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Zhang JG, Zhou CK, Gao Y, Zhang XM, Ma K, Peng ZR, Luo XY, Liu ZZ, Lin XQ, Chen W, Yang YJ. Trained immunity driven by Enterococcus faecalis ribosomal protein S11 enhances antigen presentation and boosts influenza vaccine efficacy via nanoparticle delivery. Int J Biol Macromol 2025:144179. [PMID: 40381785 DOI: 10.1016/j.ijbiomac.2025.144179] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2024] [Revised: 05/03/2025] [Accepted: 05/11/2025] [Indexed: 05/20/2025]
Abstract
The limited availability of adjuvants poses a significant challenge in modern vaccine development, as they play a crucial role in enhancing vaccine efficacy. Trained immunity, driven by metabolic and epigenetic reprogramming of innate immune cells, offers a novel platform for adjuvant discovery. However, current studies predominantly focus on classical inducers such as β-glucan and BCG, limiting the exploration of key genes underlying trained immune responses. Here, we introduce a phenotypic evaluation model using Galleria mellonella larvae, identifying the gut commensal Enterococcus faecalis as a potent inducer of trained immunity. Through bioactivity-guided fractionation, we identified ribosomal protein S11 (RPS11) as the active agonist. Mechanistically, RPS11 induces trained immunity through TLR4-TET2 signaling-mediated ribosomal biogenesis inhibition, thereby shaping the enhanced MHC molecule expression phenotype in trained antigen-presenting cells. Notably, RPS11 conjugated with superparamagnetic iron oxide nanoparticles (RSNPs) significantly boosted the efficacy of an influenza vaccine. These findings highlight that harnessing the synergistic effects of innate and adaptive immune memory, combined with nanoparticle-based delivery of trained immunity agonists, presents a promising strategy for advancing next-generation vaccines against infectious diseases.
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Affiliation(s)
- Jian-Gang Zhang
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Cheng-Kai Zhou
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Yu Gao
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Xiao-Mei Zhang
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Ke Ma
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Zi-Ran Peng
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Xue-Yue Luo
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Zhen-Zhen Liu
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Xiao-Qi Lin
- College of Veterinary Medicine, Jilin University, Changchun, China
| | - Wei Chen
- College of Veterinary Medicine, Jilin University, Changchun, China.
| | - Yong-Jun Yang
- College of Veterinary Medicine, Jilin University, Changchun, China.
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Gonzalez-Parra G, Mahmud MS, Kadelka C. Learning from the COVID-19 pandemic: a systematic review of mathematical vaccine prioritization models. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2024:2024.03.04.24303726. [PMID: 38496570 PMCID: PMC10942533 DOI: 10.1101/2024.03.04.24303726] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 03/19/2024]
Abstract
As the world becomes ever more connected, the chance of pandemics increases as well. The recent COVID-19 pandemic and the concurrent global mass vaccine roll-out provides an ideal setting to learn from and refine our understanding of infectious disease models for better future preparedness. In this review, we systematically analyze and categorize mathematical models that have been developed to design optimal vaccine prioritization strategies of an initially limited vaccine. As older individuals are disproportionately affected by COVID-19, the focus is on models that take age explicitly into account. The lower mobility and activity level of older individuals gives rise to non-trivial trade-offs. Secondary research questions concern the optimal time interval between vaccine doses and spatial vaccine distribution. This review showcases the effect of various modeling assumptions on model outcomes. A solid understanding of these relationships yields better infectious disease models and thus public health decisions during the next pandemic.
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Affiliation(s)
- Gilberto Gonzalez-Parra
- Instituto de Matemática Multidisciplinar, Universitat Politècnica de València, València, Spain
- Department of Mathematics, New Mexico Tech, 801 Leroy Place, Socorro, 87801, NM, USA
| | - Md Shahriar Mahmud
- Department of Mathematics, Iowa State University, 411 Morrill Rd, Ames, 50011, IA, USA
| | - Claus Kadelka
- Department of Mathematics, Iowa State University, 411 Morrill Rd, Ames, 50011, IA, USA
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Wang G, Wang Y, Ma F. Exploiting bacterial-origin immunostimulants for improved vaccination and immunotherapy: current insights and future directions. Cell Biosci 2024; 14:24. [PMID: 38368397 PMCID: PMC10874560 DOI: 10.1186/s13578-024-01207-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2023] [Accepted: 02/06/2024] [Indexed: 02/19/2024] Open
Abstract
Vaccination is a valid strategy to prevent and control newly emerging and reemerging infectious diseases in humans and animals. However, synthetic and recombinant antigens are poor immunogenic to stimulate efficient and protective host immune response. Immunostimulants are indispensable factors of vaccines, which can promote to trigger fast, robust, and long-lasting immune responses. Importantly, immunotherapy with immunostimulants is increasing proved to be an effective and promising treatment of cancer, which could enhance the function of the immune system against tumor cells. Pattern recognition receptors (PRRs) play vital roles in inflammation and are central to innate and adaptive immune responses. Toll-like receptors (TLRs)-targeting immunostimulants have become one of the hotspots in adjuvant research and cancer therapy. Bacterial-origin immunoreactive molecules are usually the ligands of PRRs, which could be fast recognized by PRRs and activate immune response to eliminate pathogens. Varieties of bacterial immunoreactive molecules and bacterial component-mimicking molecules have been successfully used in vaccines and clinical therapy so far. This work provides a comprehensive review of the development, current state, mechanisms, and applications of bacterial-origin immunostimulants. The exploration of bacterial immunoreactive molecules, along with their corresponding mechanisms, holds immense significance in deepening our understanding of bacterial pathogenicity and in the development of promising immunostimulants.
