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Research Paper
Open Access

Hippocampal subfield alterations in schizophrenia and major depressive disorder: a systematic review and network meta-analysis of anatomic MRI studies

Yuan Sun, Na Hu, Mingqi Wang, Lu Lu, Chunyan Luo, Biqiu Tang, Chenyang Yao, John A. Sweeney, Qiyong Gong, Changjian Qiu and Su Lui
J Psychiatry Neurosci February 07, 2023 48 (1) E34-E49; DOI: https://doi.org/10.1503/jpn.220086
Yuan Sun
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Na Hu
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Mingqi Wang
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Lu Lu
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Chunyan Luo
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Biqiu Tang
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Chenyang Yao
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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John A. Sweeney
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Qiyong Gong
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Changjian Qiu
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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Su Lui
From the Huaxi MR Research Center, Department of Radiology and National Clinical Research Center for Geriatrics, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Sun, Lu, Tang, Yao, Sweeney, Gong, Lui); the Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Hu, Luo); the Chinese Evidence-Based Medicine Center and Cochrane China Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Wang); the Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, Ohio, United States (Sweeney); the Mental Health Center, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Qiu); the Research Unit of Psychoradiology, Chinese Academy of Medical Sciences, Chengdu, Sichuan, China (Lui); the Functional and Molecular Imaging Key Laboratory of Sichuan Province, West China Hospital of Sichuan University, Chengdu, Sichuan, China (Lui)
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    Figure 1

    (A) Forest plot for the left parasubiculum. (B) Forest plot for the right parasubiculum. (C) Forest plot for the right HATA. CI = confidence interval; HATA = hippocampus–amygdala transition area; MDD = major depressive disorder.

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    Table 1

    Characteristics of studies included in the systematic review (part 1 of 3)

