Abstract
Patients receiving chimeric antigen receptor T cell (CAR-T) therapy may have impaired humoral responses to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccinations owing to their underlying hematologic malignancy, prior lines of therapy, and CAR-T-associated hypogammaglobulinemia. Comprehensive data on vaccine immunogenicity in this patient population are limited. A single-center retrospective study of adults receiving CD19 or BCMA-directed CAR-T therapy for B cell non-Hodgkin lymphoma or multiple myeloma was conducted. Patients received at least 2 doses of SARS-CoV-2 vaccination with BNT162b2 or mRNA-1273 or 1 dose of Ad26.COV2.S and had SARS-CoV-2 anti-spike antibody (anti-S IgG) levels measured at least 1 month after the last vaccine dose. Patients were excluded if they received SARS-CoV-2 monoclonal antibody therapy or immunoglobulin within 3 months of the index anti-S titer. The seropositivity rate (assessed by an anti-S assay cutoff of ≥.8 U/mL in the Roche assay) and median anti-S IgG titers were analyzed. Fifty patients were included in the study. The median age was 65 years (interquartile range [IQR], 58 to 70 years), and the majority were male (68%). Thirty-two participants (64%) had a positive antibody response, with a median titer of 138.5 U/mL (IQR, 11.61 to 2541 U/mL). Receipt of ≥3 vaccines was associated with a significantly higher anti-S IgG level. Our study supports current guidelines for SARS-CoV-2 vaccination among recipients of CAR-T therapy and demonstrates that a 3-dose primary series followed by a fourth booster increases antibody levels. However, the relatively low magnitude of titers and low percentage of nonresponders demonstrates that further studies are needed to optimize vaccination timing and determine predictors of vaccine response in this population.
Key words: SARS-CoV-2 vaccination, Anti-Spike antibody, CAR T cell therapy, SARS-CoV-2
Graphical Abstract
INTRODUCTION
Chimeric antigen receptor T cell (CAR-T) therapy targeting B cell maturation antigen (BCMA) and CD19 has revolutionized treatment for patients with relapsed/refractory hematologic malignancies. Evolving data demonstrate that patients who receive CD19-directed or BCMA-directed CAR-T therapy may be at high risk for severe Coronavirus disease 2019 (COVID-19) and unfavorable outcomes, such as prolonged or intractable infection 1, 2, 3, 4, 5. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination may be an effective strategy to prevent and mitigate disease severity. Current guidelines consider the primary series for immunocompromised patients to consist of 3 mRNA vaccines or 1 dose of the vector-based vaccine, followed by a second dose of the mRNA vaccine, plus a booster. However, despite these vaccination strategies, CAR-T recipients have been shown to have impaired humoral responses, likely due to the high net state of immunosuppression associated with the underlying disease, prior lines of therapy, and CAR-T-associated toxicities, such as hypogammaglobulinemia 6, 7, 8, 9, 10, 11.
Several systematic reviews that evaluated the cumulative response rate have reported a pooled post-SARS-CoV-2 vaccine serologic response between 31% and 35.9% [8,12]. However, the results of these pooled analyses are not generalizable, owing to differences in assays, selection of different cutoff values, and variability of the timing of humoral response measurement. Additionally, a recent prospective study evaluating humoral and cellular response to SARS-CoV-2 vaccinations after CD19-directed or BCMA-directed CAR-T therapy demonstrated that 3 of 5 patients (60%) with preestablished anti-Spike antibody (anti-S IgG) remained positive at day 30 post-CAR-T therapy, suggesting a potential role for vaccination prior to CAR-T therapy, although the duration of sustained immunogenicity post-CAR-T therapy remains unclear [13]. Comprehensive data on the immunogenicity and efficacy of SARS-CoV-2 vaccination among this vulnerable population of CAR-T recipients is urgently needed to optimize vaccination recommendations and identify improved strategies for protection.
