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Gepubliceerd in: Quality of Life Research 9/2021

Open Access 20-07-2021

Health-related quality of life in primary hepatic cancer: a systematic review assessing the methodological properties of instruments and a meta-analysis comparing treatment strategies

Auteurs: Kerstin Wohlleber, Patrick Heger, Pascal Probst, Christoph Engel, Markus K. Diener, André L. Mihaljevic

Gepubliceerd in: Quality of Life Research | Uitgave 9/2021

Abstract

Purpose

Patient-reported outcomes including health-related quality of life (HRQoL) are important oncological outcome measures. The validation of HRQoL instruments for patients with hepatocellular and cholangiocellular carcinoma is lacking. Furthermore, studies comparing different treatment options in respect to HRQoL are sparse. The objective of the systematic review and meta-analysis was, therefore, to identify all available HRQoL tools regarding primary liver cancer, to assess the methodological quality of these HRQoL instruments and to compare surgical, interventional and medical treatments with regard to HRQoL.

Methods

A systematic literature search was conducted in MEDLINE, the Cochrane library, PsycINFO, CINAHL and EMBASE. The methodological quality of all identified HRQoL instruments was performed according to the COnsensus-based Standards for the selection of health status Measurements INstruments (COSMIN) standard. Consequently, the quality of reporting of HRQoL data was assessed. Finally, wherever possible HRQoL data were extracted and quantitative analyses were performed.

Results

A total of 124 studies using 29 different HRQoL instruments were identified. After the methodological assessment, only 10 instruments fulfilled the psychometric criteria and could be included in subsequent analyses. However, quality of reporting of HRQoL data was insufficient, precluding meta-analyses for 9 instruments.

Conclusion

Using a standardized methodological assessment, specific HRQoL instruments are recommended for use in patients with hepatocellular and cholangiocellular carcinoma. HRQoL data of patients undergoing treatment of primary liver cancers are sparse and reporting falls short of published standards. Meaningful comparison of established treatment options with regard to HRQoL was impossible indicating the need for future research.
Opmerkingen

Supplementary Information

The online version contains supplementary material available at https://​doi.​org/​10.​1007/​s11136-021-02810-8.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Introduction

Besides survival and treatment-associated adverse events, patient-reported outcomes (PROs) are arguably the most relevant outcome parameters in oncology. A PRO is defined as ‘any outcome evaluated directly by the patient himself or herself and is based on patient’s perception of a disease and its treatment(s)’ [1]. PROs have many potential advantages as they may elucidate the relationship between clinical endpoints and the patient´s well-being [1], allowing for a more comprehensive evaluation of patients’ health [2].
Health-related quality of life (HRQoL) is a multidimensional PRO measure that is of special interest in oncology as it provides a ‘personal assessment of the burden and impact of a malignant disease and its treatment,’ [1] thus, adding valuable information for a true risk–benefit assessment. This is of special interest when prognosis is limited as in primary malignancies of the liver. HRQoL tools can be distinguished into generic, cancer-specific, cancer-type-specific and utility-(preference-)based instruments [3]. While definitions, implementation, evaluation and analyses of survival and toxicity/complication endpoints have been well standardized over the last decades, PROs are still under-evaluated and reported in most clinical settings. Multiple studies have aimed to define suitable HRQoL tools for different clinical settings, e.g. [4, 5], including cancer patients [68].
Hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (CCA) account for more than 95% of all primary malignant liver tumours. Hepatitis B and C infections are the most prominent risk factor for HCC [9]. More than 840.000 patients were newly diagnosed with HCC or CCA in 2018, and numbers are estimated to rise > 1.3 million annually until 2040 [10]. Although age-standardized incidence rates are moderate in the Western World, they are high in most parts of Asia and parts of West Africa [10], making HCC one of the most frequent tumours in these parts of the world. Prognosis is dismal with 5-year overall survival being around 15% in the USA and 5% in low-income countries [9]. Besides surgical resection, medical treatment (e.g. chemotherapy, kinase inhibitors) and interventional treatments like radiofrequency ablation (RFA) and transarterial chemoembolization (TACE) constitute the three mainstays of treatment for both HCC and CCA.
Therefore, the objectives of this systematic review and meta-analysis were threefold: (1) to perform a systematic review to identify all published HRQoL tools for primary liver cancer (HCC/CCA); (2) to assess the methodological quality and clinical relevance of these HRQoL measures; and (3) to synthesize quantitative data via means of a meta-analysis to compare surgery vs. interventional treatments vs. systemic therapies with regard to HRQoL.

Material and methods

This systematic review and meta-analysis is reported in line with current PRISMA guidelines [11]. The study was registered in the PROSPERO database on 18th July 2017 (registration number CRD42017068103).

Eligibility criteria

Studies investigating HRQoL in HCC or CCA patients were included independent of language or year of publication. All types of studies were included in our search with the exception of case reports, i.e. randomized controlled trials (RCT), cohort-type studies (CTS), case–control studies (CCS) and cross-sectional studies. Furthermore, studies in animals (non-human studies) were excluded. The patient (P) and outcome (O) terms of the PICOT (patient–intervention–comparison–outcome–time) scheme were used to build a search strategy. The search used the ‘outcome’ term to identify PROMs describing quality of life or HRQoL and the ‘patient’ term to find studies including patients with HCC or CCA. Supplement 1 shows the search strategy for MEDLINE performed via OvidSP. If studies included mixed patient populations (e.g. including HCC patients together with metastatic cancer patients and other tumours), only those trials were included in which HRQoL data could clearly be extracted for HCC and CCA patients.

Information sources

The following databases were searched [12]: (a) MEDLINE via OvidSP last searched on 18th July 2019; (b) Ovid MEDLINE In-Process & Other Non-Indexed Citations via OvidSP last searched on 18th July 2019; (c) the Cochrane library (including Cochrane reviews, other reviews, trials, technology assessments and economic evaluations) via the Cochrane homepage (Wiley online library) last searched on 18th July 2019; (d) PsycINFO via EBSCO host last searched on 18th July 2019; (e) CINAHL via EBSCO host last searched on 18th July 2019 and (f) Excerpta Medica Database (EMBASE) via EMBASE homepage last searched on 18th July 2019. The references of the included articles were hand searched to identify additional relevant studies. Where necessary, authors were directly contacted to retrieve missing information.
Sensitive search strategies were developed for all databases using wildcards and adjacency terms where appropriate. Supplement 1 shows the search strategy for MEDLINE performed via OvidSP. The search strategies for the other databases were adapted to the specific vocabulary of each database.

Study selection

Search results were imported into EndNote software (EndNote X7.7, Thomson Reuters) [13], and duplicates were removed by using the automated duplicate removal function of EndNote. Consequently, titles and abstracts of studies were screened by two authors (KW, ALM) for fulfilment of inclusion and exclusion criteria. Remaining duplicates were removed manually. For the remaining studies, full text articles were obtained, which were then screened for eligibility by two authors independently (KW, ALM). Reasons for exclusion of full text articles were recorded (Fig. 1). All remaining articles were included in the qualitative syntheses (objectives 1 and 2). For objective 3 (quantitative assessment), all articles using adequate HRQoL measures (i.e. fulfilling objective 2) were included in the assessment of quality of reporting of HRQoL data and risk of bias assessment of individual studies. HRQoL data were extracted wherever possible and grouped according to the three clinical settings: (a) surgery; (b) interventional therapy and (c) medical treatment.
HRQoL assessments were then grouped into 3-month periods. In a next step, quantitative data analysis was performed for those HRQoL measures for which ≥ 2 quantitative data time points were available. For quantitative data analysis, results of individual studies were entered in RevMan 5 software 5.3. (Review Manager, Version 5.3 Copenhagen: The Nordic Cochrane Center, The Cochrane Collaboration, 2014).

Data collection process

Data were extracted by two authors independently (KW, ALM) and collected on pre-specified piloted forms. In case, required data were not reported in the study, and authors were contacted to obtain remaining data. Differences in data extraction were resolved by consensus with a third author (MKD).

Data items

The following data items were collected: title, author, year of publication, country where study was performed, journal, language, cancer type, intervention, control, co-interventions, primary endpoint, secondary endpoints, HRQoL tool used, type of study, number of centres, start and end dates of study and intervention, number of patients (total), number of patients allocated to intervention(s), number of patients allocated to control, number of patients evaluated for HRQoL (at each point in time), number of withdrawals, exclusions, conversions, duration of follow-up, HRQoL data at baseline and during follow-up, analysis strategy, subgroups measured and subgroups reported. Furthermore, the following baseline characteristics of patients (for both intervention and control group) were recorded: age, gender, severity of illness, co-morbidities and other relevant baseline characteristics.