    Author (year)Participants, n (% female, mean age)MRI scannerSegmentation methodStudy designMain findings
    Alnæs et al.42 (2019)*†Schizophrenia, 1151 (31%, 34 y)
    Healthy controls, 2010 (44%, 33 y)
    1.5 T and 3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohort, multisite; genesSmaller volume in all subfields; larger left and right hippocampal fissure
    Brown et al.43 (2019)MDD, 24 (38%, 40 y)
    Healthy controls, 20 (25%, 40 y)
    7.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohortNo significant difference
    Cao et al.44 (2018)MDD, 24 (58%, 31 y)
    Healthy controls, 15 (66%, 33 y)
    3.0 TAutomatic (FreeSurfer 5.3¶)Longitudinal design, case–control; ECTBaseline: no significant difference Longitudinal changes: increased left CA2/3, left and right CA4, left and right granule cell layer of the dentate gyrus, left subiculum
    Cao et al.31 (2017)MDD, 86 (70%, 41 y)
    Healthy controls, 152 (63%, 35 y)
    1.5 TAutomatic (FreeSurfer 5.3¶)Cross-sectional design, case–controlNo significant difference
    Doolin et al.32 (2018)MDD, 74 (64%, 33 y)
    Healthy controls, 37 (51%, 31 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohortSmaller left CA1, left and right CA2/3, right CA4
    du Plessis et al.33 (2020)First-episode schizophrenia, 79 (27%, 23 y)
    Healthy controls, 82 (43 %, 23)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohortStatistical analysis between 2 groups was not available
    Frodl et al.45 (2014)MDD, 43 (60%, 41 y)
    Healthy controls, 43 (60%, 37 y)
    3.0 TAutomatic (FreeSurfer**)Cross-sectional design, case–control; genesSmaller CA1, CA2/3, CA4/dentate gyrus, subiculum
    Frodl et al.46 (2014)MDD, 38 (66%, 41 y)
    Healthy controls, 44 (61%, 36 y)
    3.0 TAutomatic (FreeSurfer**)Cross-sectional design, case–control; genesSmaller left CA2/3, left CA4/dentate gyrus
    Han et al.21 (2019)‡MDD, 102 (59%, 36 y)
    Healthy controls, 135 (58%, 36 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlSmaller left and right whole hippocampus, left and right CA1, left CA2/3, left and right CA4, left and right granule cell layer of the dentate gyrus, right subiculum, right presubiculum, left and right molecular layer
    Han et al.47 (2017)‡MDD, 105 (82%, 43 y)
    Healthy controls, 85 (71%, 40 y)
    3.0 TAutomatic (FreeSurfer 5.3¶)Cross-sectional design, case–control; genesNo significant difference
    Han et al.48 (2016)MDD, 20 (100%, 42 y)
    Healthy controls, 21 (100%, 42 y)
    1.5 TAutomatic (FreeSurfer 5.3**)Cross-sectional design, case–controlSmaller left whole hippocampus, left CA2/3, left CA4/dentate gyrus, left and right subiculum
    Harel et al.49 (2016)MDD, 15 (53%, 36 y)
    Healthy controls, 15 (47%, 37 y)
    3.0 TAutomatic (FreeSurfer 5.3**)Cross-sectional design, case–controlSmaller right whole hippocampus, right CA1, right CA2/3, right CA4/dentate gyrus
    Ho et al.16 (2017)Schizophrenia, 155 (32%, 32 y)
    Healthy controls, 79 (35%, 31 y)
    3.0 TAutomatic (FreeSurfer 5.3¶)Cross-sectional design, case–control; longitudinal design in a subcohort; multisiteSchizophrenia: smaller left and right whole hippocampus, left CA1 Early-course schizophrenia: smaller left and right whole hippocampus, left and right CA1, right granule cell layer of the dentate gyrus
    Longitudinal changes: decreased left and right CA1, right CA2/3, left and right granule cell layer of the dentate gyrus, right molecular layer
    Schizophrenia, 46 (22%, 43 y)
    Healthy controls, 46 (22%, 42 y)
    Smaller left and right whole hippocampus, left and right CA1, left and right CA2/3, left and right CA4, left and right granule cell layer of the dentate gyrus, left and right subiculum, left and right molecular layer, left and right hippocampal tail
    Hu et al.66 (2020)Never-treated long-term schizophrenia, 29 (55%, 46 y)
    Treated long-term schizophrenia, 40 (55%, 48 y)
    Healthy controls, 40 (55%, 48 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlNever-treated long-term schizophrenia: smaller left and right whole hippocampus, right CA1 (body), left and right CA2/3 (head), right CA2/3 (body), left and right CA4 (head), left and right CA4 (body), left and right granule cell layer of the dentate gyrus (head), left and right granule cell layer of the dentate gyrus (body), left and right subiculum (body), left and right molecular layer (body), left and right hippocampal tail
    Treated long-term schizophrenia: smaller left and right whole hippocampus, left CA4 (body), left granule cell layer of the dentate gyrus (body), left and right subiculum (body), left and right molecular layer (body), left and right hippocampal tail
