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AmbuFlex/WestChronic, Occupational Medicine, University Research Clinic, Aarhus University, Herning, DenmarkDepartment of Clinical Epidemiology, Aarhus University Hospital, Aarhus, Denmark
Patient-reported outcome (PRO) measures have been increasingly implemented in routine care to aid in clinical decision-making. However, the prognostic value of PRO measures as a tool for decision making is not easily interpreted by clinicians. Our aims were to explore the prognostic value of PRO measures at disease progression and the changes in PRO measures between treatment start (baseline) and disease progression.
Patients and Methods
Since 2014, patients with lung cancer have completed an electronic version of the European Organization for Research and Treatment of Cancer Quality of Life Questionnaires C30 and LC-13 before every outpatient visit at the Department of Oncology, Hospital Unit West, Jutland, Denmark. The patients’ responses were used in routine care. Patients receiving palliative antineoplastic treatment were eligible for analysis if the questionnaire had been completed at the initiation of first-line treatment and at disease progression. The prognostic value of the scores was evaluated using a Cox proportional hazard model. A P value < .01 was considered statistically significant.
Results
A total of 94 screened patients were included. At disease progression, survival could be predicted from the absolute score of the global health scale, 3 functional scales (physical, role, emotional), and 7 symptom scales (fatigue, pain, dyspnea, hemoptysis, lung cancer dyspnea, chest pain). In addition, changes in hemoptysis, dysphagia, dyspnea, and chest pain predicted for survival at progression.
Conclusion
PRO measures used in routine care can provide clinicians with relevant prognostic information about patients with lung cancer at disease progression. These results show the potential value of PRO measures when used in clinical decision-making.
NORDCAN: Cancer Incidence, Mortality, Prevalence and Survival in the Nordic Countries, version 7.3 (08.07.2016). Association of the Nordic Cancer Registries. Danish Cancer Society.
The early initiation of palliative care has previously shown to prolong survival, improve quality of life (QoL), and lead to less aggressive care at the end of life for patients with lung cancer.
In this context, the point of disease progression is a key time in the course of the disease. Disease progression means that the current treatment has stopped being efficient, and important decisions are required concerning whether to start second-line antineoplastic treatment or withdraw active treatment and transition to palliative care. Such essential decisions must involve reflections on the patient’s perceived symptoms and individual preferences.
In routine care, clinicians rate the patient’s functional level using the performance status score. This clinician-rated score is used to guide decision-making because it has been shown to correlate closely with prognosis and antineoplastic treatment tolerance.
However, clinicians tend to underestimate or overlook symptoms during routine consultations, which can impair such clinician-rated assessments of patients.
The use of patient-reported outcome (PRO) measures could address some of these issues. When used in routine care, these measures have been shown to improve communication, patient and clinician satisfaction, symptom control, and, even, survival.
Using patient-reported outcome measures to deliver enhanced supportive care to people with lung cancer: feasibility and acceptability of a nurse-led consultation model.
What is the value of the routine use of patient-reported outcome measures toward improvement of patient outcomes, processes of care, and health service outcomes in cancer care? A systematic review of controlled trials.
Health-related quality of life in small-cell lung cancer: a systematic review on reporting of methods and clinical issues in randomised controlled trials.
Quality of life supersedes the classic prognosticators for long-term survival in locally advanced non-small-cell lung cancer: an analysis of RTOG 9801.
Although PRO measures collected as endpoints in clinical trials have been widely analyzed, less attention has been given to confirm their prognostic value when used as a decision-making tool to predict the individual patient’s survival during routine care. Such information could help guide clinicians and patients to decide which treatment strategy would be best. Also, to the best of our knowledge, no studies have used disease progression as the key point in time to study the PRO measures used for clinical decision-making.
The present study explored the prognostic value of PRO measures completed at disease progression and changes in the PRO measures between treatment start (baseline) and disease progression.
