Skip to main content
Log in

Altered intrinsic brain activity and memory performance improvement in patients with end-stage renal disease during a single dialysis session

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Memory deficits are considered to have a great influence on self-management, dietary restriction and therapeutic regimen for end-stage renal disease (ESRD) patients with dialysis treatment. This study was aim to investigate the spontaneous brain activity and its relationship with memory performance in ESRD patients before dialysis (T1) and after 24 h (T2) during a single dialysis session. 23 ESRD patients and 25 matched healthy controls (HCs) were scanned using functional magnetic resonance imaging (fMRI) at T1, and all patients were also scanned at T2. Amplitude of low-frequency fluctuation (ALFF) and regional homogeneity (ReHo) methods were used to evaluate the spontaneous brain activity between two groups. The Auditory Verbal Learning Test-Huashan version (AVLT-H) was performed to assess memory function. Compared with HCs, ESRD group showed a significant decreases in the immediate recall total score (IR-S), short-term delayed recall score (SR-S), and long-term delayed recall score (LR-S) at T1. IR-S, SR-S, LR-S and recognition score (REC-S) were significantly increased at T2. Compared with HCs at T1, ESRD patients showed that the lower mean ALFF (mALFF) values were mainly located in dorsolateral prefrontal cortex (DLPFC), medial frontal gyrus, and precuneus. Higher ReHo in the bilateral inferior temporal gyrus and left hippocampus and lower ReHo in the right precentral gyrus, anterior cingulate cortex were found at T1 too. The mALFF values of the DLPFC and precuneus were significantly increased during a dialysis session, while no significantly difference of ReHo region was found. Furthermore, the increased mALFF values of the DLPFC were significantly positively correlated with the improvement in the IR-S. Our results indicated that increased regional spontaneous activity of the DLPFC may reflect memory performance improvement after a single dialysis treatment, which may provide insight into the effect of hemodialysis on spontaneous brain function during a single dialysis session.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Birkenhager, W. H., & Staessen, J. A. (2006). Antihypertensives for prevention of Alzheimer’s disease. Lancet Neurology, 5(6), 466–468.

    Article  Google Scholar 

  • Biswal, B. B. (2012). Resting state fMRI: a personal history. Neuroimage, 62(2), 938–944.

    Article  Google Scholar 

  • Bossola, M., Di Stasio, E., Antocicco, M., Silvestri, P., & Tazza, L. (2013). Variables associated with time of recovery after hemodialysis. Journal of Nephrology, 26(4), 787–792.

    Article  CAS  Google Scholar 

  • Bossola, M., & Tazza, L. (2016). Postdialysis fatigue: a frequent and debilitating symptom. Seminars in Dialysis, 29(3), 222–227.

    Article  Google Scholar 

  • Brkovic, T., Burilovic, E., & Puljak, L. (2016). Prevalence and severity of pain in adult end-stage renal disease patients on chronic intermittent hemodialysis: a systematic review. Patient Prefer Adherence, 10, 1131–1150.

    PubMed  PubMed Central  Google Scholar 

  • Bugnicourt, J. M., Godefroy, O., Chillon, J. M., Choukroun, G., & Massy, Z. A. (2013). Cognitive disorders and dementia in CKD: the neglected kidney-brain axis. Journal of the American Society of Nephrology, 24(3), 353–363.

    Article  CAS  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198.

    Article  CAS  Google Scholar 

  • Campbell, N. L., Boustani, M. A., Skopelja, E. N., Gao, S., Unverzagt, F. W., & Murray, M. D. (2012). Medication adherence in older adults with cognitive impairment: a systematic evidence-based review. The American Journal of Geriatric Pharmacotherapy, 10(3), 165–177.

    Article  Google Scholar 

  • Chao-Gan, Y., & Yu-Feng, Z. (2010). DPARSF: a matlab toolbox for “pipeline” data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 413.

  • Cicchetti, D., & Posner, M. I. (2005). Cognitive and affective neuroscience and developmental psychopathology. Development and Psychopathology, 17(3), 569–575.

    PubMed  Google Scholar 

  • Elias, M. F., Dore, G. A., & Davey, A. (2013). Kidney disease and cognitive function. Contributions to Nephrology, 17942–57.

