In vivo quantitative imaging of hippocampal inflammation in autoimmune neuroinflammatory conditions: a systematic review
The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflamm...
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| Published in: | Clinical and experimental immunology Vol. 210; no. 1; pp. 24 - 38 |
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| Format: | Journal Article |
| Language: | English |
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Oxford University Press
21.10.2022
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| ISSN: | 0009-9104, 1365-2249, 1365-2249 |
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| Abstract | The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflammatory pathology in ex-vivo studies. Optimizing neuroimaging correlates of hippocampal neuroinflammation would enable the direct study of functional consequences of hippocampal neuroinflammatory pathology, as well as the definition of therapeutic end-points for treatments targeting neuroinflammation, and their related affective or cognitive sequelae. However, in vivo traditional imaging of the hippocampus and its subregions is fraught with difficulties, due to methodological challenges deriving from its unique anatomical characteristics. The main objective of this review is to provide a current update on the characterization of quantitative neuroimaging correlates of hippocampal neuroinflammation by focusing on three prototypical autoimmune neuro-inflammatory conditions [multiple sclerosis (MS), systemic lupus erythematosus (SLE), and autoimmune encephalitis (AE)]. We focused on studies employing TSPO-targeting positron emission tomography (PET), quantitative magnetic resonance imaging (MRI), and spectroscopy techniques assumed to be sensitive to neuroinflammatory tissue changes. We found 18 eligible studies (14, 2, and 2 studies in MS, AE, and SLE, respectively). Across conditions, the largest effect was seen in TSPO PET and diffusion-weighted MRI studies. No study examined neuroinflammation-related changes at the hippocampal subfield level. Overall, results were largely inconsistent due to heterogeneous imaging methods, small sample sizes, and different population studies. We discuss how these data could inform future study design and conclude by suggesting further methodological directions aimed at improving the precision and sensitivity of neuroimaging techniques to characterize hippocampal neuroinflammatory pathology in the human brain. |
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| AbstractList | The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflammatory pathology in ex-vivo studies. Optimizing neuroimaging correlates of hippocampal neuroinflammation would enable the direct study of functional consequences of hippocampal neuroinflammatory pathology, as well as the definition of therapeutic end-points for treatments targeting neuroinflammation, and their related affective or cognitive sequelae. However, in vivo traditional imaging of the hippocampus and its subregions is fraught with difficulties, due to methodological challenges deriving from its unique anatomical characteristics. The main objective of this review is to provide a current update on the characterization of quantitative neuroimaging correlates of hippocampal neuroinflammation by focusing on three prototypical autoimmune neuro-inflammatory conditions [multiple sclerosis (MS), systemic lupus erythematosus (SLE), and autoimmune encephalitis (AE)]. We focused on studies employing TSPO-targeting positron emission tomography (PET), quantitative magnetic resonance imaging (MRI), and spectroscopy techniques assumed to be sensitive to neuroinflammatory tissue changes. We found 18 eligible studies (14, 2, and 2 studies in MS, AE, and SLE, respectively). Across conditions, the largest effect was seen in TSPO PET and diffusion-weighted MRI studies. No study examined neuroinflammation-related changes at the hippocampal subfield level. Overall, results were largely inconsistent due to heterogeneous imaging methods, small sample sizes, and different population studies. We discuss how these data could inform future study design and conclude by suggesting further methodological directions aimed at improving the precision and sensitivity of neuroimaging techniques to characterize hippocampal neuroinflammatory pathology in the human brain. The hippocampus is a complex brain region crucially involved in neuroinflammation. We systematically reviewed quantitative imaging studies focusing on hippocampal pathology in autoimmune neuroinflammatory conditions and identified unmet research needs and future methodological directions.
