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Abnormal brain structure implicated in patients with functional dyspepsia

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Abstract

Recent studies suggest dysfunctional brain-gut interactions are involved in the pathophysiology of functional dyspepsia (FD). However, limited studies have investigated brain structural abnormalities in FD patients. This study aimed to identify potential differences in both cortical thickness and subcortical volume in FD patients compared to healthy controls (HCs) and to explore relationships of structural abnormalities with clinical symptoms. Sixty-nine patients and forty-nine HCs underwent 3T structural magnetic resonance imaging scans. Cortical thickness and subcortical volume were compared between the groups across the cortical and subcortical regions, respectively. Regression analysis was then performed to examine relationships between the structure alternations and clinical symptoms in FD patients. Our results showed that FD patients had decreased cortical thickness compared to HCs in the distributed brain regions including the dorsolateral prefrontal cortex (dlPFC), ventrolateral prefrontal cortex (vlPFC), medial prefrontal cortex (mPFC), anterior/posterior cingulate cortex (ACC/PCC), insula, superior parietal cortex (SPC), supramarginal gyrus and lingual gyrus. Significantly negative correlations were observed between the Nepean Dyspepsia Index (NDI) and cortical thickness in the mPFC, second somatosensory cortex (SII), ACC and parahippocampus (paraHIPP). And significantly negative correlations were found between disease duration and the cortical thickness in the vlPFC, first somatosensory cortex (SI) and insula in FD patients. These findings suggest that FD patients have structural abnormalities in brain regions involved in sensory perception, sensorimotor integration, pain modulation, affective and cognitive controls. The relationships between the brain structural changes and clinical symptoms indicate that the alternations may be a consequence of living with FD.

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References

  • Benuzzi, F., Lui, F., Duzzi, D., Nichelli, P. F., & Porro, C. A. (2008). Does it look painful or disgusting? Ask your parietal and cingulate cortex. Journal of Neuroscience, 28(4), 923–931.

    Article  CAS  PubMed  Google Scholar 

  • Berman, S. M., Naliboff, B. D., Suyenobu, B., Labus, J. S., Stains, J., Ohning, G., et al. (2008). Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. Journal of Neuroscience, 28(2), 349–359.

    Article  CAS  PubMed  Google Scholar 

  • Colloca, L., Klinger, R., Flor, H., & Bingel, U. (2013). Placebo analgesia: Psychological and neurobiological mechanisms. Pain, 154(4), 511–514.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194.

    Article  CAS  PubMed  Google Scholar 

  • DeCharms, R., Maeda, F., Glover, G. H., Ludlow, D., Pauly, J. M., Soneji, D., et al. (2005). Control over brain activation and pain learned by using real-time functional MRI. Journal of Neuroscience, 102(51), 18626–18631.

    CAS  Google Scholar 

  • Derbyshire, S. W. (2003). A systematic review of neuroimaging data during visceral stimulation. American Journal of Gastroenterology, 98(1), 12–20.

    Article  PubMed  Google Scholar 

  • Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980.

    Article  PubMed  Google Scholar 

  • Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97(20), 11050–11055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.

    Article  CAS  PubMed  Google Scholar 

  • Henke, P. G., & Savoie, R. J. (1982). The cingulate cortex and gastric pathology. Brain Research Bulletin, 8(5), 489–492.

    Article  CAS  PubMed  Google Scholar 

  • Jensen, K. B., Kosek, E., Petzke, F., Carville, S., Fransson, P., Marcus, H., et al. (2009). Evidence of dysfunctional pain inhibition in fibromyalgia reflected in rACC during provoked pain. Pain, 144(1), 95–100.

    Article  PubMed  Google Scholar 

  • Lee, I. S., Wang, H., Chae, Y., Preissl, H., & Enck, P. (2016). Functional neuroimaging studies in functional dyspepsia patients: A systematic review. Neurogastroenterology and Motility, 28(6), 793–805.

