Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 26, 2023 - Issue 1
473
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Occupational stress is associated with sex and subregion specific modifications of the amygdala volumes

, , , &
Article: 2247102 | Received 11 Jan 2023, Accepted 07 Aug 2023, Published online: 28 Sep 2023

References

  • Abe, K., Tei, S., Takahashi, H., & Fujino, J. (2022). Structural brain correlates of burnout severity in medical professionals: A voxel-based morphometric study. Neuroscience Letters, 772, 1. https://doi.org/10.1016/j.neulet.2022.136484
  • Albert, K., Pruessner, J., & Newhouse, P. (2015). Estradiol levels modulate brain activity and negative responses to psychosocial stress across the menstrual cycle. Psychoneuroendocrinology, 59, 14–10. https://doi.org/10.1016/j.psyneuen.2015.04.022
  • Asberg, M., Grape, T., Krakau, I., Nygren, A., Rohde, M., Wahlberg, A., et al. (2010). [Stress as the cause of mental illness]. Lakartidningen, 107(19–20), 1307–1310.
  • Bennett, M. R., & Lagopoulos, J. (2014). Stress and trauma: BDNF control of dendritic-spine formation and regression. Progress in Neurobiology. 112, 80–99. https://doi.org/10.1016/j.pneurobio.2013.10.005
  • Bested, A. C., & Marshall, L. M. (2015). Review of myalgic encephalomyelitis/chronic fatigue syndrome: An evidence-based approach to diagnosis and management by clinicians. Rev Environ Health, 30(4), 223–249.
  • Blix, E., Perski, A., Berglund, H., & Savic, I. (2013). Long-term occupational stress is associated with regional reductions in brain tissue volumes. PLOS One, 8(6), e64065. https://doi.org/10.1371/journal.pone.0064065
  • Bonne, O., Brandes, D., Gilboa, A., Gomori, J. M., Shenton, M. E., Pitman, R. K., & Shalev, A. Y. (2001). Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. American Journal of Psychiatry, 158(8), 1248–1251. https://doi.org/10.1176/appi.ajp.158.8.1248
  • Brown, E. M., Pierce, M. E., Clark, D. C., Fischl, B. R., Iglesias, J. E., Milberg, W. P., McGlinchey, R. E., & Salat, D. H. (2020). Test-retest reliability of FreeSurfer automated hippocampal subfield segmentation within and across scanners. NeuroImage, 210, 116563. https://doi.org/10.1016/j.neuroimage.2020.116563
  • Chen, L. W., Sun, D., Davis, S. L., Haswell, C. C., Dennis, E. L., Swanson, C. A., Whelan, C. D., Gutman, B., Jahanshad, N., Iglesias, J. E., Thompson, P., Wagner, H. R., Saemann, P., LaBar, K. S., & Morey, R. A,. (2018). Smaller hippocampal CA1 subfield volume in posttraumatic stress disorder. Depression and Anxiety, 35(11), 1018–1029. https://doi.org/10.1002/da.22833
  • Chiappiniello, A., Tarducci, R., Muscio, C., Bruzzone, M. G., Bozzali, M., Tiraboschi, P., Nigri, A., Ambrosi, C., Chipi, E., Ferraro, S., Festari, C., Gasparotti, R., Gianeri, R., Giulietti, G., Mascaro, L., Montanucci, C., Nicolosi, V., Rosazza, C., Serra, L., … Jovicich, J. (2021). Automatic multispectral MRI segmentation of human hippocampal subfields: An evaluation of multicentric test-retest reproducibility. Brain Structure and Function, 226(1), 137–150. https://doi.org/10.1007/s00429-020-02172-w
  • Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. https://doi.org/10.1006/nimg.1998.0395
  • De Bellis, M. D., Hall, J., Boring, A. M., Frustaci, K., & Moritz, G. (2001). A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry, 50(4), 305–309. https://doi.org/10.1016/s0006-3223(01)01105-2
