ASH-ASTCT COVID-19 Vaccination for HCT and CAR T Cell Recipients: Frequently Asked Questions
(Version 1.0; last updated January 28, 2021)
Input from Fareed Khawaja, MD; Roy F. Chemaly, MD, PhD; Sanjeet Dadwal, MD; Steven A. Pergam, MD, MPH; John Wingard, MD; Jeffery Auletta, MD; Zeinab El Boghdadly, MBBCh; Maheen Abidi, MD; Alpana Waghmare, MD; Zainab Shahid, MD; Joshua Hill, MD; Tobias M. Hohl, MD, PhD; Mini Kamboj, MD; Genovefa Papanicolaou, MD; and Michael Boeckh, MD.
The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) pandemic continues to cause excess morbidity and mortality in the US and worldwide. Hematopoietic cell transplant (HCT) and chimeric antigen receptor T (CAR T) cell recipients are at higher risk for serious complications from the virus, including hospitalization, ICU admission and death from COVID-19 ).1-4 These patients are commonly also burdened with other conditions associated with COVID-19–related mortality, including older age, cardiovascular disease, renal dysfunction, profound immunosuppression, and other complications of prior therapies or their underlying disease, which further contribute to worse outcomes.
In the United States, two novel messenger RNA (mRNA) vaccines have been approved through the Food and Drug Administration’s (FDA’s) Emergency Use Authorizations. The BNT162b2 Covid-19 Vaccine (Pfizer/BioNTech) and the mRNA-1273 SARS-CoV-2 Vaccine (Moderna) have both been shown in large phase III clinical trials to be more than 90% effective at preventing COVID-19 illness and major complications.5,6 Despite varied approaches to local allocation of vaccines among states and U.S. territories, HCT and CAR T cell recipients should be prioritized to be vaccinated as early in the allocation process as possible, although data on vaccine safety and efficacy are not yet available in these populations and will likely not be available for months after vaccinations begin in the United States. However, given the high level of protection afforded to those vaccinated in the clinical trials, the American Society of Transplantation and Cellular Therapy (ASTCT) and the American Society of Hematology (ASH) strongly support early access to vaccines for these vulnerable patients, along with their caregivers, family, and household contacts when vaccine supply permits.
This document will be updated periodically when new data become available. All current guidance is based on opinions of the ASTCT/ASH COVID-19 Vaccine expert panel. Furthermore, the expert panel recognizes that vaccine supply varies between states due to federal and state allocation, and our opinion is not meant to supersede vaccine eligibility as determined by the state or federal government.
Section A: Recommendations on timing of COVID-19 vaccine in HCT and CAR T cell recipients, and considerations for delay
When should COVID-19 vaccines be administered to autologous HCT, allogeneic HCT, and CAR T cell recipients?
HCT or CAR T cell recipients are often immunosuppressed for months following treatment due to conditioning regimens, maintenance therapies, immunosuppressive drugs, hypogammaglobinemia, and/or graft-versus-host disease (GvHD), blunting immune response, and decreasing vaccine efficacy.7-9 These patients are also at risk of severe and life-threatening COVID-19 if they are infected.1-4 Based on prior antigen-based vaccine trials in allogeneic HCT recipients, initiating vaccination series three (3) months versus six (6) months after transplantation did not affect the induction of immune responses.8,10-12 No clinical trial data regarding the optimal time to initiate vaccinations in HCT and CAR T cell recipients are available but it is of high priority. Based on current evidence demonstrating high efficacy and safety in the general population, including individuals with underlying conditions, currently available mRNA SARS-CoV-2 vaccines could be offered as early as three (3) months following HCT or CAR T cell therapies, although efficacy may be reduced compared to results in general populations, as suggested from evidence about the impact of influenza vaccinations on community outbreaks.11
When should delay of vaccination be considered in HCT or CAR T cell recipients?
Cytotoxic or B-cell–depleting therapies after HCT or CAR T cell therapy are often used for maintenance or to treat HCT complications and may contribute to poor vaccine immune responses.13 Patients scheduled for such therapies should complete their COVID-19 vaccination prior to initiation or between cycles of cytotoxic or B-cell–depleting therapies if possible. Based on a phase I trial of the mRNA SARS-CoV-2 vaccines, peak neutralizing antibodies developed seven (7) to 14 days after the second dose of the series.14 HCT and CAR T recipients scheduled to undergo cytotoxic or B-cell–depleting therapies could be offered the COVID-19 vaccine prior to therapy and allowed at least two (2) weeks to pass after the second dose to allow memory T cell formation prior to giving cytotoxic or B-cell depleting therapies if feasible.
