCCN FACT Colorectal Cancer
Symptom Index (NCCN
FACT FCSI-19) [2]
[25]
Scale
Table 1 (continued)
Not reported
N=50 colorectal cancer
patients
N=11 colorectal cancer
patient
N=33 rectal cancer
patients
ICC=0.76
(4 weeks)
Range of α from 0.75
to 0.84 for respective
subscales
N=391 metastatic colorectal
cancer patients
Not reported
r=0.83
(not specified)
Not reported
Range of α from 0.31 to 0.89
for respective subscales
Not reported
Test–retest reliability
Internal consistency
Sample
Concurrent
Correlation with Chinese
version of FACT-C, FACT-G
and GLICP-GM
Construct
Correlation with relevant
constructs of the SF-36, QLQ-C30
and QLQ-CR38
Criterion
Discriminates known groups;
responsiveness to clinical change
Not reported
Construct
Correlation with relevant
constructs of the EQ-5D
Criterion
Discriminates known groups;
responsiveness to clinical change
Validity
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Not reported
Not reported
ICC=0.60 to >0.70
(3–5 days)
α=0.90
Not reported
N=662 postoperative
gastric cancer patients
N=221 post-operative
esophageal cancer
patients
N=114 gastric cancer
patients
20 - gastroesophageal reflux;
deglutition dysfunction; limited
activity due to decreased food;
diarrhea symptoms; dumping
syndrome symptoms; transfer
dysfunction; hypoglycemic
symptoms
22 - dysphagia; eating restriction;
pain; reflux; anxiety; single
items
Dysfunction after Upper
Gastrointestinal Surgery
Scale (DAUGS 20)
[12-14]
Not reported
Not reported
r=0.73 to 0.89
(1 week)
Range of α from 0.72
to 0.80 for respective
subscales
Not reported
Range of α from 0.67
to 0.87 for respective
subscales
Not reported
N=219 gastric cancer
patients
N=491 esophageal
cancer patients
N=300 esophageal, gastric,
and esophago-gastric
junction cancer patients
N=65 oesophagus and
oesophago-gastric
junction cancer patients
18 - dysphagia; deglutition;
eating related items; reflux;
pain; anxiety
25 - dysphagia; eating restrictions;
reflux; odynophagia; pain;
anxiety
15 - physical function; activities
of daily living; emotional
function; social function;
symptoms
[39]
EORTC Oesophageal Cancer
Module (QLQ-OES18) [16-17]
EORTC Oesophagus,
Oesophago-Gastric
Junction and Stomach
Module (QLQ-OG25) [30]
Esophageal Quality of Life
Questionnaire (EQOL) [31]
EORTC Gastric Cancer
Module (QLQ-STO22) [28]
Test–retest reliability
Internal consistency
Sample
Number of items - domains covered
Scale
Table 2 Oesophageal and gastric cancer measures
Construct
Based on EORTC QLQ-C30
Concurrent
Correlates with MOS SF-36
Criterion
Responsiveness to clinical
change
Construct
Developed from EORTC
QLQ-OES18 and EORTC
QLQ-STO22
Correlation analysis with core
questionnaire (QLQ-C30)
Criterion
Discriminates known groups
Construct
Multitrait scaling analysis:
repeated item deletion
Developed from EORTC
QLQ-OES24
Correlation analysis with core
questionnaire (QLQ-C30)
Criterion
Discriminates known groups
Construct
Multitrait Scaling Analysis:
refined module
Correlations with QLQ-C30
Criterion
Discriminates known groups;
responsiveness to change
Not reported
Construct
Factor analysis
Criterion
Discriminates known groups
Validity
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r=0.98 (2–3 days)
α=0.91
N=86 stomach cancer
patients
39 - disease-specific quality
of life
Quality of Life Instrument
for Patients with Stomach
Cancer (QLICP-ST) [36]
Attempted but poor validation work
ICC=0.88 (2 weeks)
α=0.89
N=140
Postoperative gastric
cancer patients
17 - physical well-being; mental
well-being; digestion;
defecation
Gastrointestinal Quality
of Life Index (C-GIQLI) [35]
a
ICC=0.88 (2 weeks)
Not reported
Not reported
Not reported
α=0.86
19 - physical, functional,
emotional and social
well-being, and additional
concerns (gastric-cancer
specific)
FACT Gastric cancer
subscale (FACT-Ga) [33]
Not reported
α>0.80
N=83
Oesophageal cancer patients
N=82 gastric cancer patients
17 - eating; appetite; swallowing;
pain; talking/communicating;
mouth dryness; breathing
difficulty; coughing;
weight loss
FACT Esophageal Cancer
Subscale (FACT-E) [32]
Test–retest reliability
Internal consistency
Sample
[34]
Number of items - domains covered
Scale
Table 2 (continued)
Construct
Factor analysis
Item-own correlation
Criterion
Responsiveness to clinical
change
Constructa
Factor analysis
Correlations with
WHOQOL-BREF-HK
Construct
Correlations with anxiety and
depression measures
Criterion
Discriminates known groups;
responsiveness to clinical
change
Not reported
Construct
Correlation with relevant
