Feasibility and Utility of Incorporating Patient-Reported Outcomes into Surveillance Strategies for Advanced Lung Cancer

Figures & data

Table 1 Identified Literature Overview

	Author	Year	Study Type	Patient Number	Treatment	Methods	PROs Outcomes	Results	Category
1	King-Kallimanis et al^Citation56	2018	Randomized controlled trials	695	Anti-PD-1/PD-L1	EORTC QLQ-C30, EORTC LC-13, LCSS baseline and after 3 months	Examine age-related differences in patient-reported symptoms and functional domains	No large differences at baseline or in the distributions of change from baseline in PROS between younger and older patients	C4
2	Wu et al^Citation68	2018	Randomized controlled trials	301	Afatinib vs chemotherapy	EORTC QLQ-C30 every 21 days until progression	EGFR Mutation Type Influence patient-reported outcomes	First-line afatinib improved lung cancer-related symptoms and GHS/QoL compared with chemotherapy	C1
3	Bordoni et al^Citation57	2018	Randomized controlled trials	850	Atezolizumab or docetaxel	EORTC QLQ-30, EORTC LC-13 day 1 of every cycle and at treatment discontinuation	Evaluate the QoL of patient treated with atezolizumab or docetaxel	PROS data support the clinical benefit of atezolizumab in patients with previously treated advanced or metastatic NSCLC	C4
4	Lee et al^Citation59	2018	Randomized controlled trials	419	Osimertinib Versus Chemotherapy	EORTC QLQ-30, EORTC LC-13 baseline, 3 months, 1 year	Evaluate the QoL of patient treated with Osimertinib or Chemotherapy	A higher proportion of patients treated with osimertinib had improvement in global health status/quality of life	C4
5	Walker et al^Citation40	2017	Prospective observational	145	Platinum-based doublets including combinations with bevacizumab or pemetrexed	EORTC QLQ-30, EORTC LC-13, MDASI, RALS baseline,1 year	Effect of Brain Metastasis on patient reported outcomes	PROSmeasures show disease progression is associated with worsening HR QoL. Delaying disease progression can sustain better HRQL and reduce symptom burden	C2
6	McCarrier et al^Citation62	2017	Prospective observational	51	Routine cancer care	NSCLC-SAQ	Development of a patient reported outcome Instrument	NSCLC-SAQ is currently undergoing quantitative testing to confirm its measurement properties and support FDA qualification	C6
7	Blackhall et al^Citation52	2015	Post hoc analysis	343	Crizotinib vs chemotherapy	EORTC QLQ-30, EORTC LC-13, EQ-5D baseline, day 1 of each cycle and end of treatment	Evaluate the QoL of patient treated with crizoinib or Chemotherapy	The benefits of crizotinib in improving symptoms and QoL are demonstrated regardless of whether the comparator is pemetrexed or docetaxel	C3
8	LeBlanc et al^Citation53	2016	Prospective observational	97	Chemotherapy or palliative	Electronic patient-reported outcomes: Patient Care Monitor Patient Care Monitor(PCM) v2.0 four assessments in 6 months	Characterized patients’ symptoms	Patients with aNSCLC face a significant symptom burden, which increases with proximity to death	C3
9	LeBlanc et al^Citation41	2015	Prospective observational	99	Routine cancer care	FACT - G, FACT - L, FACT - F, FAACT four assessments in 6 months	Correlation between CACS and PROs	The weight-based definition is useful in identifying patients with advanced NSCLC who are likely to have significantly inferior survival and who will develop more precipitous declines in physical function and QoL	C2
10	Von Verschuer et al^Citation51	2017	Prospective observational	1239	Carboplatin or cisplatin based doublet chemotherapy	EORTC QLQ-30, EORTC LC-13 each visit, any change in treatment or every 6 months	Evaluate the QoL of patient treated with carbo or cisplatin	HR QoL data comparing treatments show no difference between carboplatin and cisplatin	C3
11	Shallwani et al^Citation50	2016	Observational	47	First line chemotherapy	SF-36,LCS, SCFS, PG-SGA pre and post chemotherapy	Identify predictors of change in HR QOL in patients undergoing chemotherapy	Pre-chemotherapy 6MWT distance and fatigue severity predicted change in the mental component of HR QOL in patients with advanced NSCLC undergoing chemotherapy, while physical performance declined during treatment	C3