Patients and Methods
PRO Measures in Routine Care
Electronic PRO measures have been applied in routine care in the Department of Oncology, Hospital Unit West Jutland, Denmark, since 2014. All patients with lung cancer are encouraged to complete an electronic version of the European Organization for Research and Treatment of Cancer (EORTC) quality of life questionnaires (QLQs) C30 and LC13 before every outpatient visit.
The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
Symptom severity and functional impairment are represented by color bars to the clinicians in the electronic medical records, providing an easy overview of longitudinal symptom development. This information is used by clinicians for decision support and symptom monitoring. All PRO data analyzed in the present study were collected prospectively during routine care.
Patients
The patients screened for eligibility included patients with lung cancer who had received first-line palliative antineoplastic treatment in the Department of Oncology, Hospital Unit West Jutland, from 2014 to 2018, with ≥1 completed PRO questionnaire available.
The inclusion criteria were (1) non–small-cell lung cancer and small-cell lung cancer (SCLC); (2) stage III or IV disease in first-line palliative antineoplastic treatment within the defined study period, and (3) PRO questionnaire completion at the initiation of first-line antineoplastic therapy and at the date of disease progression.
Patients were excluded from the analyses if (1) the date of disease progression was uncertain, (2) the questionnaire had been completed > 14 days before the date of determined disease progression, or (3) the questionnaire had been completed after the results of the computed tomography scan had been communicated. The latter criterion was used to avoid having the assessments be influenced by the patient’s knowledge of the scan result showing disease progression before completion.
The electronic medical records of all screened patients were reviewed for clinical information. The baseline data included age, sex, stage, pathologic features, treatment, performance status, and date of treatment initiation. The date of progressive disease was obtained from the electronic medical records, and date of death was obtained from the Danish Central Personal Registry (data extracted July 2, 2019).
Health-Related QLQs
The EORTC QLQ-C30, version 3.0, and the lung cancer-specific QLQ-LC13 questionnaires have proven psychometric properties with high validity and reliability for lung cancer patients.
The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
The QLQ-C30 is a multidimensional 30-item questionnaire consisting of a global health score, 5 function domains (physical, role, cognitive, emotional, social), 8 symptom scales (fatigue, pain, nausea and vomiting, dyspnea, insomnia, appetite loss, constipation, diarrhea), and an item about financial difficulties. The QLQ-LC13 has 10 additional lung cancer-specific symptom scales (lung cancer dyspnea, cough, hemoptysis, sore mouth, dysphagia, peripheral neuropathy, alopecia, pain in chest, arm, or shoulder). All items are graded by the severity experienced during the previous week, and most use a 4-point scale (1, not at all; 2, a little; 3, quite a bit; and 4, very much). The scores were converted to a health-related (HR)QoL scale ranging from 0 to 100 points according to the recommendations from the EORTC scoring manual.
To describe the cohort, the patient characteristics were registered at baseline, defined as the date of first-line treatment initiation. Survival was measured at 2 points: first, as median survival and the interval to progression measured from baseline; and second, as overall survival measured from disease progression to death.
The HRQoL measures were analyzed as continuous variables in the longitudinal mean comparison. A paired t test was used to compare the longitudinal group mean HRQoL score changes between treatment start and disease progression.
A score change of > 10 points was considered the minimal important difference and was used to classify symptom development as deteriorating, stable, or improving.
The prognostic value of the HRQoL scores was evaluated using the Cox proportional hazard model and presented using Kaplan-Meier plots. For the overall survival analysis, patients were dichotomized into 2 categories: patients with symptom deterioration and patients with symptom improvement or stability, measured from treatment initiation to progression. Univariate analyses of overall survival stratified by the change in HRQoL scores were performed for all scales. A median split was used to dichotomize the patients to assess the prognostic value of the absolute HRQoL scores.
To reduce the risk of false-positive results through multiple testing, P < .01 was considered statistically significant. All analyses were performed using the STATA software package, version 16 (StataCorp, College Station, TX).