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Affiliation(s)
- Guangyu Wang
- College of Food Science and Engineering, Collaborative Innovation Center for Modern Grain Circulation and Safety/Key Laboratory of Grains and Oils Quality Control and Processing, Nanjing University of Finance and Economics, Nanjing, Jiangsu, 210023, China
| | - Yongkang Wang
- College of Food Science and Engineering, Collaborative Innovation Center for Modern Grain Circulation and Safety/Key Laboratory of Grains and Oils Quality Control and Processing, Nanjing University of Finance and Economics, Nanjing, Jiangsu, 210023, China
| | - Fang Ma
- Institute of Veterinary Immunology & Engineering, National Research Center of Engineering and Technology for Veterinary Biologicals, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.
- School of Food and Biological Engineering, Jiangsu University, Zhenjiang, 212013, China.
- GuoTai (Taizhou) Center of Technology Innovation for Veterinary Biologicals, Taizhou, 225300, China.
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Espinosa O, Mora L, Sanabria C, Ramos A, Rincón D, Bejarano V, Rodríguez J, Barrera N, Álvarez-Moreno C, Cortés J, Saavedra C, Robayo A, Franco OH. Predictive models for health outcomes due to SARS-CoV-2, including the effect of vaccination: a systematic review. Syst Rev 2024; 13:30. [PMID: 38229123 PMCID: PMC10790449 DOI: 10.1186/s13643-023-02411-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/12/2022] [Accepted: 12/04/2023] [Indexed: 01/18/2024] Open
Abstract
BACKGROUND The interaction between modelers and policymakers is becoming more common due to the increase in computing speed seen in recent decades. The recent pandemic caused by the SARS-CoV-2 virus was no exception. Thus, this study aims to identify and assess epidemiological mathematical models of SARS-CoV-2 applied to real-world data, including immunization for coronavirus 2019 (COVID-19). METHODOLOGY PubMed, JSTOR, medRxiv, LILACS, EconLit, and other databases were searched for studies employing epidemiological mathematical models of SARS-CoV-2 applied to real-world data. We summarized the information qualitatively, and each article included was assessed for bias risk using the Joanna Briggs Institute (JBI) and PROBAST checklist tool. The PROSPERO registration number is CRD42022344542. FINDINGS In total, 5646 articles were retrieved, of which 411 were included. Most of the information was published in 2021. The countries with the highest number of studies were the United States, Canada, China, and the United Kingdom; no studies were found in low-income countries. The SEIR model (susceptible, exposed, infectious, and recovered) was the most frequently used approach, followed by agent-based modeling. Moreover, the most commonly used software were R, Matlab, and Python, with the most recurring health outcomes being death and recovery. According to the JBI assessment, 61.4% of articles were considered to have a low risk of bias. INTERPRETATION The utilization of mathematical models increased following the onset of the SARS-CoV-2 pandemic. Stakeholders have begun to incorporate these analytical tools more extensively into public policy, enabling the construction of various scenarios for public health. This contribution adds value to informed decision-making. Therefore, understanding their advancements, strengths, and limitations is essential.
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Affiliation(s)
- Oscar Espinosa
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS) & Economic Models and Quantitative Methods Research Group, Centro de Investigaciones para el Desarrollo, Universidad Nacional de Colombia, Bogotá, D.C., Colombia.
| | - Laura Mora
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS), Bogotá, Colombia
| | - Cristian Sanabria
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS), Bogotá, Colombia
| | - Antonio Ramos
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS) & Economic Models and Quantitative Methods Research Group, Centro de Investigaciones para el Desarrollo, Universidad Nacional de Colombia, Bogotá, D.C., Colombia
| | - Duván Rincón
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS), Bogotá, Colombia
| | - Valeria Bejarano
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS) & Economic Models and Quantitative Methods Research Group, Centro de Investigaciones para el Desarrollo, Universidad Nacional de Colombia, Bogotá, D.C., Colombia
| | - Jhonathan Rodríguez
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS) & Economic Models and Quantitative Methods Research Group, Centro de Investigaciones para el Desarrollo, Universidad Nacional de Colombia, Bogotá, D.C., Colombia
| | - Nicolás Barrera
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS), Bogotá, Colombia
| | | | - Jorge Cortés
- Faculty of Medicine, Universidad Nacional de Colombia, Bogotá, D.C., Colombia
| | - Carlos Saavedra
- Faculty of Medicine, Universidad Nacional de Colombia, Bogotá, D.C., Colombia
| | - Adriana Robayo
- Directorate of Analytical, Economic and Actuarial Studies in Health, Instituto de Evaluación Tecnológica en Salud (IETS), Bogotá, Colombia
| | - Oscar H Franco
- University Medical Center Utrecht, Utrecht University & Harvard T.H. Chan School of Public Health, Harvard University, Cambridge, USA
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Piret J, Boivin G. The impact of trained immunity in respiratory viral infections. Rev Med Virol 2024; 34:e2510. [PMID: 38282407 DOI: 10.1002/rmv.2510] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/25/2023] [Revised: 12/20/2023] [Accepted: 12/27/2023] [Indexed: 01/30/2024]
Abstract
Epidemic peaks of respiratory viruses that co-circulate during the winter-spring seasons can be synchronous or asynchronous. The occurrence of temporal patterns in epidemics caused by some respiratory viruses suggests that they could negatively interact with each other. These negative interactions may result from a programme of innate immune memory, known as trained immunity, which may confer broad protective effects against respiratory viruses. It is suggested that stimulation of innate immune cells by a vaccine or a pathogen could induce their long-term functional reprogramming through an interplay between metabolic and epigenetic changes, which influence the transcriptional response to a secondary challenge. During the coronavirus disease 2019 pandemic, the circulation of most respiratory viruses was prevented by non-pharmacological interventions and then resumed at unusual periods once sanitary measures were lifted. With time, respiratory viruses should find again their own ecological niches. This transition period provides an opportunity to study the interactions between respiratory viruses at the population level.