Graphical Abstract The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflammatory pathology in ex-vivo studies. Optimizing neuroimaging correlates of hippocampal neuroinflammation would enable the direct study of functional consequences of hippocampal neuroinflammatory pathology, as well as the definition of therapeutic end-points for treatments targeting neuroinflammation, and their related affective or cognitive sequelae. However, in vivo traditional imaging of the hippocampus and its subregions is fraught with difficulties, due to methodological challenges deriving from its unique anatomical characteristics. The main objective of this review is to provide a current update on the characterization of quantitative neuroimaging correlates of hippocampal neuroinflammation by focusing on three prototypical autoimmune neuro-inflammatory conditions [multiple sclerosis (MS), systemic lupus erythematosus (SLE), and autoimmune encephalitis (AE)]. We focused on studies employing TSPO-targeting positron emission tomography (PET), quantitative magnetic resonance imaging (MRI), and spectroscopy techniques assumed to be sensitive to neuroinflammatory tissue changes. We found 18 eligible studies (14, 2, and 2 studies in MS, AE, and SLE, respectively). Across conditions, the largest effect was seen in TSPO PET and diffusion-weighted MRI studies. No study examined neuroinflammation-related changes at the hippocampal subfield level. Overall, results were largely inconsistent due to heterogeneous imaging methods, small sample sizes, and different population studies. We discuss how these data could inform future study design and conclude by suggesting further methodological directions aimed at improving the precision and sensitivity of neuroimaging techniques to characterize hippocampal neuroinflammatory pathology in the human brain. The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflammatory pathology in ex-vivo studies. Optimizing neuroimaging correlates of hippocampal neuroinflammation would enable the direct study of functional consequences of hippocampal neuroinflammatory pathology, as well as the definition of therapeutic end-points for treatments targeting neuroinflammation, and their related affective or cognitive sequelae. However, in vivo traditional imaging of the hippocampus and its subregions is fraught with difficulties, due to methodological challenges deriving from its unique anatomical characteristics. The main objective of this review is to provide a current update on the characterization of quantitative neuroimaging correlates of hippocampal neuroinflammation by focusing on three prototypical autoimmune neuro-inflammatory conditions [multiple sclerosis (MS), systemic lupus erythematosus (SLE), and autoimmune encephalitis (AE)]. We focused on studies employing TSPO-targeting positron emission tomography (PET), quantitative magnetic resonance imaging (MRI), and spectroscopy techniques assumed to be sensitive to neuroinflammatory tissue changes. We found 18 eligible studies (14, 2, and 2 studies in MS, AE, and SLE, respectively). Across conditions, the largest effect was seen in TSPO PET and diffusion-weighted MRI studies. No study examined neuroinflammation-related changes at the hippocampal subfield level. Overall, results were largely inconsistent due to heterogeneous imaging methods, small sample sizes, and different population studies. We discuss how these data could inform future study design and conclude by suggesting further methodological directions aimed at improving the precision and sensitivity of neuroimaging techniques to characterize hippocampal neuroinflammatory pathology in the human brain.The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory roles. It has exquisite vulnerability to neuroinflammatory processes, with some of its subregions found to be specific sites of neuroinflammatory pathology in ex-vivo studies. Optimizing neuroimaging correlates of hippocampal neuroinflammation would enable the direct study of functional consequences of hippocampal neuroinflammatory pathology, as well as the definition of therapeutic end-points for treatments targeting neuroinflammation, and their related affective or cognitive sequelae. However, in vivo traditional imaging of the hippocampus and its subregions is fraught with difficulties, due to methodological challenges deriving from its unique anatomical characteristics. The main objective of this review is to provide a current update on the characterization of quantitative neuroimaging correlates of hippocampal neuroinflammation by focusing on three prototypical autoimmune neuro-inflammatory conditions [multiple sclerosis (MS), systemic lupus erythematosus (SLE), and autoimmune encephalitis (AE)]. We focused on studies employing TSPO-targeting positron emission tomography (PET), quantitative magnetic resonance imaging (MRI), and spectroscopy techniques assumed to be sensitive to neuroinflammatory tissue changes. We found 18 eligible studies (14, 2, and 2 studies in MS, AE, and SLE, respectively). Across conditions, the largest effect was seen in TSPO PET and diffusion-weighted MRI studies. No study examined neuroinflammation-related changes at the hippocampal subfield level. Overall, results were largely inconsistent due to heterogeneous imaging methods, small sample sizes, and different population studies. We discuss how these data could inform future study design and conclude by suggesting further methodological directions aimed at improving the precision and sensitivity of neuroimaging techniques to characterize hippocampal neuroinflammatory pathology in the human brain. |
| Author | Colasanti, A Cercignani, M Nwaubani, P |
| Author_xml | – sequence: 1 givenname: P orcidid: 0000-0002-5397-4947 surname: Nwaubani fullname: Nwaubani, P – sequence: 2 givenname: M surname: Cercignani fullname: Cercignani, M – sequence: 3 givenname: A orcidid: 0000-0001-6017-801X surname: Colasanti fullname: Colasanti, A |
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| CitedBy_id | crossref_primary_10_1016_j_dcn_2025_101564 crossref_primary_10_3389_fmed_2023_1183535 crossref_primary_10_1038_s41598_025_85648_1 crossref_primary_10_1136_lupus_2025_001643 crossref_primary_10_1001_jamanetworkopen_2024_42803 crossref_primary_10_1177_0271678X231197380 crossref_primary_10_1093_cei_uxad018 crossref_primary_10_1186_s12974_024_03188_3 |
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| Keywords | autoimmune hippocampus MRI neuroinflammation neuroimaging |
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| Snippet | The hippocampus is a morphologically complex region of the brain limbic system centrally involved in important cognitive, affective, and behavioural regulatory... |
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| SubjectTerms | Complications Encephalitis Hippocampus Hippocampus - diagnostic imaging Hippocampus - pathology Humans Inflammation Inflammation - pathology Limbic system Lupus Erythematosus, Systemic - pathology Magnetic resonance imaging Magnetic Resonance Imaging - methods Medical imaging Multiple Sclerosis Neuroimaging Neuroimaging - methods Pathology Population studies Positron emission tomography Positron-Emission Tomography - methods Receptors, GABA - metabolism Review Series: Imaging Immunological Processes in Neuroinflammatory Diseases Part 2 (Series Editors: Sandra Amor & David Owen) Spectroscopy Systemic lupus erythematosus |
| Title | In vivo quantitative imaging of hippocampal inflammation in autoimmune neuroinflammatory conditions: a systematic review |
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