METHODS
Study Design
This single-center retrospective study of adults age ≥18 years receiving commercially available CD19-directed or BCMA- directed CAR-T therapy for B cell non-Hodgkin lymphoma or multiple myeloma from March 2018 through May 2022 was performed at Dana-Farber Cancer Institute (DFCI). Patients were identified through the DFCI Commercial Immune Effector Cells Database. This study was approved by the DFCI Office for Human Research Studies. Demographic data, treatment characteristics, SARS-CoV-2 vaccination history, and report of COVID-19 via PCR and anti-S IgG titers (Roche assay) were collected from the electronic medical record. Additionally, exposure to potential variables that could affect the immune response to SARS-CoV-2 vaccinations, such as cytokine release syndrome, immune effector cell-associated neurotoxicity syndrome (ICANS), and administration of corticosteroids or tocilizumab, was captured from the electronic medical record.
CD19-directed or BCMA-directed CAR-T recipients were included if they had received vaccination with ≥2 doses of BNT162b2 (Pfizer, BioNTech; 30 μg) or mRNA-1273 (Moderna; 50 or 100 μg) or 1 dose of Ad26.COV2.S (Janssen; .5 mL) and had SARS-CoV-2 anti-S IgG measured at least 1 month after CAR-T therapy and at least 1 month after the last vaccine dose. Anti-S IgG was assessed using the commercially available Roche Elecsys anti-SARS-CoV-2 S assay, which has a cutoff point at .80 U/mL (≥.80 U/mL is reactive; nonreactive set to <.40 U/mL) and an upper limit of 12,500 U/mL [14]. A positive anti-S response for the study was defined as ≥.80 U/mL. Participants who received vaccination after CAR-T therapy waited at least 3 months from infusion, with no other specific criteria for the vaccination schedule (Supplementary Figure S1). CAR-T recipients who received SARS-CoV-2 monoclonal antibody (mAb) therapy or immunoglobulin within 3 months of the index anti-S titer were excluded. Participants were followed for 3 months before their first COVID-19 vaccination through receipt of their index anti-S IgG result. Participants were censored on the first day of any additional antineoplastic therapy after disease relapse. The primary endpoint was the percentage of participants who developed a positive anti-S response.
Statistical Analysis
Categorical data are expressed as number (percentage) and continuous data are expressed as median (interquartile range [IQR]). The Wilcoxon rank-sum test was used to analyze nonparametric continuous variables. Multivariable log10-transformed linear regression was used to identify characteristics that predict vaccine response. The following prespecified covariates were included based on clinical significance: ≥3 SARS-CoV-2 vaccinations, ICANS requiring high-dose corticosteroid (≥20 mg/day of prednisone equivalent), IgG <400 mg/dL, days from vaccination to anti-S IgG, and vaccination after CAR-T therapy. Stata version 14.2 (StataCorp, College Station, TX) and Prism version 9.4.1 (GraphPad Software, Sane Diego, CA) were used for analyses.
RESULTS
A total of 401 individuals underwent CD19 or BCMA CAR-T therapy during the study period, of whom 50 met the inclusion criteria and were included in our analysis (Supplementary Figure S2). The median age of the cohort was 65 years (IQR, 58 to 70 years), 68% were male, and 88% received CD19-targeted CAR-T therapy for the treatment of B cell non-Hodgkin lymphoma (Table 1 ). Participants received different types and combinations of vaccines (Supplementary Table S1); most received a total of 3 mRNA vaccines (Table 2 ). The majority of participants (n = 32; 64%) received at least 1 vaccination after CAR-T therapy, with a median time from CAR-T therapy to vaccination of 174 days (IQR, 110 to 294 days).
Table 1.
