Bacillus Calmette-Guérin vaccination induces a trained innate immunity phenotype in adults over 50 years of age: A randomized trial in Guinea-Bissau
The beneficial effects of Bacillus Calmette-Guérin (BCG) as an intervention against non-mycobacterial infections have been extensively studied in randomized trials. These non-specific effects have been linked to a heterologous increase of pro-inflammatory cytokine production by innate immune cells....
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creator | Berendsen, Mike Leonardus Theodorus Bles, Pauli de Bree, Louise Charlotte Johanna Jensen, Kristoffer Jarlov Jensen, Clara Clipet Wejse, Christian Mendes, Delfim Vicente Netea, Mihai Gheorghe Benn, Christine Stabell |
description | The beneficial effects of Bacillus Calmette-Guérin (BCG) as an intervention against non-mycobacterial infections have been extensively studied in randomized trials. These non-specific effects have been linked to a heterologous increase of pro-inflammatory cytokine production by innate immune cells. It is unknown if BCG induces such responses in older individuals from TB-endemic countries.
In a single-blinded trial in Guinea-Bissau, 40 adults over 50 years of age were randomized 1:1 in a block of 40 to intradermal injection of BCG-Japan (intervention) or solvent (placebo). Production of interleukin (IL)-1β, IL-6, IL-10, interferon (IFN)-γ and tumor necrosis factor (TNF)-α was measured by ELISA in supernatant of peripheral blood mononuclear cells stimulated with Mycobacterium tuberculosis and heterologous pathogens. The trial was registered at clinicaltrials.gov (NCT02953327).
Between January 25 and March 7, 2017, 40 individuals were randomized. Two months after vaccination, BCG-Japan recipients (n = 11) had higher production of IFN-γ to M. tuberculosis stimulation (Geometric mean ratio (GMR): 3·91 [95 % Confidence Interval (CI), 1·53–9·96]) and increased release of the pro-inflammatory innate cytokines IL-1β, IL-6 and TNF-α to non-specific stimuli (GMR TNF-α: 1·47 [95 % CI, 0·98–2·19]) than their controls (n = 13). Both the specific and non-specific responses were more pronounced among those with a positive QuantiFERON at baseline.
BCG-Japan can induce a trained immunity phenotype in older adults. These effects were particularly strong in previously M. tuberculosis exposed individuals. Future randomized trials are needed to determine BCG's potential to protect the older populations from infections-driven morbidity and mortality. |
doi_str_mv | 10.1016/j.vaccine.2024.126439 |
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In a single-blinded trial in Guinea-Bissau, 40 adults over 50 years of age were randomized 1:1 in a block of 40 to intradermal injection of BCG-Japan (intervention) or solvent (placebo). Production of interleukin (IL)-1β, IL-6, IL-10, interferon (IFN)-γ and tumor necrosis factor (TNF)-α was measured by ELISA in supernatant of peripheral blood mononuclear cells stimulated with Mycobacterium tuberculosis and heterologous pathogens. The trial was registered at clinicaltrials.gov (NCT02953327).
Between January 25 and March 7, 2017, 40 individuals were randomized. Two months after vaccination, BCG-Japan recipients (n = 11) had higher production of IFN-γ to M. tuberculosis stimulation (Geometric mean ratio (GMR): 3·91 [95 % Confidence Interval (CI), 1·53–9·96]) and increased release of the pro-inflammatory innate cytokines IL-1β, IL-6 and TNF-α to non-specific stimuli (GMR TNF-α: 1·47 [95 % CI, 0·98–2·19]) than their controls (n = 13). Both the specific and non-specific responses were more pronounced among those with a positive QuantiFERON at baseline.
