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Feasibility of collecting longitudinal patient-reported outcomes in individuals with relapsed or refractory large B-cell lymphoma who received chimeric antigen receptor T-cell (CART) therapy
BMC Cancer volume 24, Article number: 984 (2024)
Abstract
Purpose
Chimeric antigen receptor T-cell (CART) therapy has shown clinical efficacy in refractory and relapsed large B-cell lymphomas, but is associated with serious acute and long-term toxicities. To understand the patient perspective, we measured a patient-reported outcome (PRO), specifically, health-related quality of life (HRQoL), at multiple time points over one year.
Methods
This was a prospective feasibility study of a cohort of patients who were eligible for standard of care CART therapy, tisagenlecleucel. Demographic data and disease characteristics were collected. HRQoL was measured using FACT-Lym at baseline, and months 1, 3, 6 and 12. FACT-Lym includes FACT-G (physical, social, emotional and functional well-being domains), plus a lymphoma subscale.
Results
Thirty-four of 35 patients approached, consented to participate. Two of them did not receive their infusion due to progressive disease. 50% were female and median age was 62 (23–77). Twenty-nine patients (91%) completed baseline FACT-Lym and 20 of 21 (95%) eligible patients completed 12-month FACT-Lym. 52% completed all 4 post-baseline FACT-Lym measures. Exploratory analyses for changes in FACT-Lym scores are reported.
Conclusion
It is feasible to measure longitudinal PROs in patients who receive CART therapy. This study will inform future studies in evaluating the patient perspective on CART therapy.
Introduction
Chimeric antigen receptor T-cell (CART) therapy is an effective immunotherapy for patients with relapsed or refractory large B-cell lymphomas [1,2,3]. Prior to CART availability, patients with large B-cell lymphoma who had received two or more prior lines of therapy experienced poor overall outcomes [4]. The recent results of CART therapy in such patients are very promising but must be balanced against toxicities associated with CART therapy, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS) [5]. Acute CART associated toxicities can be severe, resulting in organ dysfunction, resuscitative measures, and occasionally death. Following the acute phase of CART therapy, patients are at risk of long-term toxicities such as infection, hypogammaglobulinemia, prolonged cytopenias, and secondary malignancies [6].
In the pivotal trials studying CART therapy in the third line setting, authors reported classical outcomes such as toxicity, as graded by the clinician, and efficacy in the form of response rates, progression-free survival, and overall survival [1,2,3]. In addition to living longer, patients diagnosed with cancer also want to liver better, which is a critical outcome that can only be assessed from the patient perspective. Patient-reported outcomes (PROs) are unique in that they are reported directly from the patient without clinician interpretation or bias. PROs, which can be measures of symptom burden, health related quality-of-life (HRQoL) and therapy effectiveness, have become increasingly important in hematologic clinical research [7, 8]. Secondary publications from JULIET and TRANSCEND reported HRQoL PROs in those who achieved at least a partial response to CART therapy [9, 10]. In these tightly run clinical trials, HRQoL improved over time [9, 10].
There is a need to study the impact of the CART experience, with its complex procedures and acute and long-term toxicities on the patient. To better understand the patient perspective of standard of care CART therapy, we prospectively collected HRQoL over a 12-month period, in patients with relapsed or refractory large B-cell lymphomas receiving tisagenlecleucel CART therapy in a Canadian outpatient CART centre. We report the feasibility of collecting longitudinal HRQoL in this dynamic and complex setting along with exploratory findings of HRQoL changes from baseline.