EORTC QLQ-30 subscales
Criterion
Discriminates known groups;
responsiveness to clinical
change
Validity
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NCCN FACT
Hepatobiliary Cancer
Symptom Index (NCCN FACT
FHSI-18) [2]
[10]
18 - energy; pain; weight loss; fatigue;
jaundice–bother; ill feelings; nausea;
abdominal discomfort; meeting
familial needs; appetite; sleep quality;
worry; sadness; treatment side
effects–bother; ability to do usual
activities; overall QoL
N=50 hepatobiliary cancer
patients
Not reported
Not reported
Not reported
r=0.77–0.86
(3–7 days)
α=0.79
N=51 hepatobiliary cancer
patients
NCCN FACT Hepatobiliary Symptom
Index (NCCN FACT FHSI-8) [44]
75 - symptoms of liver disease; effects
of liver disease; concentration;
memory; quality of social interaction;
health distress; sleep; loneliness;
hopelessness; stigma; sexual
functioning/problems
8 - Hepatobiliary specific symptoms and
issues (pain; fatigue; nausea;
weight loss; jaundice)
Not reported
Not reported
Range of α from 0.63
to 0.91 for respective
subscales
N=200 patients awaiting liver
transplantation
Liver Disease Quality of Life
Questionnaire (LDQOL 1.0) [43]
No patient sample
Not reported
Range of α from 0.76
to 0.97 for respective
subscales
N=158 hepatobiliary cancer
patients
[42]
ICC=0.82
(3–7 days)
α=0.85
N=51 hepatobiliary cancer
patients
18 - abdominal discomfort; weight loss;
bowel control; digestion; diarrhea;
appetite; physical appearance; back
pain; fatigue; constipation; daily
activities; jaundice–bother; fevers;
itching; change in food taste;
chills; dry mouth
FACT—Hepatobiliary (FACT-Hep)
[41]
Not reported
Not reported
Not reported
Range of α from 0.69
to 0.93 for respective
subscales
ICC=0.64 to 0.87
(1 week)
N=158 hepatocellular cancer
patients
Not reported
Not reported
Test–retest reliability
Range of α from 0.34
to 0.72 for respective
subscales
18 - fatigue; body image; jaundice;
nutrition; pain; fevers; sexual interest;
abdominal swelling and body image
EORTC Hepatocellular Carcinoma
Module (QLQ-HCC18) [39]
N=102 colorectal cancer patients
with hepatic metastases
N=356 colorectal cancer patients
with hepatic metastases
Internal consistency
N=272 hepatocellular cancer
patients
21 - eating; pain; fatigue; relationships;
psychosocial; single items
EORTC Liver Metastases Colorectal
Module (QLQ-LMC21) [37]
[38]
Sample
[40]
Number of items - domains covered
Scale
Table 3 Liver cancer symptom measures
Not reported
Not reported
Construct
Significant, negative correlations with
POMS. Significant positive correlations
with FACTG, and FACT-Hep
Criterion
Discriminates known groups
Construct
Relevant scales correlated
with PCS and MCS of SF-36
Criterion
Discriminates known groups
Criterion
Discriminates known groups;
responsiveness to clinical change
Construct
Strong negative correlations
with POMS, correlation with relevant
subscale of ISEL, diverged with
MCSDS
Criterion
Discriminates known groups
Construct
Multitrait Scaling Analysis
Correlation with relevant subscales
of QLQ-C30
Criteriona
Discriminates known groups;
responsiveness to clinical change
Not reported
Construct
Multitrait Scaling Analysis
Criterion
Discriminates known groups;
responsiveness to clinical change
Not reported
Validity
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Table 4 Objectively defined quality criteria
Construct
Items within each domain converged
with one another, and diverged with
items of other domains
Correlation with relevant domains of
the FLIC
Criterion
Discriminates known groups;
responsiveness to clinical change
Concurrent
Correlation with FACT-G and FACT-Hep
Criterion
Discriminates known groups
Criteria
Labels
Definition
Comprehensiveness
Limited
Total comprehensiveness score
of 3 or below
Moderate
Total comprehensiveness score
of 4 or 5
Internal consistency
r=0.71–0.86
(1–2 days)
Range of σ from 0.68 to 0.81
for respective subscales
N=105 liver cancer patients
Total comprehensiveness score of 6
Poor
α<0.70
Acceptable
α between 0.70 and 0.80
High
α>0.80
Limited
One sample, one type of validity
Moderate
One sample, multiple validities
Extensive
Multiple samples, multiple validities
Attempted but poor validation work
Reliability
a
Quality of Life for Patients with
Liver Cancer (QOL-LC) [45]
[11]
Extensive
these studies, systematic and comprehensive literature reviews
were conducted on symptom prevalence. Further, since ratings of symptom severity and prevalence often vary depending on the source, both patients and health care professionals
were consulted [10].