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Affiliation(s)
- Jocelyne Piret
- Research Center of the CHU de Québec-Université Laval, Quebec City, Quebec, Canada
| | - Guy Boivin
- Research Center of the CHU de Québec-Université Laval, Quebec City, Quebec, Canada
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Lee YC, Liu L, Yuan L, Risk M, Heinrich K, Witteveen-Lane M, Hayek S, Malosh R, Pop-Busui R, Jiang B, Shen C, Chesla D, Kennedy R, Xu S, Sims M, Homayouni R, Zhao L. Influenza vaccine effectiveness against hospitalized SARS-CoV-2 infection. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2023:2023.10.27.23297682. [PMID: 37961376 PMCID: PMC10635222 DOI: 10.1101/2023.10.27.23297682] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/15/2023]
Abstract
Background Some studies conducted before the Delta and Omicron variant-dominant periods have indicated that influenza vaccination provided protection against COVID-19 infection or hospitalization, but these results were limited by small study cohorts and a lack of comprehensive data on patient characteristics. No studies have examined this question during the Delta and Omicron periods (08/01/2021 to 2/22/2022). Methods We conducted a retrospective cohort study of influenza-vaccinated and unvaccinated patients in the Corewell Health East(CHE, formerly known as Beaumont Health), Corewell Health West(CHW, formerly known as Spectrum Health) and Michigan Medicine (MM) healthcare system during the Delta-dominant and Omicron-dominant periods. We used a test-negative, case-control analysis to assess the effectiveness of the influenza vaccine against hospitalized SARS-CoV-2 outcome in adults, while controlling for individual characteristics as well as pandameic severity and waning immunity of COVID-19 vaccine. Results The influenza vaccination has shown to provided some protection against SARS-CoV-2 hospitalized outcome across three main healthcare systems. CHE site (odds ratio [OR]=0.73, vaccine effectiveness [VE]=27%, 95% confidence interval [CI]: [18-35], p<0.001), CHW site (OR=0.85, VE=15%, 95% CI: [6-24], p<0.001), MM (OR=0.50, VE=50%, 95% CI: [40-58], p <0.001) and overall (OR=0.75, VE=25%, 95% CI: [20-30], p <0.001). Conclusion The influenza vaccine provides a small degree of protection against SARS-CoV-2 infection across our study sites.
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Reyes H, Méndez C, Kalergis AM. Statistical explanation of the protective effect of four COVID-19 vaccine doses in the general population. Front Public Health 2023; 11:1253762. [PMID: 37808972 PMCID: PMC10556658 DOI: 10.3389/fpubh.2023.1253762] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/06/2023] [Accepted: 09/06/2023] [Indexed: 10/10/2023] Open
Abstract
Objectives To assess the effectiveness of four doses of the vaccine against SARS-CoV-2 in the general population and the impact of this on the severity of the disease by age group. Methods By using data from the health authority public data base, we build statistical models using R and the GAMLSS library to explain the behavior of new SARS-CoV-2 infections, active COVID-19 cases, ICU bed requirement total and by age group, and deaths at the national level. Results The four doses of vaccine and at least the interaction between the first and second doses were important explanatory factors for the protective effect against COVID-19. The R2 for new cases per day was 0.5644 and for occupied ICU beds the R2 is 0.9487. For occupied ICU beds for >70 years R2 is 0.9195 and with the interaction between 4 doses as the main factor. Conclusions Although the increase in the number of vaccine doses did not adequately explain the decrease in the number of COVID-19 cases, it explained the decrease in ICU admissions and deaths nationwide and by age group.