BCG-Japan can induce a trained immunity phenotype in older adults. These effects were particularly strong in previously M. tuberculosis exposed individuals. Future randomized trials are needed to determine BCG's potential to protect the older populations from infections-driven morbidity and mortality.</description><identifier>ISSN: 0264-410X</identifier><identifier>ISSN: 1873-2518</identifier><identifier>EISSN: 1873-2518</identifier><identifier>DOI: 10.1016/j.vaccine.2024.126439</identifier><identifier>PMID: 39423450</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>Adults ; Age ; Aged ; Bacillus ; Bacillus Calmette-Guerin vaccine ; Bacillus Calmette-Guérin ; BCG ; BCG Vaccine - administration & dosage ; BCG Vaccine - immunology ; Boosting ; COVID-19 vaccines ; Cytokines ; Cytokines - immunology ; Female ; Guinea-Bissau ; HIV ; Hospitals ; Human immunodeficiency virus ; Humans ; Immune system ; Immunity (Disease) ; Immunity, Innate ; Immunosenescence ; Infant mortality ; Inflammation ; Innate immunity ; Interferon-gamma - immunology ; Interleukin 6 ; Leukocytes (mononuclear) ; Leukocytes, Mononuclear - immunology ; Lithium ; Male ; Microorganisms ; Middle Aged ; Morbidity ; Mycobacterium tuberculosis - immunology ; Non-specific effects ; Older adults ; Older people ; Pandemics ; Peripheral blood mononuclear cells ; Phenotypes ; Psychologists ; Single-Blind Method ; Streptococcus infections ; Trained Immunity ; Tuberculosis ; Tuberculosis - immunology ; Tuberculosis - prevention & control ; Tumor Necrosis Factor-alpha ; Tumor necrosis factor-TNF ; Tumor necrosis factor-α ; Vaccination ; Vaccines ; γ-Interferon</subject><ispartof>Vaccine, 2024-12, Vol.42 (26), p.126439, Article 126439</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. All rights reserved.</rights><rights>2024. Elsevier Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1860-e7af1633372131de781030ee0af5202fd52103efcc6fee8252090b239724d1ed3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.vaccine.2024.126439$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39423450$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Berendsen, Mike Leonardus Theodorus</creatorcontrib><creatorcontrib>Bles, Pauli</creatorcontrib><creatorcontrib>de Bree, Louise Charlotte Johanna</creatorcontrib><creatorcontrib>Jensen, Kristoffer Jarlov</creatorcontrib><creatorcontrib>Jensen, Clara Clipet</creatorcontrib><creatorcontrib>Wejse, Christian</creatorcontrib><creatorcontrib>Mendes, Delfim Vicente</creatorcontrib><creatorcontrib>Netea, Mihai Gheorghe</creatorcontrib><creatorcontrib>Benn, Christine Stabell</creatorcontrib><title>Bacillus Calmette-Guérin vaccination induces a trained innate immunity phenotype in adults over 50 years of age: A randomized trial in Guinea-Bissau</title><title>Vaccine</title><addtitle>Vaccine</addtitle><description>The beneficial effects of Bacillus Calmette-Guérin (BCG) as an intervention against non-mycobacterial infections have been extensively studied in randomized trials. These non-specific effects have been linked to a heterologous increase of pro-inflammatory cytokine production by innate immune cells. It is unknown if BCG induces such responses in older individuals from TB-endemic countries.
In a single-blinded trial in Guinea-Bissau, 40 adults over 50 years of age were randomized 1:1 in a block of 40 to intradermal injection of BCG-Japan (intervention) or solvent (placebo). Production of interleukin (IL)-1β, IL-6, IL-10, interferon (IFN)-γ and tumor necrosis factor (TNF)-α was measured by ELISA in supernatant of peripheral blood mononuclear cells stimulated with Mycobacterium tuberculosis and heterologous pathogens. The trial was registered at clinicaltrials.gov (NCT02953327).
