Abstract
PURPOSE:
S1826 was an international phase 3 randomized trial that demonstrated improved progression-free survival of nivolumab plus doxorubicin, vinblastine, and dacarbazine (N+AVD) over brentuximab vedotin plus AVD (BV+AVD) in newly diagnosed advanced stage classic Hodgkin lymphoma (cHL). Here we report results of enrolled participants with HIV.
PARTICIPANTS AND METHODS:
People with HIV (PWH) with a CD4+ T-cell above ≥200 cells/μL and on effective ART with an undetectable HIV viral load within 6 months prior to enrollment were eligible. Participants were randomly assigned in a 1:1 ratio to receive six 28-day cycles of either N+AVD or BV+AVD intravenously. The primary endpoint was progression-free survival.
RESULTS:
16 eligible PWH were enrolled, 11 received N+AVD and 5 received BV+AVD. The median follow-up duration was 32.7 months in the N+AVD arm and 26.7 months in the BV+AVD arm. The 2-year PFS rate was 77.9% in N+AVD arm and 75.0% in the BV+AVD arm. The 2-year OS was 85.7% in the N+AVD arm and 75.0% in the BV+AVD arm. Grade ≥ 3 adverse events were observed in 45% of participants in the N+AVD arm and 50% in the BV+AVD arm with more frequent febrile neutropenia, and severe infections observed in the BV+AVD arm.
CONCLUSIONS:
N+AVD is safe and effective in newly diagnosed HIV-associated advanced stage cHL. Clinicaltrials.gov number NCT03907488
Introduction
People with HIV (PWH) are at 5- to 20 times higher risk of developing classic Hodgkin lymphoma (cHL) throughout their lifetime than people without HIV.1,2 HIV-associated cHL is more likely to exhibit poor prognostic features, occur at older ages, and present at more advanced stages than HIV-negative cHL.3 Unfortunately, therapeutic trials for cancer have often excluded PWH due to perceived concerns about safety. The ECHELON-1 study, which demonstrated an overall survival (OS) advantage of brentuximab vedotin plus doxorubicin, vinblastine, and dacarbazine (BV+AVD) over doxorubicin, bleomycin, vinblastine, and dacarbazine (ABVD) in advanced stage (stage III-IV) cHL, excluded PWH regardless of the use of antiretroviral therapy (ART) or the degree of viral suppression.4,5 Subsequently, the safety and efficacy of BV+AVD in advanced stage cHL was established by the AIDS Malignancy Consortium (AMC) 085 study that demonstrated a similar 2-year progression-free survival (PFS) of 87% and OS of 92%.6
PD-1 inhibitors have demonstrated a remarkable efficacy in relapsed/refractory cHL,7-20 and their safety and efficacy was demonstrated in a small retrospective study of relapsed/refractory HIV-associated cHL across a wide spectrum of CD4+ T-cell counts.21 S1826 was an international phase 3 open-label randomized trial comparing nivolumab plus AVD (N+AVD) or BV+AVD in untreated stage III-IV cHL.22 At a median follow-up time of 2.1 years, the 2-year PFS was 92% in the N+AVD arm and 83% in the BV+AVD arm, establishing N+AVD as a new standard of care in the upfront treatment of advanced stage cHL. PWH were eligible, and here we report the safety and outcomes of enrolled participants with HIV.
Methods
Study Design and Population
This study is a subgroup analysis of PWH and untreated stage III-IV cHL enrolled on S1826. The detailed inclusion/exclusion criteria and primary results have been reported elsewhere.22 PWH were eligible if they had a CD4+ T-cell count ≥200 cells/μL and were on ART with an undetectable HIV viral load within 6 months prior to enrollment. However, baseline CD4+ T-cell counts, ART regimens, and HIV viral load were not recorded or monitored throughout treatment. Patients with hepatitis B virus were eligible if they were on suppressive therapy and had an undetectable viral load. Patients previously treated and cured of hepatitis C were also eligible.
Treatment and Follow-Up
Participants were randomly assigned in a 1:1 ratio to receive six 28-day cycles of either N+AVD or BV+AVD, as described previously.22 Granulocyte colony-stimulating factor (G-CSF) prophylaxis was mandatory in the BV+AVD group and optional in the N+AVD group. Response assessments were performed using PET-CT scans at the end of treatment and subsequently with CT or MRI imaging at 1 and 2 years after randomization.
Outcomes
The primary outcome of PFS was defined as the time from randomization to disease progression or death from any cause. Secondary outcomes included OS, overall response rate (ORR), and the incidence of adverse events (AEs). Response to therapy was assessed using the 2014 Lugano criteria.23 AEs were graded using the Common Terminology Criteria for Adverse Events v5.0 (http://ctep.cancer.gov).
Statistical Analysis
Baseline demographic and clinical characteristics were summarized using descriptive statistics. Kaplan-Meier analyses were used to estimate PFS and OS. Due to the small sample size, quantitative comparative analyses of the outcome measures between cohorts were not performed. In accordance with SWOG policy, modified intention-to-treat analysis was performed — patients who were deemed to be ineligible on the basis of pathology review or violation of the eligibility criteria were excluded.