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Affiliation(s)
- Humberto Reyes
- Millennium Institute on Immunology and Immunotherapy, Santiago, Chile
- Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
| | - Constanza Méndez
- Millennium Institute on Immunology and Immunotherapy, Santiago, Chile
- Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
| | - Alexis M. Kalergis
- Millennium Institute on Immunology and Immunotherapy, Santiago, Chile
- Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
- Departamento de Endocrinología, Facultad de Medicina, Escuela de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
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Thomas M, Ismail S, Hameed M, Kazi SST, Chandra P, Raza T, Paul T, Sattar HA, Suliman AM, Mohamed SSI, Ibrahim EAS, Subahi EAAAE. A cross-sectional study from Qatar on the effect of influenza vaccination on the severity of COVID-19. Medicine (Baltimore) 2023; 102:e35107. [PMID: 37713897 PMCID: PMC10508454 DOI: 10.1097/md.0000000000035107] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/05/2023] [Accepted: 08/16/2023] [Indexed: 09/17/2023] Open
Abstract
To assess and compare the severity of corona virus disease 2019 (COVID-19) infection in patients with and without a history of influenza vaccination. In this cross-sectional study descriptive statistics were used to analyze COVID-19-related parameters, including demographics, comorbidities, and severity. Normally distributed data with mean, standard deviation, and 95% confidence interval (CI) were reported, while non-normally distributed data was presented with median and inter-quartile range. Categorical data was summarized using frequencies and percentages. Associations were assessed using Pearson Chi-square, Fisher Exact, t test, or Mann-Whitney U test. Univariate and multivariate logistic regression methods were used to evaluate the relationship between disease severity, clinical outcomes, influenza vaccination status, and other predictors. Significance was considered for p values < 0.05. Statistical analyses were done using SPSS V.27.0 (IBM Corp) and Epi Info (CDC) software. Between March 2020 and December 2020 before the availability of COVID-19 vaccination, 148,215 severe acute respiratory syndrome corona virus 2 positive patients were studied, with 3519 vaccinated against influenza, and 144,696 unvaccinated. After random sampling at 1:2 ratio, the final analysis included 3234 vaccinated and 5640 unvaccinated patients. The majority (95.4%) had mild or asymptomatic COVID-19, while 4.6% had severe or critical cases as defined by World Health Organization severity grading. Multivariate logistic regression analysis revealed that the vaccinated group had significantly less severe (adjusted odds ratio [OR] 0.683; 95% CI 0.513-0.911, P = .009) and critical (adjusted OR 0.345; 95% CI 0.145-0.822, P = .016) COVID-19 and were less likely to require oxygen therapy (adjusted OR 0.696; 95% CI 0.531-0.912, P = .009) after adjusting for confounders like age, gender and comorbidities. No significant differences in Intensive care unit admissions (adjusted OR 0.686; 95% CI 0.425-1.11, P = .122), mechanical ventilation (adjusted OR 0.631; 95% CI 0.308-1.295, P = .209) and mortality (adjusted OR 1.105; 95% CI 0.348-3.503, P = .866) were noted between the 2 groups. Influenza vaccination may significantly reduce the severity of COVID-19 but has no significant effect on intensive care unit admissions, mechanical ventilation and all- cause mortality.
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Affiliation(s)
- Merlin Thomas
- Department of Pulmonary Medicine, Hamad General Hospital, Doha, Qatar
- Department of Medicine, Weil Cornell Medical College, Doha, Qatar
| | - Shanima Ismail
- Department of Pulmonary Medicine, Hamad General Hospital, Doha, Qatar
| | - Mansoor Hameed
- Department of Pulmonary Medicine, Hamad General Hospital, Doha, Qatar
- Department of Medicine, Weil Cornell Medical College, Doha, Qatar
| | | | - Prem Chandra
- Medical Research Center, Academic Health Systems, Hamad Medical Corporation, Doha, Qatar
| | - Tasleem Raza
- Department of Pulmonary Medicine, Hamad General Hospital, Doha, Qatar
- Department of Medical Intensive care, Hamad General Hospital, Doha, Qatar
| | - Theresa Paul
- Department of Geriatric Medicine, Hamad General hospital, Doha, Qatar
| | | | - Aasir M. Suliman
- Department of Pulmonary Medicine, Hamad General Hospital, Doha, Qatar
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Netea MG, Ziogas A, Benn CS, Giamarellos-Bourboulis EJ, Joosten LAB, Arditi M, Chumakov K, van Crevel R, Gallo R, Aaby P, van der Meer JWM. The role of trained immunity in COVID-19: Lessons for the next pandemic. Cell Host Microbe 2023; 31:890-901. [PMID: 37321172 PMCID: PMC10265767 DOI: 10.1016/j.chom.2023.05.004] [Citation(s) in RCA: 25] [Impact Index Per Article: 12.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/02/2023] [Revised: 05/03/2023] [Accepted: 05/08/2023] [Indexed: 06/17/2023]
Abstract
Trained immunity is a long-term increase in responsiveness of innate immune cells, induced by certain infections and vaccines. During the last 3 years of the COVID-19 pandemic, vaccines that induce trained immunity, such as BCG, MMR, OPV, and others, have been investigated for their capacity to protect against COVID-19. Further, trained immunity-inducing vaccines have been shown to improve B and T cell responsiveness to both mRNA- and adenovirus-based anti-COVID-19 vaccines. Moreover, SARS-CoV-2 infection itself induces inappropriately strong programs of trained immunity in some individuals, which may contribute to the long-term inflammatory sequelae. In this review, we detail these and other aspects of the role of trained immunity in SARS-CoV-2 infection and COVID-19. We also examine the learnings from the trained immunity studies conducted in the context of this pandemic and discuss how they may help us in preparing for future infectious outbreaks.
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Affiliation(s)
- Mihai G Netea
- Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Department of Immunology and Metabolism, Life & Medical Sciences Institute, University of Bonn, Bonn, Germany.
