Review

. 2021 Oct;9(10):3546-3567.

doi: 10.1016/j.jaip.2021.06.006. Epub 2021 Jun 18.

The Risk of Allergic Reaction to SARS-CoV-2 Vaccines and Recommended Evaluation and Management: A Systematic Review, Meta-Analysis, GRADE Assessment, and International Consensus Approach

Matthew Greenhawt¹, Elissa M Abrams², Marcus Shaker³, Derek K Chu⁴, David Khan⁵, Cem Akin⁶, Waleed Alqurashi⁷, Peter Arkwright⁸, James L Baldwin⁶, Moshe Ben-Shoshan⁹, Jonathan Bernstein¹⁰, Theresa Bingemann¹¹, Katharina Blumchen¹², Aideen Byrne¹³, Antonio Bognanni¹⁴, Dianne Campbell¹⁵, Ronna Campbell¹⁶, Zain Chagla¹⁷, Edmond S Chan¹⁸, Jeffrey Chan¹⁹, Pasquale Comberiati²⁰, Timothy E Dribin²¹, Anne K Ellis²², David M Fleischer²³, Adam Fox²⁴, Pamela A Frischmeyer-Guerrerio²⁵, Remi Gagnon²⁶, Mitchell H Grayson²⁷, Caroline C Horner²⁸, Jonathan Hourihane²⁹, Constance H Katelaris³⁰, Harold Kim³¹, John M Kelso³², David Lang³³, Dennis Ledford³⁴, Michael Levin³⁵, Jay Lieberman³⁶, Richard Loh³⁷, Doug Mack³⁸, Bruce Mazer⁹, Giselle Mosnaim³⁹, Daniel Munblit⁴⁰, S Shahzad Mustafa⁴¹, Anil Nanda⁴², John Oppenheimer⁴³, Kirsten P Perrett⁴⁴, Allison Ramsey⁴¹, Matthew Rank⁴⁵, Kara Robertson⁴⁶, Javed Sheikh⁴⁷, Jonathan M Spergel⁴⁸, David Stukus²⁷, Mimi L K Tang⁴⁹, James M Tracy⁵⁰, Paul J Turner⁵¹, Anna Whalen-Browne⁵², Dana Wallace⁵³, Julie Wang⁵⁴, Susan Waserman⁵⁵, John K Witry⁵⁶, Margitta Worm⁵⁷, Timothy K Vander Leek⁵⁸, David B K Golden⁵⁹