Ethical Considerations
The S1826 trial received approval from the Central Institutional Review Board in Rockville, MD, and all participants provided written informed consent. This analysis adheres to the principles of the Declaration of Helsinki and was approved by the appropriate ethics committees.
Results
Sixteen participants with HIV met the inclusion criteria for this subgroup analysis. PWH were older (median age 46 vs. 26 years) and predominantly male (100% vs. 55%) (Table 1) compared with the HIV-negative cohort. The HIV subgroup had a higher proportion of Black participants (31% vs. 11%), stage IV disease (75% vs. 63%), IPS score of 4-7 (69% vs. 31%), and B-symptoms (75% vs. 58%) compared with participants without HIV.
Table 1.
Baseline characteristics of participants with and without HIV on S1826
| Baseline Characteristics | HIV+ N = 16 (2%)1 |
HIV− N = 954 (98%)1 |
|---|---|---|
| Age | ||
| Median (Min, Max) | 46 (30, 66) | 26 (12, 83) |
| 12-17 years | 0 (0%) | 236 (25%) |
| 18-60 years | 14 (88%) | 625 (66%) |
| > 60 years | 2 (13%) | 93 (10%) |
| Female sex | 0 (0%) | 426 (45%) |
| Race | ||
| White | 7 (44%) | 726 (76%) |
| Black | 5 (31%) | 109 (11%) |
| Asian | 2 (13%) | 26 (3%) |
| Native American | 0 (0%) | 3 (0%) |
| Pacific Islander | 0 (0%) | 2 (0%) |
| Multi-Racial | 0 (0%) | 9 (1%) |
| Other/Unknown | 2 (13%) | 79 (8%) |
| Hispanic ethnicity | 4 (25%) | 120 (13%) |
| Unknown | 0 | 51 |
| Stage | ||
| III | 4 (25%) | 349 (37%) |
| IV | 12 (75%) | 605 (63%) |
| B symptoms present | 12 (75%) | 549 (58%) |
| IPS Score | ||
| 0-3 | 5 (31%) | 655 (69%) |
| 4-7 | 11 (69%) | 299 (31%) |
| Bulky disease > 10 cm | 3 (19%) | 280 (29%) |
| EBV Status | ||
| EBV+ | 10 (77%) | 91 (18%) |
| EBV− | 3 (23%) | 418 (82%) |
| Unknown | 3 | 445 |
| Intent for radiation | 5 (31%) | 568 (60%) |
n (%)
Among PWH, 11 were assigned to receive N+AVD and 5 for BV+AVD (Table 2). Median age at diagnosis was 46 years in the N+AVD cohort and 45 in the BV-AVD cohort. The N+AVD arm had more participants who were Black (45% vs 0%) and had a lower IPS score of 0-3 (45% vs. 0%) than the BV+AVD arm. Tumor EBV status was available for 13 participants, with similar proportions of EBV+ in both arms (6/8 [75%] in N+AVD arm and 4/5 [80%] in BV+AVD arm). One participant in the BV+AVD arm withdrew consent prior to receiving study treatment and was excluded from safety and efficacy analysis (Supplementary Figure 1) All investigational agents were discontinued early in 1 participant (9%) on the N+AVD arm and 2 participants (40%) on the BV+AVD arm (Supplementary Table 1). Dose reduction of BV was undertaken in 2 (40%) participants. G-CSF use was mandatory in the BV+AVD arm but optional in the N+AVD arm, with 8 (73%) participants receiving it in the latter arm.
Table 2.
Baseline characteristics of S1826 participants with HIV and classic Hodgkin lymphoma
| Baseline Characteristics | Nivolumab + AVD N = 11 |
Brentuximab vedotin + AVD N = 5 |
|---|---|---|
| Age | ||
| Median (Min, Max) | 46 (35, 66) | 45 (30, 63) |
| 12-17 years | 0 (0%) | 0 (0%) |
| 18-60 years | 10 (91%) | 4 (80%) |
| > 60 years | 1 (9%) | 1 (20%) |
| Sex | ||
| Men | 11 (100%) | 5 (100%) |
| Race | ||
| White | 4 (36%) | 3 (60%) |
| Black | 5 (45%) | 0 (0%) |
| Asian | 1 (9%) | 1 (20%) |
| Other/Unknown | 1 (9%) | 1 (20%) |
| Hispanic ethnicity | 2 (18%) | 2 (40%) |
| Stage | ||
| III | 3 (27%) | 1 (20%) |
| IV | 8 (73%) | 4 (80%) |
| B symptoms present | 8 (73%) | 4 (80%) |
| IPS Score | ||
| 0-3 | 5 (45%) | 0 (0%) |
| 4-7 | 6 (55%) | 5 (100%) |
| Bulky disease > 10 cm | 2 (18%) | 1 (20%) |
The median follow-up duration was 32.7 months in the N+AVD arm and 26.7 months in the BV+AVD arm. The 2-year PFS rate was 77.9% in N+AVD arm and 75.0% in the BV+AVD arm (Figure 1a). There were a total of 3 PFS events, one disease progression in N+AVD arm and two deaths, one in each arm (cardiogenic shock 2 years following treatment [in complete remission] in the N+AVD arm and sepsis during treatment in the BV+AVD arm). The 2-year OS was 85.7% in the N+AVD arm and 75.0% in the BV+AVD arm (Figure 1b). End-of-treatment response data were available for 11 participants in the N+AVD arm and 4 patients in the BV+AVD arm. The ORR was 100% (all Deauville 1-3) in the N+AVD group and 75% in the BV+AVD group (3 with Deauville 1-3 and 1 with Deauville 5).