| | - Athanasios Ziogas
- Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands
| | - Christine Stabell Benn
- Bandim Health Project, OPEN, Department of Clinical Research, University of Southern Denmark, Copenhagen, Denmark; Danish Institute for Advanced Study, University of Southern Denmark, Odense, Denmark
| | | | - Leo A B Joosten
- Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Department of Medical Genetics, Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania
| | - Moshe Arditi
- Departments of Pediatrics and Biomedical Sciences, Guerin Children's and Smidt Heart Institute, Cedars-Sinai Medical Center, Los Angeles, USA
| | - Konstantin Chumakov
- Office of Vaccines Research and Review, Food and Drug Administration, Global Virus Network Center of Excellence, Silver Spring, MD, USA
| | - Reinout van Crevel
- Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands; Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK
| | - Robert Gallo
- Institute of Human Virology, University of Maryland School of Medicine, Baltimore, Global Virus Network, Baltimore, MD, USA
| | - Peter Aaby
- Bandim Health Project, OPEN, Department of Clinical Research, University of Southern Denmark, Copenhagen, Denmark
| | - Jos W M van der Meer
- Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, the Netherlands
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da Costa CG, Jalalizadeh M, Yadollahvandmiandoab R, Buosi K, Reis LO. Effect of BCG on Respiratory Complications Caused by COVID-19: A Scoping Review. Int J Gen Med 2022; 15:8727-8741. [PMID: 36601650 PMCID: PMC9807169 DOI: 10.2147/ijgm.s393861] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2022] [Accepted: 12/15/2022] [Indexed: 12/29/2022] Open
Abstract
INTRODUCTION Bacillus Calmette-Guérin (BCG) has been shown to have protective effects against respiratory viruses. We conducted a scoping review of the literature to clarify the available evidence regarding the effect of BCG therapy in preventing respiratory complications of coronavirus disease 2019 (COVID-19). METHODS We searched PubMed, Embase, CENTRAL, Scopus, and Web of Science for related studies up to October 2022. RESULTS In total, 35 publications and trials were included. One animal study, two observational studies, and six finalized trials measured the effect of BCG administration on respiratory complications of COVID-19. The remaining publications included eight unfinished trials, 12 ecological studies, and six observational studies that did not directly measure respiratory complications but assessed overall mortality of the disease and were included as an adjunct to our study. All trials involved vaccinating adults to protect them against severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection, and measured respiratory symptoms or the need for intensive respiratory support as the primary or secondary aim of the study. One trial that exclusively included at-risk adults between 18 and 60 years old showed a decreased chance of respiratory complications as the secondary outcome of the study. Another trial that exclusively evaluated this effect on the elderly (60 years and older) as the primary aim of the study reported no protective effect against respiratory complications. The remaining literature provided mostly inconclusive evidence. CONCLUSION The majority of the literature on the protective effect of BCG against respiratory complications of COVID-19 is inconclusive.
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Affiliation(s)
| | - Mehrsa Jalalizadeh
- Department of UroScience, School of Medical Sciences, University of Campinas – UNICAMP, Campinas, São Paulo, Brazil
| | - Reza Yadollahvandmiandoab
- Department of UroScience, School of Medical Sciences, University of Campinas – UNICAMP, Campinas, São Paulo, Brazil
| | - Keini Buosi
- Department of UroScience, School of Medical Sciences, University of Campinas – UNICAMP, Campinas, São Paulo, Brazil
| | - Leonardo O Reis
- Department of UroScience, School of Medical Sciences, University of Campinas – UNICAMP, Campinas, São Paulo, Brazil
- Pontifical Catholic University of Campinas, PUC, Campinas, São Paulo, Brazil
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Rakshit S, Adiga V, Ahmed A, Parthiban C, Chetan Kumar N, Dwarkanath P, Shivalingaiah S, Rao S, D’Souza G, Dias M, Maguire TJA, Doores KJ, Zoodsma M, Geckin B, Dasgupta P, Babji S, van Meijgaarden KE, Joosten SA, Ottenhoff THM, Li Y, Netea MG, Stuart KD, De Rosa SC, McElrath MJ, Vyakarnam A. Evidence for the heterologous benefits of prior BCG vaccination on COVISHIELD™ vaccine-induced immune responses in SARS-CoV-2 seronegative young Indian adults. Front Immunol 2022; 13:985938. [PMID: 36268023 PMCID: PMC9577398 DOI: 10.3389/fimmu.2022.985938] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/05/2022] [Accepted: 08/26/2022] [Indexed: 11/15/2022] Open
Abstract
This proof-of-concept study tested if prior BCG revaccination can qualitatively and quantitively enhance antibody and T-cell responses induced by Oxford/AstraZeneca ChAdOx1nCoV-19 or COVISHIELD™, an efficacious and the most widely distributed vaccine in India. We compared COVISHIELD™ induced longitudinal immune responses in 21 BCG re-vaccinees (BCG-RV) and 13 BCG-non-revaccinees (BCG-NRV), all of whom were BCG vaccinated at birth; latent tuberculosis negative and SARS-CoV-2 seronegative prior to COVISHIELD™ vaccination. Compared to BCG-NRV, BCG-RV displayed significantly higher and persistent spike-specific neutralizing (n) Ab titers and polyfunctional CD4+ and CD8+ T-cells for eight months post COVISHIELD™ booster, including distinct CD4+IFN-γ+ and CD4+IFN-γ- effector memory (EM) subsets co-expressing IL-2, TNF-α and activation induced markers (AIM) CD154/CD137 as well as CD8+IFN-γ+ EM,TEMRA (T cell EM expressing RA) subset combinations co-expressing TNF-α and AIM CD137/CD69. Additionally, elevated nAb and T-cell responses to the Delta mutant in BCG-RV highlighted greater immune response breadth. Mechanistically, these BCG adjuvant effects were associated with elevated markers of trained immunity, including higher IL-1β and TNF-α expression in CD14+HLA-DR+monocytes and changes in chromatin accessibility highlighting BCG-induced epigenetic changes. This study provides first in-depth analysis of both antibody and memory T-cell responses induced by COVISHIELD™ in SARS-CoV-2 seronegative young adults in India with strong evidence of a BCG-induced booster effect and therefore a rational basis to validate BCG, a low-cost and globally available vaccine, as an adjuvant to enhance heterologous adaptive immune responses to current and emerging COVID-19 vaccines.