Baseline Patient Characteristics (N = 50)
| Characteristic | Value |
|---|---|
| Age at first dose, yr, median (IQR) | 65 (58-70) |
| Male sex, n (%) | 34 (68) |
| CAR T cell product, n(%) | |
| Axicabtagene ciloleucel | 29 (58) |
| Lisocabtagene maraleucel | 10 (20) |
| Brexucabtagene autoleucel | 5 (10) |
| Idecabtagene vicleucel | 6 (12) |
| CAR T cell type, n (%) | |
| CD19 | 44 (88) |
| BCMA | 6 (12) |
| Underlying disease, n (%) | |
| B-cell non-Hodgkin lymphoma | 44 (88) |
| Diffuse large B cell lymphoma | 23 (46) |
| Transformed follicular lymphoma | 6 (12) |
| Mantel cell lymphoma | 5 (10) |
| Follicular lymphoma | 4 (8) |
| Other | 6 (12) |
| Multiple myeloma | 6 (12) |
| IgG | 4 (8) |
| IgA | 2 (4) |
| Ethnicity, n (%) | |
| Non-Hispanic | 49 (98) |
| Race, n (%) | |
| White | 45 (90) |
| African American | 3 (6) |
| Other | 2 (4) |
| Obesity, BMI ≥30 kg/m2, n (%) | 14 (28) |
| Previous hematopoietic stem cell transplantation, n (%) | 22 (44) |
| Autologous | 21 (42) |
| Allogenic | 1 (2) |
| Prevaccine absolute neutrophil count, K/μL, median (IQR) | 2.64 (2.04-3.91) |
| Prevaccine absolute lymphocyte count, K/μL, median (IQR) | .88 (.58-1.55) |
| Prevaccine IgG level, mg/dL, median (IQR) | 807.00 (451.50-943.50) |
| Prevaccine CD4 level, cells/μL, median (IQR) | 150.00 (61.00-302.25) |
| Hypogammaglobulinemia (IgG <400 mg/dL) prior to vaccination, n (%) | 7 (14) |
Table 2.
Treatment Characteristics
| Characteristic | Value |
|---|---|
| Anti-CD20 within 6 mo of vaccination through anti-S IgG result, n (%) | 17 (34) |
| Tocilizumab within 3 mo of vaccination through anti-S IgG result, n (%) | 23 (46) |
| Corticosteroids within 3 mo of vaccination through anti-S IgG result, n (%) | 11 (22) |
| ICANS within 3 mo of vaccination through anti-S IgG result, n (%) | 8 (16) |
| Cytokine release syndrome within 3 mo of vaccination through anti-S IgG result, n (%) | 25 (50) |
| Number of vaccines received, n (%) | |
| 1 | 1 (2) |
| 2 | 9 (18) |
| 3 | 32 (64) |
| 4 | 8 (16) |
| Vaccines received post-CAR T cell therapy, n (%) | 32 (64) |
| Time from CAR T cell therapy to vaccination d, median (IQR) | 174 (110-294) |
| Time from last vaccination to anti-S IgG, d, median (IQR) | 140 (71-211) |
| Time from CAR T cell therapy to anti-S IgG, d, median (IQR) | 152 (90-279) |
Overall, 32 participants (64%) developed a positive anti-S IgG antibody response after at least 1 vaccine, with a median SARS-CoV-2 anti-S IgG titer of 138.5 U/mL (IQR, 111.6 to 2541.0 U/mL) among these responders. Of these, 12 participants (37.5%) had an antibody response of .8 to 50 U/mL, 5 (15.6%) had an antibody response of 51 to 150 U/mL, 2 (6.3%) had an antibody response of 150 to 300 U/mL, and 13 (40.6%) had an antibody response of >300 U/mL. The median time from last vaccination to anti-S IgG result was 140 days (IQR, 71 to 211 days). Although 4 participants (8%) in the cohort tested positive for SARS-CoV-2 via PCR, these infections occurred >3 months beyond the reported index anti-S IgG, except for 1 participant who had a positive PCR result on the day of the negative index anti-S IgG (Supplementary Table S2).
The median anti-S IgG titers for all CAR-T recipients increased as the number of vaccinations increased (2.4 U/mL after 2 doses versus 7.3 U/mL after 3 doses versus 71.3 U/mL after 4 doses) (Supplementary Table 3, Figure 1 A). In our log10-transformed multivariable linear regression, we identified that among responders, receipt of ≥3 vaccines was associated with a significantly higher anti-S IgG titers compared to receipt of <3 vaccines, after adjusting for hypogammaglobulinemia, ICANS, vaccination before or after CAR-T therapy, and time from vaccine to anti-S IgG (Supplementary Table S4). However, it is notable that 14 of the 40 participants (35%) who had received ≥3 SARS-CoV-2 vaccinations could not mount a positive response, demonstrating that even additional doses were not sufficient to seroconvert all participants.