Human intravenous immunoglobulin (IVIG) is often given to HCT or CAR T cell recipients with hypogammaglobinemia due to poor B cell function. As SARS-CoV-2 becomes more widespread, antibodies to SARS-CoV-2 may become detectable in pooled IVIG. Theoretically, the anti-SARS-CoV-2 antibodies in pooled IVIG may dampen the immune response to the vaccines and interfere with serologic testing; for this reason, IVIG recipients were excluded from the phase III mRNA COVID-19 vaccine trials.5,6 However, based on recent Centers for Disease Control and Prevention (CDC) recommendations, no delay in vaccination is recommended for patients who are receiving IVIG. These recommendations may change when more data are available.
When should HCT and CAR T cell recipients receive their second dose of the COVD-19 vaccine if they become infected with SARS-CoV-2 between doses?
If vaccines become infected prior to the second dose, the CDC recommends delaying the second dose of either the Moderna or Pfizer series.15 However, these patients were originally restricted from receiving the second dose in the phase III clinical trials.5,6 Further analysis of patients with asymptomatic infection between doses is ongoing. Based on data from patients previously infected with COVID-19 prior to mRNA vaccination series, HCT and CAR T cell recipients infected with COVID-19 between the first and the second vaccinations could be offered the second dose of their respective vaccines once symptoms have resolved and isolation precautions are discontinued, as there is no indication so far of vaccine-associated enhanced disease (VAED) or other serious adverse events.
When can the current COVID-19 vaccines be given after therapy with SARS-CoV-2 monoclonal antibodies or convalescent plasma in HCT and CAR T cell recipients?
No safety and efficacy data have been published on the use of mRNA SARS-CoV-2 vaccines after receipt of SARS-CoV-2 monoclonal antibodies or convalescent plasma in patients given these treatments due to COVID-19 disease; these patients were specifically excluded from the phase III mRNA COVID-19 vaccine trials.5,6 CDC guidelines recommend delaying vaccination for 90 days based on the half-life of SARS-CoV-2–specific antibodies, and based on the evidence that true reinfection with the virus after natural infection is extremely uncommon within three (3) months.15-17 Currently, we recommend delaying COVID-19 vaccination for 90 days in HCT and CAR T cell recipients if they received either SARS-CoV-2 monoclonal antibodies or COVID-19 convalescent plasma, in alignment with the CDC recommendations.
Can SARS-CoV-2 monoclonal antibodies be given to HCT and CAR T cell recipients who develop COVID-19 after receipt of mRNA COVID-19 vaccines?
Efficacy of mRNA vaccines in HCT and CAR T cell recipients is unknown as clinical trials did not include these patient populations. However, if SARS-CoV-2 infection is acquired after receiving the COVID-19 vaccine, these patients are still eligible for monoclonal antibodies under Emergency Use Authorization (EUA) guidance or convalescent plasma as part of treatment of COVID-19. Individuals who develop infection and receive monoclonal antibodies after the first dose of the vaccine should delay the second dose for 90 days.
Section B: COVID-19 vaccine safety in HCT and CAR T cell recipients
Has the mRNA SARS-CoV-2 vaccine platform previously been investigated in the immunocompromised patient population?
While there are no other licensed mRNA vaccines in the United States, mRNA-vaccine platforms have been studied in the treatment of cancer and other infections, such as influenza, Zika, rabies, and cytomegalovirus.18,19 Further investigation is warranted to study the immunogenicity and durability of the response of mRNA vaccines among this population.
What is known about the safety of mRNA SARS-CoV-2 vaccines?
The mRNA SARS-CoV-2 vaccines were administered to nearly 70,000 study participants, and safety data through at least two (2) months median follow-up has not raised any significant concerns.6,20-23 HCT and CAR T cell recipients were excluded from these trials; however, individuals with well controlled HIV infection and CD4>350 were included. Similar to other vaccines, short-term adverse effects included local injection site reactions, fever, fatigue, and headache, and they typically resolved within one (1) to two (2) days. Adults older than 55 years experienced decreased frequency and severity of local injection site reactions and systemic adverse effects. Serious adverse effects were seen in 0.5-1.5% of study participants across the three reported trials with similar distribution in control and vaccine arms. In addition, no causal relationship has been established with neurological adverse events. Patients with prior history of Guillain-Barre Syndrome and Bell’s palsy may receive the COVID-19 vaccines.
Although extrapolation of safety data to HCT and CAR T cell recipients is difficult, significant adverse effects are not anticipated, and the benefits from vaccines may outweigh any short-term or long-term adverse effects. Close monitoring for early and late postvaccination effects is warranted.
