Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-27T02:49:30.543Z Has data issue: false hasContentIssue false

Evaluation of gray matter reduction in patients with typhoon-related posttraumatic stress disorder using causal network analysis of structural MRI

Published online by Cambridge University Press:  17 September 2020

Hui Juan Chen*
Affiliation:
Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), NO. 19, XIUHUA ST, XIUYING DIC, Haikou, 570311, Hainan, P.R. China
Rongfeng Qi
Affiliation:
Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, Jiangsu 210002, China
Jun Ke
Affiliation:
Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, Jiangsu 210002, China Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu Province 215006, China
Jie Qiu
Affiliation:
Department of Ultrasound, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), NO. 19, XIUHUA ST, XIUYING DIC, Haikou, 570311, Hainan, P.R. China
Qiang Xu
Affiliation:
Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, Jiangsu 210002, China
Yuan Zhong
Affiliation:
Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, Jiangsu 210002, China
Guang Ming Lu
Affiliation:
Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, Jiangsu 210002, China
Feng Chen*
Affiliation:
Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), NO. 19, XIUHUA ST, XIUYING DIC, Haikou, 570311, Hainan, P.R. China
*
Author for correspondence: Feng Chen, E-mail: [email protected]
Author for correspondence: Feng Chen, E-mail: [email protected]

Abstract

Background

The structural changes recent-onset posttraumatic stress disorder (PTSD) subjects were rarely investigated. This study was to compare temporal and causal relationships of structural changes in recent-onset PTSD with trauma-exposed control (TEC) subjects and non-TEC subjects.

Methods

T1-weighted magnetic resonance images of 27 PTSD, 33 TEC and 30 age- and sex-matched healthy control (HC) subjects were studied. The causal network of structural covariance was used to evaluate the causal relationships of structural changes in PTSD patients.

Results

Volumes of bilateral hippocampal and left lingual gyrus were significantly smaller in PTSD patients and TEC subjects than HC subjects. As symptom scores increase, reduction in gray matter volume began in the hippocampus and progressed to the frontal lobe, then to the temporal and occipital cortices (p < 0.05, false discovery rate corrected). The hippocampus might be the primary hub of the directional network and demonstrated positive causal effects on the frontal, temporal and occipital regions (p < 0.05, false discovery rate corrected). The frontal regions, which were identified to be transitional points, projected causal effects to the occipital lobe and temporal regions and received causal effects from the hippocampus (p < 0.05, false discovery rate corrected).

Conclusions

The results offer evidence of localized abnormalities in the bilateral hippocampus and remote abnormalities in multiple temporal and frontal regions in typhoon-exposed PTSD patients.