    Hu et al.50 (2019)Nonresponding MDD, 13 (38%, 36 y)
    Early responding MDD, 25 (44%, 36 y)
    Healthy controls, 55 (62%, 36 y)
    3.0 TAutomatic (FreeSurfer 5.3**)Cross-sectional design, case–control, cohortMDD: no significant difference Nonresponding MDD: larger left and right CA1, left CA2/3, left CA4/dentate gyrus, left and right subiculum
    Huang et al.67 (2013)§Unmedicated MDD, 9 (44%, 33 y)
    Medicated MDD, 11 (55%, 37 y)
    Healthy controls, 27 (70%, 33 y)
    4.7 TManualCross-sectional design, case–controlUnmedicated MDD: smaller CA1–3 (body), dentate gyrus
    Hýža et al.51 (2016)First-episode schizophrenia, 58 (0%, 23 y)
    Healthy controls, 58 (0%, 24 y)
    1.5 TAutomatic (FreeSurfer 5.2**)Cross-sectional design, case–controlLarger left CA1
    Jiang et al.52 (2019)Schizophrenia with symptom remission after ECT, 10 (50%, 30 y)
    Schizophrenia without symptom remission after ECT, 11 (55%, 28 y)
    Schizophrenia treated by ECT (with and without symptom remission), 21 (52%, 29 y)
    Schizophrenia with symptom remission after antipsychotic medication, 12 (75%, 31 y)
    Schizophrenia without symptom remission after antipsychotic medication, 9 (33%, 30 y)
    Schizophrenia treated by antipsychotic medication (with and without symptom remission), 21 (57%, 31 y)
    Healthy controls, 23 (52%, 31 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Longitudinal design, cohort; ECTLongitudinal changes: schizophrenia treated by ECT (with and without symptom remission), increased left and right whole hippocampus
    Kakeda et al.53 (2018)First-episode MDD, 40 (50%, 47 y)
    Healthy controls, 47 (28%, 41 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlNo significant difference
    Kawano et al.68 (2015)First-episode schizophrenia, 19 (53%, 25 y)
    Subchronic schizophrenia, 6 (50%, 22 y)
    Chronic schizophrenia, 9 (33%, 37 y)
    Healthy controls, 15 (33%, 25 y)
    1.5 TAutomatic (FreeSurfer 5.1**)Cross-sectional design, case–control; longitudinal design in a subcohortBaseline: first-episode schizophrenia, smaller left CA2/3, left CA4/ dentate gyrus
    Subchronic schizophrenia: smaller left whole hippocampus, left CA2/3, left CA4/ dentate gyrus
    Chronic schizophrenia: smaller left whole hippocampus, left CA2/3, left CA4/ dentate gyrus
    Kraus et al.54 (2019)Acute MDD, 20 (70%, 31 y)
    Remitted MDD, 28 (57%, 27 y)
    Healthy controls, 22 (55%, 26 y)
    7 TAutomatic (FreeSurfer 6.0¶)Longitudinal design, open-label trialTime 1: remitted MDD, larger right hippocampal fissure
    Longitudinal changes: no significant difference
    Time 2: remitted MDD, larger right HATA
    Li et al.55 (2018)First-episode schizophrenia, 41 (59%, 24 y)
    Healthy controls, 39 (51%, 24 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control; longitudinal design; antipsychoticsBaseline: larger left and right CA4, left and right granule cell layer of the dentate gyrus, left and right molecular layer
    Longitudinal changes: decreased left and right whole hippocampus, left CA1, left CA2/3, left and right CA4, left and right granule cell layer of the dentate gyrus, left and right molecular layer, left and right hippocampal tail, left fimbria
    After treatment: larger left and right CA4
    Maller et al.20 (2018)MDD, 182 (52%, 33 y)
    Healthy controls, 68 (50%, 30 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Open-label trialBaseline: larger hippocampal tail
    Mathew et al.69 (2014)Schizophrenia, 219 (34%, 35 y)
    Healthy controls, 337 (55%, 37 y)
    UnknownAutomatic (FreeSurfer 5.1**)Cross-sectional design, case–control, multisiteSmaller left and right whole hippocampus, left and right CA1, left and right CA2/3, left and right CA4/dentate gyrus, left and right subiculum, left and right presubiculum
    Mikolas et al.56 (2019)MDD, 85 (67%, 39 y)
    Healthy controls, 67 (67%, 36 y)
    3.0 TAutomatic (FreeSurfer 5.3¶)Cross-sectional design, case–control; genesSmaller whole hippocampus, CA1, CA2/3, CA4, granule cell layer of the dentate gyrus, molecular layer
    Na et al.57 (2014)MDD, 45 (76%, 42 y)
    Healthy controls, 72 (71%, 41 y)
    3.0 TAutomatic (FreeSurfer 5.0**)Cross-sectional design, case–control; genesNo significant difference
    Na et al.34 (2018)MDD, 47 (100%, 45 y)
    Healthy controls, 30 (100%, 43 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control; genesNo significant difference
    Nakahara et al.35 (2020)Schizophrenia, 176 (25%, 39 y)
    Healthy controls, 173 (29%, 38 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, multisiteSmaller CA1, CA4, granule cell layer of the dentate gyrus, molecular layer, hippocampal tail; larger hippocampal fissure