  • Falleti, M. G., Maruff, P., Collie, A., & Darby, D. G. (2006). Practice effects associated with the repeated assessment of cognitive function using the CogState battery at 10-minute, one week and one month test-retest intervals. Journal of Clinical and Experimental Neuropsychology, 28(7), 1095–1112.

    Article  Google Scholar 

  • Fried, P. J., Rd, R. R., Moss, M. B., Valerocabré, A., & Pascualleone, A. (2014). Causal evidence supporting functional dissociation of verbal and spatial working memory in the human dorsolateral prefrontal cortex. European Journal of Neuroscience, 39(11), 1973–1981.

    Article  Google Scholar 

  • Griva, K., Newman, S. P., Harrison, M. J., Hankins, M., Davenport, A., Hansraj, S. et al (2003). Acute neuropsychological changes in hemodialysis and peritoneal dialysis patients. Health Psychology, 22(6), 570–578.

    Article  Google Scholar 

  • Keightley, M. L., Saluja, R. S., Chen, J. K., Gagnon, I., Leonard, G., Petrides, M. et al (2014). A functional magnetic resonance imaging study of working memory in youth after sports-related concussion: is it still working? Journal of Neurotrauma, 31(5), 437–451.

    Article  Google Scholar 

  • Kielstein, H., Suntharalingam, M., Perthel, R., Song, R., Schneider, S. M., Martens-Lobenhoffer, J. et al (2015). Role of the endogenous nitric oxide inhibitor asymmetric dimethylarginine (ADMA) and brain-derived neurotrophic factor (BDNF) in depression and behavioural changes: clinical and preclinical data in chronic kidney disease. Nephrology, Dialysis, Transplantation, 30(10), 1699–1705.

    Article  CAS  Google Scholar 

  • Kielstein, J. T., & Bernstein, H. G. (2014). The reversible part of cognitive impairment in chronic kidney disease: can mice help men break the TEMPOLimit? Nephrology, Dialysis, Transplantation, 29(3), 476–478.

    Article  Google Scholar 

  • Kielstein, J. T., Donnerstag, F., Gasper, S., Menne, J., Kielstein, A., Martens-Lobenhoffer, J. et al (2006). ADMA increases arterial stiffness and decreases cerebral blood flow in humans. Stroke, 37(8), 2024–2029.

    Article  Google Scholar 

  • Kurella, M., Chertow, G. M., Fried, L. F., Cummings, S. R., Harris, T., Simonsick, E. et al (2005). Chronic kidney disease and cognitive impairment in the elderly: the health, aging, and body composition study. Journal of the American Society of Nephrology, 16(7), 2127–2133.

    Article  Google Scholar 

  • Kurella, M., Chertow, G. M., Luan, J., & Yaffe, K. (2004). Cognitive impairment in chronic kidney disease. Journal of the American Geriatrics Society, 52(11), 1863–1869.

    Article  Google Scholar 

  • Latimer, C. S., Brewer, L. D., Searcy, J. L., Chen, K. C., Popovic, J., Kraner, S. D. et al (2014). Vitamin D prevents cognitive decline and enhances hippocampal synaptic function in aging rats. Proceedings of the National Academy of Sciences of the United States of America, 111(41), E4359–E4366.

    Article  CAS  Google Scholar 

  • Lee, S. T., Chu, K., Park, J. E., Jung, K. H., Jeon, D., Lim, J. Y. et al (2012). Erythropoietin improves memory function with reducing endothelial dysfunction and amyloid-beta burden in Alzheimer’s disease models. Journal of Neurochemistry, 120(1), 115–124.

    Article  CAS  Google Scholar 

  • Li, C., Su, H. H., Qiu, Y. W., Lv, X. F., Shen, S., Zhan, W. F. et al (2014). Regional homogeneity changes in hemodialysis patients with end stage renal disease: in vivo resting-state functional MRI study. PLoS One, 9(2), e87114.

  • Li, F., Lui, S., Yao, L., Hu, J., Lv, P., Huang, X. et al (2016). Longitudinal changes in resting-state cerebral activity in patients with first-episode Schizophrenia: a 1-year follow-up functional MR Imaging Study. Radiology, 279(3), 867–875.