Methods
Study design and population
This was a prospective observational cohort study conducted at the Juravinski Hospital and Cancer Centre (JHCC), a tertiary care centre serving 2.3 million people in Ontario, Canada. Consecutive patients, who were referred and approved by Ontario Health - Cancer Care Ontario (OH-CCO) for commercial CART therapy (tisagenlecleucel was the only CART therapy available at the time of conducting this study), were approached to participate in this study. OH-CCO is an agency of the Ontario Ministry of Health that provides funding to Ontario institutions for CART therapy and includes in its processes the need for patient-specific approval by an expert panelist. Patients were eligible for study if they were planned to receive standard of care (SOC) CART therapy. SOC CART therapy was available for patients 18 years of age or older, with a diagnosis of diffuse large B cell lymphoma (DLBCL), primary mediastinal B cell lymphoma (PMBCL) or transformed follicular lymphoma (tFL), according to the 2016 WHO Classification of Tumors of Hematopoietic and Lymphoid Tissue, and had received at least two prior lines of therapy. The protocol was reviewed by Hamilton Integrated Research Ethics Board (HIREB) and all patients signed an informed consent form.
Setting
At the JHCC, we were the first Canadian site to offer tisagenlecleucel CART therapy in the outpatient setting. Patients received their lymphodepleting chemotherapy and CART infusion with tisagenlecleucel in our Oncology Day Services (ODS) department, with daily outpatient follow-up for a minimum of ten days depending on sequelae, followed by visits every three days until 30 days from infusion. Admission is mandated for patients developing symptoms of CRS, ICANS or other clinical concerns related to therapy such as infection, gastrointestinal concerns or poor nutrition. ODS is an outpatient department that is fully integrated within the hospital, offering nursing and clinical review services 12 h per day, 365 days per year. Clinicians could elect to admit patients for their CART therapy on the basis of clinical factors such as co-morbidities, rapidity of lymphoma growth or lack of caregiver support.
Procedure
Autologous T-cells were collected from each patient via apheresis, followed by a 3–4 week waiting period for T-cell engineering and shipping. During that time, at the discretion of their treating physician, select patients received bridging therapy with corticosteroids, chemotherapy, immunotherapy and/or radiation. Once autologous CART cells were available, patients received lymphodepleting chemotherapy with cyclophosphamide (250 mg/m2) and fludarabine (25 mg/m2) 5, 4 and 3 days prior to CART infusion. One patient received bendamustine (90 mg/m2) as an alternative chemotherapy. Lymphodepletion and CART infusion were administered as an outpatient in the ODS department at the Juravinski Hospital. Although outpatient CART is the default CART procedure at the JHCC, clinicians could decide to administer CART therapy as an inpatient if the patient was deemed to be high medical risk or for caregiver concerns.
Outcomes
Primary outcome: PRO collection feasibility
Patient-reported HRQoL was measured using Functional Assessment of Cancer Therapy – Lymphoma (FACT-Lym) (Supplementary) [11]; a validated 42-item questionnaire answered by the patient on a 5-point Likert scale on day 0 prior to infusion (baseline), and standard of care follow-up appointments at months 1, 3, 6 and 12 following CART infusion. Patients completed FACT-Lym questionnaires on paper for in-person visits and over the phone (statements and answer choices were read aloud for patients to select) for those who attended virtual appointments. The need for virtual visits was dictated by infection control (COVID-19). FACT-Lym includes FACT-G (physical, social, emotional and functional well-being domains), plus a lymphoma specific subscale (Lym-S). A score of 0 represents worst HRQoL and higher scores indicate an improvement (score range, 0-168). FACT-Lym Trial Outcome Index (TOI) is a composite of physical and functional well-being and Lym-S. Minimal important differences (MID) have been estimated using anchor (performance status and disease progression) and distribution methods; LymS 2.9–5.4, TOI 5.5–11, and total FACT-Lym 6.5–11.2 [12]. The LymS MID was confirmed as 3–5 points [11]. Feasibility of implementing FACT-Lym administration was determined by recruitment rate, completion rate at each time point, reason for attrition and the quality of the data as measured by the degree of missing data [13].
Exploratory secondary outcomes
Secondary outcomes were changes in HRQoL from baseline to the 1-, 3-, 6- and 12-month evaluation. Other exploratory analyses included the rates of severe CRS and ICANS, defined as Grade 3 or 4 using consensus grading scales [5], overall response rate at 3 months as per the Cheson criteria [14], and overall survival (defined below).