    Nguyen et al.58 (2019)First-episode MDD, 38 (47%, 47 y)
    Healthy controls, 39 (28%, 41 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control; genesNo significant difference
    Ohi et al.36 (2021)Schizophrenia, 138 (60%, 42 y)
    Healthy controls, 162 (33%, 37 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlSmaller right HATA; larger right hippocampal fissure
    Orfei et al.59 (2017)Schizophrenia, 45 (33%, 40 y)
    Healthy controls, 45 (33%, 40 y)
    3.0 TAutomatic (FreeSurfer**)Cross-sectional design, case–controlSmaller left and right whole hippocampus, left and right CA1, left and right CA2/3, left and right CA4/dentate gyrus, left subiculum, left and right presubiculum, left and right hippocampal fissure
    Ota et al.23 (2017)Schizophrenia, 20 (25%, 37 y)
    MDD, 36 (47%, 38 y)
    Healthy controls, 35 (46%, 39 y)
    3.0 TAutomatic (ASHS)Cross-sectional design, case–controlSchizophrenia: smaller whole hippocampus, CA1, dentate gyrus than healthy controls, smaller whole hippocampus, dentate gyrus than MDD without medication MDD: no significant difference
    Otsuka et al.60 (2019)First-episode MDD, 27 (41%, 46 y);
    Healthy controls, 42 (26%, 41 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control; genesNo significant difference
    Roddy et al.70 (2019)MDD, 80 (71%, 35 y)
    Healthy controls, 83 (59%, 32 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlSmaller left CA1, left and right CA2/3, left and right CA4, left and right granule cell layer of the dentate gyrus, left and right subiculum, left hippocampal tail; larger right molecular layer
    Sasabayashi et al.37 (2021)Schizophrenia, 77 (49%, 29 y)
    Healthy controls, 87 (47%, 26 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohortSmaller left and right CA1, left and right molecular layer, left hippocampal tail
    Tannous et al.71 (2020)MDD, 71 (55%, 32 y)
    Healthy controls, 46 (54%, 32 y)
    7.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohortNo significant difference
    Tesli et al.61 (2020)†Schizophrenia with a history of violence, 24 (4%, 34 y)
    Schizophrenia with no history of violence, 51 (2%, 29 y)
    Healthy controls, 90 (3%, 33 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–control, cohort, multisiteSchizophrenia with a history of violence: smaller whole hippocampus, CA1, molecular layer, fimbria, HATA; larger hippocampal fissure
    Schizophrenia with no history of violence: no significant difference
    Travis et al.62 (2015)§MDD, 15 (80%, 38 y)
    Healthy controls, 15 (67%, 35 y)
    4.7 TManualCross-sectional design, case–control, cohortSmaller dentate gyrus (body)
    Travis et al.63 (2016)§MDD, 14 (64%, 36 y)
    Healthy controls, 14 (71%, 33 y)
    4.7 TManualCross-sectional design, case–control, cohortNo significant difference
    Vargas et al.64 (2018)Schizophrenia, 91 (26%, 38 y)
    Healthy controls, 70 (56%, 18 y)
    3.0 TAutomatic (FreeSurfer 5.3**)Cross-sectional design, case–controlSmaller left and right whole hippocampus, right CA1, left and right CA2/3, left and right CA4/dentate gyrus, left and right subiculum, left and right presubiculum
    Xiu et al.38 (2021)First-episode schizophrenia, 39 (59%, 29 y)
    Healthy controls, 30 (57%, 28 y)
    3.0 TAutomatic (FreeSurfer 5.3¶)Cross-sectional design, case–controlNo significant difference
    Xu et al.39 (2018)MDD, 15 (100%, 35 y)
    Healthy controls, 12 (100%, 34 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlSmaller left fimbria
    Yuan et al.40 (2020)MDD, 41 (59%, 35 y)
    Healthy controls, 44 (59%, 33 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlNo significant difference
    Zheng et al.41 (2019)*Schizophrenia, 69 (16%, 38 y)
    Healthy controls, 72 (29%, 36 y)
    3.0 TAutomatic (FreeSurfer 6.0¶)Cross-sectional design, case–controlSmaller left and right whole hippocampus, left CA1, left subiculum, left and right presubiculum, right parasubiculum, left and right molecular layer, left hippocampal tail
    Zhou et al.65 (2020)MDD, 44 (64%, 35 y) Healthy controls, 45 (53%, 33 y)3.0 TAutomatic (FreeSurfer 6.0¶)Longitudinal design; ketamine treatmentBaseline: smaller left and right whole hippocampus Longitudinal changes: increased right whole hippocampus, right CA4 (head), left CA4 (body), left granule cell layer of the dentate gyrus (body), right molecular layer (head)
    • ASHS = Automatic Segmentation of Hippocampal Subfields; CA = cornu ammonis; ECT = electroconvulsive therapy; HATA = hippocampus–amygdala transition area; MDD = major depressive disorder.