Evaluation of methodological quality of the HRQoL measures

The methodological quality of HRQoL measures was assessed based on specific psychometric criteria. Owing to the lack of uniform consensus on how to appraise PRO measures, criteria were applied based on published recommendations [3, 14] in accordance with U.S. Food and Drug Administration guidance [15] and the Oxford University PROMs Group guidelines and the COnsensus-based Standards for the selection of health status Measurements INstruments (COSMIN) [16]. The criteria and benchmarks laid out in Table 1 were used for evaluation and have been used in previous publications [4, 5]. A rating scale described in previous publications was applied to allocate a mark for each domain [4, 5]: 0 no evidence reported;—evidence not in favour; + evidence in favour; ± conflicting evidence. Lack of basic psychometric evaluation was defined by a priori consensus as evaluation of less than 2 positive ( +) aspects (other than feasibility and interpretability) in HCC/CCA patients. Evaluation was limited to primary hepatic cancers (HCC/CCA), i.e. the psychometric properties of some instruments might have been evaluated in other types of cancer, but not in HCC/CCA patients. In case of lack of psychometric data for a given instrument, searches were conducted in Medline to identify additional studies that have evaluated the psychometric properties of the HRQoL instrument in closely related patient cohorts (e.g. patients with chronic liver disease).
Table 1
Psychometric criteria used to assess the quality of the patient-reported outcome measures
Domain
Criteria
Test–retest reliability
Test–retest: the intraclass correlation/weighted κ score should be ≥ 0.70 for group comparisons and ≥ 0.90 if scores are going to be used for decisions about an individual based on their score. The mean difference (paired t test or Wilcoxon signed-rank test) between time points 1 and 2, and the 95% CI should also be reported
Internal consistency
A Cronbach’s α score of ≥ 0.70 is considered good, and it should not exceed ≥ 0.92 for group comparisons as this is taken to indicate that items in the scale could be redundant. Item correlations should be ≥ 0.20
Content validity
This is assessed qualitatively during the development of an instrument. To achieve good content validity, there must be evidence that the instrument has been developed by consulting patients and experts as well as undertaking a literature review. Patients should be involved in the development stage and item generation. The opinion of patient representatives should be sought on the constructed scale
Construct validity
A correlation coefficient of ≥ 0.60 is taken as strong evidence of construct validity. Authors should make specific directional hypotheses and estimate the strength of correlation before testing
Criterion validity
A good argument should be made as to why an instrument is standard and correlation with the standard should be ≥ 0.70
Responsiveness
There are a number of methods to measure responsiveness, including t tests, effect size, standardized response means or Guyatt’s responsiveness index. There should be statistically significant changes in score of an expected magnitude
Appropriateness
Assessment whether the content of the instrument is appropriate to the questions which the clinical trial is intended to address
Interpretability
Subjective assessment whether the scores of the instrument are interpretable for patients or physicians
Acceptability
Acceptability is measured by the completeness of the data supplied; ≥ 80% of the data should be complete
Feasibility
Qualitative assessment whether the instrument is easy to administer and process
Floor-Ceiling effect
A floor or ceiling effect is considered if 15% of respondents are achieving the lowest or the highest score on the Instrument
Adapted from [4, 5]

Evaluation of the quality of reporting of HRQoL data

For assessment of reporting, the studies were analysed using the following questions: (a) Is HRQoL data analysis described in methods section? (b) Has an a priori statistical analysis plan for HRQoL outcomes been implemented, addressing common problems like missing data, multiple testing? (c) Is HRQoL raw data presented? (d) Is individual patient data reported? (e) Which summary scores are used for HRQoL data? (f) Which time points of HRQoL assessment are described in the methods section? g.) For which time points is HRQoL data reported in the results section?

Assessment of risk of bias in individual studies

For RCTs risk of bias was judged using The Cochrane Collaboration tool of for assessing quality and risk of bias [17]. Risk of bias for non-randomized, interventional trials was assessed with the ROBINS-I tool (Risk Of Bias In Non-randomized Studies—of Interventions, formerly known as ACROBAT-NRSI) as recommended by the Cochrane collaboration [11]. Non-randomized, non-interventional studies were assessed using the Newcastle–Ottawa risk of bias tool [18], and cross-sectional studies were assessed using the AHRQ checklist. RCTs were judged to be at an overall high risk of bias if there was a serious risk of bias in any of the following domains: random sequence generation, allocation concealment, missing data. For non-randomized trials, the following overall risk of bias judgement for individual studies was used in line with Cochrane recommendations [11]: (a) low risk of bias: the study is judged to be at low risk of bias for all domains; (b) moderate risk of bias: the study is judged to be at low or moderate risk of bias for all domains; (c) serious risk of bias: the study is judged to be at serious risk of bias in at least one domain, but not at critical risk of bias in any domain; (d) Critical risk of bias: the study is judged to be at critical risk of bias in at least one domain.

Statistical analysis

Data were entered in RevMan 5 software 5.3. (Review Manager, Version 5.3 Copenhagen: The Nordic Cochrane Center, The Cochrane Collaboration, 2014) [19]. As level of significance, an alpha of 0.05 was determined. A random-effect model (inverse variance) was used as there has been clinical heterogeneity between the included trials. Heterogeneity was evaluated using I2 statistic. Results lower than 25% were considered as low, between 25% and 75% as possibly moderate, and results of I2 over 60% were considered as a considerable heterogeneity. HRQoL in HCC/CCA patients was compared by meta-analysis for the following types of interventions: (a) surgery; (b) interventional therapies (e.g. TACE, RFA) and (c) systemic therapies (e.g. chemotherapy). Only studies using the FACT-G/FACT-Hep could be used for meta-analysis (see results section). As these subscores are continuous variables, the mean difference in the FACT-G/FACT-Hep subscores was used as effect measure.

Results

Study selection

We identified 3811 studies by database search and 12 additional studies by hand search resulting in a total of 3823 records. 453 of those studies were duplicates (Fig. 1). After screening titles and abstracts, the other 2888 records were excluded according to inclusion and exclusion criteria. Subsequently, the other 358 articles were excluded after full text analyses for the following reasons: no HRQoL tool (n = 74), other type of cancer (no HCC/CCA) (n = 48), no primary data (n = 198), ongoing study without report (n = 21), double publication (n = 15) and no full text available (n = 2). The remaining 124 studies were included in the final qualitative syntheses (Fig. 1).

Study characteristics

The characteristics of the 124 included studies are listed in Table 2 [20140]. Most studies were cohort-type studies (n = 50; 40.3%), either with (n = 12; 24%) or without control group (n = 38; 76%). The remaining studies were RCTs (n = 41; 33.1%), non-randomized controlled trials (n = 18; 14.5%), cross-sectional studies (n = 7; 5.6%) or case–control studies (n = 8; 6.5%) (Supplement 2). A total of 21,496 patients were included in all studies. Frequently studies investigated HCC patients only (Supplement 2). Most studies were single-centre studies (n = 83; 66.9%; supplement 2). The country of origin is depicted in Supplement 2.
Table 2
Baseline characteristics of the included studies
 
Author
Type of cancer
Study type
Country
Number of centers
Type of intervention
Intervention
Number of patients
Study description
QoL also primary vs. Secondary endpoint
PROM
Comment
1
Saleh et al. [20]
HCC
RCT
Egypt
2
Interventional
RFA
32
RFA vs. hepatic resection
Secondary
Questionnaire by Abdelbary
 
Surgical
Liver resection
28
2
Abou-Alfa et al. [21]
HCC
RCT
19 countries
95
Medical
Cabozantinib
470
Cabozantinib vs. placebo in patients with previous sorafenib therapy
Secondary
EQ-5D
 
Placebo
Placebo
237
3
Aliberti et al. [22]
CCA
CTS
Italy
1
Interventional
TACE with Doxorubicin loaded beads
11
TACE with slow-Release Doxorubicin-Eluting
Beads vs. palliative chemotherapy
Unclear
ESAS
 
Medical
Palliative CTx
9
 
4
Barbare et al. [23]
HCC
RCT
France
78
Medical
Tamoxifen
210
Tamoxifen vs. best supportive care
Secondary
Spitzer QoL Index
 
Placebo
Best supportive care
210
5
Barbare et al. [24]
HCC
RCT
France
79
Medical
Octreotide
135
Octreotide vs. placebo
Secondary
EORTC QLQ-C30
 
Placebo
Placebo
137
6
Becker et al. [25]
HCC
RCT
Germany, Switzerland
7
Medical
Octreotide
61
Octreotide vs. placebo
Secondary
EORTC QLQ-C30
 
Placebo
Placebo
59
7
Berr et al. [26]
CCA
CTS
Germany
1
Interventional
23
23
Photodynamic therapy + biliary stenting
Secondary
Spitzer QoL Index
 
8
Bianchi et al. [27]
HCC
CCS
Italy
4
No intervention
None. Patients with HCC
101
Comparison of QoL in patients with HCC vs. liver cirrhosis
Primary
SF-36 + Nottingham Health Profile
 