12	Sebastian et al^Citation34	2018	Randomized controlled trials	161	Chemotherapy vs osimertinib	PRO-CTCAE first weekly for 18 weeks and then every 3 weeks for up to 57 weeks	Evaluate the QoL of patient treated with chemo or osimertinib	Symptoms were generally mild and not frequent, with some differences in symptom patterns between the two treatment groups	C1
13	Brady et al^Citation65	2017	Prospective observational	72	Surgery, radiotherapy, chemotherapy	EAT-10, SWAL- QOL	Impact of dysphagia on QOL	Dysphagia is a potential symptom in advanced lung cancer which may impact QOL	C3
14	Walker et al^Citation49	2017	Prospective observational	147	First line (±bevacizumab)	EORTC QLQ-C30, EORTC QLQ-LC13, MDASI-LC, RALS every cycle during active treatment and monthly in fu for up to 1 year	Impact of disease progression on effectiveness outcomes and QoL	Newly diagnosed advanced NSCLC patients with baseline BM experienced a significantly faster and clinically meaningful deterioration in PRO-based HR QOL compared with those without baseline BM	C3
15	Felip et al^Citation48	2017	Randomized controlled trials	795	1ʹ Platinum-Based Chemotherapy, 2ʹ Afatinib Versus Erlotinib	EORTC QLQ-C30, EORTC QLQ-LC13 first visit of each treatment at the end of treatment, and 28 days after treatment	Evaluate the QoL of patient treated with afatinib or erlotinib	Significantly more patients who received afatinib versus erlotinib experienced improved scores for GHS/QoL	C3
16	Brahmer et al^Citation58	2017	Randomized controlled trials	299	Pembrolizumab vs chemotherapy	EORTC QLQ-C30, EORTC QLQ-LC13, EQ-5D baseline and w15	Evaluate the QoL of patient treated with pembrolizumab or chemotherapy	Pembrolizumab improves or maintains health-related QOL compared with that for chemotherapy	C4
17	Reck et al^Citation66	2018	Randomized controlled trials	582	Nivolumab or docetaxel	LCSS, EQ-5D at baseline, on day 1 of every other cycle for 6 months, two follow-up visits after treatment discontinuation; EQ-5D assessments continued every 3 months for 12 months and then every 6 months thereafter	Evaluate the QoL of patient treated with nivolumab or docetaxel	Nivolumab improved disease-related symptoms and overall health status versus docetaxel for second-line treatment of advanced non-squamous NSCLC	C3
18	Denis et al^Citation43	2017	Randomized controlled trials	60	Chemotherapy or tyrosine kinase inhibitor	E-FAP every three months	Web-mediated follow-up (SR) improved OS due to early relapse detection and better PS at relapse	A web-mediated follow-up algorithm based on self-reported symptoms improved OS due to early relapse detection and better performance status at relapse	C2
19	Sztankay et al^Citation36	2017	Prospective observational	83	First-line palliative chemotherapy	EORTC QLQ-C30, EORTC QLQ-LC13 each chemotherapy cycle to the start of second-line palliative chemotherapy or at study completion	Symptom severity during MT compared with first-line therapy	HR QOL and symptom burden improve between first-line treatment to MT, the integration of patient-reported outcomes is required to enable shared decision-making and personalised healthcare	C1
20	Sloan et al^Citation42	2016	Prospective observational	1466	Surgery, chemotherapy, radiotherapy	NCCTG, EORTC QLQ-LC13, FACT - L, LCSS follow-up	Correlation between being physically active and QOL	Being physically active was related to profound advantages in QOL and survival in a large sample of lung cancer survivors	C2
21	Wang et al^Citation61	2016	Prospective observational	92	IMRT, BPT, 3DCRT, chemoradiotherapy	MDASI baseline, weekly during and after therapy for up to 12 weeks	Valutate MDASI ability to detect symptom	Patients receiving PBT reported significantly less severe symptoms than did patients receiving IMRT or 3DCRT	C5
22	Spigel et al^Citation67	2019	Randomized controlled trials	1426	Nivolumab	EQ-5D, LCSS every 3 months for the first 12 months, then every 6 months	Evaluate the QoL of patient treated with nivolumab	The median overall survival for patients with an ECOG PS of 2 was lower than for the overall population but comparable with historical data	C1
23	Nguyen et al^Citation46	2018	Prospective observational	32	Concurrent chemoradiation	EORTC QLQ-C30 baseline, during therapy, at therapy stop and till 1 year after therapy end every 3 months	Evaluate the QoL of patient treated with concurrent chemoradiation	Measuring PROs can help to identify issues for improvement of the value of care delivered	C3