Affiliations

¹ Section of Allergy and Clinical Immunology, Food Challenge and Research Unit, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, Colo. Electronic address: Matthew.Greenhawt@childrenscolorado.org.
² Department of Pediatrics and Child Health, Section of Allergy and Immunology, The University of Manitoba, Winnipeg, Man, Canada.
³ Dartmouth-Hitchcock Medical Center, Section of Allergy and Immunology, Lebanon; Dartmouth Geisel School of Medicine, Hanover, NH.
⁴ Department of Medicine, McMaster University Department of Health Research Methods, Evidence and Impact, McMaster University; The Research Institute of St. Joe's Hamilton; Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
⁵ Division of Allergy and Immunology, Department of Medicine, University of Texas Southwestern Medical Center, Dallas, Texas.
⁶ Division of Allergy and Clinical Immunology, Department of Internal Medicine, University of Michigan School, Ann Arbor, Mich.
⁷ Department of Pediatrics and Emergency Medicine, University of Ottawa, Ottawa, Ont, Canada.
⁸ Lydia Becker Institute of Immunology and Inflammation, University of Manchester, Manchester, UK.
⁹ Division of Allergy, Immunology, and Dermatology, Department of Pediatrics, McGill University Health Center-Montreal Children's Hospital, Montreal, Quebec, Canada.
¹⁰ Division of Immunology, Department of Internal Medicine, University of Cincinnati, Cincinnati, Ohio.
¹¹ Division of Allergy, Immunology, and Rheumatology, University of Rochester School of Medicine and Dentistry, Rochester, NY.
¹² Department of Paediatric and Adolescent Medicine, Paediatric Pneumology, Allergology, and Cystic Fibrosis, University Hospital Frankfurt, Frankfurt am Main, Germany.
¹³ Children's Health Ireland at Crumlin, Crumlin, Ireland.
¹⁴ Department of Health Research Methods, Evidence and Impact, Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
¹⁵ The Children's Hospital at Westmead, Sydney, New South Wales, Australia.
¹⁶ Department of Emergency Medicine, Mayo Clinic, Rochester, Minn.
¹⁷ Division of Infectious Diseases, Department of Medicine, McMaster University, Hamilton, Ont, Canada.
¹⁸ BC Children's Hospital, Division of Allergy and Immunology, The University of British Columbia, Vancouver, BC, Canada.
¹⁹ Department of Emergency Medicine, Southlake Regional Medical Center, Newmarket, Ont, Canada.
²⁰ Department of Clinical and Experimental Medicine, Section of Pediatrics, University of Pisa, Pisa, Italy, Department of Clinical Immunology and Allergology, I.M. Sechenov First Moscow State Medical University, Moscow, Russia.
²¹ Division of Emergency Medicine, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio.
²² Division of Allergy and Immunology, Department of Medicine, Queen's University, Kingston, Ont, Canada.
²³ Section of Allergy and Clinical Immunology, Food Challenge and Research Unit, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, Colo.
²⁴ Guy's and St. Thomas' NHS Foundation Trust, London, United Kingdom.
²⁵ Laboratory of Allergic Diseases, Food Allergy Research Section, National Institutes of Allergy and Infectious Diseases, the National Institutes of Health, Bethesda, Md.
²⁶ Clinique Spécialisée en Allergie de la Capitale, Quebec, Quebec, Canada.
²⁷ Division of Allergy and Immunology, Department of Clinical Pediatrics, Nationwide Children's Hospital, The Ohio State University College of Medicine, Columbus, Ohio.
²⁸ Division of Allergy and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St. Louis, Mo.
²⁹ Department of Paediatrics, Royal College of Surgeons, Dublin, Ireland.
³⁰ Campbelltown Hospital, Western Sydney University, New South Wales, Australia.
³¹ Western University, Londo, McMaster University, Hamilton, Ont, Canada.
³² Division of Allergy, Asthma, and Immunology, Scripps Clinic, San Diego, Calif.
³³ Department of Allergy and Clinical Immunology, Respiratory Institute, Cleveland Clinic, Cleveland, Ohio.
³⁴ Division of Allergy and Immunology, Department of Medicine, University of South Florida Morsani College of Medicine, Tampa, Fla.
³⁵ Division of Paediatric Allergology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
³⁶ Division of Allergy and Immunology, The University of Tennessee, Memphis, Tenn.
³⁷ Immunology Department, Perth Children's Hospital, Perth, Western Australia, Australia.
³⁸ McMaster University Hamilton, Halton Pediatric Allergy, Burlington, Ont, Canada.
³⁹ Division of Pulmonary, Allergy, and Critical Care, Department of Medicine, NorthShore University Health System, Evanston, Ill.
⁴⁰ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia, Inflammation, Repair, Development Section, National Heart and Lung Institute, Faculty of Medicine, Imperial College London, London, UK.
⁴¹ Rochester Regional Health, University of Rochester School of Medicine and Dentistry, Rochester, NY.
⁴² Asthma and Allergy Center, Lewisville and Flower Mound, Texas, Division of Allergy and Immunology, University of Texas Southwestern Medical Center, Dallas, Texas.
⁴³ UMDMJ Rutgers University School of Medicine, New Brunswick, NJ.
⁴⁴ Murdoch Children's Research Institute, Department of Paediatrics, University of Melbourne, Royal Children's Hospital, Parkville, Victoria, Australia.
⁴⁵ Division of Allergy, Asthma, and Clinical Immunology, Mayo Clinic, Scottsdale, Division of Pulmonology, Phoenix Children's Hospital, Phoenix, Ariz.
⁴⁶ Division of Clinical Immunology and Allergy, St. Joseph's Health Care, the Schulich School of Medicine and Dentistry, Western University, London, Ont, Canada.
⁴⁷ Kaiser Permanente Los Angeles Medical Center, Los Angeles, Calif.
⁴⁸ Division of Allergy and Immunology, Children's Hospital of Philadelphia, Department of Pediatrics, Perelman School of Medicine at University of Pennsylvania, Philadelphia, Pa.
⁴⁹ Murdoch Children's Research Institute, University of Melbourne, Royal Children's Hospital, Department of Allergy and Immunology, Royal Children's Hospital, Parkville, Victoria, Australia.
⁵⁰ Allergy, Asthma, and Immunology Associates, PC, Associate Professor of Pediatrics, University of Nebraska School of Medicine, Omaha, Neb.
⁵¹ Imperial College Healthcare NHS Trust and Royal Brompton and Harefield NHS Foundation Trust, London, UK.
⁵² Division of Clinical Immunology and Allergy, Department of Medicine, Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
⁵³ Nova Southeastern University College of Allopathic Medicine, Fort Lauderdale, Fla.
⁵⁴ Division of Pediatric Allergy and Immunology, Department of Pediatrics, Icahn School of Medicine at Mount Sinai, the Jaffe Food Allergy Institute, New York, NY.
⁵⁵ Department of Medicine, Clinical Immunology, and Allergy, McMaster University, Hamilton, Ont, Canada.
⁵⁶ Division of Emergency Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio.
⁵⁷ Division of Allergology and Immunology, Department of Dermatology, Venereology, and Allergology, Charité- Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
⁵⁸ Pediatric Allergy and Asthma, Department of Pediatrics, University of Alberta, Edmonton, Alta, Canada.
⁵⁹ Division of Allergy and Clinical Immunology, Johns Hopkins University School of Medicine, Baltimore, Md.