    • ↵* Overlapped data.

    • ↵† Overlapped data.

    • ↵‡ Overlapped data.

    • ↵§ Overlapped data.

    • ↵** Atlas by van Leemput and colleagues.72

    • ↵¶ Atlas by Iglesias and colleagues.15

    • View popup
    Table 2:

    Main characteristics of the studies included in the network meta-analysis (part 1 of 2)

    Author (year)No. participants (female)Participant age, yAge at onset, yIllness duration, yMean no. of episodesScore of severity (scale type)Medication statusSubstance misuseMRI field strength, subfield segmentationStudy design
    PatientsHealthy controlsp for sexPatientsHealthy controlsp for age
    Ho et al.16 (2017)155 (49)79 (28)0.6632.531.20.3025.96.6NA40.6 (PANSS)CPZ-eq: 212.32 ± 191.25 mg/dNo substance misuse 3 mo preceding the study3.0 T, automatic (FreeSurfer 5.3)Cross-sectional design; case–control; longitudinal in a subcohort; multisite
    46 (10)46 (10)> 0.9942.941.90.6124.518.2NA81.6 (PANSS)CPZ-eq: 532.45 ± 447.16 mg/d
    Zheng et al.41 (2019)69 (11)72 (21)0.0637.735.90.046NANANANANANA3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    du Plessis et al.33 (2020)79 (21)82 (35)0.0323.023.00.9722.36*0.64First-episode schizophrenia91.27 (PANSS)Treated ≤ 1 moFirst-episode schizophrenia: 35 (44%)
    Controls: 22 (27%)
    3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control; cohort
    Nakahara et al.35 (2020)176 (44)173 (50)0.3938.937.60.2721.917.1NA57.9 (PANSS)CPZ-eq: 372 ± 390 mg/d (n = 144)None3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control; multisite
    Ohi et al.36 (2021)138 (83)162 (54)< 0.05†42.036.7< 0.05†26.216.3NA33.9 (PANSS positive symptoms and PANSS negative symptoms)CPZ-eq: 519.0 ± 524.0 mg/dNA3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    Sasabayashi et al.37 (2021)77 (38)87 (41)> 0.05†28.826.3< 0.05†22.85.6NA68.7 (PANSS)HPD-eq: 10.6 ± 8.3 mg/d (n = 65)None3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control; cohort
    Xiu et al.38 (2021)39 (23)30 (17)0.8528.927.50.5426.95*1.95First-episode schizophrenia44.5 (MCCB)All naiveNone3.0 T, automatic (FreeSurfer 5.3)Cross-sectional design; case–control
    Cao et al.31 (2017)86 (60)152 (96)> 0.05†41.235.4< 0.05†32.3*8.93‡10.5 (HDRS-17)On medication: 4Drug use disorder < 101.5 T, automatic (FreeSurfer 5.3)Cross-sectional design; case–control
    Doolin et al.32 (2018)74 (47)37 (19)> 0.0532.930.9> 0.05NANAFirst-episode MDD (n = 39) > 1 (n = 35)23.46 (HDRS-17)On medication: 47 Medication-free: 27NA3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control; cohort;
    Maller et al.20 (2018)182 (95)68 (34)> 0.0533.029.60.04822.2*10.89.621.36 (HDRS-17)All naive or with a washout period ≥ 5 half-livesNA3.0 T, automatic (FreeSurfer 6.0)Open-label trial
    Na et al.34 (2018)47 (47)30 (30)> 0.0545.343.00.4140.6*4.7NA12.9 (HDRS-17)On medication: 35NA3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control; genes
    Xu et al.39 (2018)15 (15)12 (12)> 0.0534.634.10.51NANANA33.13 (HDRS-24)NANone3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    Han et al.21 (2019)102 (60)135 (78)> 0.05†36.036.0> 0.05†32.3*3.7First-episode MDD (n = 25) > 1 (n = 77)13.93 (HDRS-17)On medication: mostNone3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    Roddy et al.70 (2019)80 (57)83 (49)0.1434.531.50.1332.1*2.4First-episode MDD (n = 43) > 1 (n = 37)22.2 (HDRS-17)NANone3.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    Yuan et al.40 (2020)41 (24)44 (26)0.9634.833.30.5418.3*16.5§< 3 (n = 18), ≥ 3 (n = 13)¶18.3 (HDRS-17)Naive: 16 Untreated ≥ 3 w: 25MDD with drug use disorder: 17 MDD without drug use disorder: 243.0 T, automatic (FreeSurfer 6.0)Cross-sectional design; case–control
    • CPZ-eq = chlorpromazine equivalent; HDRS-17 or -24 = 17- or 24-item Hamilton Depression Rating Scale; HPD-eq = haloperidol equivalent; MCCB = MATRICS Consensus Cognitive Battery; MDD = major depressive disorder; NA = not available; PANSS = Positive and Negative Syndrome Scale.

    • ↵* Determined based on the difference between patient mean age and illness duration.