Statistical methods
Feasibility outcomes were reported as rates. Reasons for missing PRO data were documented. No correction for missing data was performed for this feasibility study. No statistical testing for exploratory analysis was performed, as the objective of this study was descriptive.
Patient characteristics, including baseline laboratory markers CRP, ferritin and LDH, along with treatment characteristics and outcomes, were summarized using descriptive statistics. The Kaplan-Meier method was used to estimate overall survival, defined from the date of infusion until death due to any cause. Patients alive at the time of data analysis were censored on the last date the patient was confirmed to be alive. Two-sided, 95% confidence intervals were constructed for outcomes of interest.
Results
Baseline characteristics
Out of 35 eligible patients approached between January 2020 and June 2021, 34 consented to participate in the study. Among those 34 patients registered to the study, two did not receive their lymphodepleting chemotherapy nor their CART infusion due to progressive disease. Baseline demographics and disease characteristics are described in Table 1 for all 34 patients consented, as well as the 32 who received CART infusion. 50% were female and median age was 62 (23–77), with 11% over age 65 years.
CART infusion and toxicity
Twenty-one (21/32, 65.7%) patients required bridging therapy prior to CART infusion. Ten received chemotherapy (plus or minus corticosteroids), 10 received radiation with or without steroids, and one received chemotherapy, radiation, and corticosteroids. Median time from leukapheresis to CART cell infusion was 48.5 days (range 34–131). The upper end of the range was an outlier, as the delay to CART infusion was due to physician discretion, not product engineering or delivery.
Of the 32 patients who received CART infusion, 22 (68.8%) received an outpatient CART infusion; 18 (81.8%) of whom were later admitted to hospital. Median days to admission was 4 days (range 3 to 4). Median length of stay in hospital was 9 days (range 2 to 18 days). For patients with a planned admission on day of infusion, the median length of stay was 10 days. Twenty-six patients (81.2%) developed any grade CRS; 6 (18.8%) of whom developed grade 3 or 4 CRS. There were 6 (18.8%) patients who developed ICANS grade 1 or 2, with none developing grade 3 or 4 ICANS. There were no CRS or ICANS related deaths. Details regarding CART toxicity are found in Table 2. Seven of the 28 patients admitted at some point (25%) required transfer to the ICU for a median of 3 days (range 1 to 5). Baseline CRP, LDH and platelet count are found in the supplementary material.
Eleven patients had died at the time of data analysis. The remaining 21 patients were followed for at least one year. Those who died were included in those time points able to be captured prior to death. Overall response rate at 3 months was 53.1%, with 43.8% in complete response. One year (95% CI) overall survival was 65.6% (46.6 to 79.3) (Figure S1). 40.6% of patients received additional therapies following CART therapy and 9.4% developed a secondary malignancy (1 AML; 2 therapy-related MDS).
Health-related quality of life – feasibility and longitudinal changes
We recruited 34 of the 35 patients approached (97.1%). Twenty-nine patients completed a baseline FACT-Lym and 27 completed at least one post-baseline FACT-Lym measure (Table 3). Notably, 95% of patients who were alive and still on-study at 12 months completed their 12-month FACT-Lym assessment, and 11 of the last 21 patients (52%) completed the FACT-Lym for all follow-up timepoints at which they were alive. The percentages of patients with an MID at each timepoint compared to baseline are reported in Table 3.
Figure 1 illustrates exploratory longitudinal changes in HRQoL as change from baseline for FACT-Lym total scores and domains. Median change in FACT-Lym total scores at month 12 and FACT-TOI score at months 6 and 12 demonstrated a minimal important difference (Fig. 1A). Figure 1B illustrates changes in scores for the five domains of FACT-Lym, with worsening in the physical and functional domain and lymphoma subscale at day 30 followed by improvement over time. The emotional domain did not demonstrate change beyond 3 months, and the social domain demonstrated worse scores at 12 months.