PMID: 34153517
PMCID: PMC8248554
DOI: 10.1016/j.jaip.2021.06.006

Review

The Risk of Allergic Reaction to SARS-CoV-2 Vaccines and Recommended Evaluation and Management: A Systematic Review, Meta-Analysis, GRADE Assessment, and International Consensus Approach

Matthew Greenhawt et al. J Allergy Clin Immunol Pract. 2021 Oct.

. 2021 Oct;9(10):3546-3567.

doi: 10.1016/j.jaip.2021.06.006. Epub 2021 Jun 18.

Authors

Affiliations

¹ Section of Allergy and Clinical Immunology, Food Challenge and Research Unit, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, Colo. Electronic address: Matthew.Greenhawt@childrenscolorado.org.
² Department of Pediatrics and Child Health, Section of Allergy and Immunology, The University of Manitoba, Winnipeg, Man, Canada.
³ Dartmouth-Hitchcock Medical Center, Section of Allergy and Immunology, Lebanon; Dartmouth Geisel School of Medicine, Hanover, NH.
⁴ Department of Medicine, McMaster University Department of Health Research Methods, Evidence and Impact, McMaster University; The Research Institute of St. Joe's Hamilton; Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
⁵ Division of Allergy and Immunology, Department of Medicine, University of Texas Southwestern Medical Center, Dallas, Texas.
⁶ Division of Allergy and Clinical Immunology, Department of Internal Medicine, University of Michigan School, Ann Arbor, Mich.
⁷ Department of Pediatrics and Emergency Medicine, University of Ottawa, Ottawa, Ont, Canada.
⁸ Lydia Becker Institute of Immunology and Inflammation, University of Manchester, Manchester, UK.
⁹ Division of Allergy, Immunology, and Dermatology, Department of Pediatrics, McGill University Health Center-Montreal Children's Hospital, Montreal, Quebec, Canada.
¹⁰ Division of Immunology, Department of Internal Medicine, University of Cincinnati, Cincinnati, Ohio.
¹¹ Division of Allergy, Immunology, and Rheumatology, University of Rochester School of Medicine and Dentistry, Rochester, NY.
¹² Department of Paediatric and Adolescent Medicine, Paediatric Pneumology, Allergology, and Cystic Fibrosis, University Hospital Frankfurt, Frankfurt am Main, Germany.
¹³ Children's Health Ireland at Crumlin, Crumlin, Ireland.
¹⁴ Department of Health Research Methods, Evidence and Impact, Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
¹⁵ The Children's Hospital at Westmead, Sydney, New South Wales, Australia.
¹⁶ Department of Emergency Medicine, Mayo Clinic, Rochester, Minn.
¹⁷ Division of Infectious Diseases, Department of Medicine, McMaster University, Hamilton, Ont, Canada.
¹⁸ BC Children's Hospital, Division of Allergy and Immunology, The University of British Columbia, Vancouver, BC, Canada.
¹⁹ Department of Emergency Medicine, Southlake Regional Medical Center, Newmarket, Ont, Canada.
²⁰ Department of Clinical and Experimental Medicine, Section of Pediatrics, University of Pisa, Pisa, Italy, Department of Clinical Immunology and Allergology, I.M. Sechenov First Moscow State Medical University, Moscow, Russia.
²¹ Division of Emergency Medicine, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio.
²² Division of Allergy and Immunology, Department of Medicine, Queen's University, Kingston, Ont, Canada.
²³ Section of Allergy and Clinical Immunology, Food Challenge and Research Unit, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, Colo.
²⁴ Guy's and St. Thomas' NHS Foundation Trust, London, United Kingdom.
²⁵ Laboratory of Allergic Diseases, Food Allergy Research Section, National Institutes of Allergy and Infectious Diseases, the National Institutes of Health, Bethesda, Md.
²⁶ Clinique Spécialisée en Allergie de la Capitale, Quebec, Quebec, Canada.
²⁷ Division of Allergy and Immunology, Department of Clinical Pediatrics, Nationwide Children's Hospital, The Ohio State University College of Medicine, Columbus, Ohio.