    • ↵† Inferred based on the results of the corresponding analysis of variance or χ2 test.

    • ↵‡ Median.

    • ↵§ One participant lacked information on illness duration.

    • ↵¶ Ten participants lacked information on number of prior episodes.

    • View popup
    Table 3

    Direct volume comparisons between patients with schizophrenia and healthy controls

    Region of interestMean difference (95% CI), mm3p value*I2, %No. of studiesNo. of patients with schizophreniaNo. of healthy controls
    Left whole hippocampus†−127.840 (−209.381 to −46.298)0.005496700649
     Left CA1†−21.721 (−36.328 to −7.113)0.00607779731
     Left CA3−4.555 (−9.580 to 0.471)0.08427779731
     Left CA4†−6.875 (−11.728 to −2.021)0.008457779731
     Left granule cell layer of the dentate gyrus†−8.430 (−14.089 to −2.771)0.006447779731
     Left subiculum†−10.245 (−18.124 to −2.366)0.01367779731
     Left presubiculum†−7.667 (−14.219 to −1.116)0.0326578606
     Left parasubiculum†−3.041 (−4.531 to −1.551)< 0.00105539576
     Left molecular layer†−17.412 (−27.110 to −7.714)0.00207779731
     Left hippocampal tail†−24.456 (−40.346 to −8.566)0.006747779731
     Left fimbria−2.008 (−5.401 to 1.385)0.25205539576
     Left hippocampal fissure†4.941 (1.953 to 7.930)0.00405539576
     Left HATA†−2.044 (−3.156 to −0.932)0.002235539576
    Right whole hippocampus†−108.803 (−182.105 to −35.500)0.01356700649
     Right CA1†−16.337 (−29.533 to −3.140)0.02327779731
     Right CA3−2.776 (−7.850 to 2.299)0.28307779731
     Right CA4−4.929 (−10.152 to 0.293)0.07477779731
     Right granule cell layer of the dentate gyrus†−6.657 (−11.976 to −1.338)0.02387779731
     Right subiculum†−8.764 (−17.057 to −0.472)0.04987779731
     Right presubiculum−7.051 (−14.077 to −0.024)0.0606578606
     Right parasubiculum†−2.899 (−4.797 to −1.001)0.01275539576
     Right molecular layer†−13.845 (−25.233 to −2.457)0.02237779731
     Right hippocampal tail†−17.221 (−31.208 to −3.234)0.02187779731
     Right fimbria†−4.201 (−6.586 to −1.816)0.00305539576
     Right hippocampal fissure†9.849 (6.728 to 12.970)< 0.00105539576
     Right HATA†−2.727 (−3.787 to −1.667)< 0.00105539576
    • CA = cornu ammonis; CI = confidence interval; HATA = hippocampus–amygdala transition area.

    • ↵* Adjusted.

    • ↵† Statistically significant difference.

    • View popup
    Table 4

    Direct volume comparisons between patients with MDD and healthy controls

    Region of interestMean difference (95% CI), mm3p value*I2, %No. of studiesNo. of patients with MDDNo. of healthy controls
    Left whole hippocampus−74.998 (−175.651 to 25.656)0.26885422325
     Left CA1−13.373 (−28.894 to 2.147)0.24838598546
     Left CA3†−7.491 (−12.873 to −2.109)0.04718598544
     Left CA4†−8.137 (−13.724 to −2.549)0.04697557504
     Left granule cell layer of the dentate gyrus−6.711 (−13.427 to 0.005)0.22746535508
     Left subiculum−7.580 (−16.215 to 1.055)0.24668596546
     Left presubiculum0.247 (−6.656 to 7.150)0.94725494466
     Left parasubiculum0.465 (−1.220 to 2.151)0.77404347222
     Left molecular layer−2.925 (−15.559 to 9.710)0.77815493464
     Left hippocampal tail−3.943 (−25.319 to 17.433)0.78884445436
     Left fimbria−4.641 (−10.825 to 1.543)0.267429192
     Left hippocampal fissure4.000 (−1.544 to 9.544)0.26NA17579
     Left HATA0.628 (−1.139 to 2.396)0.7002258149
    Right whole hippocampus−39.031 (−127.489 to 49.426)0.50845421325
     Right CA1−9.269 (−22.842 to 4.303)0.29718598547
     Right CA3−4.766 (−10.052 to 0.520)0.17668598548
     Right CA4−7.333 (−13.175 to −1.491)0.09687557502
     Right granule cell layer of the dentate gyrus−6.295 (−12.299 to −0.292)0.17626535508
     Right subiculum−8.339 (−17.172 to 0.495)0.17778597547
     Right presubiculum2.210 (−4.963 to 9.384)0.65805495466
     Right parasubiculum1.117 (−1.101 to 3.335)0.47634348223
     Right molecular layer1.735 (−12.626 to 16.095)0.81845495466
     Right hippocampal tail2.729 (−15.585 to 21.042)0.81894448436
     Right fimbria−4.211 (−9.167 to 0.745)0.18029292
     Right hippocampal fissure5.000 (−0.544 to 10.544)0.17NA17881
     Right HATA†2.413 (0.958 to 3.868)0.01272260149
    • CA = cornu ammonis; CI = confidence interval; HATA = hippocampus–amygdala transition area; MDD = major depressive disorder; NA, not available.