Between January 25 and March 7, 2017, 40 individuals were randomized. Two months after vaccination, BCG-Japan recipients (n = 11) had higher production of IFN-γ to M. tuberculosis stimulation (Geometric mean ratio (GMR): 3·91 [95 % Confidence Interval (CI), 1·53–9·96]) and increased release of the pro-inflammatory innate cytokines IL-1β, IL-6 and TNF-α to non-specific stimuli (GMR TNF-α: 1·47 [95 % CI, 0·98–2·19]) than their controls (n = 13). Both the specific and non-specific responses were more pronounced among those with a positive QuantiFERON at baseline.
BCG-Japan can induce a trained immunity phenotype in older adults. These effects were particularly strong in previously M. tuberculosis exposed individuals. Future randomized trials are needed to determine BCG's potential to protect the older populations from infections-driven morbidity and mortality.</description><subject>Adults</subject><subject>Age</subject><subject>Aged</subject><subject>Bacillus</subject><subject>Bacillus Calmette-Guerin vaccine</subject><subject>Bacillus Calmette-Guérin</subject><subject>BCG</subject><subject>BCG Vaccine - administration & dosage</subject><subject>BCG Vaccine - immunology</subject><subject>Boosting</subject><subject>COVID-19 vaccines</subject><subject>Cytokines</subject><subject>Cytokines - immunology</subject><subject>Female</subject><subject>Guinea-Bissau</subject><subject>HIV</subject><subject>Hospitals</subject><subject>Human immunodeficiency virus</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunity (Disease)</subject><subject>Immunity, Innate</subject><subject>Immunosenescence</subject><subject>Infant mortality</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interferon-gamma - immunology</subject><subject>Interleukin 6</subject><subject>Leukocytes (mononuclear)</subject><subject>Leukocytes, Mononuclear - immunology</subject><subject>Lithium</subject><subject>Male</subject><subject>Microorganisms</subject><subject>Middle Aged</subject><subject>Morbidity</subject><subject>Mycobacterium tuberculosis - immunology</subject><subject>Non-specific effects</subject><subject>Older adults</subject><subject>Older people</subject><subject>Pandemics</subject><subject>Peripheral blood mononuclear cells</subject><subject>Phenotypes</subject><subject>Psychologists</subject><subject>Single-Blind Method</subject><subject>Streptococcus infections</subject><subject>Trained Immunity</subject><subject>Tuberculosis</subject><subject>Tuberculosis - immunology</subject><subject>Tuberculosis - prevention & control</subject><subject>Tumor Necrosis Factor-alpha</subject><subject>Tumor necrosis factor-TNF</subject><subject>Tumor necrosis factor-α</subject><subject>Vaccination</subject><subject>Vaccines</subject><subject>γ-Interferon</subject><issn>0264-410X</issn><issn>1873-2518</issn><issn>1873-2518</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1uEzEUhS0EomngEUCW2LCZ4L_5Y4PaiIZKldiAxM5y7TvgaMYO_okUHoR1t7xGeTEcTWDRDSvLx-eca90PoReUrCihzZvtaq-0tg5WjDCxoqwRvH-EFrRrecVq2j1GC1LESlDy5Qydx7glhNSc9k_RGe8F46ImC_TzUmk7jjnitRonSAmqTf79K1iH536VrHfYOpM1RKxwCqoMNUUpT4DtNGVn0wHvvoHz6bArksPK5DFF7PcQcE3u7w6gQrkOWH2Ft_gCB-WMn-yP0pOCVeMxs8mlV1WXNkaVn6EngxojPD-dS_T56v2n9Yfq5uPmen1xU2naNaSCVg204Zy3jHJqoO0o4QSAqKEuaxlMzYoAg9bNANCxIvbklvG-ZcJQMHyJXs-9u-C_Z4hJTjZqGEflwOcoOaUdJ6ITvFhfPbBufQ6u_K64BDt2FwRLVM8uHXyMAQa5C3ZS4SApkUdwcitP4OQRnJzBldzLU3u-ncD8S_0lVQzvZgOUdewtBBm1BafB2AA6SePtf0b8AZ8Hrdk</recordid><startdate>20241202</startdate><enddate>20241202</enddate><creator>Berendsen, Mike Leonardus Theodorus</creator><creator>Bles, Pauli</creator><creator>de Bree, Louise Charlotte Johanna</creator><creator>Jensen, Kristoffer Jarlov</creator><creator>Jensen, Clara