Figure 1.
Median anti-S IgG stratified by number of vaccines received, CAR-T target, and timing of vaccines in relation to CAR T therapy.
Eighteen participants (36%) received all SARS-CoV-2 vaccinations before CAR-T therapy and had a higher median anti-S IgG titer compared to participants who received at least 1 vaccination after CAR-T therapy (192.2 U/mL versus 3.3 U/mL; P = .029) (Supplementary Table S3, Figure 1B). Of those who received SARS-CoV-2 vaccinations before CAR-T therapy, 2 participants (11.1%) received BCMA-targeted CAR-T therapy for multiple myeloma and 16 (88.9%) received CD19-targeted CAR-T therapy for B cell non-Hodgkin lymphoma. Thirty-two participants (64%) received at least 1 SARS-CoV-2 vaccination after CAR-T therapy, and of these, 4 participants (12.5%) received BCMA-targeted CAR-T therapy for multiple myeloma and 28 (87.5%) received CD19-targeted CAR-T therapy for B cell non-Hodgkin lymphoma. Additional patient characteristics are provided in Supplementary Table S5.
The median anti-S IgG titer was similar in recipients of BCMA-targeted CAR-T therapy and recipients of CD19-targeted CAR-T therapy was similar (9.9 U/mL versus 9.3 U/mL; P = .90) (Supplementary Table S3, Figure 1C).
DISCUSSION
In our cohort, 64% of CD19-directed or BCMA-directed CAR-T recipients developed a positive response to SARS-CoV-2 vaccinations, although with a relatively low median titer compared to other published data using the same assay in healthy controls. Here the median anti-S IgG titer from the CAR-T participants was lower than the median anti-S IgG titer in a cohort of healthy healthcare workers from our institution after receipt of a 2-dose mRNA COVID-19 vaccine series: 7.76 U/mL (IQR, .4 to 359.0 U/mL) at a median of 140 days after the last vaccine dose versus 4382.5 U/mL (IQR, 1787.5 to 6640.0 U/mL) at 28 days after the last vaccine dose and 767.5 U/mL (IQR, 743.5 to 932.5 U/mL) at approximately 235 days after last vaccine dose [15]. Although the assay cutoff does not reflect a correlate of protection, which has not been established and differs by vaccine type, host characteristics, and circulating SARS-CoV-2 variants [16], higher antibody levels are clearly associated with greater vaccine-induced protection against symptomatic COVID-19 17, 18, 19.
In our analysis, receipt of ≥3 vaccines was associated with significantly higher anti-S antibody titers in those who had positive anti-S titers after the second dose, which is consistent reported results in healthy adults and patients with hematologic malignancies [20,21]. It is important to note that in our analysis, 35% of participants who received ≥3 vaccinations were unable to mount a humoral response to vaccination, highlighting that additional doses do not necessarily increase the rate of seroconversion in certain patients in this highly immunosuppressed population. Additional studies are warranted to identify factors that predict vaccine response for CAR-T recipients and to clarify the optimal timing of doses before and after CAR-T therapy.
Although the majority of our participants received SARS-CoV-2 vaccination after CAR-T therapy, an interesting finding in our study is the higher seropositivity rate in those who received vaccinations only before CAR-T and had not yet been revaccinated after CAR-T therapy compared to those who received at least 1 vaccination after CAR-T therapy (77.8% vs 56.3%). Additionally, the median anti-S IgG was significantly higher among those who received SARS-CoV-2 vaccination before CAR-T therapy compared to those who received at least 1 vaccination after CAR-T therapy. However, after adjusting for potential covariates, this finding was no longer statistically significant.