Study Approval
The present study was conducted as a quality assurance project and internally approved by the department management. According to Danish law, such projects do not require research approval from the health authorities.
Of the 584 screened patients, 94 met the inclusion criteria and were included in the analyses. The reasons for noneligibility are shown in Figure 1. The most common reason for noneligibility was a missing PRO report at disease progression (n = 263). The date of progressive disease could not be determined for 120 patients, either because disease progression had not yet occurred at the study cutoff or because the exact date could not be extracted from the medical records.
Figure 1Flow Chart of Patient Selection. ∗Patients Who Completed the Questionnaire Later Than the Day of First Treatment Were Excluded From the Analyses. ∗∗Patients Who Completed the Questionnaire > 2 Weeks Before the Ambulatory Visit or After the Computed Tomography Results Had Been Communicated Were Excluded From the Analyses
The baseline patient characteristics are listed in Table 1. The median age was 70 years, and 62.8% of the patients were male. For patients who were not eligible for analysis, the median age was 69 years (interquartile range, 65-75 years), and 55% were male.
Table 1Patient Baseline Characteristics
Characteristic
Value
Age, y
Median
70
IQR
64-74
Gender, n (%)
Male
59 (62.8)
Female
35 (37.2)
Total
94 (100.0)
Histologic type, n (%)
SCLC
22 (23.4)
NSCLC
72 (76.6)
Stage, n (%)
IIIb
3 (3.2)
IV
91 (96.8)
First-line treatment, n (%)
Chemotherapy
80 (85.1)
Targeted therapy
5 (5.3)
Immunotherapy
7 (7.4)
Palliative radiotherapy
2 (2.1)
Performance status at baseline, n (%)
0
39 (41.5)
1
38 (40.4)
2
5 (5.3)
3
3 (3.2)
4
0 (0)
NA
9 (9.6)
Time to progression, mo
Median
5.9
IQR
3.0-8.4
Survival from baseline, mo
Median
10.5
IQR
6.6-19.1
Abbreviations: IQR = interquartile range; NA = not available; NSCLC = non–small-cell lung cancer; SCLC = small cell lung cancer.
Of the 94 patients included in the present study, all had received palliative antineoplastic treatment, and most patients (96.8%) had had stage IV lung cancer. The vast majority of patients (85.1%) had received chemotherapy. The median time from treatment initiation to disease progression was 5.9 months. The median overall survival from the initiation of first-line treatment was 10.5 months. At the time of data extraction, 88 patients (93.6%) had died.
Longitudinal Changes in HRQoL Scores
The longitudinal deteriorations in the group mean scores between baseline and disease progression were observed in several HRQoL scales (Table 2). In contrast, no scale scores had improved significantly in the study period. The functional scales were the most sensitive to the changes between first-line treatment and disease progression. The functional scales showing the largest mean deteriorations were physical (−10.5; 95% confidence interval [CI], −14.8 to −6.1; P < .001), role (−11; 95% CI, −17.2 to −4.8; P < .001), and social functioning (−9.8; 95% CI, −15.5 to −4.0; P = .001). The global health score had deteriorated by 7.3 points (95% CI, −12.8 to −1.9; P = .009). For the symptom scales, fatigue (11.5; 95% CI, 6.0-17.0; P < .001) and pain (12.0; 95% CI, 5.5-18.5; P < .001) had the largest mean deterioration. The group mean worsening for nausea and vomiting (4.3; 95% CI, 1.3-7.3; P = .005), alopecia (12.3; 95% CI, 6.2-18.4; P < .001), peripheral neuropathy (9.1, 95% CI, 4.5-13.7; P < .001), and sore mouth (6.2; 95% CI, 1.6-10.7; P = .009) most likely represented adverse effects from chemotherapy. The symptom baseline scores were comparable across gender and histologic type. However, the deteriorations were larger in the non–small-cell lung cancer group than in the SCLC group. Also, we observed that most patients (data not shown) with SCLC experienced initial chemotherapy-induced symptom improvement that later deteriorated toward the onset of progression. For the SCLC group, this resulted in a smaller mean difference between treatment start and progression.
