Epcoritamab Plus Lenalidomide and Rituximab in Practice: A Focus on EPCORE FL-1

Treatment Landscape

Approximately 20% of patients with follicular lymphoma (FL) relapse experience disease progression within 24 months of initiating first-line treatment (POD24). Historically, these patients experience shorter remissions with each subsequent line of therapy, highlighting the need for treatment options beyond front-line regimens.^1,2 The treatment landscape for relapsed or refractory (R/R) FL has changed with the availability of 2 bispecific CD20 x CD3 T-cell engagers (TCEs): mosunetuzumab (Lunsumio; Genentech) and epcoritamab (Epkinly; Genmab, AbbVie).

Although mosunetuzumab and epcoritamab are approved as monotherapy for the treatment of R/R FL in the third line and beyond, data from the multicountry, open-label, phase 3 EPCORE FL-1 trial (NCT05409066) have led to FDA approval of epcoritamab in combination with lenalidomide (Revlimid; Bristol Myers Squibb) and rituximab (Rituxan; Genentech: epcoritamab-R2). This regimen has also been incorporated into the National Comprehensive Cancer Network B-cell lymphoma guidelines for R/R FL after 1 or more prior lines of therapy.^3-6

Epcoritamab-R2 joins tafasitamab (Monjuvi; Incyte) plus lenalidomide and rituximab as a second-line, chemotherapy-free treatment option for R/R FL. Additional options include chemotherapy-based regimens that combine a CD20-directed antibody with cyclophosphamide/doxorubicin/vincristine/prednisone, cyclophosphamide/vincristine/prednisone, or bendamustine in patients who are bendamustine-naive.³

Key studies that have provided a foundation for EPCORE FL-1 include the AUGMENT (NCT01938001), EPCORE NHL-1 (NCT03625037), and EPCORE NHL-2 (NCT04663347) trials.^7-9 AUGMENT was a phase 3, randomized, multicenter trial evaluating rituximab-lenalidomide (R2) vs rituximab with placebo in patients with R/R FL and marginal zone lymphoma without rituximab-refractory disease. At a 5-year follow-up, the median progression-free survival (PFS) was 27.6 months vs 14.3 months (HR, 0.50; 95% CI, 0.38-0.66; P < .0001), with 5-year overall survival (OS) rates of 83.2% vs 77.3%, respectively.¹⁰

EPCORE NHL-1 is a multicohort, single-arm, phase 1/2 trial that evaluated epcoritamab monotherapy in patients with R/R B-cell lymphomas. In phase 2 of the trial, patients with R/R FL achieved an overall response rate (ORR) of 82.0% and a complete response (CR) rate of 62.5%.^7,9 The trial led to the FDA’s accelerated approval of epcoritamab monotherapy for R/R FL in 2024.

At a 3-year follow-up of patients with R/R FL in the pooled expansion cohort, which includes those enrolled in EPCORE NHL-1 and NHL-3 (NCT04542824), the median PFS without and with adjustment for COVID-19 deaths were 15.4 months (95% CI, 9.5-34) and 34.2 months (95% CI, 13.2-not reached), respectively; the median OS was not reached regardless of COVID-19 adjustment.¹¹

The second arm in EPCORE NHL-2 evaluated epcoritamab-R2 in patients with R/R FL in varying dosing schedules, with an ORR of 96% and a CR rate of 87% among 111 patients.¹² The rationale for this combination is informed by observations that epcoritamab was efficacious when combined with rituximab in preclinical studies, which demonstrated that a dual CD20-targeting mechanism and epcoritamab peak trimer formation occurred with a limited CD20 receptor occupancy of 20% to 30%.^4,13,14 Furthermore, in preclinical studies, lenalidomide combined with epcoritamab appeared to enhance immune cell activation and epcoritamab-mediated killing.^13,14

In this clinical spotlight, we aim to highlight points from EPCORE FL-1 to consider when operationalizing epcoritamab-R2 and discuss implications in the shifting treatment paradigm for R/R FL.