Clipet</creator><creator>Wejse, Christian</creator><creator>Mendes, Delfim Vicente</creator><creator>Netea, Mihai Gheorghe</creator><creator>Benn, Christine Stabell</creator><general>Elsevier Ltd</general><general>Elsevier Limited</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T2</scope><scope>7T5</scope><scope>7U9</scope><scope>C1K</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>7X8</scope></search><sort><creationdate>20241202</creationdate><title>Bacillus Calmette-Guérin vaccination induces a trained innate immunity phenotype in adults over 50 years of age: A randomized trial in Guinea-Bissau</title><author>Berendsen, Mike Leonardus Theodorus ; Bles, Pauli ; de Bree, Louise Charlotte Johanna ; Jensen, Kristoffer Jarlov ; Jensen, Clara Clipet ; Wejse, Christian ; Mendes, Delfim Vicente ; Netea, Mihai Gheorghe ; Benn, Christine Stabell</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1860-e7af1633372131de781030ee0af5202fd52103efcc6fee8252090b239724d1ed3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adults</topic><topic>Age</topic><topic>Aged</topic><topic>Bacillus</topic><topic>Bacillus Calmette-Guerin vaccine</topic><topic>Bacillus Calmette-Guérin</topic><topic>BCG</topic><topic>BCG Vaccine - administration & dosage</topic><topic>BCG Vaccine - immunology</topic><topic>Boosting</topic><topic>COVID-19 vaccines</topic><topic>Cytokines</topic><topic>Cytokines - immunology</topic><topic>Female</topic><topic>Guinea-Bissau</topic><topic>HIV</topic><topic>Hospitals</topic><topic>Human immunodeficiency virus</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immunity (Disease)</topic><topic>Immunity, Innate</topic><topic>Immunosenescence</topic><topic>Infant mortality</topic><topic>Inflammation</topic><topic>Innate immunity</topic><topic>Interferon-gamma - immunology</topic><topic>Interleukin 6</topic><topic>Leukocytes (mononuclear)</topic><topic>Leukocytes, Mononuclear - immunology</topic><topic>Lithium</topic><topic>Male</topic><topic>Microorganisms</topic><topic>Middle Aged</topic><topic>Morbidity</topic><topic>Mycobacterium tuberculosis - immunology</topic><topic>Non-specific effects</topic><topic>Older adults</topic><topic>Older people</topic><topic>Pandemics</topic><topic>Peripheral blood mononuclear cells</topic><topic>Phenotypes</topic><topic>Psychologists</topic><topic>Single-Blind Method</topic><topic>Streptococcus infections</topic><topic>Trained Immunity</topic><topic>Tuberculosis</topic><topic>Tuberculosis - immunology</topic><topic>Tuberculosis - prevention & control</topic><topic>Tumor Necrosis Factor-alpha</topic><topic>Tumor necrosis factor-TNF</topic><topic>Tumor necrosis factor-α</topic><topic>Vaccination</topic><topic>Vaccines</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Berendsen, Mike Leonardus Theodorus</creatorcontrib><creatorcontrib>Bles, Pauli</creatorcontrib><creatorcontrib>de Bree, Louise Charlotte Johanna</creatorcontrib><creatorcontrib>Jensen, Kristoffer Jarlov</creatorcontrib><creatorcontrib>Jensen, Clara Clipet</creatorcontrib><creatorcontrib>Wejse, Christian</creatorcontrib><creatorcontrib>Mendes, Delfim Vicente</creatorcontrib><creatorcontrib>Netea, Mihai Gheorghe</creatorcontrib><creatorcontrib>Benn, Christine Stabell</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Health and Safety Science Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>MEDLINE - Academic</collection><jtitle>Vaccine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Berendsen, Mike Leonardus Theodorus</au><au>Bles, Pauli</au><au>de Bree, Louise Charlotte Johanna</au><au>Jensen, Kristoffer Jarlov</au><au>Jensen, Clara Clipet</au><au>Wejse, Christian</au><au>Mendes, Delfim