  • DeCasien, A. R., Guma, E., Liu, S., & Raznahan, A. (2022). Sex differences in the human brain: a roadmap for more careful analysis and interpretation of a biological reality. Biology of Sex Differences, 13(1), 43. England: © 2022. The Author(s) p. https://doi.org/10.1186/s13293-022-00448-w
  • Fanselow, M. S., & Dong, H. W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1), 7–19. https://doi.org/10.1016/j.neuron.2009.11.031
  • Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9(2), 195–207. https://doi.org/10.1006/nimg.1998.0396
  • Fish, A. M., Nadig, A., Seidlitz, J., Reardon, P. K., Mankiw, C., McDermott, C. L., Blumenthal, J. D., Clasen, L. S., Lalonde, F., Lerch, J. P., Chakravarty, M. M., Shinohara, R. T., & Raznahan, A. (2020). Sex-biased trajectories of amygdalo-hippocampal morphology change over human development. NeuroImage, 204, 116122. https://doi.org/10.1016/j.neuroimage.2019.116122
  • Galea, L. A., McEwen, B. S., Tanapat, P., Deak, T., Spencer, R. L., & Dhabhar, F. S. (1997). Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience, 81(3), 689–697. https://doi.org/10.1016/S0306-4522(97)00233-9
  • Gan, J. O., Bowline, E., Lourenco, F. S., & Pickel, V. M. (2014). Adolescent social isolation enhances the plasmalemmal density of NMDA NR1 subunits in dendritic spines of principal neurons in the basolateral amygdala of adult mice. Neuroscience, 258, 174–183. https://doi.org/10.1016/j.neuroscience.2013.11.003
  • Gavelin, H. M., Neely, A. S., Dunås, T., Eskilsson, T., Järvholm, L. S., & Boraxbekk, C. J. (2020). Mental fatigue in stress-related exhaustion disorder: Structural brain correlates, clinical characteristics and relations with cognitive functioning. NeuroImage. Clinical, 27, 102337. https://doi.org/10.1016/j.nicl.2020.102337
  • Glise, K., Wiegner, L., & Jonsdottir, I. H. (2020). Long-term follow-up of residual symptoms in patients treated for stress-related exhaustion. BMC Psychology, 8(1), 26. https://doi.org/10.1186/s40359-020-0395-8
  • Gould, E., Tanapat, P., McEwen, B. S., Flügge, G., & Fuchs, E. (1998). Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proceedings of the National Academy of Sciences of the United States of America, 95(6), 3168–3171. https://doi.org/10.1073/pnas.95.6.3168
  • Grossi, G., Perski, A., Osika, W., & Savic, I. (2015). Stress-related exhaustion disorder–clinical manifestation of burnout? A review of assessment methods, sleep impairments, cognitive disturbances, and neuro-biological and physiological changes in clinical burnout. Scandinavian Journal of Psychology, 56(6), 626–636. https://doi.org/10.1111/sjop.12251
  • Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., Shirtcliff, E. A., Pollak, S. D., & Davidson, R. J. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77(4), 314–323. https://doi.org/10.1016/j.biopsych.2014.04.020
  • Hayes, J. P., Hayes, S., Miller, D. R., Lafleche, G., Logue, M. W., & Verfaellie, M. (2017). Automated measurement of hippocampal subfields in PTSD: Evidence for smaller dentate gyrus volume. Journal of Psychiatric Research, 95, 247–252. https://doi.org/10.1016/j.jpsychires.2017.09.007
  • Henigsberg, N., Kalember, P., Petrović, Z. K., & Šečić, A. (2019). Neuroimaging research in posttraumatic stress disorder - Focus on amygdala, hippocampus and prefrontal cortex. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 90, 37–42. https://doi.org/10.1016/j.pnpbp.2018.11.003
  • Hillerer, K. M., Slattery, D. A., & Pletzer, B. (2019). Neurobiological mechanisms underlying sex-related differences in strress related disorders. Efects. of Neuroactive Steroids on the Hippocampus.Front Neuroendocrin, 55, 1–55.