    Article  PubMed  Google Scholar 

  • Li, S., Yuan, X., Pu, F., Li, D., Fan, Y., Wu, L., et al. (2014). Abnormal changes of multidimensional surface features using multivariate pattern classification in amnestic mild cognitive impairment patients. Journal of Neuroscience, 34(32), 10541–10553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, P., Zeng, F., Zhou, G., Wang, J., Wen, H., Deneen, K., et al. (2013a). Alterations of the default mode network in functional dyspepsia patients: A resting-state fmri study. Neurogastroenterology and Motility, 25(6), e382–e388.

    Article  CAS  PubMed  Google Scholar 

  • Liu, P., Qin, W., Wang, J., Zeng, F., Zhou, G., Wen, H., et al. (2013b). Identifying neural patterns of functional dyspepsia using multivariate pattern analysis: A resting-state fMRI study. PloS One, 8(7), e68205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, P., Zeng, F., Yang, F., Wang, J., Liu, X., Wang, Q., et al. (2014). Altered structural covariance of the striatum in functional dyspepsia patients. Neurogastroenterology and Motility, 26(8), 1144–1154.

    Article  CAS  PubMed  Google Scholar 

  • Lu, C. L., Wu, Y. T., Yeh, T. C., Chen, L. F., Chang, F. Y., Lee, S. D., et al. (2004). Neuronal correlates of gastric pain induced by fundus distension: A 3T-fMRI study. Neurogastroenterology and Motility, 16(5), 575–587.

    Article  PubMed  Google Scholar 

  • Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure and Function, 214(5), 655–667.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nielsen, F. Å., Balslev, D., & Hansen, L. K. (2005). Mining the posterior cingulate: Segregation between memory and pain components. NeuroImage, 27(3), 520–532.

    Article  PubMed  Google Scholar 

  • Roy, M., Piché, M., Chen, J.-I., Peretz, I., & Rainville, P. (2009). Cerebral and spinal modulation of pain by emotions. Proceedings of the National Academy of Sciences of the United States of America, 106(49), 20900–20905.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz-Klaus, B. (2009). Neurotoxic lesion of the rostral perirhinal cortex blocks stress-induced exploratory behavioral changes in male rats. Stress, 12(2), 186–192.

    Article  CAS  PubMed  Google Scholar 

  • Stephan, K. E., Iglesias, S., Heinzle, J., & Diaconescu, A. O. (2015). Translational perspectives for computational neuroimaging. Neuron, 87(4), 716–732. doi:10.1016/j.neuron.2015.07.008.

    Article  CAS  PubMed  Google Scholar 

  • Tack, J., Talley, N. J., Camilleri, M., Holtmann, G., Hu, P., Malagelada, J. R., et al. (2006). Functional gastroduodenal disorders. Gastroenterology, 130(5), 1466–1479.

    Article  PubMed  Google Scholar 

  • Van Oudenhove, L., Vandenberghe, J., Dupont, P., Geeraerts, B., Vos, R., Bormans, G., et al. (2009). Cortical deactivations during gastric fundus distension in health: Visceral pain-specific response or attenuation of ‘default mode’ brain function? A H(2)(15)O-PET study. Neurogastroenterology and Motility, 21(3), 259–271.

    Article  CAS  PubMed  Google Scholar 

  • Van Oudenhove, L., Vandenberghe, J., Dupont, P., Geeraerts, B., Vos, R., Dirix, S., et al. (2010a). Abnormal regional brain activity during rest and (anticipated) gastric distension in functional dyspepsia and the role of anxiety: A H(2)(15)O -PET study. American Journal of Gastroenterology, 105(4), 913–924.

    Article  PubMed  Google Scholar 

  • Van Oudenhove, L., Vandenberghe, J., Dupont, P., Geeraerts, B., Vos, R., Dirix, S., et al. (2010b). Regional brain activity in functional dyspepsia: A H(2)(15)O-PET study on the role of gastric sensitivity and abuse history. Gastroenterology, 139(1), 36–47.

    Article  PubMed  Google Scholar 

  • Vandenberghe, J., Dupont, P., Van Oudenhove, L., Bormans, G., Demyttenaere, K., Fischler, B., et al. (2007). Regional cerebral blood flow during gastric balloon distention in functional dyspepsia. Gastroenterology, 132(5), 1684–1693.