The most important symptoms for each GI cancer subtype
were extracted from these studies, and placed into broad
symptom classes (Table 5). Given that it is important for a
measure to include an adequate amount of broad symptom
classes in addition to more specific items, these two criteria
were rated separately. When rating broad symptom classes, a
score of 3 was given to measures that included ≥ 80% of
classes, a score of 2 was given to those that included > 50%
(but less than 80%), and a score of 1 was given to those that
included ≤ 50%. The same criteria were applied when rating
specific 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 score
of 1 to those that included ≤ 50%). After rating each measure on
these two criteria, the two scores were aggregated to create a
total comprehensiveness score ranging from limited (aggregate
score of 3 or less) to extensive (aggregate score of 6) (Table 4).
To rate measures that assessed gastric and oesophageal cancer symptoms simultaneously [15, 30], the relevant broad
symptom classes and specific items for both of these cancers
were amalgamated due to their high overlap.
22 - physical function; psychological
function; social function;
symptoms/side effects
α=0.89
N=50 hepatobiliary cancer
patients (stage III and IV)
Not reported
Internal consistency
Number of items - domains covered
Scale
Table 3 (continued)
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Validity
Sample
Test–retest reliability
Validity
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Reliability was defined as internal consistency, and is reported as
Cronbach’s alpha for the full scale and the subscales (whenever
possible). Test–retest reliability is also reported to reveal
whether a given scale is sensitive to change in longitudinal
research and clinical trials. Additionally, two searches were
conducted on Health Canada and the US National Institutes of
Health clinical trial databases to fully consider data on sensitivity to clinical change of relevant measures that may have
been embedded in clinical trials.
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Table 5 Relevant broad symptom classes and specific symptoms
Colorectal Liver Oesophageal Gastric
cancer
cancer cancer
cancer
Bowel-related items
Control of bowels
X
Diarrhea
X
Pain
Abdominal pain/discomfort
Abdominal swelling/cramps
X
X
Back pain
X
X
X
X
Pain/discomfort when eating
X
Chest pain
X
General pain
X
X
X
X
X
X
Eating-/taste-related items
Appetite
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
Reflux
X
X
Heartburn
X
Trouble with acid/bile
X
X
X
X
Fatigue
Lack of energy
X
X
Feeling fatigued
X
X
Physical appearance
Jaundice
X
Deglutition
Being able to swallow saliva
X
Choking when swallowing
X
Dysphagia
Eating solid foods
X
Eating soft foods
X
X
X
Drinking liquids
X
X
Other symptoms
Itching
X
Nausea
X
X
Weight loss
X
X
X
X
Results
Thirty-six articles reporting on 26 instruments met inclusion
criteria (Fig. 1). All identified instruments were self-report;
none were based on interview. No disagreements on study
inclusion emerged among reviewers. Detailed descriptions of
instruments and validation information are listed in alphabetical order in Tables 1, 2 and 3 [2, 10–45]. Based on criteria
made explicit in Table 4, we decided to recommend those
scales that (1) were rated as at least moderately comprehensive, (2) had a mean internal consistency score of ≥ 0.70 and
(3) had been rated as at least moderately well validated. As is
apparent in Tables 1, 2 and 3, 22 measures were designed
specifically for use in GI cancer patients, whereas 4 [24, 26,
35, 43] were originally developed in non-GI cancer populations, but subsequently validated for GI cancer.
It is important to note that all EORTC and FACT questionnaires described below are designed to be administered alongside a more generic QoL questionnaire (EORTC QLQ-C30
and FACT-G, respectively) [46, 47]. Therefore, the comprehensiveness of EORTC and FACT questionnaires were rated
accordingly.