    Article  Google Scholar 

  • Liang, X., Wen, J., Ni, L., Zhong, J., Qi, R., Zhang, L. J. et al (2013). Altered pattern of spontaneous brain activity in the patients with end-stage renal disease: a resting-state functional MRI study with regional homogeneity analysis. PLoS One, 8(8), e71507.

  • Lin, B. M., Curhan, S. G., Wang, M., Eavey, R., Stankovic, K. M., & Curhan, G. C. (2016). Hypertension, diuretic use, and risk of hearing loss. The American Journal of Medicine, 129(4), 416–422.

    Article  CAS  Google Scholar 

  • Luo, S., Qi, R. F., Wen, J. Q., Zhong, J. H., Kong, X., Liang, X. et al (2016). Abnormal intrinsic brain activity patterns in patients with end-stage renal disease undergoing peritoneal dialysis: a resting-state functional MR imaging study. Radiology, 278(1), 181–189.

    Article  Google Scholar 

  • Murray, A. M., Bell, E. J., Tupper, D. E., Davey, C. S., Pederson, S. L., Amiot, E. M. et al (2016). The brain in kidney disease (BRINK) cohort study: design and baseline cognitive function. American Journal of Kidney Diseases, 67(4), 593–600.

    Article  Google Scholar 

  • Murray, A. M., Pederson, S. L., Tupper, D. E., Hochhalter, A. K., Miller, W. A., Li, Q. et al (2007). Acute variation in cognitive function in hemodialysis patients: a cohort study with repeated measures. American Journal of Kidney Diseases, 50(2), 270–278.

    Article  Google Scholar 

  • Ni, L., Wen, J., Zhang, L. J., Zhu, T., Qi, R., Xu, Q. et al (2014). Aberrant default-mode functional connectivity in patients with end-stage renal disease: a resting-state functional MR imaging study. Radiology, 271(2), 543–552.

    Article  Google Scholar 

  • Pliskin, N. H., Yurk, H. M., Ho, L. T., & Umans, J. G. (1996). Neurocognitive function in chronic hemodialysis patients. Kidney International, 49(5), 1435–1440.

    Article  CAS  Google Scholar 

  • Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage, 84320–341.

  • Qiu, Y., Lv, X., Su, H., Jiang, G., Li, C., & Tian, J. (2014). Structural and functional brain alterations in end stage renal disease patients on routine hemodialysis: a voxel-based morphometry and resting state functional connectivity study. PLoS One, 9(5), e98346.

  • Richardson, M. P., Strange, B. A., Thompson, P. J., Baxendale, S. A., Duncan, J. S., & Dolan, R. J. (2004). Pre-operative verbal memory fMRI predicts post-operative memory decline after left temporal lobe resection. Brain, 127(Pt 11), 2419–2426.

    Article  Google Scholar 

  • Schaechter, J. D., Kraft, E., Hilliard, T. S., Dijkhuizen, R. M., Benner, T., Finklestein, S. P. et al (2002). Motor recovery and cortical reorganization after constraint-induced movement therapy in stroke patients: a preliminary study. Neurorehabil Neural Repair, 16(4), 326–338.

    Article  Google Scholar 

  • Schneider, S., Malecki, A.-K., Boenisch, O., Schönfeld, R., & Kielstein, J. T. (2012) Cognitive function at 2443 µmol/l creatinine. BMC Nephrology. 86.

  • Schneider, S. M., Malecki, A. K., Müller, K., Schönfeld, R., Girndt, M., Mohr, P. et al (2015). Effect of a single dialysis session on cognitive function in CKD5D patients: a prospective clinical study. Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association - European Renal Association, 30(9), 1551–1559.

    Article  CAS  Google Scholar 

  • Scribner, B. H., Buri, R., Caner, J. E., Hegstrom, R., & Burnell, J. M. (1960). The treatment of chronic uremia by means of intermittent hemodialysis: a preliminary report. Transactions - American Society for Artificial Internal Organs, 6114 – 122.