Type
Original Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Bremner, J. D., Narayan, M., Staib, L. H., Southwick, S. M., McGlashan, T., & Charney, D. S. (1999). Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. American Journal of Psychiatry, 156, 17871795. doi: 10.1176/ajp.156.11.1787.Google ScholarPubMed
Bremner, J. D., Vermetten, E., Vythilingam, M., Afzal, N., Schmahl, C., Elzinga, B., & Charney, D. S. (2004). Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biological Psychiatry, 55, 612620. doi: 10.1016/j.biopsych.2003.10.001.CrossRefGoogle ScholarPubMed
Bromis, K., Calem, M., Reinders, A., Williams, S. C. R., & Kempton, M. J. (2018). Meta-analysis of 89 structural MRI studies in posttraumatic stress disorder and comparison with major depressive disorder. American Journal of Psychiatry, 175, 989998. doi: 10.1176/appi.ajp.2018.17111199.CrossRefGoogle ScholarPubMed
Bruce, S. E., Buchholz, K. R., Brown, W. J., Yan, L., Durbin, A., & Sheline, Y. I. (2012). Altered emotional interference processing in the amygdala and insula in women with Post-Traumatic Stress Disorder. NeuroImage Clinical, 2, 4349. doi: 10.1016/j.nicl.2012.11.003.CrossRefGoogle ScholarPubMed
Chen, X., Jiang, Y., Chen, L., He, H., Dong, L., Hou, C., … Luo, C. (2017). Altered hippocampo-cerebello-cortical circuit in schizophrenia by a spatiotemporal consistency and causal connectivity analysis. Frontiers in Neuroscience, 11, 25. doi: 10.3389/fnins.2017.00025.CrossRefGoogle ScholarPubMed
Chen, F., Ke, J., Qi, R., Xu, Q., Zhong, Y., Liu, T., … Lu, G. (2018). Increased inhibition of the amygdala by the mPFC may reflect a resilience factor in post-traumatic stress disorder: A resting-state fMRI granger causality analysis. Frontiers in Psychiatry, 9, 516. doi: 10.3389/fpsyt.2018.00516.CrossRefGoogle ScholarPubMed
Chen, H. J., Zhang, L., Ke, J., Qi, R., Xu, Q., Zhong, Y., … Chen, F. (2019). Altered resting-state dorsal anterior cingulate cortex functional connectivity in patients with post-traumatic stress disorder. The Australian and New Zealand Journal of Psychiatry, 53, 6879. doi: 10.1177/0004867418812674.CrossRefGoogle ScholarPubMed
Fan, X., Yan, H., Shan, Y., Shang, K., Wang, X., Wang, P., … Zhao, G. (2016). Distinctive structural and effective connectivity changes of semantic cognition network across left and right mesial temporal lobe epilepsy patients. Neural Plasticity, 2016, 8583420. doi: 10.1155/2016/8583420.CrossRefGoogle ScholarPubMed
Jatzko, A., Rothenhofer, S., Schmitt, A., Gaser, C., Demirakca, T., Weber-Fahr, W., … Braus, D. F. (2006). Hippocampal volume in chronic posttraumatic stress disorder (PTSD): MRI study using two different evaluation methods. Journal of Affective Disorders, 94, 121126. doi: 10.1016/j.jad.2006.03.010.CrossRefGoogle ScholarPubMed
Jiang, Y., Luo, C., Li, X., Duan, M., He, H., Chen, X., … Yao, D. (2018). Progressive reduction in gray matter in patients with schizophrenia assessed with MR imaging by using causal network analysis. Radiology, 287, 729. doi: 10.1148/radiol.2018184005.CrossRefGoogle ScholarPubMed
Karl, A., Schaefer, M., Malta, L. S., Dorfel, D., Rohleder, N., & Werner, A. (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience and Biobehavioral Reviews, 30, 10041031. doi: 10.1016/j.neubiorev.2006.03.004.CrossRefGoogle ScholarPubMed
Ke, J., Zhang, L., Qi, R., Xu, Q., Zhong, Y., Liu, T., … Chen, F. (2018). Typhoon-related post-traumatic stress disorder and trauma might lead to functional integration abnormalities in intra- and inter-resting state networks: A resting-state Fmri independent component analysis. Cellular Physiology and Biochemistry : International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, 48, 99110. doi:10.1159/000491666.CrossRefGoogle ScholarPubMed
Kelley, L. P., Weathers, F. W., McDevitt-Murphy, M. E., Eakin, D. E., & Flood, A. M. (2009). A comparison of PTSD symptom patterns in three types of civilian trauma. Journal of Traumatic Stress, 22, 227235. doi: 10.1002/jts.20406.CrossRefGoogle ScholarPubMed
Klugah-Brown, B., Luo, C., Peng, R., He, H., Li, J., Dong, L., & Yao, D. (2019). Altered structural and causal connectivity in frontal lobe epilepsy. BMC Neurology, 19, 70. doi: 10.1186/s12883-019-1300-z.CrossRefGoogle ScholarPubMed
Lei, D., Li, L., Li, L., Suo, X., Huang, X., Lui, S., … Gong, Q. (2015). Microstructural abnormalities in children with post-traumatic stress disorder: A diffusion tensor imaging study at 3.0 T. Scientific Reports, 5, 8933. doi: 10.1038/srep08933.CrossRefGoogle Scholar
Lui, S., Zhou, X. J., Sweeney, J. A., & Gong, Q. (2016). Psychoradiology: The frontier of neuroimaging in psychiatry. Radiology, 281, 357372. doi: 10.1148/radiol.2016152149.CrossRefGoogle ScholarPubMed
Meng, Y., Qiu, C., Zhu, H., Lama, S., Lui, S., Gong, Q., & Zhang, W. (2014). Anatomical deficits in adult posttraumatic stress disorder: A meta-analysis of voxel-based morphometry studies. Behavioural Brain Research, 270, 307315. doi: 10.1016/j.bbr.2014.05.021.CrossRefGoogle ScholarPubMed
Nardo, D., Högberg, G., Lanius, R. A., Jacobsson, H., Jonsson, C., Hällström, T., & Pagani, M. (2013). Gray matter volume alterations related to trait dissociation in PTSD and traumatized controls. Acta Psychiatrica Scandinavica, 128, 222233. doi: 10.1111/acps.12026.CrossRefGoogle ScholarPubMed