No intervention
None. Patients with liver cirrhosis
202
9
Blazeby et al. [28]
HCC
CTS
Great Britain, Hong Kong, Taiwan
6
Mixed
Mixed treatments
158
Development of the HCC18 supplement
Primary
EORTC QLQ-HCC18
 
10
Boulin et al. [29]
HCC
NRCT
France
1
Interventional
15 mg Idarubicin
6
Phase II-Studies of TACE with DC-Beads loaded with idarubicin
Secondary
EORTC QLQ-C30
QoL data is reported in Anota et al. 2016
Interventional
10 mg Idarubicin
6
Interventional
5 mg Idarubicin
9
11
Brans et al. [30]
HCC
CTS
Belgium
1
Interventional
131I-lipiodol instillation
26
Instillation of 131I-Lipiodol in the proper hepatic artery during a hepatic angiography
Primary
EORTC QLQ-C30
 
12
Bruix et al. [31]
HCC
RCT
21 countries
152
Medical
Regorafenib
374
Regorafinib vs. placebo in patients with disease progression under sorafenib
Secondary
FACT-G, FACT-Hep, EQ-5D
 
Placebo
Placebo
193
13
Brunocilla et al. [32]
HCC
CTS
Italy
1
Medical
Sorafenib
36
Sorafenib treatment in patients with HCC
Secondary
FACT-Hep
 
14
Cao et al. [33]
HCC
CTS
China
1
Interventional
TACE
155
TACE in patients with HCC
Primary
MDASI
 
15
Cebon et al. [34]
HCC
CTS
Australia
13
Medical
Octreotide
63
Octreotide until tumour progression or toxicity
Unclear
FACT-Hep + Pt DATA Form
 
16
Chang-Chien et al. [35]
HCC
CTS
Taiwan
3
Surgical
Surgery
284
QoL evaluation after surgical treatment for HCC
Primary
FACT-Hep + EORTC QLQ-C30 + SF-36
 
17
Chay et al. [36]
HCC
RCT
Singapore
1
Medical
Coriolus versicolor
9
Coriolus versicolor vs. placebo
Secondary
EORTC QLQ-C30 + FACT-Hep
 
Placebo
Placebo
6
18
Chen et al. [39]
HCC
CTS
China
1
Interventional
TACE
142
TACE (peripheric embolization)
Secondary
EORTC QLQ-C30
 
19
Cheng et al. [38]
HCC
RCT
China, South Korea, Taiwan
23
Medical
Sorafenib
150
Sorafenib vs. placebo
Unclear
FACT-Hep + FHSI-8
 
Placebo
Placebo
76
20
Cheng et al. [40]
HCC
RCT
23 countries
136
Medical
Sunitinib
530
Sunitinib vs. Sorafenib
Secondary
EQ-5D
 
Medical
Sorafenib
544
 
21
Chie et al. [41]
HCC
CTS
Taiwan, UK, China Japan, Italy, France
6
Surgical
Surgical treatment
53
Cross-cultural validation study for EORTC QLQ-HCC18
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
Chie et al. 2015 reports on the same data
Interventional
Ablation
53
Interventional
Embolization
65
Medical
Systemic therapy
24
No intervention
Off-treatment
32
22
Chie et al. [42]
HCC
CTS
Taiwan, UK, Italy, Japan, France
7
Mixed
Asian patients
181
Comparison of QoL in Asian vs. European HCC patients undergoing different types of treatments
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
Mixed
European patients
46
 
23
Chiu et al. [43]
HCC
CTS
Taiwan
3
Surgical
Hepatic resection
332
HCC patients that underwent hepatic resection
Primary
FACT-Hep + SF-36
 
24
Chow et al. [44]
HCC
RCT
9 countries
10
Medical
Tamoxifen twice daily
120
Tamoxifen vs. tamoxifen + placebo vs. placebo
Secondary
EORTC QLQ-C30
 
Medical
Tanoxifen in the morning + placebo at night
74
 
Placebo
Placebo
130
 
25
Chow et al. [45]
HCC
RCT
6 countries
7
Medical
Megestrolacetate
123
Megestrolacetate vs. placebo
Secondary
EORTC QLQ-C30
 
Placebo
Placebo
62
 
26
Chow et al. [46]
HCC
CTS
4 countries
7
Medical
Sorafenib
29
Sorafenib 14 days post radio embolization
Secondary
EQ-5D
 
27
Chung et al. [47]
HCC
CSS
Taiwan
3
Mixed
Mixed treatments
100
Symptom evaluation of HCC patients with different types of treatments
Primary
MDASI
 
28
Cowawintaweewat et al. [48]
HCC
CTS
Thailand
1
Medical
Active Hexose Correlated Compound Treatment
34
AHCC vs. placebo
Primary
Questionnaire by Cowawintaweewat
 
Placebo
Placebo
10
 
29
Darwish Murad et al. [49]
CCA
CTS
USA
1
Surgical
Neoadjuvant radio-chemotherapy + LT
79
Neoadjuvant radio-chemotherapy + LT for CCA vs. LT for other indication than CCA
Primary
EQ-5D + SF-36 + NIDDK-QA
 
Surgical
LT for other indication than CCA
110
 
30
Dimitroulopoulos et al. [50]
HCC
NRCT
Greece
1
Medical
Positive ocreotide scan: Sandostatin
15
Sandostatin vs. no sandostatin
Secondary
EORTC QLQ-C30
 
Medical
Negative Octreoscan o refusing octreotide: no sandostatin
13
 
31
Dimitroulopoulos et al. [51]
HCC
RCT
Greece
1
Medical
Octreoscan positive: octreotide s.c. and octreotide long-acting formulation
30
Octreotide vs. Placebo with positive Octreoscan compared to patients with negative Octreoscan
Secondary
EORTC QLQ-C30
 
Placebo
Octreoscan positive: placebo
30
 
Medical
Octreoscan negative: only follow-up
60
 
32
Doffoël et al. [52]
HCC
RCT
France
15
Interventional
Tamoxifen + TACE
62
Tamoxifen + TACE vs. Tamoxifen
Secondary
Spitzer QoL Index
 
Medical
Tamoxifen
61
 
33
Dollinger et al. [53]
HCC
RCT
Germany
12
Medical
Thymostimulin
67
Thymostimulin vs. placebo
Secondary
FACT-Hep
 
Placebo
Placebo
68
 
34
Dumoulin et al. [54]
CCA
CTS
Germany
1
Interventional
Metal stent and photodynamic therapy
24
PDT vs. historic control
Unclear
EORTC QLQ-C30
 
No intervention
Historic control
20
 
35
Eltawil et al. [55]
HCC + CCA
CTS
Canada
1
Interventional
TACE
48
TACE for primary liver cancer
Primary
WHOQoL-BREF
 
36
Fan et al. [56]
HCC
CTS
Taiwan
2
Mixed
Surgery, TACE or systemic therapy
286
QoL of HCC patients treated with surgery, TACE or systemic therapy was compared to healthy norm values
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
37
Gill et al. [57]
HCC
CSS
13 countries
online- based
Mixed
Different treatments
256
All HCC patients were invited to complete the QoL survey
Primary
Questionnaire by Gill
 
38
Gmur et al. [58]
HCC
CTS
Switzerland
1
Mixed
Different treatments
242
Evaluation of the predictive value of QoL on survival
Primary
FACT-Hep
 
39
Guiu et al. [163]
HCC
NRCT
France
1
Interventional
Idarubicin 15 mg
4
Phase II study of TACE with DC-Beads with Idarubicin
Secondary
EORTC QLQ-C30
 
Interventional
Idarubicin 20 mg
4
 
Interventional
Idarubicin 25 mg
2
 
40
Hakim et al. [59]
HCC
RCT
Zimbabwe
n.a
Medical
Adriamycin 20 mg weekly
112
Adriamycin vs. best supportive care
Unclear
FLIC
 
Medical
Adriamycin 80 mg monthly
 
No intervention
Best supportive care
 
41
Hamdy et al. [60]
HCC
CTS
Egypt
1
Intervention 1
RFA
40
QoL compared in patients with HCC vs. chronic liver disease
Primary
SF-36
 
Intervention 2
TACE
40
 
Control
Patients with HCV but without HCC
40
 
42
Hartrumpf et al. [61]
HCC
CTS
Germany
1
Interventional
TACE
148
TACE for patients with HCC
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
43
He et al. [62]
HCC
NRCT
China
1
Surgical
Liver transplantation
22
Liver transplantation vs. hepatic resection vs. RFA
Primary
SF-36
 
Surgical
Hepatic resection
68
 
Interventional
RFA
38
 
44
Hebbar et al. [63]
HCC
RCT
France
17
Interventional
TACE + sunitinib
39
TACE + sunitinib vs. TACE + placebo
Secondary
unclear
 