Table 2Mean HRQoL Scores and Group Changes in Scores From Baseline to Progression (n = 94)
How the HRQoL scores for the individual patients changed between treatment start and disease progression are shown in Figure 2, including the development of selected scores of high clinical importance in the palliative treatment of patients with lung cancer. Each line represents an individual patient. The data in Figure 2 show that a large proportion of patients experience symptom deterioration through first line treatment to disease progression, with fewer patients experiencing symptom improvement or stable symptoms. Also, the changes were larger (steeper slopes) for the patients who had experienced deterioration compared with that for patients with improvement. Overall, these observations have confirmed that many patients experience declining health on several scales at disease progression. Of the presented symptoms, the proportion of patients experiencing deterioration was pronounced for global health status, physical functioning, pain, fatigue and dyspnea,. The number of patients with worsening dysphagia was smaller yet highly severe for those experiencing it.
Figure 2Individual Changes in Health-related Quality of Life (HRQoL) Scores Between Treatment Start and Disease Progression. The Time of Confirmed Disease Progression Is Shown on the Right. The Lines Symbolize an Individual Patient's Development in HRQoL Scores From Treatment Start to Disease Progression. The Horizontal Length of the Line Represents the Duration From Treatment Start to Disease Progression. The Slope of the Lines Describes the Altitude of Change in Severity From Treatment Start to Disease Progression. The Colors Illustrate the Direction of Change in the Scores Between Treatment Start and Disease Progression: Red Diamonds, Deterioration; Orange Triangles, Stable Disease; Green Squares, Improvement; Dashed Lines, Minimal Important Difference (>10-point Change From Baseline to Progression). ∗One Patient Was Excluded From the Visual Presentation Because of Long Progression-free Survival
Prognostic Value of Absolute Scores at Disease Progression
The hazard ratios (HRs) computed from the absolute HRQoL scores are presented in Table 3. Three of the four scales providing statistically significant prognostic information according to the HRQoL score changes were also significant when assessed using the absolute scores: dyspnea, hemoptysis and pain in the chest. The absolute score of dysphagia offered no significant information at progression (P = .025). Additionally, 7 other HRQoL scales predicted for survival using the absolute score. These scales were global health, 3 functional scales (physical, role, emotional), and 3 additional symptom scales (fatigue, pain, lung cancer dyspnea; Table 3). Symptoms that are known side effects of chemotherapy (nausea and vomiting, sore mouth, neuropathy, alopecia) were not prognostic for survival.
Table 3Univariate Cox Regression Analysis of Overall Survival Stratified by HRQoL Score
Change of >10 points from baseline to progression recorded as improved/stable for median scores or less and deteriorated for scores greater than the median.
Abbreviations: CI = confidence interval; HR = hazard ratio; HRQoL = health-related quality of life; OS = overall survival.
a Absolute score stratified by the median score.
b Change of >10 points from baseline to progression recorded as improved/stable for median scores or less and deteriorated for scores greater than the median.
Prognostic Value of Changes in HRQoL Scores From Baseline to Progression
Changes in 4 HRQoL scales from treatment start to disease progression were associated with survival (Table 3). This was shown for patients with deterioration in hemoptysis (HR, 3.29; 95% CI, 1.47-7.37; P = .002), dysphagia (HR, 2.54; 95% CI, 1.47-4.37; P = .001), dyspnea (HR, 1.90; 95% CI, 1.21-2.98; P = .004), and pain in the chest (HR, 1.94; 95% CI, 1.17-3.22; P = .008). Survival measured from disease progression is presented using Kaplan-Meier curves in Figure 3 for selected scales. The median survival was more than doubled if no deterioration had occurred compared with that for patients who had experienced symptom worsening. At disease progression, ≥ 50% of all patients had experienced deterioration in terms of physical function, role function, and/or fatigue.