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Affiliation(s)
- Srabanti Rakshit
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Vasista Adiga
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
- Department of Biotechnology, PES University, Bangalore, India
| | - Asma Ahmed
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Chaitra Parthiban
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Nirutha Chetan Kumar
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | | | | | - Srishti Rao
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - George D’Souza
- Division of Nutrition, St. John’s Research Institute, Bangalore, India
| | - Mary Dias
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | | | - Katie J. Doores
- Department of Pulmonary Medicine, St. John’s Medical College, Bangalore, India
| | - Martijn Zoodsma
- Department of Infectious Diseases, School of Immunology and Microbial Sciences, King’s College London, London, United Kingdom
- Department of Computational Biology for Individualized Infection Medicine, Centre for Individualized Infection Medicine (CiiM), a joint venture between the Helmholtz Centre for Infection Research (HZI) and the Hannover Medical School (MHH), Hannover, Germany
| | - Busranur Geckin
- TWINCORE, a joint venture between the Helmholtz Centre for Infection Research, (HZI) and the Hannover Medical School (MHH), Hannover, Germany
| | - Prokar Dasgupta
- Department of Internal Medicine and Radboud Center for infectious Diseases, Radboud University Medical Center, Nijmegen, Netherlands
| | - Sudhir Babji
- Peter Gorer Department of Immunobiology, Liver Renal Urology Transplant Gastro/Gastrointestinal Surgery, Inflammation Biology, King’s College London, London, United Kingdom
| | | | - Simone A. Joosten
- The Wellcome Trust Research Laboratory, Christian Medical College, Vellore, India
| | - Tom H. M. Ottenhoff
- The Wellcome Trust Research Laboratory, Christian Medical College, Vellore, India
| | - Yang Li
- Department of Infectious Diseases, School of Immunology and Microbial Sciences, King’s College London, London, United Kingdom
- Department of Computational Biology for Individualized Infection Medicine, Centre for Individualized Infection Medicine (CiiM), a joint venture between the Helmholtz Centre for Infection Research (HZI) and the Hannover Medical School (MHH), Hannover, Germany
| | - Mihai G. Netea
- TWINCORE, a joint venture between the Helmholtz Centre for Infection Research, (HZI) and the Hannover Medical School (MHH), Hannover, Germany
| | - Kenneth D. Stuart
- Department of Infectious Diseases, Leiden University Medical Center, Leiden, Netherlands
| | - Stephen C. De Rosa
- Centre for Global Infectious Disease Research, Seattle Children’s Research Institute, Seattle, WA, United States
| | - M. Juliana McElrath
- Centre for Global Infectious Disease Research, Seattle Children’s Research Institute, Seattle, WA, United States
- Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Centre, Seattle, WA, United States
| | - Annapurna Vyakarnam
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
- Department of Medicine, University of Washington School of Medicine, Seattle, WA, United States
- *Correspondence: Annapurna Vyakarnam, ;
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Yang L, Shi S, Na C, Li B, Zhao Z, Yang T, Yao Y. Rotavirus and Norovirus Infections in Children Under 5 Years Old with Acute Gastroenteritis in Southwestern China, 2018-2020. J Epidemiol Glob Health 2022; 12:292-303. [PMID: 35857268 PMCID: PMC9297278 DOI: 10.1007/s44197-022-00050-8] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/10/2022] [Accepted: 07/05/2022] [Indexed: 11/29/2022] Open
Abstract
OBJECTIVE Rotaviruses and noroviruses are important causes of acute gastroenteritis in children. While previous studies in China have mainly focused on rotavirus, we investigated the incidence of norovirus in addition to rotavirus in Southwestern China. METHODS From January 2018 to December 2020, cases of rotavirus or norovirus infections among children under five ages with acute gastroenteritis were evaluated retrospectively. RESULTS The detection rate of rotavirus was 24.5% (27,237/111,070) and norovirus was 26.1% (4649/17,797). Among 17,113 cases submitted for dual testing of both rotavirus and norovirus, mixed rotavirus/norovirus infections were detected in 5.0% (859/17,113) of cases. While there was no difference in norovirus incidence in outpatient compared to hospitalized cases, rotavirus was detected two times more in outpatients compared to hospitalized cases (26.6% vs.13.6%; P < 0.001). Both rotavirus and norovirus infections peaked in children aged 12-18 months seeking medical care with acute gastroenteritis (35.6% rotavirus cases; 8439/23,728 and 32.5% norovirus cases; 1660/5107). Rotavirus infections were frequent between December and March of each year while norovirus was detected earlier from October to December. Our results showed significant correlation between virus detection and environmental factors such as average monthly temperature but not relative humidity. In addition, we observed a reduction in the detection rates of rotavirus and norovirus at the beginning of the SARS-CoV-2 pandemic in 2020. CONCLUSION Our results indicate that rotavirus and norovirus are still important viral agents in pediatric acute gastroenteritis in Southwestern China.