EPCORE FL-1 Trial Overview

The EPCORE FL-1 trial was a global, randomized, open-label, multicenter phase 3 trial enrolling 488 patients across 189 sites in 30 countries.⁴ Eligible patients included adults 18 years and older with measurable, stage II, III, or IV histologically confirmed CD20+ R/R classical FL. Patients must have received at least 1 prior antilymphoma-directed therapy that contained an anti-CD20 monoclonal antibody (mAb) and chemotherapy, have an ECOG performance status of 0 to 2, and meet at least 1 criterion from the Groupe d’Etude des Lymphomes Folliculaires Criteria. Patients were excluded if they had received only prior anti-CD20 mAb monotherapy and/or radiation therapy, had stage I disease, had lenalidomide-refractory disease, or had received lenalidomide within 12 months before randomization.

Patients were randomly assigned to receive epcoritamab-R2 (n = 243; receiving epcoritamab 48 mg full dose) or R2 alone (n = 245). During the study, a protocol amendment changed the epcoritamab step-up dosing (SUD) schedule from 2 SUDs to 3 SUDs to reduce the risk of cytokine release syndrome (CRS). After this amendment, 133 patients in the epcoritamab-R2 arm received the 3-SUD regimen. For CRS prevention in the epcoritamab-R2 arm, patients received premedications before the first 4 epcoritamab doses, including oral and intravenous (IV) hydration, an antihistamine, an antipyretic (eg, acetaminophen), and corticosteroids (dexamethasone preferred). Postmedications included 2 L to 3 L of oral fluids within 24 hours after epcoritamab administration and daily corticosteroids (dexamethasone preferred) for 3 days after epcoritamab dosing. Starting with the fifth epcoritamab dose, pre- and postmedication for epcoritamab was required only if patients had grade 2 or higher CRS with the fourth epcoritamab dose.

After a median follow-up of 14.8 months, epcoritamab-R2 reduced the risk for disease progression by 79% (HR, 0.21; 95% CI, 0.14-0.31; P < .0001), with an ORR of 95% (95% CI, 92-97) vs 79% (95% CI, 74-84; P < .0001). Further survival and response data from EPCORE FL-1 are presented in Table 1. Subgroup analyses demonstrated the benefit of epcoritamab-R2 vs R2 in all subgroups, including high-risk populations such as POD24, bulky disease, and those with double-refractory disease.

Generally, epcoritamab-R2 was well tolerated, with neutropenia and infections being the most common treatment-emergent adverse events (TEAEs). Neutropenia occurred in 74% (69% grade 3) of patients, resulting in growth factor use in 150 (61.7%), but febrile neutropenia was uncommon, occurring in 6%. All-grade infections occurred in 77% (33% grade 3) of patients; notable opportunistic infections in the epcoritamab-R2 arm included cytomegalovirus (CMV) in 8%, herpes simplex virus (HSV) in 8%, and Pneumocystis jirovecii in less than 1%, none of which were fatal. Overall, 19% of patients treated with epcoritamab-R2 discontinued treatment due to TEAEs, with discontinuation rates of 9%, 3%, and 19% for epcoritamab, rituximab, and lenalidomide, respectively. Dose reductions for lenalidomide occurred in 57 (23%) patients who received epcoritamab-R2 and in 44 (18%) who received R2.

CRS occurred in 26% of patients who received the 3-SUD regimen, with 21% grade 1 and 5% grade 2, most commonly after the first full dose of epcoritamab 48 mg. CRS was more common in the group who received the 2-SUD regimen (Table 1). Median time to CRS onset was 34.9 hours (IQR, 20.2-100.1), and median time to CRS resolution was 24 hours (IQR 11.3-72). One event of grade 1 immune effector cell–associated neurotoxicity syndrome (ICANS) occurred.

Abbreviations: CR, complete response; CRS, cytokine release syndrome; EFS, event-free survival; ICANS, immune effector cell–associated neurotoxicity syndrome; NE, not evaluable; ORR, overall response rate; OS, overall survival; PFS, progression-free survival; PR, partial response; SD, stable disease.

Practical Considerations When Using Epcoritamab-R2

Treatment Schedule and Administration

Epcoritamab-R2 is administered in 28-day cycles for up to 12 cycles. Epcoritamab is administered on a 3-SUD schedule during cycle 1, with the first full dose given on day 22 (priming doses). It is then administered weekly for cycles 2 to 3, and once every 4 weeks during cycles 4 through 12.⁵ Rituximab is given weekly during cycle 1 and on day 1 of cycles 2 through 5. Lenalidomide 20 mg orally is administered on days 1 through 21 of each 28-day cycle for cycles 1 through 12 (Figure 1).