Figure 3Overall Survival From Disease Progression Stratified by Changes in Health-related Quality of Life Score. Deterioration, Symptom Worsening > 10 Points From Baseline to Progression; No Deterioration, Symptom Worsening < 10 Points From Baseline to Progression
In the present explorative study of lung cancer patients completing PRO measures as a part of routine care, we identified specific scales from the QLQ-C30 and LC13 questionnaires that seem to predict a patient’s survival at disease progression. The absolute HRQoL scores predicted survival for several scales, including global health score, physical functioning, fatigue, and pain at disease progression. In addition, previous changes in 4 HRQoL scores (dyspnea, hemoptysis, dysphagia, pain in the chest) predicted for survival at disease progression. Thus, we have demonstrated that PRO measures collected in routine care can provide clinicians with relevant prognostic information, supplementing the standard clinical assessment of patients with lung cancer. Some symptom deterioration had resulted from side effects due to treatment, and other symptoms had less prognostic importance. Such symptoms may still be important to measure; however, clinicians should be informed of the specific properties of the individual scales.
Overall, the change in the HRQoL scores added little prognostic information to that of the absolute scores. These results indicate that the patient’s current health condition at disease progression is more important than any previous change, presumably because a decline in an HRQoL score will not be equally severe for all patients. In addition, 1 study showed that the absolute scores identified patients' most bothersome QoL issues better than did changes in the scores compared with those at the previous visit.
Thus, the absolute HRQoL scores might have higher clinical value than the score changes.
Several studies have reported prognostic significance for HRQoL in patients with advanced or metastatic lung cancer. All the identified studies had used a post hoc analysis of HRQoL data collected to evaluate the effect of an intervention. Most studies had analyzed the baseline HRQoL scores as prognostic factors.
The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
Quality of life supersedes the classic prognosticators for long-term survival in locally advanced non-small-cell lung cancer: an analysis of RTOG 9801.
Quality of life analyses from the randomized, open-label, phase III pointbreak study of pemetrexed-carboplatin-bevacizumab followed by maintenance pemetrexed-bevacizumab versus paclitaxel-carboplatin-bevacizumab followed by maintenance bevacizumab in patients.
Quality of life supersedes the classic prognosticators for long-term survival in locally advanced non-small-cell lung cancer: an analysis of RTOG 9801.
Is a patient’s self-reported health-related quality of life a prognostic factor for survival in non-small-cell lung cancer patients? A multivariate analysis of prognostic factors of EORTC study 08975.
Early change in patient-reported health during lung cancer chemotherapy predicts clinical outcomes beyond those predicted by baseline report: results from Eastern Cooperative Oncology Group study 5592.
Early change in patient-reported health during lung cancer chemotherapy predicts clinical outcomes beyond those predicted by baseline report: results from Eastern Cooperative Oncology Group study 5592.
However, to the best of our knowledge, the present study is the first to show that such prognostic properties could also apply to the use of PRO measures in daily clinical decision-making.
An important perspective of our findings was that several functional scales gave significant prognostic information. These scales represent topics that are often highly relevant for patients’ daily living and QoL. Role functioning describes a patient’s ability to work and maintain daily activities during treatment. Such topics might rarely be addressed by clinicians if not directly related to treatment or the disease. Therefore, assessing PRO measures in routine care enables clinicians to increase their awareness on several aspects of a patient’s life, providing a more complete picture of the individual patient. Such highly relevant information should be used and prioritized when evaluating patient preferences in the palliative treatment of metastatic cancer.