Interventional
TACE + placebo
39
 
45
Heits et al. [64]
HCC
CSS
Germany
1
Surgical
Liver transplantation
173
QoL in HCC patients after LT was compared to healthy norm values
Primary
EORTC QLQ-C30
 
46
Hinrichs et al. [65]
HCC
CTS
Germany
1
Interventional
TACE
62
TACE for patients with HCC
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
47
Hoffmann et al. [66]
HCC
RCT
Germany
4
Medical
TACE + sorafenib
24
TACE + sorafenib vs. TACE + placebo until tumour progression or liver transplantation
Secondary
EORTC QLQ-C30 + EORTC QLQ-HCC18
QoL data is reported in Hoffmann et al. 2015
Placebo
TACE + placebo
26
48
Hsu et al. [67]
HCC
CTS
Taiwan
1
No intervention
No intervention
300
Evaluation of the influence of the mini nutritional assessment on functional status and QoL
Unclear
EORTC QLQ-C30
 
49
Huang et al. [37]
HCC
NRCT
China
1
Interventional
RFA
121
Patients with a HBV associated solitary HCC with diameter of 3 cm or less underwent RFA vs. hepatic resection
Primary
FACT-Hep
 
Surgical
Hepatic resection
225
 
50
Jie et al. [68]
HCC
CTS
China
1
No intervention
Informed patients
126
QoL in patients informed vs. uninformed of their diagnosis
Primary
EORTC QLQ-C30
 
No intervention
Uninformed patients
92
 
51
Johnson et al. [69]
HCC
RCT
26 countries
173
Medical
Brivanib
577
Brivanib vs. placebo as first-line therapy in patients with unresectable, advanced HCC
Secondary
EORTC QLQ-C30
 
Placebo
Placebo
578
 
52
Kensinger et al. [70]
HCC
NRCT
USA
1
Surgical
LT for HCC with "MELD exception points"
106
Liver transplantation for HCC ± "exception points" vs. liver transplantation without HCC
Primary
SF-36
 
Surgical
LT for HCC without "MELD exception points
33
 
Surgical
LT without HCC
363
 
53
Kirchhoff et al. [71]
HCC
RCT
Germany
5
Interventional
Transient transarterial chemoocclusion
35
Transient transarterial chemoocclusion (TACO) using degradable starch microspheres (DSM) vs. transarterial chemoperfusion without DSM
Secondary
EORTC QLQ-C30
 
Interventional
Transarterial chemoperfusion
35
 
54
Koeberle et al. [72]
HCC
RCT
Switzerland, Austria
8
Medical
Sorafenib + Everolimus
59
Patients with unresectable or metastatic HCC and Child–Pugh ≤ 7 liver dysfunction
Secondary
EORTC QLQ-C30 + LASA by Bernhard
 
Medical
Sorafenib
46
 
55
Kolligs et al. [73]
HCC
RCT
Germany
2
Interventional
Selective internal radiation therapy (SIRT)
13
SIRT vs. TACE in unresectable HCC
Primary
FACT-Hep
 
Interventional
Transarterial chemoembolization (TACE)
15
 
56
Kondo et al. [74]
HCC
CCS
Japan
1
Interventional
Percutaneous ethanol injection therapy (PEIT) or RFA
97
QoL in patients receiving PEIT or RFA vs. QoL in patients with chronic liver disease who had neither current evidence nor history of HCC
Primary
SF-36
 
No intervention
Chronic liver disease
97
 
57
Kudo et al. [75]
HCC
RCT
20 countries
154
Medical
Levatinib
478
Levatinib vs. Sorafenib as first-line treatment in patients with unresectable HCC
Secondary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
Medical
Sorafenib
476
 
58
Kuroda et al. [76]
HCC
NRCT
Japan
1
Medical
Branched-chain amino acid—enriched nutrition
20
BCAA-enriched nutrition vs standard diet
Secondary
SF-8
 
No intervention
Standard diet
15
 
59
Lee et al. [77]
HCC
NRCT
Taiwan
1
Surgical
Hepatic resection
121
Hepatic resection vs. TACE vs. PEI vs. best supportive care
Primary
EORTC QLQ-C30 + WHOQoL-BREF
 
Interventional
TACE
31
 
Interventional
Percutaneous ethanol injection (PEI)
8
 
No intervention
Best supportive care
1
 
60
Lee [164]
HCC
CTS
South Korea
1
Mixed
Mixed treatments
40
QoL in patients receiving different types of treatments
Primary
SF-12
 
61
Lei et al. [78]
HCC
NRCT
China
1
Surgical
Liver transplantation
95
LT vs. hepatic resection
Primary
SF-36
 
Surgical
Hepatic resection
110
 
62
Li et al. [79]
HCC
NRCT
China
1
Interventional
High intensity focussed ultrasound therapy (HIFU) + best supportive care
151
HIFU vs. best supportive care
Unclear
QOL-LC
 
No intervention
Best supportive care
30
 
63
Li et al. (2013)
HCC
RCT
China
1
Medical
TACE + Celecoxib + Lanreotide
133 (total)
TACE + Celecoxib + Lanreotide vs. TACE + Celecoxib
Unclear
EORTC QLQ-C30
 
Medical
TACE + Celecoxib
 
64
Li et al. [80]
HCC
CTS
China
1
No intervention
No intervention
472
Evaluation of the prognostic value of QoL
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
65
Liu et al. [81]
HCC
CTS
China
2
Surgical
Hepatic resection + thrombectomy
65
Hepatic resection + thrombectomy vs. chemotherapy
Unclear
FACT-Hep
 
Medical
Systemic therapy
50
 
66
Llovet et al. [82]
HCC
RCT
21 countries
121
Medical
Sorafenib
303
Sorafenib vs. placebo in patients with advanced HCC who had not received previous systemic treatment
Secondary
FHSI-8
 
Placebo
Placebo
299
 
67
Lv et al. [83]
HCC
RCT
China
1
Medical
Parecoxib
60
Parecoxib vs. placebo in HCC patients receiving TACE
Unclear
Questionnaire by Lv
 
Placebo
Placebo
60
 
68
Manesis et al. [84]
HCC
RCT
Greece
1
Medical
Triptorelin + Tamoxifen
33
Triptorelin + Tamoxifen vs. Triptorelin + Flutamid vs. placebo
Secondary
Spitzer QoL Index
 
Medical
Triptorelin + Flutamid
23
 
Placebo
Placebo
29
 
69
Meier et al. [85]
HCC
CTS
USA
1
No intervention
No intervention
130
Qol in patients with therapy naive HCC and liver cirrhosis
Unclear
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
70
Meyer et al. [86]
HCC
RCT
Great Britain
1
Interventional
Transarterial chemoembolization: with cisplatin
44
TACE vs. TAE
Secondary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
Interventional
Transarterial embolization
42
 
71
Mihalache et al. [87]
CCA
CTS
Romania
1
Mixed
Curative + palliative treatments: surgery, stenting, chemotherapy, drainage etc
133
QoL in patients with curative and palliative treatment for CCA
Unclear
EORTC QLQ-C30
 
72
Mikoshiba et al. [88]
HCC
CTS
Japan
1
Mixed
Different treatments
192
Validation of the Japanese version of EORTC QLQ-HCC18
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18 + FACT-Hep
 
73
Mikoshiba et al. [89]
HCC
CSS
Japan
1
No intervention
Depressive Symptoms
36
QoL in HCC patients with or without depressive symptoms
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
No intervention
Without depressive symptoms
91
 
74
Mise et al. [90]
HCC
CTS
Japan
1
Surgical
Hepatic resection
108
QoL in patients receiving hepatic resection for HCC
Primary
SF-36
 
75
Montella et al. [91]
HCC
CTS
Italy
1
Medical
Sorafenib
60
Sorafenib in patients > 70 years of age with advanced HCC
Unclear
FHSI-8
 
76
Müller et al. [92]
HCC
RCT
Austria
1
Interventional
Octreotide + PEI
31
Octreotide + PEI vs. Octreotide
Unclear
VAS by Priestman & Baum
 
Medical
Octreotide
30
 
77
Norjiri et al. [93]
HCC
RCT
Japan
1
Medical
Branched-chain amino acid (Aminoleban EN) supplementation
25
Branched-chain amino acid enriched nutrition vs. standard diet in HCC patients with up to 3 tumour nodules < 3 cm receiving RFA
Secondary
SF-8
 
No intervention
Standard diet
26
 
78
Nowak et al. [94]
HCC
CTS
Australia
13
Medical
Octreotide
46
Octreotide
Primary
FACT-Hep + Pt DATA Form
Part of a larger Phase II trial (Cebon J, et al. Br J Cancer 2006; 95: 853–61.)
79
Nugent et al. [95]
HCC
RCT
USA
1
Interventional
Stereotactic body radiation therapy
12
SBRT vs. TACE as bridging therapy before liver transplantation for HCC
Secondary
SF-36
 