Figure 1. Progression-free (panel A) and overall survival (Panel B) for subgroup of PWH enrolled on S1826 (Modified Intention-to-Treat Population).
AVD indicates doxorubicin, vinblastine, and dacarbazine
Grade 3 or higher AEs were seen in 45% of participants in the N+AVD arm and 50% of participants in the BV+AVD arm (Supplementary Table 2). Although neutropenia was higher in proportion in the N+AVD arm, grade 3 or higher neutropenia and febrile neutropenia occurred more frequently in the BV+AVD arm (50% vs. 36% and 50% vs. 18%, respectively), including 1 case each of enterocolitis and sepsis. Peripheral sensory neuropathy occurred in 27% patients in the N+AVD group and 50% in the BV+AVD group, all ≤2 grade. Liver enzyme abnormalities were seen more frequently in the N+AVD arm, but only 1 grade 3 event occurred, which was related to alcohol use off-treatment. No cases of immune-related adverse events were reported in either treatment arm.
Discussion
Among the participants with HIV and cHL enrolled in S1826, N+AVD was safe and effective. The baseline cohort characteristics mirrored the epidemiology of PWH and cHL in the United States,24 enhancing the generalizability of the findings. PFS among participants with HIV appeared shorter than what was observed in the overall cohort, potentially related to the higher proportion of adverse disease features in the PWH subcohort. Also, due to the small number of PWH enrolled to the study, one death event in each study arm had an outsized impact on PFS.
While direct comparisons with historical trials (e.g., AMC085 or S0816)6,25,26 suggest somewhat lower PFS among PWH in the current study, such cross-trial inferences are inherently confounded by differences in cohort size, patient selection, staging, and response assessments. For instance, the S1826 HIV subcohort had a higher proportion of individuals with stage IV disease than AMC085, and the latter also enrolled participants with stage II disease. It is important to note that landmark trials in advanced stage cHL, including ECHELON-1 and German Hodgkin Study Group HD21, excluded PWH,27 underscoring the persistent gap in inclusive clinical trial design.
Although this analysis is not designed to directly compare N+AVD and BV+AVD due to the small number of PWH enrolled, N+AVD had an overall excellent safety profile among PWH. The incidence of febrile neutropenia was lower in the N+AVD arm. There were also more serious infections and episodes of sepsis, including one death on treatment, in the BV+AVD arm. The rates of peripheral neuropathy were higher in BV+AVD arm compared with N+AVD. The one death in the N+AVD arm occurred more than 2 years following treatment completion and was unrelated to treatment toxicity or cHL recurrence. Although S1826 did not evaluate the effects of N+AVD on CD4+ T-cell counts and HIV control, the absence of AIDS-defining opportunistic infections and immune-related adverse events is encouraging. We were also unable to assess the effects of ART regimen on toxicity. While S1826 excluded participants with CD4+ T-cell counts <200 cells/μL, other prospective and retrospective studies have demonstrated that PD-1 blockade is safe and effective even in those with CD4+ T-cell counts <50 cells/μL.21,28-30 Future real-world data of N+AVD in HIV-associated with cHL will help determine if the same T-cell spring effects are observed with N+AVD as demonstrated in studies of single-agent PD-1 blockade and with BV-AVD.6,29
In summary, these data indicate that N+AVD is safe and effective in PWH with newly diagnosed advanced stage cHL, with no unexpected toxicities related to the PD-1 blockade. Our data suggest that PWH with advanced stage cHL should be considered for N+AVD. S1826 highlights the feasibility and reinforces the importance of expanding eligibility criteria in future studies to improve evidence-based care for this population.
Supplementary Material
Funding:
Funding provided by the National Cancer Institute of the National Institutes of Health U10CA180888, U10CA180819; and in part by BMS. This paper was supported by the Leukemia & Lymphoma Society CDP grant- Scholar in Clinical Research (G.G., A.F.H.), the American Cancer Society award RSG-24-1317006-01-CTPS (G.G.), the V Foundation Clinical Scholar Program award VC2021-002 (A.F.H.).
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