Discussion
CART therapy in a dynamic and complex outpatient setting. We were able to recruit 97.1% of patients approached to participate and 95% of patients who were alive and still on-study at 12 months completed their 12-month FACT-Lym assessment. 12-month attrition was largely due to death. FACT-Lym completion rates were lower at day 30 (63%) and 3 months (50%), likely a reflection of patients feeling unwell and less stable. Our results support the development of a larger study measuring long-term PROs in patients who received CART therapy.
In addition to feasibility, we report the longitudinal changes in HRQoL in patients who received tisagenlecleucel for relapsed or refractory large B-cell lymphoma. As expected, FACT-Lym scores initially worsened during the acute CART experience and took six months to improve beyond baseline scores. Clinically meaningful changes were seen in the composite scores, FACT-Lym total and FACT-TOI. PRO data from the JULIET trial also demonstrated clinically meaningful improvements in FACT-Lym scores in those who achieved and maintained at least a partial response from baseline scores at 3, 6, 12, and 18 months [9]. They were unable to assess non-responders as these patients either succumbed to their disease or withdrew from the JULIET trial to pursue alternative therapies. In ZUMA-7, a study comparing CART therapy versus standard of care autologous hematopoietic stem cell transplantation, authors found earlier improvements in QoL; however, they only included responders for QoL assessment [15]. A recent scoping review of 14 studies of PROs (HRQoL and patient-reported symptoms) in CART therapy indicates that after a decline in the early phase after infusion, there is a general improvement in PROs, at least in some domains in responding patients [16].
Interestingly, our exploratory analysis does not demonstrate improvement in the emotional or social well-being domains. Similar findings have been demonstrated in clinical trials [15, 17]. This is consistent with the fact that patients with cancer have higher rates of depression and anxiety compared to the general population [18] and individuals with hematologic cancers have some of the highest reported rates of depression and anxiety amongst cancer types [19]. Despite higher rates of depression and anxiety in patients with cancer, only 5% see a mental health professional [20]. Changes in cognition may impact PRO scores. Two studies evaluated long-term, defined as 6–12 months, cognitive changes following CART therapy [21, 22]. Ruark and others found that 50% of patients reported at least one cognitive difficulty or clinically meaningful depression or anxiety in long-term follow-up [21]. Barata and others found that cognition worsened from month 3 to month 12 following CART therapy [22]. Our study highlights a potential need for future studies to investigate the role of social and mental health interventions in CART therapy and potential barriers for accessing this care in patients with cancer.
To the best of our knowledge, outside of a feasibility study measuring the adoption of a wearable vital sign tracker to implement PRO completion [23], our study is the first to report the feasibility of measuring a PRO in patients who received commercial CART therapy. This is important as the CART journey is complex with patients moving from clinic to ODS to hospital and to sometimes geographically isolated homes. In the recent scoping review of PROs (HRQoL and patient-reported symptoms) in CART therapy (24), Efficace and others identified seven observational studies [21,22,23,24,25,26,27] measuring PROs in CART therapy. These observational studies were largely uncontrolled and heterogenous. In addition to the pilot study using wearables [23], two were a cross-sectional design and did not measure the collection of PROs at multiple time points [21, 26]. One study was retrospective, evaluating standard of care PRO measures [27]. The remaining three trials were prospective; however, they did not report feasibility, missing data, MID, or attrition [22, 24, 25], which are important outcomes in PRO research. There is currently insufficient data to understand the long-term effects of CART on PROs.
In addition to a PRO, we report our initial experience with administering tisagenlecleucel in the outpatient setting at a Canadian hospital and cancer centre. Compared to the JULIET trial, our real-world data demonstrated similar toxicity and response rates in a similar patient population [1]. However, we did observe a superior median one year (95% CI) overall survival of 65.6% (46.6, 79.3) compared to 40% (95% CI, 32 to 49) [1]. This may reflect the fact that there are more treatment options after CART therapy failure that were not available at the time of JULIET. Another explanation could be that we observed lower rates of bridging therapy (65.7%) compared to the JULIET trial (92%) [1]; knowing that bridging therapy is associated with inferior OS [28].