Epcoritamab-Specific Pre- and Postmedication Considerations

Epcoritamab-associated pre- and postmedications are required for cycle 1 of epcoritamab-R2 only to prevent CRS. If no grade 2 or higher CRS occurs and priming doses need to be repeated, these epcoritamab-associated pre- and postmedications can be omitted starting with the fifth epcoritamab dose (cycle 2, day 1).⁵ Depending on the sequence of epcoritamab and IV rituximab, premedications given for epcoritamab can also serve as rituximab premedications (see sequence of administration of epcoritamab-R2).

Recommended premedications prior to cycle 1 epcoritamab priming doses (see Table 2).

In the trial, 24 hours before the priming doses of epcoritamab in cycle 1, patients were instructed to consume 2 L to 3 L of oral fluids, and antihypertensive medications could be held at the discretion of the provider.⁵ On the day of all cycle 1 epcoritamab doses, 30 to 60 minutes before epcoritamab administration, patients received an antihistamine (eg, diphenhydramine 50 mg IV/oral), an antipyretic (eg, acetaminophen 650-1000 mg oral), 500 mL of isotonic IV fluids, and a glucocorticoid of dexamethasone 15 mg or equivalent. On the day after epcoritamab, patients were instructed to consume 2 L to 3 L of oral fluids, and for 3 days, starting the day after epcoritamab, to take dexamethasone 15 mg or equivalent orally.⁵

Although the epcoritamab package insert states that dexamethasone or an equivalent can be used, dexamethasone is the preferred glucocorticoid for CRS prophylaxis, based on data with other TCEs showing lower CRS rates with dexamethasone compared with other corticosteroids.15 In practice, dexamethasone is commonly administered at a 16-mg dose rather than the 15-mg dose recommended in the package insert because the commercially available tablet strength is 4 mg.

See Table 2 for a detailed outline of epcoritamab-specific pre- and post-medications.

Rituximab-Specific Considerations

Rituximab premedications are shared with epcoritamab in cycle 1. For cycle 2 and onward, antihistamine, acetaminophen, and other institution-specific rituximab premedications would continue.

The first dose of rituximab should be given IV to assess for tolerability. If patients complete 1 full dose of IV rituximab without severe adverse reactions, a switch to the subcutaneous (SC) formulation can be considered, pending payer preference.¹⁶

Sequence of Administration of Epcoritamab-R2

In the EPCORE FL-1 trial, premedications were administered first, followed by rituximab (as first or second medication) and/or lenalidomide (as first or second medication), and then epcoritamab. Institutions can consider administering epcoritamab before rituximab so that the premedications given for epcoritamab can also serve as rituximab premedication; because epcoritamab SC injection is brief and no epcoritamab-associated CRS/ICANS has been reported immediately after administration, this approach should not delay rituximab administration. If the order of administration is reversed (IV rituximab given before epcoritamab) and the rituximab infusion is prolonged due to a rituximab-associated infusion reaction, premedications with shorter half-lives (eg, acetaminophen and diphenhydramine) may need to be repeated before epcoritamab administration.

Site-of-Care Considerations and the Pharmacist’s Role

The low incidence of CRS with the 3-SUD dosing schedule of epcoritamab in EPCORE FL-1 supports outpatient SUD and monitoring with epcoritamab-R2 without the need for hospital admission. When used for FL, the epcoritamab package insert does not state any requirements for hospitalization after epcoritamab administration for CRS monitoring, and EPCORE FL-1 allowed for patients to receive epcoritamab priming doses without hospital admission if the following criteria were met^4,5:

• Patient and caregiver must reside within 30 minutes of a facility with access to tocilizumab and/or other anticytokine therapies, an intensive care unit, and a multidisciplinary team with expertise in critical care medicine, infectious diseases, cardiology, and nephrology.
• Patient and caregiver must reside or stay at this facility for at least 24 hours following administration of the first full dose of epcoritamab (cycle 1, day 22)
• Patients must return to the facility on day 23 of cycle 1 to assess vital signs
• Patient and caregiver must be taught to recognize early symptoms of CRS and neurological events/ICANS, and they must be instructed on self-temperature monitoring
• Patient monitored oral temperature 3 times a day for the first 4 days post epcoritamab administration for the first 4 doses of epcoritamab (during cycle 1)
• Patient was assessed for comorbidities that may complicate CRS or neurological event/ICANS diagnoses or events (eg, dementia, congestive heart failure, chronic kidney disease, or chronic lung disease)
• On epcoritamab administration days, vitals were assessed before and 1 hour post epcoritamab administration

In clinical practice, institutions can adapt the criteria used in the EPCORE FL-1 trial and include patient-specific characteristics, such as tumor burden, performance status, and the presence of lymphoma-related complications, to select patients for outpatient SUD and monitoring. Another important framework institutions should have in place when providing TCEs to patients is a clear triage pathway for managing CRS, along with communication about assigned roles and responsibilities within the multidisciplinary team for patient education and related follow-up calls.

One key area where pharmacists can assist the multidisciplinary team in implementing and using epcoritamab-R2 is by providing education to the multidisciplinary team, patients, and caregivers, particularly regarding CRS-related premedications, postmedications, and home self-monitoring. Another potential area includes performing follow-ups after the first cycle of epcoritamab to ensure patients are monitoring their temperature and taking their CRS postmedications.

Another consideration for implementing epcoritamab-R2, and where pharmacists play an important role, is creating a chemotherapy order set and scheduling template, given the complex dosing schedule and pre- and postmedication requirements. Additionally, because epcoritamab is commercially available in 2 concentrations and aliquots are required to prepare certain SUDs, it is critical that institutions and pharmacists ensure that the pharmacy preparing epcoritamab has safeguards in place to prevent concentration-related errors and confirm that all epcoritamab doses are prepared correctly.

Given that lenalidomide is only available via a Risk Evaluation and Mitigation Strategies (REMS) program, pharmacists can also help facilitate patient access to lenalidomide if the pharmacist’s institution does not have a pharmacy that can dispense lenalidomide.¹⁷

Dose adjustments and drug holding are also key considerations with this regimen. In the EPCORE FL-1 trial, patients with creatinine clearance of less than 60 mL/min had their lenalidomide starting dose reduced to 10 mg daily for 2 cycles; if tolerated, lenalidomide could be increased to 15 mg daily.⁴ If epcoritamab, rituximab, or lenalidomide need to be held, dose adjusted, or permanently discontinued for toxicity, then it may still be clinically appropriate to continue the other drug(s), depending on what AE occurred.

For example, if patients experience lenalidomide-related neuropathy, it may still be appropriate to continue epcoritamab at full dose while the lenalidomide is being held and dose adjusted, depending on the patient’s clinical status. On the other hand, if patients experience grade 4 neutropenia, it would be clinically appropriate to hold all 3 drugs. The EPCORE FL-1 trial protocol contains details of which drugs were recommended to be held based on specific AEs.⁴

Supportive Care

Infectious Prophylaxis

In the EPCORE FL-1 study, 71% of patients treated with epcoritamab-R2 received HSV prophylaxis, and 8% developed HSV infections; thus, HSV prophylaxis is strongly recommended. Clinicians can also consider CMV monitoring given the 8% incidence in the epcoritamab-R2 arm.⁴

Patients should receive P jirovecii pneumonia prophylaxis throughout cycle 1 of epcoritamab-R2 and during any subsequent cycles where high-dose corticosteroids (prednisone 20-mg equivalents or higher daily) are used for more than 4 weeks.¹⁸

Given the high rates of grade 3 or higher neutropenia and the 61% of patients treated with epcoritamab-R2 in the EPCORE FL-1 trial who received growth factor prophylaxis, it is important to consider granulocyte colony-stimulating factor support if patients experience neutropenia.