What is the safety of mRNA SARS-CoV-2 vaccines in patients with unknown prior SARS-CoV-2 exposure?
Based on prior studies in severe acute respiratory syndrome coronavirus 1 (SARS-CoV-1) and Middle East respiratory syndrome (MERS), there is a theoretical concern that formation of low titer neutralizing antibodies can precipitate a VAED.24 Although there were no HCT or CAR T cell recipients enrolled in the current clinical trials, there were no instances of suspected VAED among the individuals enrolled, including people who had history of cancer and other underlying diseases. These trials included a subset of study participants who were seropositive for SARS-CoV-2 at time of study entry and participants who developed COVID-19 in the vaccine arm. Health care providers should be vigilant for any aberrant postvaccination immune responses among transplant recipients, given their likely disordered immune responses.
What are the risks of serious allergic reactions from mRNA SARS-CoV-2 vaccines?
The potential for anaphylaxis to either mRNA vaccines is low at ~11/million for the Pfizer/BioNTech and 2.5/million for the Moderna vaccine. In individuals with history of anaphylaxis to other vaccines, counselling for a potential similar reaction is recommended and should be monitored for 30 minutes if vaccinated. All individuals who receive vaccine need to be monitored on site immediately following vaccination for at least 15 minutes. Individuals with drug or food allergies are still recommended to receive the mRNA vaccines. Patients who are allergic to components of the mRNA vaccines are advised to not get vaccinated.15 The CDC website provides detailed guidance on vaccine ingredients and triaging candidates based on their history of allergic reactions.15
Is it safe to combine routine post-transplant vaccines with SARS-CoV-2 vaccines?
The safety and efficacy of mRNA SARS-CoV-2 vaccines have not been studied when combined with other vaccines. The mRNA SARS-CoV-2 vaccines should be administered alone, separate from routine post-transplant vaccines. The interval between mRNA SARS-CoV-2 vaccine and other vaccines should be at least 14 days, both before or after its administration as per the CDC recommendations for the general population.15
Should COVID-19 vaccines be administered to HCT and CAR T cell recipients actively infected with SARS-CoV-2?
Although data from vaccine clinical trials have demonstrated safety in patients previously infected with COVID-19,5,6 the mRNA SARS-CoV-2 vaccines are not an effective treatment for ongoing COVID-19 disease. HCT or CAR T cell therapy recipients with recent COVID-19 should be offered the vaccine once symptoms resolve.
What are some considerations or concerns post–COVID-19 vaccination among HCT and CAR T cell recipients?
A study in immunocompetent individuals (<56 years of age) showed that COVID-19 mRNA vaccine BNT162b1 elicits CD4+ and CD8+ T cell responses, in particular a Th1 cell response characterized by increased production of IFNγ, IL-2 and IL-12.25 Because no HCT or CAR T cell recipients were enrolled in the mRNA vaccine trials, it remains unknown whether post-vaccination inflammatory reactions or immune activation could increase the risk for GVHD, hemophagocytic lymphohistiocytosis, transplant-associated thrombotic microangiopathy, or other immune system–related complications. Close monitoring and reporting of such events are strongly advised.
Section C: Recommendations for special HCT and CAR T cell recipient populations
What additional factors should be considered regarding COVID-19 vaccines for pediatric HCT and CAR T cell recipients?
In the United States, current EUAs allow vaccination for persons 16 and 18 years and older for the Pfizer-BioNTech vaccines and the Moderna mRNA vaccines, respectively. As in adults, there are no specific data on safety or efficacy available for pediatric HCT and CAR T cell recipients. Within age groups that qualify for vaccination under the EUAs, considerations for timing of vaccine administration are similar to those in adults. Considerations for vaccination of household contacts, use of serologic assays, use of monoclonal antibodies and convalescent plasma in the context of vaccination and co-administration with other vaccines, are the same as in adults.
Should people scheduled for HCT or CAR T therapy receive COVID-19 vaccinations prior to their procedures? Should stem cell donors receive the COVID-19 vaccination to prevent disease in transplant recipients?
To enhance vaccine immune response in HCT recipients, vaccine series have been initiated prior to transplantation in some studies, with some success in autologous HCT recipients receiving their first dose of a vaccine series prior to transplantation.26-28 However, these vaccine series included up to three (3) doses after transplantation, and the SARS-CoV-2 mRNA vaccines have not been studied in this context. The current EUAs for the COVID-19 vaccines restrict their use to two doses at specific time intervals only; deviations from the established EUAs are discouraged by the FDA, CDC, and other societies.29 Additionally, allogeneic HCT recipients receiving influenza vaccination prior to transplantation had poor immunogenic responses. At this time, transplant candidates should not be offered the COVID-19 vaccine before HCT nor CAR T cell therapies unless in the context of a research protocol.