  • Holmes, T. H., & Rahe, R. H. (1967). The Social readjustment rating scale. Journal of Psychosomatic Research, 11(2), 213–218. https://doi.org/10.1016/0022-3999(67)90010-4
  • Iglesias, J. E., Augustinack, J. C., Nguyen, K., Player, C. M., Player, A., Wright, M., Roy, N., Frosch, M. P., McKee, A. C., Wald, L. L., Fischl, B., & Van Leemput, K. (2015). A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI. NeuroImage, 115, 117–137. https://doi.org/10.1016/j.neuroimage.2015.04.042
  • Kajantie, E., & Phillips, D. I. (2006). The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology, 31(2), 151–178. https://doi.org/10.1016/j.psyneuen.2005.07.002
  • Karl, A., Schaefer, M., Malta, L. S., Dörfel, D., Rohleder, N., & Werner, A. (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience & Biobehavioral Reviews. 30(7), 1004–1031. https://doi.org/10.1016/j.neubiorev.2006.03.004
  • Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine, 61(2), 154–162. https://doi.org/10.1097/00006842-199903000-00006
  • Kitayama, N., Vaccarino, V., Kutner, M., Weiss, P., & Bremner, J. D. (2005). Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: A meta-analysis. Journal of Affective Disorders, 88(1), 79–86. https://doi.org/10.1016/j.jad.2005.05.014
  • Kogler, L., Gur, R. C., & Derntl, B. (2015). Sex differences in cognitive regulation of psychosocial achievement stress: brain and behavior. Human Brain Mapping, 36(3), 1028–1042. https://doi.org/10.1002/hbm.22683
  • Kogler, L., Müller, V. I., Seidel, E.-M., Boubela, R., Kalcher, K., Moser, E., Habel, U., Gur, R. C., Eickhoff, S. B., & Derntl, B. (2016). Sex differences in the functional connectivity of the amygdalae in association with cortisol. NeuroImage, 134, 410–423. https://doi.org/10.1016/j.neuroimage.2016.03.064
  • Kuo, J. R., Kaloupek, D. G., & Woodward, S. H. (2012). Amygdala volume in combat-exposed veterans with and without posttraumatic stress disorder: a cross-sectional study. Archives of General Psychiatry, 69(10), 1080–1086. https://doi.org/10.1001/archgenpsychiatry.2012.73
  • Lakshminarasimhan, H., & Chattarji, S. (2012). Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLOS One. 7(1), e30481. https://doi.org/10.1371/journal.pone.0030481
  • Landré, L., Destrieux, C., Baudry, M., Barantin, L., Cottier, J.-P., Martineau, J., Hommet, C., Isingrini, M., Belzung, C., Gaillard, P., Camus, V., & El Hage, W. (2010). Preserved subcortical volumes and cortical thickness in women with sexual abuse-related PTSD. Psychiatry Research: Neuroimaging, 183(3), 181–186. https://doi.org/10.1016/j.pscychresns.2010.01.015
  • Lazarus, R. S., & Folkman, S. (1987). Transactional theory and research on emotions and coping. European Journal of Personality, 1(3), 141–169. https://doi.org/10.1002/per.2410010304
  • Lee, D., Kim, W., Lee, J. E., Lee, J., Lee, S.-K., Chang, S.-J., Jeung, D. Y., Hyun, D.-S., Ryu, H.-Y., Kim, C., & Jung, Y.-C. (2021). Regional gray matter volume related to high occupational stress in firefighters. Journal of Korean Medical Science, 36(50), e335. https://doi.org/10.3346/jkms.2021.36.e335
  • McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105–122. https://doi.org/10.1146/annurev.neuro.22.1.105
  • McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews, 87(3), 873–904. https://doi.org/10.1152/physrev.00041.2006
  • Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005). Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America, 102(26), 9371–9376. https://doi.org/10.1073/pnas.0504011102
  • Morey, R. A., Clarke, E. K., Haswell, C. C., Phillips, R. D., Clausen, A. N., Mufford, M. S., et al. (2020). Amygdala nuclei volume and shape in military veterans with posttraumatic stress disorder. Biol Psychiatry Cogn Neurosci Neuroimaging, 5(3), 281–290.