24	Mendoza et al^Citation60	2019	Prospective observational	460	Treatment-naïve	MDASI between 30 days prediagnosis and 45 days postdiagnosis	Assessment of baseline QoL for palliative therapy evaluation, disease-related symptoms differentation and control	Quantification of pretreatment symptom burden can inform patient-specific palliative therapy and differentiate disease-related symptoms from treatment-related toxicities. Poorly controlled symptoms could negatively affect treatment adherence and therapeutic outcomes	C5
25	Novello et al^Citation47	2015	RANDOMIZED controlled trials	1314	Nintedanib plus docetaxel vs placebo plus docetaxel	EORTC QLQ-C30, EORTC QLQ-LC13, EQ-5D, EQ-5D screening, day 1 of each cycle, at the end of active treatment, first FU	Evaluate the QoL of patient treated with second-line nintedanib	The significant OS benefit observed with the addition of nintedanib to docetaxel therapy was achieved with no detrimental effect on patient self-reported QoL	C3
26	Pèrol et al^Citation44	2016	Randomized controlled trials	1253	Ramucirumab plus docetaxel vs placebo plus docetaxel	LCSS baseline, every 3-week cycle, the summary visit,and at the 30-day FU	Evaluate the QoL of patient treated with ramucirumab plus docetaxel vs placebo plus docetaxel	Adding ramucirumab to docetaxel did not impair patient QoL, symptoms, or functioning	C3
27	Boye et al^Citation45	2016	Randomized controlled trials	218	Pemetrexed plus cisplatin followed by gefitinib maintenance therapy or gef monotherapy	LCSS baseline, at each study visit, after discontinuation	Evaluate the QoL of patient treated with pemetrexed plus cisplatin followed by gef maintenance therapy or gef monotherapy	LCSS scoresn were more favorable in the G group than in the PC/G group	C3
28	Wood et al^Citation54	2019	Prospective observational	1030	First line	EQ-5D, WPAI:GH, EORTC QLQ-C30 (+ZBI for caregivers)	Linking patient clinical factors to patient and caregiver burden	As patients’ functionality deteriorates as measured by the ECOG-PS, so do their outcomes related to health utility, work productivity, activity impairment and HR QoL. This deterioration is also reflected in increased caregiver burden and activity impairment	C3
29	Barlesi et al^Citation55	2019	Randomized controlled trials	1034+427 caregivers	Pembrolizumab vs Docetaxel	EORTC QLQ-C30, EORTC QLQ-LC13, EQ-5D cycles 1, 2, 3, 5, and every 4 cycles until discontinuation and30-day safety assessment	Evaluate the QoL of patient treated with pembrolizumab vs docetaxel	HR QoL and symptoms are maintained or improved to a greater degree with pembrolizumab than with docetaxel	C4
30	Geater et al^Citation35	2015	Randomized controlled trials	364	Afatinib or gemcitabine followed by cisplatin d1 and gem d8	EORTC QLQ-C30, EORTC QLQ-LC13 randomization and every 3 weeks until PD or start of new treatment	Evaluate the QoL of patient treated with Afatinib Versus Cisplatin/Gemcitabine	Afatinib improved PFS and PROs versus chemotherapy in EGFR mutation-positive NSCLC patients. Progression was associated with statistically significant worsening in QoL	C1
31	Reck et al^Citation39	2019	Randomized controlled trials	583	Nivolumab plus ipilimumab versus chemotherapy	LCSS, EQ-5D baseline, w6, w12, w18, w24, w30, w36	Evaluate the QoL of patient treated with nivolumab plus ipilimumab versus chemotherapy	First-line nivolumab þ ipilimumab demonstrated early, sustained improvements in PROs versus chemotherapy	C2
32	Kawata et al^Citation38	2019	Randomized controlled trials	208	Two dosing regimens of brigatinib	EORTC QLQ-C30 every cycle	Evaluate the impact of brigatinib treatment on health utilities using two published algorithms	Converting QLQ-C30 scores into utilities in trials using established mapping algorithms can improve evaluation of medicines from the patient perspective. Both algorithms suggested that brigatinib improved health utility in crizotinib-refractory ALK + NSCLC patients	C1
33	McGee et al^Citation37	2018	Retrospective observational	528	Surgery, chemotherapy, radiotherapy	ESAS prior to each outpatient consultation	ESAS scale to identify patient-reported factors that may predict for treatment decisions in advanced NSCLC	Novel role for the ESAS as a prognostic tool that could complement existing patient assessment models	C1

