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Safety and Efficacy of Bnt162b Mrna Covid19 Vaccine in Patients with Chronic Lymphocytic Leukemia

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Safety and Efficacy of Bnt162b Mrna Covid19 Vaccine in Patients with Chronic Lymphocytic Leukemia Safety and efficacy of BNT162b mRNA Covid19 Vaccine in patients with chronic lymphocytic leukemia by Ohad Benjamini, Lior Rokach, Gilad Itchaki, Andrei Braester, Lev Shvidel, Neta Goldschmidt, Shirley Shapira, Najib Dally, Abraham Avigdor, Galia Rahav, Yaniv Lustig, Shirley Shapiro Ben David, Riva Fineman, Alona Paz, Osnat Bairey, Aaron Polliack, Ilana Levy, and Tamar Tadmor. Collaborative Groups: Israeli CLL study group (ICLLSG)) Received: May 12, 2021. Accepted: June 22, 2021. Citation: Ohad Benjamini, Lior Rokach, Gilad Itchaki, Andrei Braester, Lev Shvidel, Neta Goldschmidt, Shirley Shapira, Najib Dally, Abraham Avigdor, Galia Rahav, Yaniv Lustig, Shirley Shapiro Ben David, Riva Fineman, Alona Paz, Osnat Bairey, Aaron Polliack, Ilana Levy, and Tamar Tadmor. Collaborative Groups: Israeli CLL study group (ICLLSG)). Safety and efficacy of BNT162b mRNA Covid19 Vaccine in patients with chronic lymphocytic leukemia. Haematologica. 2021 Jul 29. doi: 10.3324/haematol.2021.279196. [Epub ahead of print] Publisher's Disclaimer. E-publishing ahead of print is increasingly important for the rapid dissemination of science. Haematologica is, therefore, E-publishing PDF files of an early version of manuscripts that have completed a regular peer review and have been accepted for publication. E-publishing of this PDF file has been approved by the authors. After having E-published Ahead of Print, manuscripts will then undergo technical and English editing, typesetting, proof correction and be presented for the authors' final approval; the final version of the manuscript will then appear in a regular issue of the journal. All legal disclaimers that apply to the journal also pertain to this production process. Safety and efficacy of BNT162b mRNA Covid19 Vaccine in patients with chronic lymphocytic leukemia Ohad Benjamini1,2, Lior Rokach3, Gilad Itchaki4, Andrei Braester5, Lev Shvidel6, Neta Goldschmidt7, Shirley Shapira8, Najib Dally9, Abraham Avigdor1,2, Galia Rahav10,2, Yaniv Lustig11, Shirley Shapiro Ben David8, Riva Fineman12, Alona Paz13,14, Osnat Bairey4, Aaron Polliack7, Ilana Levy15, and Tamar Tadmor14,15 on behalf of the Israeli CLL study group (ICLLSG). Type of article: Original article Corresponding author: Tamar Tadmor, Bnai Zion Medical center, Haifa, Israel 31048. [email protected]. Tel: +972506268114, Fax: +97248359962 Affiliation: 1Hematology Division, Chaim Sheba Medical Center, Tel-Hashomer, 2Sackler Faculty of Medicine, Tel-Aviv University, Israel. 3Department of Software and Information Systems Engineering, Ben-Gurion University of the Negev, Beer- Sheva, Israel. 4Institute of Hematology, Davidoff Cancer Center, Rabin Medical Center, Petah Tikva, Israel. 5Department of Hematology Galilee Medical Center, Nahariya, Israel. 6Hematology Institute, Kaplan Medical Center, Rehovot, Israel. 7Hematology, Hadassah Medical Center, Jerusalem, Israel. 8Health Division, Maccabi Healthcare Services, Tel Aviv, 9Division of Hematology, Ziv Medical Center, Safed, Israel. 10The Infectious Disease Unit, Sheba Medical Center, Tel-Hashomer, Israel. 11Central Virology Laboratory, Ministry of Health and Sheba Medical Center, Tel- Hashomer, Israel. 12Department of Hematology and BMT, Rambam Health Care Campus, Haifa, Israel. 13Infectious Disease Unit, Bnai Zion Medical Center, Haifa, Israel. 14The Ruth and Bruce Rappaport Faculty of Medicine, Technion, Haifa, Israel. 15Hematology Unit, Bnai Zion Medical Center, Haifa, Israel. Keywords: Chronic lymphocytic leukemia, CLL, Covid-19, BNT162b2 mRNA Covid-19 Vaccine, Immune response Running Head: Covid19 Vaccine in patients with CLL Word count: Trial registration; ClinicalTrials.gov NCT04862806 Acknowledgments: we thank the study coordinators, with special thanks to Mrs. Andrea Shoukair. No conflict of interest to declare Figures: 4 Tables: 4 Grant by Janssen pharmaceutical number EV00261620 Author's contributions: Tamar Tadmor and Ohad Benjamini designed, organized and wrote the manuscript Lior Rokach- performed al statistical and machine learning analysis including 7 parameters models, and was involved in writing the manuscript. Aaron Poliiack helped in writing the manuscript. Gilad Itchaki, Andrei Braester, Lev shvidel, Neta Goldschmidt, Shirley Shapira8, Najib Dally, Abraham Avigdor, Galia Rahav Yaniv Lustig, Shirley Shapiro Ben David, Riva Fineman, Alona Paz, and Ilana Levy contributed patient's data. Abstract: Patients with chronic lymphocytic leukemia (CLL) have a suboptimal humoral response to vaccination. Recently, a BNT162b2 mRNA COVID-19 vaccine was introduced with a high efficacy of 95% in immunocompetent individuals. We investigated the safety and efficacy of BNT162b2 mRNA Covid-19 vaccine in patients with CLL from nine medical centers in Israel, In total 400 patients were included, of which 373 were found to be eligible for the analysis of antibody response. The vaccine appeared to be safe and only grade 1-2 adverse events were seen in 50% of the patients. Following the second dose, antibody response was detected in 43% of the cohort. In treatment- naïve patients 61% responded to the vaccine, while only 18%, 37% and 5% of patients with CLL ongoing, previously treated with BTKi, or recent anti CD20 antibody developed responses respectively. 