The neuroinflammatory component of negative affect in patients with chronic pain
Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis th...
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| Published in | Molecular psychiatry Vol. 26; no. 3; pp. 864 - 874 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.03.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [
11
C]PBR28. The relationship between [
11
C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region’s functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. |
|---|---|
| AbstractList | Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [
C]PBR28. The relationship between [
C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region's functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [11C]PBR28. The relationship between [11C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region's functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition.Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [11C]PBR28. The relationship between [11C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region's functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4±13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9±13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET) / magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [ 11 C]PBR28. The relationship between [ 11 C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared to controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region’s functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [ 11 C]PBR28. The relationship between [ 11 C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region’s functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 ± 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 ± 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [11C]PBR28. The relationship between [11C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region’s functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA, previous studies have implicated neuroinflammation in the pathophysiology of both depression and chronic pain. Here, we tested the hypothesis that NA in pain patients is linked to elevations in the brain levels of the glial marker 18 kDa translocator protein (TSPO), and changes in functional connectivity. 25 cLBP patients (42.4 [plus or minus] 13 years old; 13F, 12M) with chronic low back pain (cLBP) and 27 healthy control subjects (48.9 [plus or minus] 13 years old; 14F, 13M) received an integrated (i.e., simultaneous) positron emission tomography (PET)/magnetic resonance imaging (MRI) brain scan with the second-generation TSPO ligand [.sup.11C]PBR28. The relationship between [.sup.11C]PBR28 signal and NA was assessed first with regression analyses against Beck Depression Inventory (BDI) scores in patients, and then by comparing cLBP patients with little-to-no, or mild-to-moderate depression against healthy controls. Further, the relationship between PET signal, BDI and frontolimbic functional connectivity was evaluated in patients with mediation models. PET signal was positively associated with BDI scores in patients, and significantly elevated in patients with mild-to-moderate (but not low) depression compared with controls, in anterior middle and pregenual anterior cingulate cortices (aMCC, pgACC). In the pgACC, PET signal was also associated with this region's functional connectivity to the dorsolateral PFC (pgACC-dlPFC), and mediated of the association between pgACC-dlPFC connectivity and BDI. These observations support a role for glial activation in pain-comorbid NA, identifying in neuroinflammation a potential therapeutic target for this condition. |
| Audience | Academic |
| Author | Akeju, O. Napadow, V. Hooker, J. M. Torrado-Carvajal, A. Zhang, Y. Kim, M. Protsenko, E. Loggia, M. L. Wasan, A. D. Albrecht, D. S. Edwards, R. R. Bergan, C. Kucyi, A. |
| AuthorAffiliation | 3 Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS, Boston, MA 5 Departments of Anesthesiology and Psychiatry, University of Pittsburgh, Pittsburgh, PA 2 Department of Anesthesia, Critical Care and Pain Medicine, MGH / HMS, Boston, MA 4 Department of Neurology, Stanford University Medical Center, Stanford, CA 1 A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS), Boston, MA |
| AuthorAffiliation_xml | – name: 5 Departments of Anesthesiology and Psychiatry, University of Pittsburgh, Pittsburgh, PA – name: 4 Department of Neurology, Stanford University Medical Center, Stanford, CA – name: 1 A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS), Boston, MA – name: 3 Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS, Boston, MA – name: 2 Department of Anesthesia, Critical Care and Pain Medicine, MGH / HMS, Boston, MA |
| Author_xml | – sequence: 1 givenname: D. S. surname: Albrecht fullname: Albrecht, D. S. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 2 givenname: M. orcidid: 0000-0003-3148-1540 surname: Kim fullname: Kim, M. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 3 givenname: O. surname: Akeju fullname: Akeju, O. organization: Department of Anesthesia, Critical Care and Pain Medicine, MGH/HMS – sequence: 4 givenname: A. orcidid: 0000-0002-1540-2809 surname: Torrado-Carvajal fullname: Torrado-Carvajal, A. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 5 givenname: R. R. surname: Edwards fullname: Edwards, R. R. organization: Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS – sequence: 6 givenname: Y. surname: Zhang fullname: Zhang, Y. organization: Department of Anesthesia, Critical Care and Pain Medicine, MGH/HMS – sequence: 7 givenname: C. surname: Bergan fullname: Bergan, C. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 8 givenname: E. surname: Protsenko fullname: Protsenko, E. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 9 givenname: A. surname: Kucyi fullname: Kucyi, A. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS), Department of Neurology, Stanford University Medical Center – sequence: 10 givenname: A. D. surname: Wasan fullname: Wasan, A. D. organization: Departments of Anesthesiology and Psychiatry, University of Pittsburgh – sequence: 11 givenname: J. M. surname: Hooker fullname: Hooker, J. M. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) – sequence: 12 givenname: V. surname: Napadow fullname: Napadow, V. organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS), Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, HMS – sequence: 13 givenname: M. L. surname: Loggia fullname: Loggia, M. L. email: marco.loggia@mgh.harvard.edu organization: A.A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School (MGH/HMS) |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31138890$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2019 COPYRIGHT 2021 Nature Publishing Group The Author(s), under exclusive licence to Springer Nature Limited 2019. |
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| Snippet | Negative affect (NA) is a significant cause of disability for chronic pain patients. While little is known about the mechanism underlying pain-comorbid NA,... |
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| SubjectTerms | 59/36 59/57 59/78 631/378 692/699/476/1414 Adult Affect (Psychology) Behavioral Sciences Biological Psychology Brain - diagnostic imaging Brain diseases Chronic pain Chronic Pain - diagnostic imaging Comorbidity Development and progression Emotions Health aspects Humans Inflammation Low back pain Magnetic Resonance Imaging Medicine Medicine & Public Health Middle Aged Neural networks Neuroglia Neuroimaging Neuronal-glial interactions Neurosciences Pain Pharmacotherapy Positron emission tomography Psychiatry Psychological aspects Receptors, GABA |
| Title | The neuroinflammatory component of negative affect in patients with chronic pain |
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