²⁸ Division of Allergy and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St. Louis, Mo.
²⁹ Department of Paediatrics, Royal College of Surgeons, Dublin, Ireland.
³⁰ Campbelltown Hospital, Western Sydney University, New South Wales, Australia.
³¹ Western University, Londo, McMaster University, Hamilton, Ont, Canada.
³² Division of Allergy, Asthma, and Immunology, Scripps Clinic, San Diego, Calif.
³³ Department of Allergy and Clinical Immunology, Respiratory Institute, Cleveland Clinic, Cleveland, Ohio.
³⁴ Division of Allergy and Immunology, Department of Medicine, University of South Florida Morsani College of Medicine, Tampa, Fla.
³⁵ Division of Paediatric Allergology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
³⁶ Division of Allergy and Immunology, The University of Tennessee, Memphis, Tenn.
³⁷ Immunology Department, Perth Children's Hospital, Perth, Western Australia, Australia.
³⁸ McMaster University Hamilton, Halton Pediatric Allergy, Burlington, Ont, Canada.
³⁹ Division of Pulmonary, Allergy, and Critical Care, Department of Medicine, NorthShore University Health System, Evanston, Ill.
⁴⁰ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia, Inflammation, Repair, Development Section, National Heart and Lung Institute, Faculty of Medicine, Imperial College London, London, UK.
⁴¹ Rochester Regional Health, University of Rochester School of Medicine and Dentistry, Rochester, NY.
⁴² Asthma and Allergy Center, Lewisville and Flower Mound, Texas, Division of Allergy and Immunology, University of Texas Southwestern Medical Center, Dallas, Texas.
⁴³ UMDMJ Rutgers University School of Medicine, New Brunswick, NJ.
⁴⁴ Murdoch Children's Research Institute, Department of Paediatrics, University of Melbourne, Royal Children's Hospital, Parkville, Victoria, Australia.
⁴⁵ Division of Allergy, Asthma, and Clinical Immunology, Mayo Clinic, Scottsdale, Division of Pulmonology, Phoenix Children's Hospital, Phoenix, Ariz.
⁴⁶ Division of Clinical Immunology and Allergy, St. Joseph's Health Care, the Schulich School of Medicine and Dentistry, Western University, London, Ont, Canada.
⁴⁷ Kaiser Permanente Los Angeles Medical Center, Los Angeles, Calif.
⁴⁸ Division of Allergy and Immunology, Children's Hospital of Philadelphia, Department of Pediatrics, Perelman School of Medicine at University of Pennsylvania, Philadelphia, Pa.
⁴⁹ Murdoch Children's Research Institute, University of Melbourne, Royal Children's Hospital, Department of Allergy and Immunology, Royal Children's Hospital, Parkville, Victoria, Australia.
⁵⁰ Allergy, Asthma, and Immunology Associates, PC, Associate Professor of Pediatrics, University of Nebraska School of Medicine, Omaha, Neb.
⁵¹ Imperial College Healthcare NHS Trust and Royal Brompton and Harefield NHS Foundation Trust, London, UK.
⁵² Division of Clinical Immunology and Allergy, Department of Medicine, Evidence in Allergy Group, McMaster University, Hamilton, Ont, Canada.
⁵³ Nova Southeastern University College of Allopathic Medicine, Fort Lauderdale, Fla.
⁵⁴ Division of Pediatric Allergy and Immunology, Department of Pediatrics, Icahn School of Medicine at Mount Sinai, the Jaffe Food Allergy Institute, New York, NY.
⁵⁵ Department of Medicine, Clinical Immunology, and Allergy, McMaster University, Hamilton, Ont, Canada.
⁵⁶ Division of Emergency Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio.
⁵⁷ Division of Allergology and Immunology, Department of Dermatology, Venereology, and Allergology, Charité- Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
⁵⁸ Pediatric Allergy and Asthma, Department of Pediatrics, University of Alberta, Edmonton, Alta, Canada.
⁵⁹ Division of Allergy and Clinical Immunology, Johns Hopkins University School of Medicine, Baltimore, Md.