Abbreviations: CACS, Cancer Anorexia-Cachexia Syndrome; 6MWT, 6-minWalk Test; BM, brain Metastasis; GHS, global Health Status; MT, maintenance Therapy; PC/G, maintenance Gefitinib; G, gefitinib Monotherapy; IMRT, Intensity-Modulated Radiation Therapy; 3DCRT, three-Dimensional Conformal Radiation Therapy; PBT, Proton-Beam Therapy; C1, PROs as Guide in Therapeutic Choice; C2, PROs as Indicator of Disease Progression; C3, Agreement Between PROs and the Evaluated Parameter; C4, PROs to Evaluate the Effects of Immunotherapy; C5, Need to Deepen the Knowledge of PRO; C6, Use of a New Electronic PRO.

Figure 1 Flowchart of study selection.

Table 2 Results Classification in Categories About the Topic of the Article

Topic	Number of Studies
PROs as guide in therapeutic choice	7
PROs as indicator of disease progression	5
Agreement between PROs and the evaluated parameter	13
PROs to evaluate the effects of immunotherapy	5
Need to deepen the knowledge of PRO	2
Use of a new electronic PRO	1

Abbreviation: PROs, Patient-Reported Outcomes.

Table 3 Literature Data

Author	Number of Patients Complied PROs (%)	Compliance	Results
King-Kallimanis et al^Citation56	695 (100)	90–80% >95%	No large differences at baseline or in the distributions of change from baseline in PROs between younger and older patients
Wu et al^Citation68	301(100)	90%	First-line afatinib improved lung cancer-related symptoms and GHS/QoL compared with chemotherapy
Bordoni et al^Citation57	850(100)	>95%, >80%	PROs data support the clinical benefit of atezolizumab in patients with previously treated advanced or metastatic NSCLC
Lee et al^Citation59	419(100)	88–72% 60%	A higher proportion of patients treated with osimertinib had improvement in global health status/quality of life
Walker et al^Citation40	145(100)	98%	PROs measures show disease progression is associated with worsening HR QOL. Delaying disease progression can sustain better HRQL and reduce symptom burden
McCarrier et al^Citation62	10(19.6)	nr	NSCLC-SAQ is currently undergoing quantitative testing to confirm its measurement properties and support FDA qualification
Blackhall et al^Citation52	343(100)	83–100%	The benefits of crizotinib in improving symptoms and QOL are demonstrated regardless of whether the comparator is pemetrexed or docetaxel
LeBlanc et al^Citation53	97(100)	nr	Patients with a NSCLC face a significant symptom burden, which increases with proximity to death
LeBlanc et al^Citation41	99(100)	nr	The weight-based definition is useful in identifying patients with advanced NSCLC who are likely to have significantly inferior survival and who will develop more precipitous declines in physical function and QOL
von Verschuer et al^Citation51	495(39.96)	87–68%	HR QOL data comparing treatments show no difference between carboplatin and cisplatin
Shallwani et al^Citation50	47(100)	nr	Pre-chemotherapy 6MWT distance and fatigue severity predicted change in the mental component of HR QOL in patients with advanced NSCLC undergoing chemotherapy, while physical performance declined during treatment
Sebastian et al^Citation34	161(100)	nr	Symptoms were generally mild and not frequent, with some differences in symptom patterns between the two treatment groups
Brady et al^Citation65	72(100)	nr	Dysphagia is a potential symptom in advanced lung cancer which may impact QOL
Walker^Citation49	147(100)	98%	Newly diagnosed advanced NSCLC patients with baseline BM experienced a significantly faster and clinically meaningful deterioration in PRO-based HR QOL compared with those without baseline BM
Felip et al^Citation48	795(100)	95%	Significantly more patients who received afatinib versus erlotinib experienced improved scores for (GHS)/QoL.