Interventional
TACE
15
 
80
Ortner et al. [96]
CCA
RCT
Germany, Switzerland, Austria
4
Interventional
Photodynamic therapy + Stenting
20
Photodynamic therapy + Stenting vs. Stenting
Secondary
EORTC QLQ-C30
 
Interventional
Stenting
19
 
Interventional
Non-randomized PDT + Stenting
31
 
81
Otegbayo et al. [97]
HCC + CCA
CTS
Nigeria
1
No intervention
Unclear
34
QoL in patients with HCC
Primary
WHOQoL-BREF
 
82
Palmieri et al. [98]
HCC
CCS
Italy
1
No intervention
HCC
24
QoL in patients with HCC vs. CLD vs. healthy controls
Primary
SF-36
 
No intervention
CLD
22
 
No intervention
Healthy controls
20
 
83
Park et al. [117]
CCA
RCT
South Korea
1
Interventional
Photodynamic therapy + S-1
21
Photodynamic therapy ± S-1 for patients with unresectable hilar cholangiocarcinoma
Secondary
DDQ-15
 
Interventional
Photodynamic therapy
22
 
84
Poon et al. [99]
HCC
CTS
China
1
Surgical
Hepatic resection
66
Hepatic resection vs. TACE
Primary
FACT-G
 
Interventional
TACE
10
 
85
Poon et al. [100]
HCC
RCT
China
1
Medical
TACE plus branched-chain amino acid as supplement
41
Branched-chain amino acid enriched nutrition vs. standard diet in HCC patients with unresectable tumour
Secondary
FACT-G
 
 
No intervention
Standard diet
43
 
86
Qiao et al. [101]
HCC
CSS
China
1
No intervention
No intervention
140
QoL and TNM stage in patients with HCC
Primary
FACT-Hep
Drop-out 2 patients for disease progression. 3 patients excluded as > 5 items missing
87
Ryu et al. [102]
HCC
CSS
South Korea
1
No intervention
High symptom scores
53
Effect of symptoms on QoL in patients with HCC
Primary
FACT-Hep
 
No intervention
Low symptom scores
127
 
88
Salem et al. [103]
HCC
NRCT
USA
1
Interventional
TACE
27
TACE vs. 90Y radioembolization
Primary
FACT-Hep
 
Interventional
Radioembolization
29
 
89
Shomura et al. [104]
HCC
CTS
Japan
1
Medical
Sorafenib
54
QoL during sorafenib treatment
Primary
SF-36
 
90
Shun et al. [105]
HCC
CTS
Taiwan
2
Interventional
Stereotactic radiation therapy
99
QoL during SRT treatment for HCC
Primary
FLIC
 
91
Shun et al. [106]
HCC
CTS
Taiwan
1
Interventional
TACE
89
QoL during TACE for HCC
Primary
SF-12
 
92
Somjaivong et al. [107]
CCA
CSS
Thailand
2
No intervention
No intervention
260
Evaluation of the influence of symptoms, social support, uncertainty and coping on QoL
Primary
FACT-Hep
 
93
Steel et al. [108]
HCC
NRCT
USA
1
Interventional
Hepatic arterial infusion with 90Y-Micosphere
14
90Y-Microsphere vs. Cisplatin during hepatic arterial infusion for HCC
Primary
FACT-Hep
Butt et al. 2014 and Steel et al. 2006 report on the same data
Interventional
Cisplatin infusion of Cisplatin into the hepatic artery
14
94
Steel et al. [109] (1)
HCC
CCS
USA
1
No intervention
HCC
21
Evaluation of the influence of sexual functioning on QoL
Secondary
FACT-Hep
 
No intervention
CLD
23
 
95
Steel et al. [110] (2)
HCC
CCS
USA
1
No intervention
HCC
82
QoL evaluation by patients themselves vs. caregivers
Primary
FACT-Hep
Steel et al. 2006 reports on the same data
No intervention
Caregivers
82
96
Steel et al. [111]
HCC
CCS
USA
1
No intervention
HCC
83
Comparison of QoL in patients with HCC vs. chronic liver disease vs. healthy controls
Primary
FACT-Hep
Butt et al. 2014 reports on the same data
No intervention
Chronic liver disease
51
No intervention
Healthy controls
138
97
Steel et al. [112]
HCC + CCA
CTS
USA
1
No intervention
No intervention
321
Evaluation of the prognostic value of QoL
Secondary
FACT-Hep
 
98
Sternby Eilard et al. [113]
HCC
CTS
Sweden, Norway
4
No intervention
No intervention
205
Evaluation of the prognostic value of QoL
Primary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
99
Tanabe et al. B[114]
HCC
CTS
Japan
1
Surgical
Hepatic resection
188
Hepatic resection for HCC
Unclear
Questionnaire by Tanabe
 
100
Tian et al. [115]
HCC + CCA
RCT
China
1
Interventional
TACE with Bruceas- and iodized oil + oral injection of Ganji Decoction
49
TACE with Bruceas- and iodized oil + oral injection of Ganji Decoction vs. regular TACE
Unclear
QOL-LC
 
Interventional
TACE
48
 
101
Toro et al. [116]
HCC
NRCT
Italy
1
Surgical
Hepatic resection
14
Hepatic resection vs. TACE vs. RFA vs. no treatment
Primary
FACT-Hep
 
Interventional
TACE
15
 
Interventional
RFA
9
 
Control
No treatment
13
 
102
Treiber et al. [118]
HCC
RCT
Germany
1
Medical
Octreotide + Rofecoxib
32
Octreotide + Rofecoxib vs. Octreotide in palliative HCC
Primary
SF-36
 
Medical
Octreotide
39
 
103
Ueno et al. [119]
HCC
CTS
Japan
1
Surgical
Impaired QoL
21
Evaluation of the factors influencing QoL after hepatic resection
Primary
Questionnaire by Ueno
 
Surgical
Preserved QoL
75
 
104
Vilgrain et al. [121]
HCC
RCT
France
25
Interventional
SIRT
174
SIRT vs. Sorafenib in locally advanced and inoperable HCC
Secondary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
Medical
Sorafenib
206
 
105
Wan et al. [120]
HCC
CTS
China
1
Mixed
Different treatments
105
Development and validation study of a new QoL tool
Primary
QOL-LC
 
106
Wang et al. [122]
HCC
RCT
China
1
Interventional
TACE + RFA
43
TACE + RFA vs. TACE
Primary
FACT-G
 
Interventional
TACE
40
 
107
Wang et al. [123]
HCC
CSS
China
1
No intervention
No intervention
277
Evaluation of the influence of symptoms on QoL
Primary
FACT-Hep + MDASI
 
108
Wang et al. [124]
HCC
NRCT
China
1
Interventional
Immunotherapy + TACE or radiotherapy
42
TACE or radiotherapy with vs. without immunotherapy with DC-CTLs
Primary
EORTC QLQ-C30
 
Interventional
TACE or radiotherapy
26
 
109
Wible et al. [125]
HCC
CTS
USA
1
Interventional
TACE
73
QoL after TACE for HCC compared with healthy normal values
Primary
SF-36
 
110
Wiedmann et al. [126]
CCA
CTS
Germany
1
Interventional
Photodynamic therapy + biliary stent
23
PDT and biliary drainage in patients with hilar CCA
Secondary
Spitzer QoL Index
 
111
Woradet et al. [127]
CCA
CTS
Thailand
5
Mixed
Mixed treatments
99
QoL in patients receiving standard or palliative therapy for HCC
Primary
FACT-Hep
 
112
Xie et al. [128]
HCC
CTS
China
1
Surgical
Hepatic resection
58
Hepatic resection vs. TACE
Primary
SF-36
 
Interventional
TACE
44
 
113
Xing et al. [129]
HCC
CTS
USA
1
Interventional
TACE with Doxorubicin loaded beads
118
QoL in HCC patients receiving TACE with Doxorubicin loaded beads vs. healthy norm values
Primary
SF-36
 
114
Xing et al. [130]
HCC
CTS
USA
1
Interventional
Y90 radioembolization
30
QoL in patients with advanced infiltrative HCC and portal vein thrombosis receiving Y90 radioembolization vs. Healthy norm values
Primary
SF-36
 
115
Xu et al. [131]
HCC
RCT
China
1
Interventional
TACE + Jian Pi Li Qi Decoction
50
TACE + Jian Pi Li Qi Decoction-Decoction vs. TACE ± placebo
Primary
MDASI-GI
 
Interventional
TACE + placebo
40
 
Interventional
TACE
50
 
116
Yang et al. [132]
HCC
CTS
China
1
Mixed
Different treatments
114
Validation of the Chinese version for the EORTC QLQ-HCC18
Primary
EORTC QLQ-HCC18
 