The following scales met all criteria for scale recommendation: 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 liver
module (QLQ-LMC21) [37, 38], QoL Instrument for
Patients with Liver Cancer (QOL-LC) [45], EORTC
QLQ-STO22 [28, 29], FACT-Gastric (FACT-Ga) [33,
34], Dysfunction After Upper Gastrointestinal Surgery
(DAUGS-20) [15], FACT-esophageal (FACT-E) [32] and
the EORTC QLQ-OG25 [30]. Among these recommended
scales, five stood out as having particularly strong psychometric properties, namely, the FACT-C, FCSI-9, FHSI18, FACT-Hep and the EORTC QLQ-STO22. No further
data on sensitivity to change were found through our
literature search of Health Canada and the US National
Institutes of Health clinical trial databases on GI cancer
clinical trials.
Below, unique characteristics and applications for some
of the scales are described to reveal idiosyncratic strengths
weaknesses that are not contained in a quantitative evaluation alone.
Validity
Colorectal cancer
Given the purpose and environment in which symptom measures are typically developed, the assumption was made that
all symptom measures included in this review would have
face validity and at least some content validity. Thus, in
addition to describing domain coverage, we focused on the
description and evaluation of construct, concurrent, and criterion validity for each respective measure.
Ten symptom measures validated in 13 studies have been
created for use amongst colorectal cancer patients.
Measures relevant for all colorectal cancer patients
Five measures (Table 1) have been validated in colorectal
cancer patients, regardless of disease stage or treatment. The
Support Care Cancer (2014) 22:2941–2955
EORTC QLQ-CR29 [20, 21] and FACT-C [22] are two of the
most widely used symptom measures because of their modular approach.
Although more comprehensive than the revised scale, the
original version of the EORTC QLQ-CR29 was not included
in the present review because it is no longer in use [48, 49].
The most recent version of the EORTC QLQ-CR29 is available in 16 languages.
The FACT-C was designed for use in clinical trials and
clinical practice evaluation and is available in 36 languages.
Adelstein’s symptom scale [18] is a self-administered questionnaire developed to assess the presence, severity and type
of lower bowel symptoms that may be indicative of colorectal
cancer. This scale is designed for use in both research and
clinical settings.
While the Patient Generated Index (PGI), a general
QoL measure, was not developed specifically for colorectal cancer patients, it has been validated in pre-operative
patients with rectal cancer [26]. The PGI is unique in that
it assesses patient symptomatology and QoL in three
stages. In the first stage, patients are asked to list up to
five areas of their lives that have been affected by cancer.
In the second stage, patients are asked to rate how current
health reality meets their expectations. In the third stage,
patients assign a total of 14 imaginary points to areas of
their life they wish they could improve. Due to the selfgenerated nature of the questionnaire, an objective assessment of its comprehensiveness could not be completed.
However, comprehensiveness based on the content areas
included are comparable to those of the FCSI-19 [2].
The Quality of Life Instruments for Cancer PatientsColorectal Cancer (QLICP-CR) [27] was designed to
assess various aspects of QoL related to colorectal cancer. We were unable to access the full copy of the
original Chinese questionnaire, which precluded adequate assessment of the scale’s comprehensiveness.
However, the journal article was translated by a bilingual Chinese individual, who helped extract important
information regarding relevant psychometric properties
of the tool.
Stage and treatment-specific measures
Five measures (Table 1) have been validated in either
patients with advanced disease stage or patients receiving
surgery or chemotherapy for colorectal cancer. Both the
NCCN FACT FCSI-9 [10, 25] and the NCCN FACT
FCSI-19 [2] were designed for advanced stage colorectal
patients receiving chemotherapy. The FCSI-9 is a short,
very comprehensive and internally consistent scale. The
more recent version of the FCSI-9, the FCSI-19, is even
more comprehensive, yet no information on the scale’s
internal consistency and extent of validation is currently
2951
available. In contrast to one translation of the FCSI-19,
the FCSI-9 exists in 28 languages.
Three measures have been developed in postoperative patients who have undergone surgery for colorectal cancer
(Table 1). Among these, the Memorial Sloan–Kettering
Cancer Center Bowel Function Instrument (MSKCC-BFI)
[23] was designed for use in colorectal cancer patients who
underwent sphincter-preserving surgery. Due, in part, to its
specific application, this measure is limited with respect to
comprehensiveness.