All patients receiving CD20-targeting therapies should be tested for hepatitis B virus (HBV) before initiating CD20-targeting therapy. Patients at risk for HBV reactivation should receive appropriate HBV prophylaxis during epcoritamab-R2 therapy and for at least 12 months after the last dose of epcoritamab-R2. Patients with active HBV infection should be treated for their HBV accordingly.¹⁹

Lenalidomide-Specific Considerations

All providers who prescribe lenalidomide and all patients who receive it must enroll in the lenalidomide REMS program to mitigate the risk of embryo-fetal harm.¹⁷ Patients who are able to get pregnant or have partners who are able to get pregnant should be counseled not to get pregnant while receiving lenalidomide and about the risk of embryo-fetal harm. They should be made aware of their required, continued participation in the REMS program each month to obtain lenalidomide refills.

Patients should also receive antithrombotic therapy to mitigate lenalidomide-associated thrombotic risk based on institutional guidelines.

Emetogenicity

Overall, the emetogenic potential of the epcoritamab-R2 regimen is low on epcoritamab dosing days and minimal to low on lenalidomide dosing days.²⁰ In cycle 1 and any other cycles where dexamethasone is given as a premedication to epcoritamab, consider omitting other prophylactic antiemetics, as dexamethasone is already being given as CRS prophylaxis at a dose higher than the dexamethasone dose used for chemotherapy-induced nausea and vomiting (CINV) prevention. On days where dexamethasone is not used as a premedication for epcoritamab, utilize institution-specific low-emetogenicity CINV prophylaxis for oral anticancer agents.

Discussion

Epcoritamab-R2 represents a new standard of care for patients with R/R FL after 1 or more prior lines of therapy. Data from the subgroup analysis of the EPCORE FL-1 trial showed that epcoritamab-R2 demonstrated a favorable PFS compared with R2 in all prespecified subgroups, including POD24, bulky disease, and double refractory.⁴

Although these findings are encouraging, further analyses are needed to inform which patient populations epcoritamab-R2 is insufficient for, with a goal of optimizing outcomes for these patients. Additionally, rituximab monotherapy is a common regimen in the frontline setting for FL; however, because patients who previously received rituximab monotherapy were excluded from EPCORE FL-1, the optimal treatment sequencing for these patients remains unclear.⁴ Furthermore, as more data continue to emerge, questions remain on what the optimal CD20 x CD3 TCE combination partners and therapeutic approaches are (eg, PET/CT and/or measurable residual disease [MRD] response adapted) for patients with previously treated and untreated FL.

The optimal sequencing of treatments for FL is becoming increasingly complex, with the approval of epcoritamab-R2 and other therapeutic options for second-line R/R FL, such as tafasitamab-R2 and chemoimmunotherapy combinations. Additional novel TCE and non-TCE therapies are under investigation for patients with R/R FL after 1 or more prior lines of therapy. Examples of ongoing phase 3 trials include CELESTIMO (NCT04712097), evaluating subcutaneous mosunetuzumab plus lenalidomide vs R2, and GOLSEEK-4 (NCT06911502), evaluating golcadomide plus rituximab vs investigator’s choice.^21,22

Future Directions

An area of continued interest is the application for circulating tumor DNA MRD in the management of FL during and after completion of treatment. One method of particular interest is phased variant enrichment and detection sequencing (phasED-seq), which tracks multiple somatic mutations on a single cell-free DNA molecule. This approach is especially applicable in B-cell lymphomas because of activation-induced cytidine deaminase–mediated aberrant somatic hypermutation, a biological phenomenon that creates clusters of single-nucleotide variants in close proximity on the same DNA molecule. In a trial of previously untreated patients with FL who received frontline chemoimmunotherapy, the combination of a positive PET scan and positive phasED-seq MRD at the end of treatment was associated with a shorter PFS and with POD24.²³ The possibility of identifying patients with FL after completion of frontline treatment at a risk for POD24 may allow for preemptive treatment decisions, which may help pave the way for individualized second-line treatment strategies.

Conclusion

Epcoritamab-R2 is the first bispecific TCE-based regimen approved by the FDA for patients with R/R FL after 1 or more prior lines of therapy. This fixed-duration, chemotherapy-free combination, with a favorable safety profile, allows outpatient administration and monitoring, making this regimen an optimal choice for many patients. Oncology pharmacists remain vital in tailoring supportive care for patients, facilitating drug access, and ensuring safe preparation of therapy.

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