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Affiliation(s)
- Longyu Yang
- Yunnan Key Laboratory of Vaccine Research & Development On Severe Infectious Disease, Department of Immunogenetics, Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, 650118, Yunnan, People's Republic of China
| | - Shulan Shi
- Institute of Pediatrics, Children's Hospital Affiliated to Kunming Medical University, Kunming, Yunnan, 650228, People's Republic of China
| | - Chen Na
- Department of Pediatrics, Yanan Hospital Affiliated to Kunming Medical University, Kunming, Yunnan, 650000, People's Republic of China
| | - Bai Li
- Yunnan Key Laboratory of Vaccine Research & Development On Severe Infectious Disease, Department of Immunogenetics, Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, 650118, Yunnan, People's Republic of China
| | - Zhimei Zhao
- Yunnan Key Laboratory of Vaccine Research & Development On Severe Infectious Disease, Department of Immunogenetics, Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, 650118, Yunnan, People's Republic of China
| | - Tao Yang
- Department of Pediatrics, Yanan Hospital Affiliated to Kunming Medical University, Kunming, Yunnan, 650000, People's Republic of China.
| | - Yufeng Yao
- Yunnan Key Laboratory of Vaccine Research & Development On Severe Infectious Disease, Department of Immunogenetics, Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, 650118, Yunnan, People's Republic of China.
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Sviridov D, Miller YI, Bukrinsky MI. Trained Immunity and HIV Infection. Front Immunol 2022; 13:903884. [PMID: 35874772 PMCID: PMC9304701 DOI: 10.3389/fimmu.2022.903884] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2022] [Accepted: 06/20/2022] [Indexed: 11/13/2022] Open
Abstract
Findings that certain infections induce immunity not only against the causing agent, but also against an unrelated pathogen have intrigued investigators for many years. Recently, underlying mechanisms of this phenomenon have started to come to light. It was found that the key cells responsible for heterologous protection are innate immune cells such as natural killer cells (NKs), dendritic cells, and monocytes/macrophages. These cells are 'primed' by initial infection, allowing them to provide enhanced response to subsequent infection by the same or unrelated agent. This phenomenon of innate immune memory was termed 'trained immunity'. The proposed mechanism for trained immunity involves activation by the first stimulus of metabolic pathways that lead to epigenetic changes, which maintain the cell in a "trained" state, allowing enhanced responses to a subsequent stimulus. Innate immune memory can lead either to enhanced responses or to suppression of subsequent responses ('tolerance'), depending on the strength and length of the initial stimulation of the immune cells. In the context of HIV infection, innate memory induced by infection is not well understood. In this Hypothesis and Theory article, we discuss evidence for HIV-induced trained immunity in human monocytes, its possible mechanisms, and implications for HIV-associated co-morbidities.
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Affiliation(s)
- Dmitri Sviridov
- Laboratory of Lipoproteins and Atherosclerosis, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
- Department of Biochemistry and Molecular Biology, Monash University, Clayton, VIC, Australia
| | - Yury I. Miller
- Department of Medicine, University of California, San Diego, San Diego, CA, United States
| | - Michael I. Bukrinsky
- Department of Microbiology, Immunology and Tropical Medicine, School of Medicine and Health Sciences, The George Washington University, Washington, DC, United States
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Engelbrecht M, Heunis C, Kigozi G. COVID-19 Vaccine Hesitancy in South Africa: Lessons for Future Pandemics. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2022; 19:ijerph19116694. [PMID: 35682278 PMCID: PMC9180246 DOI: 10.3390/ijerph19116694] [Citation(s) in RCA: 16] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 05/11/2022] [Revised: 05/26/2022] [Accepted: 05/27/2022] [Indexed: 02/06/2023]
Abstract
Vaccine hesitancy, long considered a global health threat, poses a major barrier to effective roll-out of COVID-19 vaccination. With less than half (45%) of adult South Africans currently fully vaccinated, we identified factors affecting non-uptake of vaccination and vaccine hesitancy in order to identify key groups to be targeted when embarking upon COVID-19 vaccine promotion campaigns. A cross-sectional, anonymous online survey was undertaken among the South African adult population in September 2021. Our research identified race, interactive–critical vaccine literacy, trust in the government’s ability to roll out the COVID-19 vaccination programme, flu vaccination status and risk perception for COVID-19 infection as key factors influencing the uptake of COVID-19 vaccination. Respondents who did not trust in the government’s ability to roll out vaccination were almost 13 times more likely to be vaccine-hesitant compared to those respondents who did trust the government. Reliable, easy-to-understand information regarding the safety of COVID-19 vaccines is needed, but it is also important that vaccination promotion and communication strategies include broader trust-building measures to enhance South Africans’ trust in the government’s ability to roll out vaccination effectively and safely. This may also be the case in other countries where distrust in governments’ ability prevails.
