The immune response of the human brain to abdominal surgery
Objective Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic‐to‐brain signaling pathway, we lack information on how these changes appear in humans. Thi...
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| Published in | Annals of neurology Vol. 81; no. 4; pp. 572 - 582 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Wiley Subscription Services, Inc
01.04.2017
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Objective
Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic‐to‐brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short‐ and long‐term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function.
Methods
Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [11C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed.
Results
Patients showed a global downregulation of gray matter [11C]PBR28 binding of 26 ± 26% (mean ± standard deviation) at 3 to 4 days postoperatively compared to baseline (p = 0.023), recovering or even increasing after 3 months. LPS‐induced release of the proinflammatory marker tumor necrosis factor‐α in blood displayed a reduction (41 ± 39%) on the 3rd to 4th postoperative day, corresponding to changes in [11C]PBR28 distribution volume. Change in Stroop Color‐Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [11C]PBR28 binding (p = 0.027).
Interpretation
This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017;81:572–582 |
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| AbstractList | OBJECTIVESurgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic-to-brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short- and long-term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function.METHODSEight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [11 C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed.RESULTSPatients showed a global downregulation of gray matter [11 C]PBR28 binding of 26 ± 26% (mean ± standard deviation) at 3 to 4 days postoperatively compared to baseline (p = 0.023), recovering or even increasing after 3 months. LPS-induced release of the proinflammatory marker tumor necrosis factor-α in blood displayed a reduction (41 ± 39%) on the 3rd to 4th postoperative day, corresponding to changes in [11 C]PBR28 distribution volume. Change in Stroop Color-Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [11 C]PBR28 binding (p = 0.027).INTERPRETATIONThis study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017;81:572-582. Objective Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic-to-brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short- and long-term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function. Methods Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [11C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed. Results Patients showed a global downregulation of gray matter [11C]PBR28 binding of 26±26% (mean±standard deviation) at 3 to 4 days postoperatively compared to baseline (p=0.023), recovering or even increasing after 3 months. LPS-induced release of the proinflammatory marker tumor necrosis factor-[alpha] in blood displayed a reduction (41±39%) on the 3rd to 4th postoperative day, corresponding to changes in [11C]PBR28 distribution volume. Change in Stroop Color-Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [11C]PBR28 binding (p=0.027). Interpretation This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017;81:572-582 Objective Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic‐to‐brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short‐ and long‐term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function. Methods Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [11C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed. Results Patients showed a global downregulation of gray matter [11C]PBR28 binding of 26 ± 26% (mean ± standard deviation) at 3 to 4 days postoperatively compared to baseline (p = 0.023), recovering or even increasing after 3 months. LPS‐induced release of the proinflammatory marker tumor necrosis factor‐α in blood displayed a reduction (41 ± 39%) on the 3rd to 4th postoperative day, corresponding to changes in [11C]PBR28 distribution volume. Change in Stroop Color‐Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [11C]PBR28 binding (p = 0.027). Interpretation This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017;81:572–582 Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic-to-brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short- and long-term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function. Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [ C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed. Patients showed a global downregulation of gray matter [ C]PBR28 binding of 26 ± 26% (mean ± standard deviation) at 3 to 4 days postoperatively compared to baseline (p = 0.023), recovering or even increasing after 3 months. LPS-induced release of the proinflammatory marker tumor necrosis factor-α in blood displayed a reduction (41 ± 39%) on the 3rd to 4th postoperative day, corresponding to changes in [ C]PBR28 distribution volume. Change in Stroop Color-Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [ C]PBR28 binding (p = 0.027). This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017;81:572-582. Objective: Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic-to-brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short-and long-term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function. Methods: Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [C-11]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed. Results: Patients showed a global downregulation of gray matter [C-11]PBR28 binding of 26 +/- 26% (mean +/- standard deviation) at 3 to 4 days postoperatively compared to baseline (p=0.023), recovering or even increasing after 3 months. LPS-induced release of the proinflammatory marker tumor necrosis factor-a in blood displayed a reduction (41 +/- 39%) on the 3rd to 4th postoperative day, corresponding to changes in [C-11]PBR28 distribution volume. Change in Stroop Color-Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [C-11]PBR28 binding (p=0.027). Interpretation: This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Objective Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical studies have in part described this systemic-to-brain signaling pathway, we lack information on how these changes appear in humans. This study examines the short- and long-term impact of abdominal surgery on the human brain immune system by positron emission tomography (PET) in relation to blood immune reactivity, plasma inflammatory biomarkers, and cognitive function. Methods Eight males undergoing prostatectomy under general anesthesia were included. Prior to surgery (baseline), at postoperative days 3 to 4, and after 3 months, patients were examined using [ super(11)C]PBR28 brain PET imaging to assess brain immune cell