    Article  PubMed  Google Scholar 

  • Wilder-Smith, C., Schindler, D., Lovblad, K., Redmond, S., & Nirkko, A. (2004). Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut, 53(11), 1595–1601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng, F., Qin, W., Liang, F., Liu, J., Tang, Y., Liu, X., et al. (2011). Abnormal resting brain activity in patients with functional dyspepsia is related to symptom severity. Gastroenterology, 141(2), 499–506.

    Article  PubMed  Google Scholar 

  • Zeng, F., Qin, W., Yang, Y., Zhang, D., Liu, J., Zhou, G., et al. (2013). Regional brain structural abnormality in meal-related functional dyspepsia patients: A voxel-based morphometry study. PloS One, 8(7), e68383.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Gao, Y., Gao, Y., Munsell, B., & Shen, D. (2016). Detecting anatomical landmarks for fast Alzheimer's disease diagnosis. IEEE Transactions on Medical Imaging, 35(12), 2524–2533.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, G., Qin, W., Zeng, F., Liu, P., Yang, X., von Deneen, K. M., et al. (2013a). White-matter microstructural changes in functional dyspepsia: A diffusion tensor imaging study. American Journal of Gastroenterology, 108(2), 260–269.

    Article  PubMed  Google Scholar 

  • Zhou, G., Liu, P., Wang, J., Wen, H., Zhu, M., Zhao, R., et al. (2013b). Fractional amplitude of low-frequency fluctuation changes in functional dyspepsia: A resting-state fMRI study. Magnetic Resonance Imaging, 31(6), 996–1000.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Life Sciences Research Center, School of Life Science and Technology, Xidian University, Xi’an, Shaanxi, 710071, China

    Peng Liu, Geliang Wang, Yanfei Liu & Wei Qin

  2. Engineering Research Center of Molecular and Neuroimaging Ministry of Education, School of Life Science and Technology, Xidian University, Xi’an, 710071, China

    Peng Liu, Geliang Wang, Yanfei Liu & Wei Qin

  3. Acupuncture and Tuina School, Chengdu University of Traditional Chinese Medicine, Chengdu, 610075, China

    Fang Zeng, Yingying Fan & Ying Wei

  4. The Mind Research Network, Albuquerque, NM, 87106, USA

    Vince D. Calhoun

Authors
  1. Peng Liu
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  2. Geliang Wang
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  3. Fang Zeng
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  4. Yanfei Liu
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  5. Yingying Fan
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  6. Ying Wei
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  7. Wei Qin
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  8. Vince D. Calhoun
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Corresponding author

Correspondence to Peng Liu.

Ethics declarations

All research procedures were conducted in accordance with the Declaration of Helsinki, and were approved by the local institutional review board. Verbal and written consent was obtained from each subject before participation, and all methods were carried out in accordance with the approved guidelines.

Funding

This study was supported by the National Natural Science Foundation of China under Grant Nos. 81,471,738, 81,303,060, 81,271,644, 81,471,811 and 61,401,346,National Basic Research Program of China under Grant Nos. 2014CB543203 and 2015CB856403, the Special Fund for the Authors Who win the 100 Top Doctoral Dissertations Award of China No. 2014084, the Education Ministry’s New Century Excellent Talents Supporting Plan, and NIH 1R01EB006841, R01EB005846 and P20GM103472.

Conflict of interest

Peng Liu, Geliang Wang , Fang Zeng , Yanfei Liu, Yingying Fan, Ying Wei, Wei Qin and Vince D. Calhoun declare that they have no conflict of interest.

Additional information

Peng Liu, Geliang Wang, Fang Zeng and Yanfei Liu contributed equally to this paper

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Liu, P., Wang, G., Zeng, F. et al. Abnormal brain structure implicated in patients with functional dyspepsia. Brain Imaging and Behavior 12, 459–466 (2018). https://doi.org/10.1007/s11682-017-9705-z

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  • DOI: https://doi.org/10.1007/s11682-017-9705-z

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