Vicente</au><au>Netea, Mihai Gheorghe</au><au>Benn, Christine Stabell</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bacillus Calmette-Guérin vaccination induces a trained innate immunity phenotype in adults over 50 years of age: A randomized trial in Guinea-Bissau</atitle><jtitle>Vaccine</jtitle><addtitle>Vaccine</addtitle><date>2024-12-02</date><risdate>2024</risdate><volume>42</volume><issue>26</issue><spage>126439</spage><pages>126439-</pages><artnum>126439</artnum><issn>0264-410X</issn><issn>1873-2518</issn><eissn>1873-2518</eissn><abstract>The beneficial effects of Bacillus Calmette-Guérin (BCG) as an intervention against non-mycobacterial infections have been extensively studied in randomized trials. These non-specific effects have been linked to a heterologous increase of pro-inflammatory cytokine production by innate immune cells. It is unknown if BCG induces such responses in older individuals from TB-endemic countries.
In a single-blinded trial in Guinea-Bissau, 40 adults over 50 years of age were randomized 1:1 in a block of 40 to intradermal injection of BCG-Japan (intervention) or solvent (placebo). Production of interleukin (IL)-1β, IL-6, IL-10, interferon (IFN)-γ and tumor necrosis factor (TNF)-α was measured by ELISA in supernatant of peripheral blood mononuclear cells stimulated with Mycobacterium tuberculosis and heterologous pathogens. The trial was registered at clinicaltrials.gov (NCT02953327).
Between January 25 and March 7, 2017, 40 individuals were randomized. Two months after vaccination, BCG-Japan recipients (n = 11) had higher production of IFN-γ to M. tuberculosis stimulation (Geometric mean ratio (GMR): 3·91 [95 % Confidence Interval (CI), 1·53–9·96]) and increased release of the pro-inflammatory innate cytokines IL-1β, IL-6 and TNF-α to non-specific stimuli (GMR TNF-α: 1·47 [95 % CI, 0·98–2·19]) than their controls (n = 13). Both the specific and non-specific responses were more pronounced among those with a positive QuantiFERON at baseline.
BCG-Japan can induce a trained immunity phenotype in older adults. These effects were particularly strong in previously M. tuberculosis exposed individuals. Future randomized trials are needed to determine BCG's potential to protect the older populations from infections-driven morbidity and mortality.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>39423450</pmid><doi>10.1016/j.vaccine.2024.126439</doi></addata></record> |
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subjects | Adults Age Aged Bacillus Bacillus Calmette-Guerin vaccine Bacillus Calmette-Guérin BCG BCG Vaccine - administration & dosage BCG Vaccine - immunology Boosting COVID-19 vaccines Cytokines Cytokines - immunology Female Guinea-Bissau HIV Hospitals Human immunodeficiency virus Humans Immune system Immunity (Disease) Immunity, Innate Immunosenescence Infant mortality Inflammation Innate immunity Interferon-gamma - immunology Interleukin 6 Leukocytes (mononuclear) Leukocytes, Mononuclear - immunology Lithium Male Microorganisms Middle Aged Morbidity Mycobacterium tuberculosis - immunology Non-specific effects Older adults Older people Pandemics Peripheral blood mononuclear cells Phenotypes Psychologists Single-Blind Method Streptococcus infections Trained Immunity Tuberculosis Tuberculosis - immunology Tuberculosis - prevention & control Tumor Necrosis Factor-alpha Tumor necrosis factor-TNF Tumor necrosis factor-α Vaccination Vaccines γ-Interferon |
title | Bacillus Calmette-Guérin vaccination induces a trained innate immunity phenotype in adults over 50 years of age: A randomized trial in Guinea-Bissau |
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