These findings indicate possible retention of preestablished SARS-CoV-2 immunity after CAR-T therapy, which has been described in the literature, although the durability of this immunity over time remains unclear [13]. Only 1 patient in this group had anti-S IgG titers measured both before and after CAR-T therapy, both of which were >2500 U/mL. In a recent study by Walti et al. [10] that examined seroprotection against the influenza vaccine, antibody responses (at least 4-fold titer increases from baseline) occurred in 40% (n = 2) of those vaccinated before CAR-T therapy, compared with 31% (n = 4) of those vaccinated after CAR-T therapy [10]. Another study evaluating antibody response for other vaccine-preventable infections similarly showed that that seroprotection for vaccine-preventable diseases after CD19-directed CAR-T therapy was comparable to that in the general population when vaccines were administered before CAR-T [11]. These data support consideration of SARS-CoV-2 vaccination before CAR-T therapy.
Our study is limited by the small sample size and the retrospective design, which is subject to confounding. As noted above, we accounted for this potential limitation in our regression model with available data, but our findings should be confirmed in larger, prospective studies. Another limitation is that we assessed only a single anti-S IgG level, which may limit our understanding of longitudinal vaccine response and antibody decay. Additionally, without a known correlate of protection, the clinical efficacy of these findings is unknown and needs to be validated. Moreover, this study did not assess cellular immunity, which may contribute to protection against SARS-CoV-2 in this patient population. In addition, the relatively high median IgG level before vaccination suggests that our cohort might not be representative of all patients who receive CAR-T therapy. Finally, the heterogeneity in disease type, CAR-T targets, vaccination type, and timing of the vaccine and anti-S IgG titers might have impacted our results, although this was mitigated by incorporating the timing from vaccine to anti-S IgG titers and receipt of vaccines before or after CAR-T therapy into the regression model.
Our study supports current guidelines for SARS-CoV-2 vaccination in CAR-T therapy recipients and demonstrates that a 3-dose primary series followed by a fourth booster increases antibody levels in patients who are able to mount a humoral response. However, further prospective studies are needed to optimize vaccination timing before and after CAR-T therapy and to identify predictors of vaccine response in this vulnerable population. Multipronged approaches are needed to prevent COVID-19 and mitigate disease severity in patients undergoing CAR-T therapy.
ACKNOWLEDGMENTS
Financial disclosure: G.Z. has received support from the University of British Columbia/British Columbia Children's Hospital for statistical consulting on multiple projects involving continuous physiological monitoring to improve pediatric care in resource-limited settings, funded by the Bill & Melinda Gates Foundation. J.C. reports research funding from AbbVie, Bayer, Genentech, Merck, and the National Institutes of Health (NIH; Grant K12 CA087723). L.R.B. reports research support from the NIH (including National Institute of Allergy and Infectious Diseases and the National Center for Advancing Translational Sciences), the Wellcome Trust, and the Bill & Melinda Gates FoundationN.C.I. reports funding from AiCuris, Merck, Fujifilm, Astellis, and GSK. S.P.H. reports receiving research support from F2G, GSK, Merck, and ScynexisC.A.J. reports research funding from Kite/Gilead and Pfizer.
Conflict of interest statement: J.C. reports consulting for Karyopharm, MorphoSys, Incyte, and Kite PharmaL.R.B. has served on a data and safety monitoring board, safety monitoring committee, and advisory committee for the NIH and Food and Drug Administration; and is involved in HIV, COVID-19, and other vaccine clinical trials conducted in collaboration with the NIH, HIV Vaccine Trials Network, COVID Vaccine Prevention Network, International AIDS Vaccine Initiative, Crucell/Janssen, Moderna, Military HIV Research Program, the Bill & Melinda Gates Foundation, and the Ragon Institute.S.P.H. reports serving on advisory boards for F2G and Pfizer. C.A.J. reports consulting for Kite/Gilead, Novartis, BMS/Celgene, bluebird bio, Epizyme, Abintus Bio, Instil Bio, Caribou Bio, ImmPACT Bio, Morphosys, Miltenyi, and Astra Zeneca.
Authorship statement: C.A.J. and A.C.S. contributed equally to this study.
Footnotes
Financial disclosure: See Acknowledgments on page 398.e4.
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.jtct.2023.03.005.
Appendix. Supplementary materials
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