Vaccinating stem cell donors prior to stem cell harvesting has not been shown to protect HCT recipients in prior studies.30-31 Stem cell donors should not be offered the COVID-19 vaccine for the sole purpose of benefiting the HCT recipient unless under a research protocol. However, if the donor has been vaccinated, it may be desirable to wait at least two (2) weeks after the second vaccine dose before stem cell donation (if possible) as it may provide some protective effect to the recipient.
Section D: COVID-19 serologic testing post vaccination in HCT and CAR T cell recipients
What is the appropriate timing and the role of serologic testing for COVID-19 after COVID-19 vaccination?
Neutralizing antibodies against the receptor binding domain (RBD) of the spike protein are considered protective against reinfection, in contrast to antibodies against the nucleocapsid, which are not thought to be protective.32 Available vaccines will only induce antibodies to the spike protein. In healthy individuals who had mild to moderate COVID-19 infections, high titers of neutralizing antibodies lasted up to five (5) months after initial infection, with robust antibody response occurring by day 30 post-infection.33 The correlation of antibody titers with protective immunity, as well as the duration of protective immunity after COVID-19 vaccination, are not well characterized at present. Durability of response to COVID-19 mRNA-1273 vaccine was assessed in a subset of vaccine recipients.34 Neutralizing antibodies were still detectable at day 119 and day 90 after first and second dose of the vaccine, respectively.34 Lower geometric mean titer was observed in vaccine recipients aged older than 71 years compared with those younger than 70 years.34 As the role of serologic testing post vaccination in HCT and CAR T cell recipients is not clear, we do not recommend routine testing with serology unless done under a research protocol.
On the other hand, if serologic testing is desired by the patient or health care providers, we recommend testing for SARS-COV-2 antibodies against the spike protein anytime between 30 and 90 days after the second dose of the vaccine. Importantly, some of the commercially available serology assays test for antibodies against the nucleocapsid (N) protein, not the spike protein, which therefore would not detect response to COVID-19 vaccines delivering only the spike protein or mRNA; thus, utilizing an assay detecting spike protein antibodies is of utmost importance. Additionally, with increasing prevalence of SARS-CoV-2 infection in the population and vaccination uptake across the US, pooled IVIG may contain antibodies against SARS-CoV-2 spike and nucleocapsid proteins; thus, if serologic testing is desired, we do not recommended testing for SARS-CoV-2 antibodies within four (4) weeks of IVIG infusion due to a possible false positive results.
Section E: Recommendations for the close contacts of HCT and CAR T cell recipients regarding COVID-19 vaccination.
Given the lack of published data on the safety and efficacy of the COVID-19 vaccines in immunocompromised patients, what is an effective vaccine strategy to reduce viral infection and COVID-19 disease in this setting?
Viral transmission from COVID-19 positive household contacts poses the highest risk of viral spread within any population,35 but especially to immunocompromised patients. Other close contacts of these patients include health care workers, who are themselves at increased risk for exposure to COVID-19 in the community.36 Vaccination of household members, close contacts and health care providers caring for immunocompromised patients is imperative to protect immunocompromised patients from viral transmission. All close contacts are thus strongly encouraged to get vaccinated as soon as possible.
When should family members, caregivers and/or household contacts who interact with HCT and CAR T cell recipients be administered COVID-19 vaccines?
Although nosocomial transmission can occur and is associated with higher morbidity and mortality,37 community exposure is the most common source for many infections among cancer and transplant patients. With the enhanced focus on infection control efforts in health care settings, including universal masking, social distancing, symptom screening, and frequent SARS-CoV-2 testing for these high-risk patients and for health care workers, hospital and clinic-based transmission is less frequent. However, family members, caregivers, and household contacts are more likely to be the source of SARS-CoV-2 transmission to HCT and CAR T recipients in the context of being unmasked for prolonged periods of time, especially in closed and/or poorly ventilated environments. In a recent meta-analysis of 54 studies with 77,758 participants, the estimated overall household secondary attack rate was 16.6%, with higher rates of transmission associated with a symptomatic household member.35 Models suggest that more than 50% of all SARS-CoV-2 infections are a result of transmission from pre-symptomatic or asymptomatic infections.38 Therefore, efforts to separate symptomatic contacts from high-risk immunocompromised patients, although still recommended, may not be sufficient to prevent transmission, particularly in the home. Furthermore, prolonged viral shedding from infected immunocompromised patients can increase transmission risk to other family members and close contacts.39 We recommend that all close contacts of HCT and CAR T cell recipients receive COVID-19 vaccines as soon as possible, based on local allocation guidelines.