Brahmer et al^Citation58	299(100)	90–80%	Pembrolizumab improves or maintains health-related QOL compared with that for chemotherapy
Reck et al^Citation66	582(100)	98%	Nivolumab improved disease-related symptoms and overall health status versus docetaxel for second-line treatment of advanced non-squamous NSCLC
Denis et al^Citation43	60(100)	nr	A web-mediated follow-up algorithm based on self-reported symptoms improved OS due to early relapse detection and better performance status at relapse
Sztankay et al^Citation36	83(100)	84%	HR QOL and symptom burden improve between first-line treatment to MT, the integration of patient-reported outcomes is required to enable shared decision-making and personalized healthcare
Sloan et al^Citation42	1466(100)	nr	Being physically active was related to profound advantages in QOL and survival in a large sample of lung cancer survivors
Wang et al^Citation61	92(100)	96%	Patients receiving PBT reported significantly less severe symptoms than did patients receiving IMRT or 3DCRT
Spigel et al^Citation67	1426(100)	80%	The median overall survival for patients with an ECOG PS of 2 was lower than for the overall population but comparable with historical data
Nguyen et al^Citation46	32(100)	nr	Measuring PROs can help to identify issues for improvement of the value of care delivered
Mendoza et al^Citation60	460(100)	nr	Quantification of pretreatment symptom burden can inform patient-specific palliative therapy and differentiate disease-related symptoms from treatment-related toxicities. Poorly controlled symptoms could negatively affect treatment adherence and therapeutic outcomes
Novello et al^Citation47	1051(79.98)	70%	The significant OS benefit observed with the addition of nintedanib to docetaxel therapy was achieved with no detrimental effect on patient self-reported QoL
Pèrol et al^Citation44	1253(100)	75%	Adding ramucirumab to docetaxel did not impair patient QoL, symptoms, or functioning
Boye et al^Citation45	236(100)	92%	LCSS scores were more favorable in the G group than in the PCnrG group
Wood et al^Citation54	1030(100)	nr	As patients’ functionality deteriorates as measured by the ECOG-PS, so do their outcomes related to health utility, work productivity, activity impairment and HR QoL. This deterioration is also reflected in increased caregiver burden and activity impairment
Barlesi et al^Citation55	1034+427 (100)	95–85%	HR QoL and symptoms are maintained or improved to a greater degree with pembrolizumab than with docetaxel
Geater et al^Citation35	364(100)	96–88%	Afatinib improved PFS and PROs versus chemotherapy in EGFR mutation-positive NSCLC patients. Progression was associated with statistically significant worsening in QoL
Reck et al^Citation39	583(100)	90–80%	First-line nivolumab vs ipilimumab demonstrated early, sustained improvements in PROs versus chemotherapy
Kawata et al^Citation38	208(100)	nr	Converting QLQ-C30 scores into utilities in trials using established mapping algorithms can improve evaluation of medicines from the patient perspective. Both algorithms suggested that brigatinib improved health utility in crizotinib-refractory ALK + NSCLC patients
McGee et al^Citation37	528(100)	nr	Novel role for the ESAS as a prognostic tool that could complement existing patient assessment models

Abbreviations: CACS, Cancer Anorexia-Cachexia Syndrome; 6MWT, 6-minWalk Test; BM, brain metastasis; GHS, global Health Status; MT, maintenance Therapy; PCnrG, maintenance Gefitinib; G, gefitinib Monotherapy; IMRT, Intensity-Modulated Radiation Therapy; 3DCRT, three-Dimensional Conformal Radiation Therapy; PBT, Proton-Beam Therapy; Nr, not reported.

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