117
Yang et al. [133]
HCC
CTS
China
1
Interventional
TACE or TEA
17
Evaluation of survival and QoL in HCC patients receiving TACE or TEA therapy
Secondary
EORTC QLQ-C30
 
118
Yau et al. [134]
HCC
CTS
China
1
Medical
PEGylated recombinant human arginase 1
20
QoL and survival analysis of HCC patients receiving treatment with PEGylated recombinant human arginase 1
Secondary
EORTC QLQ-C30 + EORTC QLQ-HCC18
 
119
Ye et al. [135]
HCC + CCA
RCT
China
4
Medical
Shungbai San
67
Shunbai San dermal application vs. Placebo dermal application
Primary
EORTC QLQ-C30 + QOL-LC
 
Placebo
Placebo
66
 
120
Yen et al. [136]
HCC
NRCT
USA
4
Medical
Capecitabine 1000 mg/m2 + PHY906 1000 mg
3
Phase I/II study of Capecitabine/PHY906 in HCC patients
Secondary
FACT-Hep
 
Medical
Capecitabine 750 mg/m2 + PHY906 600 mg
8
 
Medical
Capecitabine 750 mg/m2 + PHY906 800 mg
31
 
121
Zhang et al. [137]
HCC
NRCT
China
1
Medical
Sorafenib
102
HCC patients with complete response after TACE or RFA who received sorafenib or not
Unclear
FACT-Hep
 
No intervention
No sorafenib
55
 
122
Zheng et al. [138]
HCC
NRCT
China
1
Surgical
Surgical treatment
29
Surgical vs. conservative treatment of spinal metastasis in HCC patients
Primary
FACT-Hep
 
No intervention
Conservative treatment
33
 
123
Zhu et al. [139]
HCC
RCT
17 countries
111
Medical
Everolimus
362
Everolimus vs. placebo
Secondary
EORTC QLQ-C30
 
Placebo
Placebo
184
 
124
Zhu et al. [140]
HCC
RCT
27 countries
154
Medical
Ramucirumab
283
Ramucirumab vs. placebo
Secondary
FHSI-8 + EQ-5D
QoL data is reported in Chau et al. 2017
Placebo
Placebo
282
Abbreviations: JPLQ-Decoction Jian Pi Li Qi Decoction (mixture of Chinese medical herbs), Shungbai San traditional mixture of Chinese medicine containing 5 main plant-based ingredients, Coriolus versicolor mushroom of the family of Basidiomycota used in the traditional Asian medicine, Aminoleban EN mixture of amino acids, hydolysed collagen, dextran, rice oil, minerals and vitamins, BCAA branched-chain amino acids, DC-CTLs dendritic cell-cytotoxic T lymphocytes, Ganji Decoction mixture of Chinese medical herbs
In total, 29 different HRQoLs in 124 studies instruments were identified by our search (Figs. 2 and 3). Of those, 26 different HRQoL PROMs were identified in HCC patients, 8 in CCA patients and 4 different tools in mixed patient cohorts. Multiple studies used more than one HRQoL tool (Table 1). The identified instruments covered all types of HRQoL (generic, cancer-specific, cancer-type-specific and utility-based HRQoL instruments) (Fig. 2).
Despite being labelled as HRQoL instruments in the studies, a number of the identified instruments solely address cancer symptoms and, thus, lack the multidimensionality that is requested for HRQoL and were, thus, excluded from further analyses (Fig. 3 step 1). These were (a) MD Anderson symptom inventory; (b) ESAS: Edmonton symptom assessment scale; (c) MD Anderson symptom inventory – gastrointestinal and (d) FHSI-8 FACT hepatobiliary symptom index. The remaining 25 instruments (117 studies) were included in the further analyses (Fig. 3). These 25 instruments use two to eight domains covering various aspects of quality of life (e.g. physical and mental health, role functioning and symptom burden). The EORTC QLQ-C30 and the FACT-G have cancer-type-specific supplements (EORTC QLQ-HCC18 and FACT-Hep) which can only be used in combination with the more general questionnaire. The questionnaires comprise 5 (EQ-5D) to 47 questions (NIDDK-QA) and have a recall period from the 24 h (EQ-5D) to 4 weeks (SF-8/12/36, Patient Benefit Form). Most of them can be completed within 10 min.

Methodological assessment of HRQoL instruments

The methodological quality of the remaining 25 HRQoL instruments was assessed as outlined in the methods section. Results are shown in Table 3. If no data for a given HRQoL instruments were available for HCC/CCA patients, additional Medline searches were performed to identify methodology studies that evaluated the PROM in closely related patient populations like chronic liver disease. These studies are indicated in Table 3.
Table 3
Overview of the methodological quality of HRQoL tools in primary liver cancer
 
Psychometric properties
References
Test–retest reliability
Internal consistency
Content validity
Criterion validity
Construct validity
Responsiveness
Acceptability
Feasibility
Floor/ceiling effects
Interpretability
Generic PROMs
          