activation. Concurrently, systemic inflammatory biomarkers, ex vivo blood tests on immunoreactivity to lipopolysaccharide (LPS) stimulation, and cognitive function were assessed. Results Patients showed a global downregulation of gray matter [ super(11)C]PBR28 binding of 26 plus or minus 26% (mean plus or minus standard deviation) at 3 to 4 days postoperatively compared to baseline (p=0.023), recovering or even increasing after 3 months. LPS-induced release of the proinflammatory marker tumor necrosis factor- alpha in blood displayed a reduction (41 plus or minus 39%) on the 3rd to 4th postoperative day, corresponding to changes in [ super(11)C]PBR28 distribution volume. Change in Stroop Color-Word Test performance between postoperative days 3 to 4 and 3 months correlated to change in [ super(11)C]PBR28 binding (p=0.027). Interpretation This study translates preclinical data on changes in the brain immune system after surgery to humans, and suggests an interplay between the human brain and the inflammatory response of the peripheral innate immune system. These findings may be related to postsurgical impairments of cognitive function. Ann Neurol 2017; 81:572-582 |
| Author | Rasmussen, Lars S. Schening, Anna Borg, Jacqueline Christensson, Eva Zetterberg, Henrik Varrone, Andrea Halldin, Christer Forsberg, Anton Erlandsson Harris, Helena Granström, Anna Cervenka, Simon Dymmel, Karin Knave, Nina Terrando, Niccolò Stridh, Pernilla Blennow, Kaj Jonsson Fagerlund, Malin Eriksson, Lars I. Maze, Mervyn Farde, Lars |
| Author_xml | – sequence: 1 givenname: Anton surname: Forsberg fullname: Forsberg, Anton organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 2 givenname: Simon surname: Cervenka fullname: Cervenka, Simon organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 3 givenname: Malin surname: Jonsson Fagerlund fullname: Jonsson Fagerlund, Malin organization: Karolinska University Hospital – sequence: 4 givenname: Lars S. surname: Rasmussen fullname: Rasmussen, Lars S. organization: Center of Head and Orthopedics, Rigshospitalet, University of Copenhagen – sequence: 5 givenname: Henrik surname: Zetterberg fullname: Zetterberg, Henrik organization: University College London Institute of Neurology – sequence: 6 givenname: Helena surname: Erlandsson Harris fullname: Erlandsson Harris, Helena organization: Karolinska University Hospital – sequence: 7 givenname: Pernilla orcidid: 0000-0003-4855-0039 surname: Stridh fullname: Stridh, Pernilla organization: Department of Clinical Neuroscience, Karolinska Institutet – sequence: 8 givenname: Eva surname: Christensson fullname: Christensson, Eva organization: Karolinska University Hospital – sequence: 9 givenname: Anna surname: Granström fullname: Granström, Anna organization: Karolinska University Hospital – sequence: 10 givenname: Anna surname: Schening fullname: Schening, Anna organization: Karolinska University Hospital – sequence: 11 givenname: Karin surname: Dymmel fullname: Dymmel, Karin organization: Karolinska University Hospital – sequence: 12 givenname: Nina surname: Knave fullname: Knave, Nina organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 13 givenname: Niccolò surname: Terrando fullname: Terrando, Niccolò organization: Basic Science Division, Duke University Medical Center – sequence: 14 givenname: Mervyn surname: Maze fullname: Maze, Mervyn organization: University of California – sequence: 15 givenname: Jacqueline surname: Borg fullname: Borg, Jacqueline organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 16 givenname: Andrea surname: Varrone fullname: Varrone, Andrea organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 17 givenname: Christer surname: Halldin fullname: Halldin, Christer organization: Center for Psychiatric Research, Karolinska Institutet – sequence: 18 givenname: Kaj surname: Blennow fullname: Blennow, Kaj organization: Sahlgrenska University Hospital of Gothenburg – sequence: 19 givenname: Lars surname: Farde fullname: Farde, Lars organization: AstraZeneca, PET Science Center, Karolinska Institutet, Karolinska University Hospital – sequence: 20 givenname: Lars I. surname: Eriksson fullname: Eriksson, Lars I. email: Lars.I.Eriksson@ki.se organization: Karolinska University Hospital |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28253549$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-440730$$DView record from Swedish Publication Index https://gup.ub.gu.se/publication/253783$$DView record from Swedish Publication Index http://kipublications.ki.se/Default.aspx?queryparsed=id:135697448$$DView record from Swedish Publication Index |
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| Snippet | Objective
Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although... Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although preclinical... Objective Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although... OBJECTIVESurgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although... Objective: Surgery launches a systemic inflammatory reaction that reaches the brain and associates with immune activation and cognitive decline. Although... |
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| SubjectTerms | Abdomen - surgery Abdominal surgery Activation analysis Aged Anesthesia benzodiazepine-receptors Binding Biomarkers Biomarkers - metabolism Blood Brain Brain - diagnostic imaging Brain - immunology Brain - metabolism Brain - physiopathology Cell activation cerebrospinal-fluid Cognitive ability Cognitive Dysfunction - etiology Cognitive Dysfunction - physiopathology Color Correlation Down-Regulation Emission Follow-Up Studies Gray Matter - diagnostic imaging Gray Matter - immunology Gray Matter - metabolism Gray Matter - physiopathology Humans Imaging Immune response Immune system Immunoreactivity in-vivo Inflammation Inflammatory response Innate immunity Lipopolysaccharides Male Males microglial activation Middle Aged neurofilament light Neuroimaging Neurosciences Neurosciences & Neurology Neurovetenskaper Patients Positron emission Positron emission tomography Positron-Emission Tomography - methods postoperative cognitive dysfunction Prostate cancer Prostatectomy Prostatectomy - adverse effects protein 18 kda Signal transduction Standard deviation Stimulation Substantia grisea Surgery T cell receptors Tomography translocator protein Tumor necrosis factor Urological surgery vivo radioligand binding |
| Title | The immune response of the human brain to abdominal surgery |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fana.24909 https://www.ncbi.nlm.nih.gov/pubmed/28253549 https://www.proquest.com/docview/1890507919 https://www.proquest.com/docview/1910218350 https://www.proquest.com/docview/1874443858 https://www.proquest.com/docview/1897391487 https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-440730 https://gup.ub.gu.se/publication/253783 http://kipublications.ki.se/Default.aspx?queryparsed=id:135697448 |
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