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15
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Gong W, Mao Y, Li Y, Qi Y. BCG Vaccination: A potential tool against COVID-19 and COVID-19-like Black Swan incidents. Int Immunopharmacol 2022; 108:108870. [PMID: 35597119 PMCID: PMC9113676 DOI: 10.1016/j.intimp.2022.108870] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2022] [Revised: 05/07/2022] [Accepted: 05/12/2022] [Indexed: 12/17/2022]
Abstract
The severe acute respiratory syndrome
coronavirus 2 (SARS-CoV-2), the causative agent of the coronavirus
disease 2019 (COVID-19), and its variants have brought unprecedented
impacts to the global public health system, politics, economy, and other
fields. Although more than ten COVID-19 specific vaccines have been
approved for emergency use, COVID-19 prevention and control still face
many challenges. Bacille Calmette–Guérin (BCG) is the only authorized
vaccine used to fight against tuberculosis (TB), it has been hypothesized
that BCG may prevent and control COVID-19 based on BCG-induced
nonspecific immune responses. Herein, we summarized: 1) The nonspecific
protection effects of BCG, such as prophylactic protection effects of BCG
on nonmycobacterial infections, immunotherapy effects of BCG vaccine, and
enhancement effect of BCG vaccine on unrelated vaccines; 2) Recent
evidence of BCG's efficacy against SARS-COV-2 infection from ecological
studies, analytical analyses, clinical trials, and animal studies; 3)
Three possible mechanisms of BCG vaccine and their effects on COVID-19
control including heterologous immunity, trained immunity, and
anti-inflammatory effect. We hope that this review will encourage more
scientists to investigate further BCG induced non-specific immune
responses and explore their mechanisms, which could be a potential tool
for addressing the COVID-19 pandemic and COVID-19-like “Black Swan”
events to reduce the impacts of infectious disease outbreaks on public
health, politics, and economy.
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Affiliation(s)
- Wenping Gong
- Tuberculosis Prevention and Control Key Laboratory/Beijing Key Laboratory of New Techniques of Tuberculosis Diagnosis and Treatment, Senior Department of Tuberculosis, The 8(th) Medical Center of PLA General Hospital, Beijing 100091, China
| | - Yingqing Mao
- Huadong Research Institute for Medicine and Biotechniques, Nanjing 210002, Jiangsu Province, China
| | - Yuexi Li
- Huadong Research Institute for Medicine and Biotechniques, Nanjing 210002, Jiangsu Province, China.
| | - Yong Qi
- Huadong Research Institute for Medicine and Biotechniques, Nanjing 210002, Jiangsu Province, China.
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17
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Rakshit S, Adiga V, Ahmed A, Parthiban C, Kumar NC, Dwarkanath P, Shivalingaiah S, Rao S, D’Souza G, Dias M, Maguire TJ, Doores K, Dasgupta P, Babji S, Ottenhoff TH, Stuart KD, De Rosa S, McElrath MJ, Vyakarnam A. BCG revaccination qualitatively and quantitatively enhances SARS-CoV-2 spike-specific neutralizing antibody and T cell responses induced by the COVISHIELD ™ vaccine in SARS-CoV-2 seronegative young Indian adults. RESEARCH SQUARE 2022:rs.3.rs-1395683. [PMID: 35262071 PMCID: PMC8902867 DOI: 10.21203/rs.3.rs-1395683/v1] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 11/27/2022]
Abstract
This study tested if prior BCG revaccination can further boost immune responses subsequently induced by a widely distributed and otherwise efficacious Oxford/AstraZeneca ChAdOx1nCoV-19 vaccine, referred to as COVISHIELD™, in India. We compared COVISHIELD™ induced longitudinal immune responses in 21 BCG re-vaccinees (BCG-RV) and 13 BCG-non-revaccinees (BCG-NRV), all of whom were BCG vaccinated at birth and latent tuberculosis negative, after COVISHIELD™ prime and boost with baseline samples that were collected pre-pandemic and pre-BCG revaccination. Compared to BCG-NRV, BCG-RV displayed significantly higher magnitude of spike-specific Ab and T cell responses, including a greater proportion of high responders; better quality polyfunctional CD4 and CD8 T cells that persisted and a more robust Ab and T cell response to the Delta mutant of SARS-CoV-2 highlighting greater breadth. Mechanistically, BCG adjuvant effects on COVISHIELD™ induced adaptive responses was associated with more robust innate responses to pathogen-associated-molecular-patterns through TNF-α and IL-1β secretion. This study provides first in-depth analysis of immune responses induced by COVISHIELD™ in India and highlights the potential of using a cheap and globally available vaccine, BCG, as an adjuvant to enhance heterologous adaptive immune responses induced by COVIDSHIELD™ and other emerging vaccines.
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Affiliation(s)
- Srabanti Rakshit
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Vasista Adiga
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Asma Ahmed
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Chaitra Parthiban
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Nirutha Chetan Kumar
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | | | | | - Srishti Rao
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - George D’Souza
- Department of Pulmonary Medicine, St. John’s Medical College, Bangalore, India
| | - Mary Dias
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
| | - Thomas J.A. Maguire
- Department of Infectious Diseases, School of Immunology and Microbial Sciences, King’s College London
| | - Katie Doores
- Department of Infectious Diseases, School of Immunology and Microbial Sciences, King’s College London
| | - Prokar Dasgupta
- Peter Gorer Department of Immunobiology, Liver Renal Urology Transplant Gastro/Gastrointestinal Surgery, Inflammation Biology, King’s College, London
| | - Sudhir Babji
- The Wellcome Trust Research Laboratory, Christian Medical College, Vellore, India
| | - Tom H.M Ottenhoff
- Dept. Infectious Diseases, Leiden University Medical Center, Leiden, The Netherlands
| | | | - Stephen De Rosa
- Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Centre, Seattle, Washington, USA
| | - M. Juliana McElrath
- Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Centre, Seattle, Washington, USA
- Department of Medicine, University of Washington School of Medicine, Seattle, Washington, USA
| | - Annapurna Vyakarnam
- Centre for Infectious Disease Research, Indian Institute of Science, Bangalore, India
- Infectious Disease Unit, St. John’s Research Institute, Bangalore, India
- Department of Immunobiology, School of Immunology & Microbial Sciences, Faculty of Life Science & Medicine, King’s College, London
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