LASA** by Bernhard (Koeberle et al.)
0
0
0
0
0
0
0
0
0
 + 
NHP
0
 + (Bianchi 2003)
0
0
0
0
 + (Bianchi 2003)
 + (Bianchi 2003)
0
 + 
SF-8
0
0
0
0
0
0
0
0
0
 + 
SF-12
0
0
0
0
0
0
0
0
0
 + 
SF-36
 + (Ünal 2001*)
 + (Bayliss 1998*, Ünal 2001*, Zhou 2013*, Casanovas Taltavull 2015*)
0
0
 + (Bayliss 1998*, Ünal 2001*, Zhou 2013*)
0
 + (Bayliss 1998*, Ünal 2001*, Zhou 2013*)
 + (Ünal 2001*)
− (Bayliss 1998*, Zhou 2013*); ± (Ünal 2001*)
 + 
Questionnaire by Abdelbary
0
0
0
0
0
0
0
0
0
 + 
Questionnaire by Cowawintaweewat
0
0
0
0
0
0
0
0
0
 + 
Questionnaire by Lv
0
0
0
0
0
0
0
0
0
 + 
Questionnaire by Tanabe
0
0
0
0
0
0
0
0
0
 + 
WHOQoL-BREF
0
 + (Lin 2018*, Lee 2007)
0
0
 ± (Lin 2018*)
0
 + 
 + 
0
 + 
Cancer specific PROMs
EORTC QLQ-C30
0
 + (Lee 2007)
0
0
0
0
 + 
 + 
0
 + 
FACT-G
 + (Yount 2002*, Zhu 2008*)
 + (Yount 2002*, Zhu 2008*)
 + (Cella 1993*)
 + (Zhu 2008*)
0
0
 + 
 + 
0
 + 
FLIC
0
0
0
0
0
0
0
0
0
 + 
Patient Benefit Form
0
0
0
0
0
0
0
0
0
 + 
Patient DATA Form
0
0
0
 ± (Nowak 2008, Cebon 2006)
 + (Nowak 2008)
− (Nowak 2008)
 ± (Nowak 2008, Cebon 2006)
 + 
− (Nowak 2008)
 + 
Priestman & Baum
0
0
0
0
0
0
0
0
0
 ± 
Spitzer QoL Index
0
0
0
0
0
0
 + (Barbare 2005, Wiedmann 2004)
 + (Berr 2000, Doffoël 2008, Barbare 2005)
0
 + 
Cancer–type-specific PROMs
DDQ-15
0
0
0
0
0
0
0
0
0
 + 
EORTC QLQ-HCC18
 + (Chie 2012, Chie 2015, Mikoshiba 2012)
 ± (Mikoshiba 2012, Chie 2012)
 + (Blazeby 2004*)
0
 ± (Mikoshiba 2012; Chie 2012, Chie 2015)
 ± (Chie 2012, Chie 2015)
 + (Meier 2015, Mikoshiba 2012, Fan 2013)
 + (Chie 2012, Chie 2015, Fan 2013, Meier 2015)
 ± (Meier 2015, Chien 2015)
 + 
FACT-Hep
 + (Heffernan 2002, Yount 2002*, Zhu 2008)
 + (Heffernan 2002, Steel 2006, Mikoshiba 2012)
 + (Heffernan 2002)
 + (Heffernan 2002; Zhu 2008)
 + (Heffernan 2002, Zhu 2008, Mikoshiba 2012)
 + (Steel 2006, Zhang 2015) ± (Nowak 2008)
 ± (Nowak 2008); + (Zhang 2015; Steel 2007; Huang 2014)
 + 
0
 + 
NIDDK-QA
 + (Kim 2000*)
 + (Kim 2000*)
 ± (Gross 1999*)
 + (Kim 2000*)
 + (Kim 2000*)
 + (Kim 2000*)
0
0
0
 + 
QOL-LC
 + (Wan 2010*)
 + (Wan 2010*)
 ± (Wan 2010*)
- (Wan 2010*)
 + (Wan 2010*)
 + (Wan 2010*)
 + (Wan 2010*)
 + 
 + (Ye 2016)
 + 
Questionnaire by Gill
0
0
0
0
0
0
0
0
0
 + 
Questionnaire by Ueno
0
0
0
0
0
0
0
0
0
 + 
Utility based PROMs
EQ-5D
 ± (Ünal 2001*)
0
0
 + (Krabbe 2003*)
0
 + (Unal 2001*, Chau 2017)
 + (Ünal 2001*, Chow 2014, Chau 2017)
 + 
 ± (Ünal 2001*)
 + 
*Publications were identified via additional search in Pubmed. These studies were not solely conducted HCC/CCA patient populations but contain closely related patient populations like patients with chronic liver disease or extrahepatic bile duct tumours
0 = not reported (no evaluation completed),—= evidence not in favour, ±  = weak evidence, +  = evidence in favour
Gross 1999 + Kim 2000: development of questionnaire and validation of psychometric properties in patients with cholestatic liver disease/liver transplantation
**linear analogue-self assessment
Marked with * are studies that investigate psychometric properties in closely related patient cohorts (not only containing HCC/CCA patients). Rating: 0 no data reported;—evidence not in favour; + evidence in favour; ± conflicting evidence (rating scale adapted from [4, 5])
The most frequently evaluated dimension in all HRQoL tools was reliability (test–retest reliability and internal consistency). With a test–retest correlation of more than 0.70, adequate performance for 6 out of 12 PROMs (SF-36, FACT-G, EORTC QLQ-HCC18, FACT-Hep, NIDDK-QA and QOL-LC) was confirmed [41, 88, 120, 141146]. For the EQ-5D, correlation coefficients ranging from 0.58 to 0.98 were observed showing that not all scales in this PROM are reliable enough [141]. Internal consistency was evaluated with the calculation of Cronbach’s α. A value greater 0.70 was considered sufficient according to COSMIN guidelines [16]. This could be observed in 8 out of 12 HRQoL tools (NHP, SF-36, WHO-BREF, EORTC QLQ-C30, FACT-G, FACT-Hep, NIDDK-QA and QOL-LC) [27, 77, 88, 120, 141, 142, 144151]. Concerning validity, rarely all three pre-defined categories (content, criterion and construct validity) were evaluated. More frequently only one or two aspects of validity were examined. Content validity was evaluated investigating the process of questionnaire creation. In case of the FACT-G, FACT-Hep and EORTC QLQ-HCC18, the process described included qualitative studies with inclusion of expert opinions, patient reports and current literature [28, 144, 152]. Merely three PROMs (FACT-Hep, FACT-Hep and NIDDK-QA) were compared to the gold standard (i.e. an already established questionnaire), thus, testing criterion validity [144146]. In order to evaluate construct validity, group comparisons using performance status (such as the Karnofsky Performance Status) were used for the EORTC QLQ-HCC18 and FACT-Hep questionnaires as it is known that a higher performance status correlates with better HRQoL [41, 88]. Construct validity within the SF-36 was evaluated using the correlation with hypothesized scores (conceptually related and unrelated scores) [141, 148, 149]. Kim et al. compared item scores between ambulatory patients and liver transplant recipients as well as examined correlations between the domain scores of NIDDK-QA vs. SF-36 and Mayo risk score, respectively [146]. The Wilcoxon signed-rank test was used by Chie et al. to evaluate if the changes in score were significant before and after treatment. For example, patients undergoing surgical treatment suffered significantly more pain compared to before which reflects an adequate responsiveness of the EORTC QLQ-HCC18 [41]. Steel et al. evaluated the clinically meaningful changes of the FACT-Hep over time and found significant decrements in all subscales from baseline to 3-month follow-up [147]. The SF-36 performed poorly during the evaluation of floor and ceiling effects with patients scoring the highest or lowest possible score in distinctly more than 15% which was the set cut-off [148, 149]. Valid acceptability and feasibility were assumed when the response rate was > 80%, or the time to complete the questionnaire was 10 or less minutes [24, 27, 46, 56, 85, 88, 120, 126, 141, 148, 149, 153]. The interpretability of all PROMs was considered acceptable as higher scores in QoL scales represent higher HRQoL, and higher scores within the symptom scales represent lower HRQoL.
Due to a lack of data concerning the basic psychometric evaluation or negative results, only the following 10 HRQoL instruments were considered methodologically adequate according to the pre-specified criteria (see methods section) and were subsequently included in further analyses (Table 3): (a) Generic HRQoL: NHP, SF-36, WHO-BREF; (b) Cancer (Condition)-specific HRQoL: EORTC QLQ-C30 and FACT-G; (c) Cancer type-specific HRQoL: EORTC QLQ-HCC18, FACT-Hep, NIDDK-QA and QOL-LC; (d) Utility (preference)-based HRQoL: EQ-5D. Only publications using one of the above-mentioned 10 HRQoL measures were included in further analyses (n = 98 studies) (Fig. 3 step 2).

Quality of reporting of HRQoL data

The remaining studies were evaluated for the quality of reporting of HRQoL data. Results are summarized in Supplement 3. Of the 98 included studies, 4 (4,1%) did not specify in their methods section at what exact time points HRQoL data were measured [28, 31, 74, 79]. Many studies showed a marked discrepancy between reported HRQoL data in the results section and the frequency of HRQoL data assessment specified in the methods section. Eight studies reported only baseline HRQoL data although these trials specified in their methods section to have assessed HRQoL also during follow-up [38, 41, 42, 58, 80, 94, 98, 139]. The other 18 studies lacked reporting of HRQoL data altogether in their results section, although assessment had been announced in the methods section (supplement 3) [25, 28, 31, 44, 50, 53, 56, 66, 71, 74, 75, 80, 95, 97, 112, 134, 136, 139]. A total of 32 studies did not report raw HRQoL data and consequently could not be used for meta-analysis [21, 25, 27, 29, 32, 34, 35, 38, 40, 4446, 4951, 53, 56, 58, 66, 71, 75, 86, 95, 97, 112, 118, 128130, 134, 136, 139]. The other 17 papers reported HRQoL data only in graphical form, which impedes meta-analysis [61, 64, 70, 7274, 87, 90, 110, 113, 118, 121, 124, 128130, 137]. Furthermore, although most studies reported the statistical methods, they used to analyse HRQoL, only 6 publications used a pre-specified statistical analysis plan addressing common methodological problems in HRQoL analysis [41, 43, 103, 104, 108, 125]. Finally, nine publications combined patient groups undergoing different treatment options (surgery/medical therapy/interventional treatment) for the reporting of HRQoL outcomes. In these cases, assignment of HRQoL outcomes to a specific treatment (surgery vs. medical therapy vs interventional treatment) was impossible [28, 42, 56, 58, 87, 88, 120, 127, 132]. In summary, only three studies remained for quantitative analyses (Fig. 3 step 3).
Supplement 4 illustrates the discrepancy between supposedly available and reported data for the FACT-Hep (A/B) and EORTC QLQ-C30 (C/D) HRQoL instruments.

Data synthesis for HRQoL tools

For generic HRQoL instruments like the SF-36, EQ-5D or WHO-BREF, no meta-analysis following treatment was possible, either because primary data were insufficiently reported (supplement 4) or only single articles reporting raw data were identified. Similarly, for cancer (type)-specific HRQoL tools like EORTC QLQ-C30, EORTC QLQ-HCC18 and QLQ-LC meta-analysis of HRQoL data, the following treatment was impeded by either insufficient reporting during follow-up (supplement 3), or studies compared interventions that were too heterogeneous for meta-analysis. Only for the FACT-G and FACT-Hep questionnaires, clinically comparable interventions were analysed in several studies: Six studies contained surgical study groups [35, 37, 43, 81, 99, 116], two studies contained data on RFA [37, 116], and 5 studies reported extractable data in TACE patients [73, 99, 103, 116, 123]. Although FACT-G or FACT-Hep was used in several studies investigating medical treatment options for HCC, these were either single-arm studies [32, 34, 94], contained placebo control groups [31, 36, 38, 53, 137] or compared two medical treatment options [72, 136], thus, precluding a comparison to interventional/surgical treatments. Similarly, some studies used the FACT-G or FACT-Hep questionnaire to compare different interventional treatments [73, 103, 116, 122], again impeding meta-analysis. Consequently, only 3 studies using the FACT-G/FACT-Hep remained for meta-analysis (Fig. 3 step 3).

Meta-analyses

For the comparison of surgical resection vs. TACE, only two studies reported raw data at baseline and during follow-up [99, 116] (supplement 5A). Poon et al. split the surgical cohort into two distinct subgroups: those with a complete follow-up of two years and those with a shorter follow-up. This is likely to introduce major bias as patients completing 2-year follow-up are likely to be healthier and have less aggressive tumour diseases. We, therefore, pooled the data for the two surgical groups. Supplement 5A shows the results of this exploratory meta-analysis of the mean difference in FACT-subscores (functional, physical, social and emotional well-being) at 12-month post-intervention/surgery. One additional analysis was possible: the comparison of surgery vs. RFA as data are reported in the two studies by Huang et al. and Toro et al. [37, 116]. Supplement 5B shows the results of the exploratory meta-analysis for the 12-month post-interventional/postoperative follow-up, again comparing mean differences in FACT-subscores.