PMID: 34153517
PMCID: PMC8248554
DOI: 10.1016/j.jaip.2021.06.006

Abstract

Concerns for anaphylaxis may hamper severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunization efforts. We convened a multidisciplinary group of international experts in anaphylaxis composed of allergy, infectious disease, emergency medicine, and front-line clinicians to systematically develop recommendations regarding SARS-CoV-2 vaccine immediate allergic reactions. Medline, EMBASE, Web of Science, the World Health Organizstion (WHO) global coronavirus database, and the gray literature (inception, March 19, 2021) were systematically searched. Paired reviewers independently selected studies addressing anaphylaxis after SARS-CoV-2 vaccination, polyethylene glycol (PEG) and polysorbate allergy, and accuracy of allergy testing for SARS-CoV-2 vaccine allergy. Random effects models synthesized the data to inform recommendations based on the Grading of Recommendation, Assessment, Development, and Evaluation (GRADE) approach, agreed upon using a modified Delphi panel. The incidence of SARS-CoV-2 vaccine anaphylaxis is 7.91 cases per million (n = 41,000,000 vaccinations; 95% confidence interval [95% CI] 4.02-15.59; 26 studies, moderate certainty), the incidence of 0.15 cases per million patient-years (95% CI 0.11-0.2), and the sensitivity for PEG skin testing is poor, although specificity is high (15 studies, very low certainty). We recommend vaccination over either no vaccination or performing SARS-CoV-2 vaccine/excipient screening allergy testing for individuals without history of a severe allergic reaction to the SARS-CoV-2 vaccine/excipient, and a shared decision-making paradigm in consultation with an allergy specialist for individuals with a history of a severe allergic reaction to the SARS-CoV-2 vaccine/excipient. We recommend further research to clarify SARS-CoV-2 vaccine/vaccine excipient testing utility in individuals potentially allergic to SARS-CoV2 vaccines or their excipients.

Keywords: Adenovirus-vector vaccine; Allergic reactions; Allergy; Allergy specialist; Anaphylaxis; COVID-19; GRADE; Polyethylene glycol; Polysorbate 80; SARS-CoV-2; Shared decision making; Skin testing; Vaccination; mRNA vaccine.

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Figures

**Figure 1**
Recommendations regarding precautions and contraindications regarding SARS-CoV-2 vaccination. *AAAAI,* American Academy of Allergy, Asthma, and Immunology; *ACAAI,* American College of Allergy, Asthma, and Immunology; *ALLSA,* Allergy Society of South Africa; *ASCIA,* Australasian Society of Clinical Immunology and Allergy; *CDC,* U.S. Centers for Disease Control and Prevention; *CSACI,* Canadian Society of Allergy and Clinical Immunology; *EAACI,* European Academy of Allergy and Clinical Immunology; *EMA,* European Medicines Agency; *NACI,* National Advisory Committee on Immunizations; *PHE/BSACI,* Public Health England/British Society for Allergy and Clinical Immunology; *WAO,* World Allergy Organization.

**Figure 2**
Adjudicated and nonadjudicated internationally reported rates of anaphylaxis to SARS-CoV-2 vaccines. *EOC,* Ente Ospedaliero Cantonale; *MGB,* Mass General Brigham; *PHAC,* Public Health Agency of Canada; *U.K. MHRA,* U.K. Medicines and Healthcare Products Regulatory Agency.

**Figure 3**
Pooled incidence of reported PEG allergy, in cases per million person-years.

**Figure 4**
Considerations for options in the approach to SARS-CoV-2 vaccination in patients with known or suspected reaction to a SARS-CoV-2 vaccine or vaccine excipient.

See this image and copyright information in PMC

Comment in

Recommendations were made for diagnosis and management of allergic reactions to COVID-19 vaccines.
Maki DG. Maki DG. Ann Intern Med. 2021 Nov;174(11):JC122. doi: 10.7326/ACPJ202111160-122. Epub 2021 Nov 2. Ann Intern Med. 2021. PMID: 34724408

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The Risk of Allergic Reaction to SARS-CoV-2 Vaccines and Recommended Evaluation and Management: A Systematic Review, Meta-Analysis, GRADE Assessment, and International Consensus Approach

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The Risk of Allergic Reaction to SARS-CoV-2 Vaccines and Recommended Evaluation and Management: A Systematic Review, Meta-Analysis, GRADE Assessment, and International Consensus Approach

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