To date, currently available vaccines are known to reduce the severity of COVID-19 disease and its complications, but data on prevention of primary infection or likelihood of transmission from vaccinated individuals are not yet available. For this reason, even vaccinated household members, caregivers, and medical staff should continue to wear masks, practice social distancing, and follow all recommendations for preventing SARS-CoV-2 acquisition and transmission.
Is there any foreseeable risk to HCT and CAR T cell recipients resulting from vaccination of close contacts with the already available or soon to be available COVID-19 vaccines?
Currently, available mRNA vaccines (Pfizer-BioNTech, Moderna) do not contain live virus; thus, these vaccines are completely safe to use in close contacts of immunocompromised patients.
Other candidate vaccines are still in ongoing clinical trials or are under FDA review. The Astra-Zeneca–Oxford vaccine consists of live simian adenovirus vector ChAdOx1, expressing the spike protein of SARS-CoV-2; but the virus has been modified to be completely replication-deficient and thus cannot be transmitted to others. This vaccine is currently not approved for use in the US.21 Similarly, the Johnson & Johnson/Janssen COVID-19 vaccine consists of a replication-defective live-virus human adenovirus 26 vector and is nontransmissible to others; the vaccine is yet to be approved for use in the United States.40 The Novavax vaccine (NVX-CoV2373) consists of protein subunits delivered with an adjuvant without any live virus and not yet approved for use in the United States.41 Therefore, when or if these vaccines become available for use in the United States, there is no foreseeable risk of SARS-CoV-2 transmission to immunocompromised patients or their close contacts. No live replication-competent SARS-CoV-2 vaccines are under development for use in the United States.
- Coll E, Fernandez-Ruiz M, Sanchez-Alvarez JE, Martinez-Fernandez JR, Crespo M, Gayoso J, et al. COVID-19 in transplant recipients: The Spanish experience. Am J Transplant. 2020.
- Pinana JL, Martino R, Garcia-Garcia I, Parody R, Morales MD, Benzo G, et al. Risk factors and outcome of COVID-19 in patients with hematological malignancies. Exp Hematol Oncol. 2020;9:21.
- Shah GL, DeWolf S, Lee YJ, Tamari R, Dahi PB, Lavery JA, et al. Favorable outcomes of COVID-19 in recipients of hematopoietic cell transplantation. J Clin Invest. 2020;130(12):6656-67.
- Vicent MG, Martinez AP, Trabazo Del Castillo M, Molina B, Sisini L, Moron-Cazalilla G, et al. COVID-19 in pediatric hematopoietic stem cell transplantation: The experience of Spanish Group of Transplant (GETMON/GETH). Pediatr Blood Cancer. 2020;67(9):e28514.
- Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N Engl J Med. 2020.
- Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. Safety and Efficacy of the BNT162b2 mRNA Covid-19 Vaccine. N Engl J Med. 2020;383(27):2603-15.
- Kamboj M, Shah MK. Vaccination of the Stem Cell Transplant Recipient and the Hematologic Malignancy Patient. Infect Dis Clin North Am. 2019;33(2):593-609.
- Cordonnier C, Labopin M, Chesnel V, Ribaud P, De La Camara R, Martino R, et al. Randomized study of early versus late immunization with pneumococcal conjugate vaccine after allogeneic stem cell transplantation. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2009;48(10):1392-401.
- Redman RL, Nader S, Zerboni L, Liu C, Wong RM, Brown BW, et al. Early reconstitution of immunity and decreased severity of herpes zoster in bone marrow transplant recipients immunized with inactivated varicella vaccine. J Infect Dis. 1997;176(3):578-85.
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- Walsh EE, Frenck RW, Jr., Falsey AR, Kitchin N, Absalon J, Gurtman A, et al. Safety and Immunogenicity of Two RNA-Based Covid-19 Vaccine Candidates. N Engl J Med. 2020;383(25):2439-50.
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- Folegatti PM, Ewer KJ, Aley PK, Angus B, Becker S, Belij-Rammerstorfer S, et al. Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial. Lancet. 2020;396(10249):467-78.
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- Sahin U, Muik A, Derhovanessian E, Vogler I, Kranz LM, Vormehr M, et al. COVID-19 vaccine BNT162b1 elicits human antibody and TH1 T cell responses. Nature. 2020;586(7830):594-9.
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