Similar to the MSKCC-BFI, the Modified Fecal
Incontinence Quality of Life Scale [24] was developed for
use in postoperative patients who underwent intersphincteric
resection.
The Bowel Function Questionnaire [19] was developed
to assess bowel dysfunction after surgery for rectal cancer.
The scale has several weaknesses including lack of comprehensiveness, no reported internal consistency and limited validation no reported internal consistency and limited validation efforts.
Gastric cancer
Five symptom measures (Table 2) have been created for use
amongst gastric cancer patients.
Measures relevant for all gastric cancer types
Three measures (Table 2) have been created for use. As with
colorectal cancer measures, the EORTC QLQ-STO22 [28, 29]
and the FACT-Ga [33, 34] are the most widely used measures.
Both the FACT-Ga (available in 28 languages) and the
EORTC QLQ-STO22 (available in 38 languages) are comprehensive measures. While the FACT-Ga has a higher overall
internal consistency and includes questions about functional
and social/family well-being, the EORTC QLQ-STO22 contains more specific symptom-related items.
The Quality of Life Instrument-Stomach Cancer (QLICPST) [36] was developed to assess aspects of QoL related to
stomach cancer. Given that the original Chinese questionnaire
was not retrievable, we were unable to assess the scale’s
comprehensiveness.
Treatment-specific measures
Two measures (Table 2) were developed for patients receiving
particular treatments for gastric cancer.
The Chinese Gastrointestinal Quality of Life Index (CGIQLI) [35] is a culturally adapted version of the
Gastrointestinal Quality of Life Index. The original scale
was developed for use in patients with gastrointestinal problems; however, Yeung and colleagues [35] validated the scale
in postoperative gastric cancer patients. While the measure’s
2952
internal consistency is adequate, its extent of validation and
comprehensiveness is limited.
The DAUGS-20 [15] was developed to assess postoperative QoL in gastric and oesophageal cancer patients who have
previously undergone upper GI tract surgery. The older version of the DAUGS-20 [12–14] was not included here because it is a precursor to the current version and no longer in
use. The DAUGS-20 is a comprehensive measure with high
internal consistency.
Liver cancer
Seven symptom measures (Table 3) have been created for use
amongst 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, the
EORTC QLQ-HCC18 (available in 23 languages) is not comprehensive, and no extant data is available on sensitivity to
change.
The FACT-Hep is available in 40 languages. It is more
comprehensive than the EORTC QLQ-HCC18, has excellent internal consistency and has been extensively
validated.
The EORTC QLQ-LMC21 [38] is the only scale specifically developed for patients with liver metastases from colorectal 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 patients
with advanced disease. Despite the limited validation
efforts for the FHSI-8, the scale is concise, comprehensive and internally consistent. The more recent version
of the FHSI-8 (the FHSI-18) has a higher internal
consistency and underwent careful development. Items
endorsed at a greater frequency by both experts and
patients were retained to create a very comprehensive
symptom index. Although the FHSI-18 has not been
translated, the FHSI-8 is available in 31 languages.
The QOL-LC [45] is a Chinese-specific measure that takes
cultural background into account.
The Liver Disease Quality of Life Questionnaire
(LDQOL 1.0) [43] was originally developed for use in
patients with several types of liver disease. Recently, a
Spanish version has been validated in patients awaiting
liver transplantation. The LDQOL 1.0 has several limitations including length (mean completion time of
36 min precludes use in many settings), modest validity
and poor comprehensiveness.
Oesophageal cancer
Four symptom measures (Table 2) have been developed for
use amongst oesophageal cancer patients.
Support Care Cancer (2014) 22:2941–2955
The EORTC oesophageal module (QLQ-OES18) [16,
17] EORTC QLQ-OG25 [30] and FACT-E [32] are
all widely used measures. The EORTC QLQ-OES18
(available in 23 languages) is very comprehensive, but
internal consistency and validity are insufficient. The
EORTC QLQ-OG25 was developed for use amongst gastric, oesophageal and esophago-gastric junction patients,
a n d c o m b i n e s t h e E O RT C Q L Q - O E S 1 8 a n d
E O RT C Q L Q - S T O 2 2 [ 2 8 , 2 9 ] . A l t h o u g h t h e
EORTC QLQ-OG25 (available in 11 languages) is very
similar to the EORTC QLQ-OES18, it covers more key
content than other oesophageal cancer measures [5]. It is
internally consistent, and more extensively validated than
the EORTC QLQ-OES18.