A major strength of the present study was that several specific baseline HRQoL scales identified to predict for survival were consistent with those reported by other studies (global health score, physical functioning, pain, dysphagia, dyspnea). Most of the other studies did not include all scales in their analyses. This could explain why some scales (eg, hemoptysis and fatigue) were not identified as prognostic for survival in any of the previous studies. It has generally been accepted that hemoptysis is a severe symptom and, therefore, consistent with the clinical experience of its prognostic value. Patients experiencing a considerable decline in their health condition would be expected to report increased worries. This might explain why the absolute scores of emotional function and insomnia were also prognostic for survival at disease progression. Another strength was that our patients could complete the questionnaires at home in a safe environment and unaffected by the doctor’s interpretation of their symptoms. A final strength of the present results is that the absolute scores and the change in scores predicted for survival on several of the same scales.
A potential weakness of the study was the risk of excluding a group of patients known to experience difficulty in completing electronic questionnaires. The baseline HRQoL scores of the included patients were better than the scores from a reference population of patients with stage IV lung cancer and another population of Scandinavian patients.
This could indicate that patients with worse symptoms completed the questionnaires to a lesser extent than did patients with milder symptoms. However, the baseline scores were highly comparable with the scores from a study describing HRQoL development in patients during maintenance chemotherapy.
Clinical decision-making and health-related quality of life during first-line and maintenance therapy in patients with advanced non-small cell lung cancer (NSCLC): findings from a real-world setting.
The age and gender distributions were similar for the study population and the noneligible patients. Also, a substantial proportion of patients had been excluded because of missing questionnaire completion at disease progression. Some explanations for this are possible. First, the collected PRO measures were used for different clinical purposes, which could have led to misunderstandings among both patients and clinicians. During a course of treatment (eg, chemotherapy every 3 weeks), PRO measures are primarily used to monitor adverse effects and to guide treatment dose modifications. However, for some patients, the therapy will end after a prescheduled number of treatment cycles, and the patients continue with follow-up. In the latter phase, the primary purpose of the PRO measures becomes to aid in decision-making and assist in optimizing palliative care. Because the aims were not obvious to all stakeholders, including the clinicians, the patients may not have known that they were supposed to continue completing the questionnaires after treatment cessation. This problem was larger in the beginning of the study period, indicating the presence of an implementation start-up issue during which patients and clinicians were still learning how to use the PRO measures in routine care.
The time to progression and type of treatment differed among patients, which made the course of symptom development very variable. Some patients responding to treatment experienced symptom improvement, which again worsened in the period leading up to progression, but others experienced a more linear symptom development. We have described the change only from treatment initiation to disease progression and not the development in between. However, although the HRQoL data were collected prospectively during routine care, the data were not collected at fixed intervals or with the aim of performing the present study. Therefore, these retrospective analyses of prospectively collected data can act merely as an indicator of prognostic value.
Also, the present study was conducted before immunotherapy had been widely implemented as the standard of care for patients with lung cancer. Thus, the prognostic significance for patients treated with immunotherapy could differ from the presented results. However, poor performance status is a known negative predictor of response to both chemotherapy and immunotherapy. Thus, a prognostic evaluation of a patient’s health status using PRO measures will also most likely be well suited to monitor patients during immunotherapy.
In the survival analyses, the patients were dichotomized by performing a median split of the absolute HRQoL scores and by a 10-point minimal important difference for longitudinal changes. Thus, the results might have been different if other thresholds had been used. Previous studies have also used a median split to construct groups of patients with high or low HRQoL scores. However, such arbitrary cutoffs cannot consider the patient’s needs or the clinical relevance.
Quality of life supersedes the classic prognosticators for long-term survival in locally advanced non-small-cell lung cancer: an analysis of RTOG 9801.