  • Morey, R. A., Gold, A. L., LaBar, K. S., Beall, S. K., Brown, V. M., Haswell, C. C., Nasser, J. D., Wagner, H. R., McCarthy, G., & Mid-Atlantic Mirecc Workgroup, f t (2012). Amygdala volume changes in posttraumatic stress disorder in a large case-controlled veterans group. Archives of General Psychiatry, 69(11), 1169–1178. https://doi.org/10.1001/archgenpsychiatry.2012.50
  • Ousdal, O. T., Milde, A. M., Hafstad, G. S., Hodneland, E., Dyb, G., Craven, A. R., Melinder, A., Endestad, T., & Hugdahl, K. (2020). The association of PTSD symptom severity with amygdala nuclei volumes in traumatized youths. Translational Psychiatry, 10(1), 288. https://doi.org/10.1038/s41398-020-00974-4
  • Pavlisa, G., Papa, J., & Pavić, L. (2006). Bilateral MR volumetry of the amygdala in chronic PTSD patients. Coll Antropol, 30(3), 565–568.
  • Savic, I. (2015). Structural changes of the brain in relation to occupational stress. Cerebral Cortex, 25(6), 1554–1564. https://doi.org/10.1093/cercor/bht348
  • Savic, I. (2020). MRS shows regionally increased glutamate levels among patients with exhaustion syndrome due to occupational stress. Cerebral Cortex, 30(6), 3759–3770. https://doi.org/10.1093/cercor/bhz340
  • Savic, I., Perski, A., & Osika, W. (2018). MRI shows that exhaustion syndrome due to chronic occupational stress is associated with partially reversible cerebral changes. Cerebral Cortex , 28(3), 894–906. https://doi.org/10.1093/cercor/bhw413
  • Saygin, Z. M., Kliemann, D., Iglesias, J. E., van der Kouwe, A. J. W., Boyd, E., Reuter, M., Stevens, A., Van Leemput, K., McKee, A., Frosch, M. P., Fischl, B., & Augustinack, J. C. (2017). High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: Manual segmentation to automatic atlas. NeuroImage, 155, 370–382. https://doi.org/10.1016/j.neuroimage.2017.04.046
  • Teicher, M. H., Anderson, C. M., & Polcari, A. (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci U S A, 109(9), E563–72.
  • Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., Millner, A., Galvan, A., Davidson, M. C., Eigsti, I.-M., Thomas, K. M., Freed, P. J., Booma, E. S., Gunnar, M. R., Altemus, M., Aronson, J., & Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13(1), 46–61. https://doi.org/10.1111/j.1467-7687.2009.00852.x
  • Veer, I. M., Oei, N. Y., van Buchem, M. A., Spinhoven, P., Elzinga, B. M., & Rombouts, S. A. (2015). Evidence for smaller right amygdala volumes in posttraumatic stress disorder following childhood trauma. Psychiatry Research: Neuroimaging, 233(3), 436–442. https://doi.org/10.1016/j.pscychresns.2015.07.016
  • Vyas, A., Bernal, S., & Chattarji, S. (2003). Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Research. 965(1-2), 290–294. https://doi.org/10.1016/S0006-8993(02)04162-8
  • Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 22(15), 6810–6818. https://doi.org/10.1523/JNEUROSCI.22-15-06810.2002
  • Vyas, A., Pillai, A. G., & Chattarji, S. (2004). Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience, 128(4), 667–673. https://doi.org/10.1016/j.neuroscience.2004.07.013
  • Wang, J., Korczykowski, M., Rao, H., Fan, Y., Pluta, J., Gur, R. C., McEwen, B. S., & Detre, J. A. (2007). Gender difference in neural response to psychological stress. Social Cognitive and Affective Neuroscience, 2(3), 227–239. https://doi.org/10.1093/scan/nsm018
  • Woon, F. L., & Hedges, D. W. (2009). Amygdala volume in adults with posttraumatic stress disorder: A meta-analysis. The Journal of Neuropsychiatry and Clinical Neurosciences, 21(1), 5–12. https://doi.org/10.1176/jnp.2009.21.1.5