The FACT-E (available in 16 languages) assesses symptoms of oesophageal cancer for use in clinical trials and
clinical practice. While the FACT-E is slightly less comprehensive than the EORTC QLQ-OES18, its internal consistency is excellent.
The Esophageal Quality of Life Questionnaire (EQOL)
[31] determines QoL associated with curative treatment modalities in oesophageal cancer patients, and is meant to be used
in conjunction with the EORTC QLQ-C30 [46]. Despite
established validity of the scale, it is limited with respect to
comprehensiveness, and no data exists on internal consistency.
Other measures
Another six measures validated in six studies [3, 50–54] were
not extensively analyzed because the focus of this review is GI
cancer subtypes with high incidence rates. Two of these measures were designed as general GI cancer symptom measures
(scale name not specified [3] and the MD Anderson Symptom
Inventory [51]).
One measure was developed to assess health-related
QoL amongst patients with cholangiocarcinoma and gallbladder cancer (EORTC QLQ-BIL21) [53]. Another
measure assesses health-related QoL in patients with GI
neuroendocrine tumours (EORTC QLQ-GINET21) [52].
A further two measures have been validated in pancreatic
cancer patients (i.e., the EORTC QLQ-PAN26 and the
GIQLI [50, 54]).
Promising tools and further recommendations
This systematic review identified 26 scales that met inclusion
criteria. Thirteen of these scales were considered to have
sufficiently good psychometric properties to permit recommendation for use, and five stood out as having the strongest
psychometric properties. The respective modules of the FACT
and EORTC QoL scales, (i.e., the FACT-C [22], EORTC QLQ
STO-22 [28, 29], FACT-Hep [41, 42] and EORTC QLQ OG-
Support Care Cancer (2014) 22:2941–2955
25 [30]), were rated as best for the major GI cancer sites
investigated. Furthermore, for symptom assessment with advanced colorectal or liver cancer, the FCSI-9 [10, 25] and
FHSI-18 [11, 12] are adequate tool options. All of the recommended tools were developed within the last 13 years and
several represent revisions of earlier versions.
With respect to colorectal cancer measures, it is important
to note that both the PGI [26] and the QLICP-CR [27] were
only validated in very small samples (n=33 and n=11, respectively). Thus, these measures may benefit from further
validation in larger samples. With respect to hepatological
cancer measures, note that despite the modular approach
adopted by the EORTC QoL group, the EORTC QLQHCC18 [39, 40] should be revised and re-validated. While
the C-GIQLI [35] is comprehensive, further validation is
recommended in other populations due to its culturally sensitive nature. Similarly, the DAUGS-20 [15], a gastric cancerspecific questionnaire with sound psychometrics, is in need of
further cross-cultural validation, as its use is currently limited
to Japanese patients. In terms of oesophageal cancer measures,
our conclusions are not significantly different from
Parameswaran and colleagues [5], but additional recommendations and more detailed analysis of psychometric properties
are added to the literature here.
When it comes to clinical practice recommendations, the
focus of this review on symptom measures should not prevent
researchers from adding generic measures of QoL, distress,
pain, sleep problems, etc., to their study, depending on the
research and/or clinical question. There is no singular gold
standard with which to rate multidimensional tools; in each
case, choosing a tool requires checking whether it has been
validated for the intended sample and context.
Several weaknesses were apparent across multiple instruments
included in this review. Repeatedly, we observed that new tools
were developed and applied to a clinical study with minimal, if
any, validation work. Some questionnaires contained subscales
with low internal consistency but no effort was made to improve
on these measures with additional test development work. This
criticism does not apply to the recommended measures.
Importantly, 10 out of 26 measures (Tables 1, 2 and 3) were
not determined as sensitive to clinical change. Thus, an area of
scale improvement represents the analysis of sensitivity to
change with longitudinal data. This criticism applies to three
recommended measures (EORTC QLQ OG-25 [30], FHSI-18
[11, 12] and FCSI-19 [2]). However, it is likely due to the
recency of tool development that no extant data on sensitivity
to change is currently available for the FHSI-18 and FCSI-19.
Conclusion
In summary, a considerable number of GI cancer site-specific
symptom measures with good psychometric properties have
2953
been identified, with submodules of the FACT being the best
tool choice for most cancer types. Further improvement of
already existing, promising measures is recommended.
Disclosures and acknowledgments No funding was received for this
manuscript. None of the authors are in any financial or personal conflict
of interest regarding this work. We are very grateful for the feedback of
Dr. Jessica McAlpine on an earlier draft of this manuscript.
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