In our outpatient CART model of care, 80% of patients were admitted due to toxicity. To maintain a successful outpatient program and ultimately maintain a sustainable CART program in a strained socialized healthcare system, there needs to be a strategy to mitigate toxicity necessitating admission to hospital. To sustain an outpatient model of CART delivery, it is important to be able to identify those at risk of severe toxicity. It is important that future studies of outpatient CART delivery incorporating alternative models of care such as remote monitoring, and strategies to mitigate toxicity include PROs to evaluate the effectiveness from the patient perspective. Our study demonstrates that PRO collection in the dynamic administration of CART therapy is feasible.
Strengths and limitations
A major strength of our study is the prospective nature of data collection, allowing for robust and granular clinical data. A second major strength is that the 12-month attrition rate of HRQoL completion was largely due to death, rather than loss of follow-up.
Despite these strengths, there are several methodological limitations to consider. First, we were unable to collect a number of HRQoL measures due to COVID. The beginning of the pandemic posed a unique barrier to PRO data collection. As a result of our experience, we are prepared for this type of barrier in future studies. To prevent missing data for future studies, we would recommend paper and electronic collection to allow for universal access to the PRO. In addition to COVID, patients feeling unwell may have played a role in poor attrition rates in the first and third month. Future studies should focus on capturing reason for attrition and develop strategies to avoid poor attrition during the acute CART setting. Second, due to a small sample size, this study was underpowered to explore significant changes in HRQoL. We were therefore only able to perform exploratory analyses for the purposes of hypothesis generation to inform future studies.
Considerations for future studies include exploring the long-term effects on cognition that would not have been captured but may have impacted HRQoL scores, particularly the emotional and social well-being domains. In addition, PROs should be measured more frequently during the acute phase of treatment and height of toxicity. Lastly, there are nuances in the patient experience that cannot be captured using a questionnaire. Qualitative work to capture the patient perspective of CART therapy would be valuable to identify areas for improvement and possible intervention.
Conclusions
Our study demonstrates that PRO collection during CART therapy is feasible. This study will inform future research study design. To facilitate outpatient CART therapy administration, we need to leverage new technologies. To measure effectiveness and acceptance of these new technologies, PROs will play an important role. Further exploration such as long-term effects on cognition, and qualitative work to better understand the patient experience are needed.
Data availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
We acknowledge Eric Hammond, RN, CART co-ordinator for his support in this study.
Funding
Freeburne Banting Foundation.
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Contributions
AB Designed and conducted the research study, analysed data, and wrote the paper. GP analysed data and wrote the paper. GF, GD, RM, and TK helped write the paper. RF and ML helped design and write the paper. All authors reviewed the manuscript.
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Ethics approval and consent to participate
The protocol was reviewed by Hamilton Integrated Research Ethics Board (HIREB) and all patients signed an informed consent form.
Consent for publication
Not applicable.
Competing interests
AB, honoraria from Novartis, BMS and Kite/Gilead; GP, honorarium from Takeda, consulting fees from Merck, Astra-Zeneca and Profound Medical, close family member who is an employee of Roche Canada and owns stock in Roche Ltd; GF none; GD Honoraria from Janssen and Roche; TK none; ML none; MR none; RF honoraria from Janssen, Novartis, BMS, Gilead, and consultancy from Novartis, Gilead.
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Balitsky, A., Pond, G., Davies, G. et al. Feasibility of collecting longitudinal patient-reported outcomes in individuals with relapsed or refractory large B-cell lymphoma who received chimeric antigen receptor T-cell (CART) therapy. BMC Cancer 24, 984 (2024). https://doi.org/10.1186/s12885-024-12574-2
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DOI: https://doi.org/10.1186/s12885-024-12574-2