Early change in patient-reported health during lung cancer chemotherapy predicts clinical outcomes beyond those predicted by baseline report: results from Eastern Cooperative Oncology Group study 5592.
suggested thresholds for clinically important symptom/functional impairment for each scale in the EORTC QLQ-C30 questionnaire for patients with different cancer diagnoses. However, because these thresholds were not designed to assess prognosis, we considered their approach unfit for dichotomization in the present survival analyses. Symptoms that are important to patients (eg, symptoms considered side effects of treatment) may not be of prognostic value. Therefore, clinical cutoffs with clinical relevance could have less prognostic significance than cutoffs specifically developed for prognostic evaluation. The present study was not designed to suggest specific cutoff scores but to explore whether symptoms with prognostic significance could be identified.
Conclusion
The results from the present study have shown that PRO measures applied in routine care can offer clinically relevant prognostic information at disease progression. Such information could help to initiate end-of-life discussions, improve palliative care, and aid decision making for patients with deteriorating health. However, because of the explorative nature of the study design, the exact risk assessments and specific symptom scores should be interpreted with caution. Future studies should aim to specify the prognostic thresholds for the individual HRQoL scores in larger patient cohorts.
Clinical Practice Points
•
Electronic PRO measures have been increasingly used in routine care for various purposes.
•
The routine use of such information has been shown to improve clinician awareness of patient-perceived symptoms and patient–caregiver communication, thereby enhancing quality of care.
•
However, the clinical significance of PROs are not easily interpreted.
•
In the present study, we identified specific PRO measures that were predictive of survival at disease progression in patients with lung cancer.
•
In addition, the absolute PRO measures at the disease progression predicted for survival.
•
These results show how PRO measures used in clinical routine care can help to initiate end-of-life discussions, improve palliative care, and aid in decision making for patients with deteriorating health.
Disclosure
The authors declare that they have no competing interests.
This work was supported by the Danish Cancer Society (grants R184-A11805, 2017), the Max Wørzner and Wife Inger Wørzner's Memorial Fund and the Department of Oncology, Hospital Unit West Juland. We thank all patients and clinical staff for ongoing support to the clinical use of patient-reported outcome measures during treatment in the Department of Oncology, Regional Hospital West Jutland. Thanks to Morten Pilgaard for language revision of our report. A special thanks to the Head of the Department, Senior Consultant Hanne Linnet, for innovative and proactive thinking concerning the implementation of patient-reported outcomes in clinical practice.
References
Ferlay J, Ervik M, Lam F, et al. Global Cancer Observatory: Cancer Today. Lyon, France: International Agency for Research on Cancer.
NORDCAN: Cancer Incidence, Mortality, Prevalence and Survival in the Nordic Countries, version 7.3 (08.07.2016). Association of the Nordic Cancer Registries. Danish Cancer Society.
Using patient-reported outcome measures to deliver enhanced supportive care to people with lung cancer: feasibility and acceptability of a nurse-led consultation model.
What is the value of the routine use of patient-reported outcome measures toward improvement of patient outcomes, processes of care, and health service outcomes in cancer care? A systematic review of controlled trials.
Health-related quality of life in small-cell lung cancer: a systematic review on reporting of methods and clinical issues in randomised controlled trials.
Quality of life supersedes the classic prognosticators for long-term survival in locally advanced non-small-cell lung cancer: an analysis of RTOG 9801.
The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
Quality of life analyses from the randomized, open-label, phase III pointbreak study of pemetrexed-carboplatin-bevacizumab followed by maintenance pemetrexed-bevacizumab versus paclitaxel-carboplatin-bevacizumab followed by maintenance bevacizumab in patients.
Is a patient’s self-reported health-related quality of life a prognostic factor for survival in non-small-cell lung cancer patients? A multivariate analysis of prognostic factors of EORTC study 08975.
Early change in patient-reported health during lung cancer chemotherapy predicts clinical outcomes beyond those predicted by baseline report: results from Eastern Cooperative Oncology Group study 5592.
Clinical decision-making and health-related quality of life during first-line and maintenance therapy in patients with advanced non-small cell lung cancer (NSCLC): findings from a real-world setting.
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