    • ↵* Adjusted.

    • ↵† Statistically significant difference.

    • View popup
    Table 5

    Indirect volume comparisons between patients with schizophrenia and patients with MDD

    Region of interestMean difference (95% CI), mm3p value*
    Left whole hippocampus−52.842 (−182.380 to 76.696)0.67
     Left CA1−8.347 (−29.661 to 12.966)0.67
     Left CA32.936 (−4.428 to 10.300)0.67
     Left CA41.262 (−6.139 to 8.663)0.77
     Left granule cell layer of the dentate gyrus−1.719 (−10.501 to 7.063)0.77
     Left subiculum−2.665 (−14.354 to 9.025)0.77
     Left presubiculum−7.914 (−17.431 to 1.602)0.34
     Left parasubiculum†−3.506 (−5.755 to −1.256)0.03
     Left molecular layer−14.488 (−30.416 to 1.440)0.32
     Left hippocampal tail−20.513 (−47.148 to 6.122)0.34
     Left fimbria2.633 (−4.420 to 9.687)0.67
     Left hippocampal fissure0.941 (−5.357 to 7.239)0.77
     Left HATA−2.672 (−4.761 to −0.584)0.08
    Right whole hippocampus−69.772 (−184.654 to 45.111)0.43
     Right CA1−7.067 (−25.997 to 11.863)0.75
     Right CA31.990 (−5.337 to 9.317)0.77
     Right CA42.404 (−5.432 to 10.240)0.77
     Right granule cell layer of the dentate gyrus−0.362 (−8.383 to 7.659)1.00
     Right subiculum−0.426 (−12.542 to 11.691)1.00
     Right presubiculum−9.261 (−19.302 to 0.780)0.25
     Right parasubiculum†−4.016 (−6.935 to −1.097)0.046
     Right molecular layer−15.580 (−33.907 to 2.748)0.25
     Right hippocampal tail−19.950 (−42.993 to 3.094)0.25
     Right fimbria0.011 (−5.489 to 5.510)1.00
     Right hippocampal fissure4.849 (−1.513 to 11.211)0.29
     Right HATA†−5.140 (−6.940 to −3.340)< 0.001
    • CA = cornu ammonis; CI = confidence interval; HATA = hippocampus–amygdala transition area; MDD = major depressive disorder.

    • ↵* Adjusted.

    • ↵† Statistically significant difference.

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Journal of Psychiatry and Neuroscience: 48 (1)
J Psychiatry Neurosci
Vol. 48, Issue 1
21 Feb 2023
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Hippocampal subfield alterations in schizophrenia and major depressive disorder: a systematic review and network meta-analysis of anatomic MRI studies
Yuan Sun, Na Hu, Mingqi Wang, Lu Lu, Chunyan Luo, Biqiu Tang, Chenyang Yao, John A. Sweeney, Qiyong Gong, Changjian Qiu, Su Lui
J Psychiatry Neurosci Feb 2023, 48 (1) E34-E49; DOI: 10.1503/jpn.220086

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Hippocampal subfield alterations in schizophrenia and major depressive disorder: a systematic review and network meta-analysis of anatomic MRI studies
Yuan Sun, Na Hu, Mingqi Wang, Lu Lu, Chunyan Luo, Biqiu Tang, Chenyang Yao, John A. Sweeney, Qiyong Gong, Changjian Qiu, Su Lui
J Psychiatry Neurosci Feb 2023, 48 (1) E34-E49; DOI: 10.1503/jpn.220086
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