  • Shen, J., Zhang, G., Yao, L., & Zhao, X. (2015). Real-time fMRI training-induced changes in regional connectivity mediating verbal working memory behavioral performance. Neuroscience, 289144–152.

  • Song, S. H., Kim, I. J., Kim, S. J., Kwak, I. S., & Kim, Y. K. (2008). Cerebral glucose metabolism abnormalities in patients with major depressive symptoms in pre-dialytic chronic kidney disease: statistical parametric mapping analysis of F-18-FDG PET, a preliminary study. Psychiatry and Clinical Neurosciences, 62(5), 554–561.

    Article  Google Scholar 

  • Song, X. W., Dong, Z. Y., Long, X. Y., Li, S. F., Zuo, X. N., & Zhu, C. Z. et al (2011). REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One, 6(9), e25031.

  • van Dijk, P. C., Zwinderman, A. H., Dekker, F. W., Schon, S., Stel, V. S., Finne, P., et al. (2007). Effect of general population mortality on the north-south mortality gradient in patients on replacement therapy in Europe. Kidney International, 71(1), 53–59.

    Article  Google Scholar 

  • Wagrowska-Danilewicz, M., & Danilewicz, M. (2007). Current position of electron microscopy in the diagnosis of glomerular diseases. Polish Journal of Pathology, 58(2), 87–92.

    PubMed  Google Scholar 

  • Williams, M. A., Sklar, A. H., Burright, R. G., & Donovick, P. J. (2004). Temporal effects of dialysis on cognitive functioning in patients with ESRD. American Journal of Kidney Diseases, 43(4), 705–711.

    Article  Google Scholar 

  • Wolk, D. A., & Dickerson, B. C. (2011a). Fractionating verbal episodic memory in Alzheimer’s disease. Neuroimage, 54(2), 1530–1539.

  • Wolk, D. A., & Dickerson, B. C. (2011b). Alzheimer’s disease Neuroimaging. Fractionating verbal episodic memory in Alzheimers disease. Neuroimage, 54(2), 1530–1539. I.

  • Zang, Y., Jiang, T., Lu, Y., He, Y., & Tian, L. (2004). Regional homogeneity approach to fMRI data analysis. Neuroimage, 22(1), 394–400.

    Article  Google Scholar 

  • Zang, Y. F., He, Y., Zhu, C. Z., Cao, Q. J., Sui, M. Q., Liang, M., et al. (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain & Development, 29(2), 83–91.

    Article  Google Scholar 

  • Zhang, L. J., Wen, J., Liang, X., Qi, R., Schoepf, U. J., Wichmann, J. L., et al. (2016). Brain default mode network changes after renal transplantation: a diffusion-tensor imaging and resting-state functional MR imaging study. Radiology, 278(2), 485–495.

    Article  Google Scholar 

  • Zhao, Q., Guo, Q., Liang, X., Chen, M., Zhou, Y., Ding, D., et al. (2015). Auditory verbal learning test is superior to rey-osterrieth complex figure memory for predicting mild cognitive impairment to Alzheimer’s disease. Current Alzheimer Research, 12(6), 520–526.

  • Zhao, Q., Lv, Y., Zhou, Y., Hong, Z., & Guo, Q. (2012). Short-term delayed recall of auditory verbal learning test is equivalent to long-term delayed recall for identifying amnestic mild cognitive impairment. PLoS One, 7(12), e51157.

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (Grant No. 81371530, 81471737) and the Research Funds of the First Affiliated Hospital of Xi’an Jiaotong University, College of Medicine (Grant No. 2014YK3).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ji-xin Liu or Ming Zhang.

Ethics declarations

Conflict of interest

Peng Li, Dun Ding, Xue-ying Ma, Hua-wen Zhang, Ji-xin Liu, and Ming Zhang declares that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Ethical statements

Informed consent was obtained from all individual participants for being included in the study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 525 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, P., Ding, D., Ma, Xy. et al. Altered intrinsic brain activity and memory performance improvement in patients with end-stage renal disease during a single dialysis session. Brain Imaging and Behavior 12, 1640–1649 (2018). https://doi.org/10.1007/s11682-018-9828-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-9828-x

Keywords

Navigation