O'Doherty, D. C., Chitty, K. M., Saddiqui, S., Bennett, M. R., & Lagopoulos, J. (2015). A systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in posttraumatic stress disorder. Psychiatry Research, 232, 133. doi: 10.1016/j.pscychresns.2015.01.002.CrossRefGoogle ScholarPubMed
O'Doherty, D. C. M., Tickell, A., Ryder, W., Chan, C., Hermens, D. F., Bennett, M. R., & Lagopoulos, J. (2017). Frontal and subcortical grey matter reductions in PTSD. Psychiatry Research Neuroimaging, 266, 19. doi: 10.1016/j.pscychresns.2017.05.008.CrossRefGoogle ScholarPubMed
Palaniyappan, L., Simmonite, M., White, T. P., Liddle, E. B., & Liddle, P. F. (2013). Neural primacy of the salience processing system in schizophrenia. Neuron, 79, 814828. doi: 10.1016/j.neuron.2013.06.027.CrossRefGoogle Scholar
Patel, R., Spreng, R. N., Shin, L. M., & Girard, T. A. (2012). Neurocircuitry models of posttraumatic stress disorder and beyond: A meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 36, 21302142. doi: 10.1016/j.neubiorev.2012.06.003.CrossRefGoogle ScholarPubMed
Ridgway, G. R., Omar, R., Ourselin, S., Hill, D. L., Warren, J. D., & Fox, N. C. (2009). Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage, 44, 99111. doi: 10.1016/j.neuroimage.2008.08.045.CrossRefGoogle ScholarPubMed
Shang, J., Lui, S., Meng, Y., Zhu, H., Qiu, C., Gong, Q., … Zhang, W. (2014). Alterations in low-level perceptual networks related to clinical severity in PTSD after an earthquake: A resting-state fMRI study. PLoS One, 9, e96834. doi: 10.1371/journal.pone.0096834.CrossRefGoogle ScholarPubMed
Smith, M. E. (2005). Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: A meta-analysis of structural MRI studies. Hippocampus, 15, 798807. doi: 10.1002/hipo.20102.CrossRefGoogle ScholarPubMed
Stark, E. A., Parsons, C. E., Van Hartevelt, T. J., Charquero-Ballester, M., McManners, H., Ehlers, A., … Kringelbach, M. L. (2015). Post-traumatic stress influences the brain even in the absence of symptoms: A systematic, quantitative meta-analysis of neuroimaging studies. Neuroscience and Biobehavioral Reviews, 56, 207221. doi: 10.1016/j.neubiorev.2015.07.007.CrossRefGoogle ScholarPubMed
Tavanti, M., Battaglini, M., Borgogni, F., Bossini, L., Calossi, S., Marino, D., … De Stefano, N. (2012). Evidence of diffuse damage in frontal and occipital cortex in the brain of patients with post-traumatic stress disorder. Neurological Sciences: Official Journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology, 33, 5968. doi: 10.1007/s10072-011-0659-4.CrossRefGoogle ScholarPubMed
Weathers, F. W., Keane, T. M., & Davidson, J. R. (2001). Clinician-administered PTSD scale: A review of the first ten years of research. Depression and anxiety, 13, 132156.CrossRefGoogle ScholarPubMed
Weng, Y., Qi, R., Chen, F., Ke, J., Xu, Q., Zhong, Y., … Lu, G. (2018). The temporal propagation of intrinsic brain activity associate with the occurrence of PTSD. Frontiers in Psychiatry, 9, 218. doi: 10.3389/fpsyt.2018.00218.CrossRefGoogle ScholarPubMed
Weng, Y., Qi, R., Zhang, L., Luo, Y., Ke, J., Xu, Q., … Lu, G. (2019). Disturbed effective connectivity patterns in an intrinsic triple network model are associated with posttraumatic stress disorder. Neurological Sciences: Official Journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology, 40, 339349. doi: 10.1007/s10072-018-3638-1.CrossRefGoogle Scholar
Woon, F. L., Sood, S., & Hedges, D. W. (2010). Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: A meta-analysis. Progress in Neuropsychopharmacology & Biological Psychiatry, 34, 11811188. doi: 10.1016/j.pnpbp.2010.06.016.CrossRefGoogle ScholarPubMed
Yehuda, R., Golier, J. A., Tischler, L., Harvey, P. D., Newmark, R., Yang, R. K., & Buchsbaum, M. S. (2007). Hippocampal volume in aging combat veterans with and without post-traumatic stress disorder: Relation to risk and resilience factors. Journal of Psychiatric Research, 41, 435445. doi: 10.1016/j.jpsychires.2005.12.002.CrossRefGoogle ScholarPubMed
Yin, Y., Jin, C., Eyler, L. T., Jin, H., Hu, X., Duan, L., … Li, L. (2012). Altered regional homogeneity in post-traumatic stress disorder: A resting-state functional magnetic resonance imaging study. Neuroscience Bulletin, 28, 541549. doi: 10.1007/s12264-012-1261-3.CrossRefGoogle ScholarPubMed
Zhang, Z., Liao, W., Xu, Q., Wei, W., Zhou, H. J., Sun, K., … Lu, G. (2017). Hippocampus-associated causal network of structural covariance measuring structural damage progression in temporal lobe epilepsy. Human Brain Mapping, 38, 753766. doi: 10.1002/hbm.23415.CrossRefGoogle ScholarPubMed
Zhao, Z., Wang, X., Fan, M., Yin, D., Sun, L., Jia, J., … Gong, J. (2016). Altered effective connectivity of the primary motor cortex in stroke: A resting-state fMRI study with granger causality analysis. PLoS One, 11, e0166210. doi: 10.1371/journal.pone.0166210.CrossRefGoogle ScholarPubMed
Zung, W. W. (1965). A self-rating depression scale. Archives of General Psychiatry, 12, 6370. doi: 10.1001/archpsyc.1965.01720310065008.CrossRefGoogle ScholarPubMed
Zung, W. W. (1971). A rating instrument for anxiety disorders. Psychosomatics, 12, 371379. doi: 10.1016/s0033-3182(71)71479-0.CrossRefGoogle ScholarPubMed
Supplementary material: File

Chen et al. supplementary material

Tables S1-S3

Download Chen et al. supplementary material(File)
File 24.3 KB