Discussion

HRQoLs represent an important domain of clinical outcomes in oncology. While definitions, implementation, evaluation and analyses of survival and toxicity/complication endpoints have been well standardized over the last decades, PROs are still under-evaluated and reported in most clinical settings. Multiple studies have aimed to define suitable HRQoL tools for different clinical settings, e.g. [4, 5], including cancer patients [68]. However, no concise evaluation has been performed for patients with primary liver cancers (HCC or CCA).
Although 124 studies were included in this systematic review, we were able to complete only the first two objectives of our study, namely to identify and evaluated HRQoL measures in HCC/CCA patients. However, meta-analysis of study results comparing the outcome of surgical, interventional or medical treatments for HCC/CCA patients in regard to HRQoL was barely possible due to the use of different HRQoL instruments, lack of data or insufficient reporting.
We identified 29 different HRQoL instruments, which indicate vast heterogeneity and lack of consensus in this field. Similar results have been reported before in other diseases [68]. Furthermore, many of the identified tools lacked basic HRQoL characteristics like multidimensionality [154, 155]. Hence many authors seemed to be unaware of the difference between mere symptom measures and HRQoL instruments. In addition, validation of HRQoL is poor for most instruments in HCC/CCA patients (Table 2). As expected, the best psychometric data were available for cancer-type-specific HRQoL instruments, like EORTC QLQ-HCC18 or the FACT-Hep. Interestingly, even for common generic and disease-specific HRQoL tools, like the Spitzer quality of life index and the EORTC QLQ-C30, data in HCC/CCA patients are sparse. Hence, evaluation of these common tools in this patient cohort seems necessary in future studies. In addition, even for HRQoL measures developed especially for liver cancer patients, psychometric properties were less stringent as might have been thought. The EORTC QLQ-HCC18 shows mixed psychometric results [41, 88]. FACT-Hep, on the other hand, although showing good psychometric properties, has been validated only in mixed patient populations including patients with liver metastases and pancreatic cancer in addition to HCC/CCA patients [144, 147]. Similarly, the preference-based HRQoL EQ-5D has been extensively evaluated in chronic liver disease, but little psychometric data are available in HCC/CCA patients. Future studies should address these shortcomings.
Nevertheless, our analysis revealed suitable HRQoL instruments with sound psychometric properties that should be used in all future HRQoL studies. These are SF-36 [156] for generic HRQoL measurement. The SF-36 is a generic HRQoL instrument consisting of 36 items divided into eight scales (Physical Functioning, Emotional Role Functioning, Physical Role Functioning Bodily Pain, General Health, Vitality, Social Functioning, Mental Health, Health Transition) [156]. The number of response choices per item ranges from two to six. The scores for each scale range from 0 to 100. A higher score indicates a better QOL. The time frame of the SF-36 is ‘last week’ [141].
For cancer-specific HRQoL measurement in HCC/CCA patients, the EORTC QLQ-C30 [157] and the FACT-G can be recommended. Both have limited, but acceptable psychometric properties in HCC/CCA patients and have been used extensively in this patient cohort. The 30-item QLQ-C30 measures five functional scales (physical, role, emotional, cognitive and social functioning), global health status, financial difficulties and eight symptom scales (fatigue, nausea and vomiting, pain, dyspnoea, insomnia, appetite loss, constipation and diarrhoea). The scores vary from 0 (worst) to 100 (best) for the global health status and functional scales, and from 0 (best) to 100 (worst) for symptomatic scales [157]. The FACT-G consists of 27 items for the assessment of four domains of QOL: (1) Physical Well-Being and (2) Socio-Family Well-Being contain seven items each; (3) Emotional Well-Being contains six items and (4) Functional Well-Being contains seven items. The time frame of the FACT-G is ‘last week’. Each item is scored on a 5-point ordinal scale, where 0 indicates not at all and 4, very much [152].
Cancer-type-specific HRQoL should be measured via the EORTC QLQ-HCC18 or FACT-Hep. The EORTC QLQ-HCC18 is an 18-item HCC-specific supplemental module developed to augment QLQ-C30 and to enhance the sensitivity and specificity of HCC-related QOL issues. It contains six multi-item scales addressing fatigue, body image, jaundice, nutrition, pain and fever, as well as two single items addressing sexual life and abdominal swelling. The scales and items are linearly transformed to a 0 to 100 score, where 100 represents the worst status [28, 88]. The FACT-Hep is a 45-item self-reported instrument that consists of the 27-item FACT-G (see above), and the 18-item hepatobiliary cancer subscale, which assesses specific symptoms of hepatobiliary cancer and side effects of treatment. The FACT-G and hepatobiliary cancer subscale scores are summed to obtain the FACT-Hep total score [37, 144]. The QoL-LC questionnaire shows good psychometric properties but has been developed and tested exclusively in Chinese patients, thus, limiting its generalizability. Similarly, NIDDK-QA as a cancer-type–specific HRQoL tool has been used in only one study and, thus, cannot be recommended currently.
For utility-based HRQoL measurement, the EQ-5D [158] has been identified as the instrument of choice. It fulfils basic psychometric requirements, and a sound database is available in HCC/CCA patients. The EQ-5D consists of five items (mobility, self-care, usual activities, pain/discomfort and anxiety/depression). Each item has three response categories: no problems, some problems and extreme problems. The sixth item is a global health evaluation scale, ranging from 0 (the worst imaginable health state) to 100 (the best imaginable health state). The time frame of the EQ-5D instrument is the present moment.
The quality reporting of the HRQoL results was insufficient overall. Few trials reported common methodological problems of HRQoL data like multiple testing, missing data or a priori hypothesis. Raw data were rarely reported and summarize measures (mean, median etc.) as well as follow-up regimes varied widely between studies. In addition, the methodological quality of the studies was generally poor. Thus, despite a total of 124 studies available, evidence regarding HRQoL in HCC/CCA patients is limited.
It is astonishing that reporting of HRQoL data does not seem to have improved over the last decades despite the publication of multiple guidelines and recommendations concerning HRQoL reporting. Few of the included studies fulfiled basic reporting standards for HRQoL like the ones proposed by Basch et al. [159], Staquet et al. [160], the International Society for QoL research (ISOQOL) [161] or the CONSORT—Patient-reported outcome extension [162].
These shortcomings in the methodological quality and reporting were the main reasons for the insufficient meta-analyses in our study. Studies had to be excluded at various points along the way (Fig. 3). The planned comparison of treatment options (surgery vs. medical treatment vs. interventional treatment) with regard to HRQoL can, therefore, be regarded exploratory at best. Future, high-quality HRQoL trials, adhering to basic reporting standards, are urgently needed to address these shortcomings.
One of the main strengths of the current study is the use of a comprehensive search strategy to identify all relevant publications. Furthermore, to our knowledge, this is the first study that assesses the methodological quality of HRQoL tools in HCC/CCA patients according to internationally accepted standards time [3, 15, 16] thereby identifying suitable HRQoL instruments for the use in future studies. In addition, this study can be used as an easy reference standard to identify available studies and raw data for the design and sample size calculation in future HCC/CCA trials. The transparent analysis process in this study can be regarded as a further strength.
The main limitation of our analysis is the heterogeneity of included studies, patients and trial designs. The variations in the application, analyses and reporting of HRQoL between studies made data synthesis difficult. The meta-analyses should regarded exploratory at best.
In summary, clear recommendations for generic, cancer-specific, cancer-type-specific and preference-based HRQoL instruments in HCC/CCA patients can be given. Meta-analysis of data comparing different treatment options in HCC/CC patients was severely limited due to methodological weaknesses of the included studies and shortcomings in reporting. Future trials should address these aspects and adhere to HRQoL reporting standards.

Declarations

Conflict of interest

All authors declare no conflict of interest.

Ethical approval

Not applicable.
Not applicable.
Not applicable.
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Metagegevens
Titel
Health-related quality of life in primary hepatic cancer: a systematic review assessing the methodological properties of instruments and a meta-analysis comparing treatment strategies
Auteurs
Kerstin Wohlleber
Patrick Heger
Pascal Probst
Christoph Engel
Markus K. Diener
André L. Mihaljevic
Publicatiedatum
20-07-2021
Uitgeverij
Springer International Publishing
Gepubliceerd in
Quality of Life Research / Uitgave 9/2021
Print ISSN: 0962-9343
Elektronisch ISSN: 1573-2649
DOI
https://doi.org/10.1007/s11136-021-02810-8