62% and 14% of patients treated with BCL2 monotherapy or combined with anti CD20 developed immune response respectively. Neutralizing antibodies demonstrated high concordance with positive serologic response to spike (S) protein. Based on our results a simple scoring model including recent treatment with anti-CD20, age younger than 70 years, treatment naïve status, and normal IGG, IGA, IGM and hemoglobin levels. The sum of all the above parameters can serve as a possible estimate to predict whether a given CLL patient will develop sufficient antibodies. In conclusion, the vaccine was found to be safe in patients with CLL, but its efficacy is limited particularly in treated patients. Introduction COVID-19 pandemic has become the main healthcare issue worldwide since its appearance at the end of 2019, affecting millions of people globaly.1 International efforts generated a vaccine against the virus, which was both safe and highly effective. In December 2020, results of a clinical trial using the BNT162b2 mRNA Covid-19 in a large cohort of people (16 years of age or more) demonstrated a 95% efficacy in preventing symptomatic infection2. This study prompted an emergency use authorization (EUA) from the FDA3. Real-world data using a nationwide vaccination setting from Israel reported high efficacy of the vaccine even in patients with multiple comorbidities4. However, the trial excluded immunosuppressed patients, as their immune response to vaccination is usually blunted. CLL is associated with varying degrees of immune deficiency due to the primary disease or to the therapy administered. These include functional defects of B and T-lymphocytes, NK cells, neutrophils and macrophages6, as well as hypogammaglobulinemia, which is evident in treatment –naïve patients and develops even more frequently following therapy for CLL 5 -6. Large retrospective studies from both Europe7,8 and US9 have already reported that patients with CLL have an increased rate of COVID-19 infection, a higher hospitalization rate and a greater risk of dying from the virus irrespective of disease stage or prior treatment status. Therefore, the role of vaccination in these patients is of major importance and in this respect, several studies have already shown that patients with CLL mount limited responses to other more frequently used vaccines like those for influenza10, pneumococcal infection 11 or varicella zoster (VZ)12. Furthermore, only limited data is available on the vaccine response in the era of novel biological agents now used to treat CLL such as BTK and BCL2 inhibitors in combination with anti CD20 antibodies13-15. A previous publication demonstrated reduced serologic response rate to the vaccine in patients with CLL compared to healthy controls particularly during therapy16. The aim of the study we report here was to investigate the safety , efficacy and the effect of therapy on the serologic response to BNT162b2 mRNA Covid-19 vaccine in patients with CLL given in 9 medical centers in different parts of Israel and . Methods Patients: This was a prospective, interventional, multicenter study that was performed on behalf of the Israeli CLL study group. The retrieved data from 9 centers in Israel provided information on a total of 400 patients who had been vaccinated with BNT162b2 mRNA Covid-19 vaccine. Diagnosis of CLL was established according to the IWCLL criteria 5. Data was collected from medical records after approval by all the individual institutes Helsinki ethics committees was registered at ClinicalTrials.gov NCT04862806 and all patients who participated gave written informed consent. The referring physicians collected demographic and clinical data from the patients’ medical records; these included clinical patient characteristics (gender, age, Binet stage, medical history including CIRS score), previous treatments (number and type), biologic features of CLL (serum IgG, IgA, IgM levels, IGHV mutation status, FISH cytogenetic profile, and TP53 mutation) whenever available. Vaccination and immune response assessment: All patients received two 30-μg doses of BNT162b2 vaccine (Pfizer), administered intramuscularly 3 weeks apart. Blood samples for Immune response evaluation to the above vaccine was assessed after 2-3 weeks (median of 19 days) following the second
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