Brain structural changes and neuropsychological impairments in male polydipsic schizophrenia

BMC Psychiatry

Toshifumi Kishimoto²  Kimihiko Kichikawa⁴  Toshiaki Taoka⁴  Naoko Kishimoto²  Koji Okada²  Jun Kosaka³  Kuniaki Kiuchi²  Soichiro Kitamura²  Makoto Inoue¹  Tomohisa Nagashima² 

[1] National Hospital Organization Yamato Mental Medical Center, Yamatokoriyama, Nara, Japan;Department of Psychiatry, Nara Medical University, Kashihara, Nara, Japan;Sakai City Mental Health Center, Sakai, Osaka, Japan;Department of Radiology, Nara Medical University, Kashihara, Nara, Japan

关键词: Brief assessment of cognition in schizophrenia;    Neuropsychological impairment;    MRI;    Volumetry;    Polydipsia;    Schizophrenia;   

Others  :  1124222
DOI  :  10.1186/1471-244X-12-210

 received in 2012-02-16, accepted in 2012-11-21,  发布年份 2012

【 摘 要 】

Background

Polydipsia frequently occurs in schizophrenia patients. The excessive water loading in polydipsia occasionally induces a hyponatremic state and leads to water intoxication. Whether polydipsia in schizophrenic patients correlates with neuropsychological impairments or structural brain changes is not clear and remains controversial.

Methods

Eight polydipsic schizophrenia patients, eight nonpolydipsic schizophrenia patients, and eight healthy controls were recruited. All subjects underwent magnetic resonance imaging (MRI) and neuropsychological testing. Structural abnormalities were analyzed using a voxel-based morphometry (VBM) approach, and patients’ neuropsychological function was assessed using the Brief Assessment of Cognition in Schizophrenia, Japanese version (BACS-J).

Results

No significant differences were found between the two patient groups with respect to the clinical characteristics. Compared with healthy controls, polydipsic patients showed widespread brain volume reduction and neuropsychological impairment. Furthermore, the left insula was significantly reduced in polydipsic patients compared with nonpolydipsic patients. These nonpolydipsic patients performed intermediate to the other two groups in the neuropsychological function test.

Conclusions

It is possible that polydipsia or the secondary hyponatremia might induce left insula volume reduction. Furthermore, this structural brain change may indirectly induce more severe neuropsychological impairments in polydipsic patients. Thus, we suggest that insula abnormalities might contribute to the pathophysiology of polydipsic patients.

【 授权许可】

   
2012 Nagashima et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Perala J, Suvisaari J, Saarni SI, Kuoppasalmi K, Isometsa E, Pirkola S, Partonen T, Tuulio-Henriksson A, Hintikka J, Kieseppa T, et al.: Lifetime prevalence of psychotic and bipolar I disorders in a general population. Arch Gen Psychiatry 2007, 64(1):19-28.
• [2]Reichenberg A: The assessment of neuropsychological functioning in schizophrenia. Dialogues Clin Neurosci 2010, 12(3):383-392.
• [3]Levitt JJ, Bobrow L, Lucia D, Srinivasan P: A selective review of volumetric and morphometric imaging in schizophrenia. Curr Top Behav Neurosci 2010, 4:243-281.
• [4]de Leon J, Verghese C, Tracy JI, Josiassen RC, Simpson GM: Polydipsia and water intoxication in psychiatric patients: a review of the epidemiological literature. Biol Psychiatry 1994, 35(6):408-419.
• [5]Goldman MB: The mechanism of life-threatening water imbalance in schizophrenia and its relationship to the underlying psychiatric illness. Brain Res Rev 2009, 61(2):210-220.
• [6]Kishimoto T, Hirai M, Ohsawa H, Terada M, Matsuoka I, Ikawa G: Manners of arginine vasopressin secretion in schizophrenic patients–with reference to the mechanism of water intoxication. Jpn J Psychiatr Neurol 1989, 43(2):161-169.
• [7]Goldman MB, Luchins DJ, Robertson GL: Mechanisms of altered water metabolism in psychotic patients with polydipsia and hyponatremia. N Engl J Med 1988, 318(7):397-403.
• [8]Elkashef AM, Leadbetter RA, Kirch DG: Structural brain imaging in patients with schizophrenia and polydipsia-hyponatremia syndrome. In Water Balance in Schizophrenia. Edited by Schnur DB, Kirch DG. Washington, DC: Psychiatric Press Inc; 1996:125-136.
• [9]Luchins DJ, Nettles KW, Goldman MB: Anterior medial temporal lobe volumes in polydipsic schizophrenic patients with and without hypo-osmolemia: a pilot study. Biol Psychiatry 1997, 42(9):767-770.
• [10]Goldman MB, Torres IJ, Keedy S, Marlow-O’Connor M, Beenken B, Pilla R: Reduced anterior hippocampal formation volume in hyponatremic schizophrenic patients. Hippocampus 2007, 17(7):554-562.
• [11]Goldman MB, Wang L, Wachi C, Daudi S, Csernansky J, Marlow-O’Connor M, Keedy S, Torres I: Structural pathology underlying neuroendocrine dysfunction in schizophrenia. Behav Brain Res 2011, 218(1):106-113.
• [12]Emsley RA, Spangenberg JJ, Roberts MC, Taljaard FJ, Chalton DO: Disordered water homeostasis and cognitive impairment in schizophrenia. Biol Psychiatry 1993, 34(9):630-633.
• [13]Schnur DB, Smith S: The polydipsia-hyponatremia syndrome and cognitive impairment: Pathophysiological implications. In Water balance in schizophrenia. Edited by Schnur DB, Kirch DG. Washington, DC: American Psychiatric Press Inc; 1996:147-163.
• [14]Schnur DB, Wirkowski E, Reddy R, Decina P, Mukherjee S: Cognitive impairments in schizophrenic patients with hyponatremia. Biol Psychiatry 1993, 33(11–12):836-838.
• [15]Torres IJ, Keedy S, Marlow-O’Connor M, Beenken B, Goldman MB: Neuropsychological impairment in patients with schizophrenia and evidence of hyponatremia and polydipsia. Neuropsychology 2009, 23(3):307-314.
• [16]Ashburner J, Friston KJ: Voxel-based morphometry–the methods. NeuroImage 2000, 11(6 Pt 1):805-821.
• [17]Bhatia T, Garg K, Pogue-Geile M, Nimgaonkar VL, Deshpande SN: Executive functions and cognitive deficits in schizophrenia: comparisons between probands, parents and controls in India. J Postgrad Med 2009, 55(1):3-7.
• [18]Lee SJ, Lee HK, Kweon YS, Lee CT, Lee KU: The impact of executive function on emotion recognition and emotion experience in patients with schizophrenia. Psychiatry Investig 2009, 6(3):156-162.
• [19]Lysaker PH, Bell MD, Bryson G, Kaplan E: Neurocognitive function and insight in schizophrenia: support for an association with impairments in executive function but not with impairments in global function. Acta Psychiatr Scand 1998, 97(4):297-301.
• [20]Mahurin RK, Velligan DI, Hazleton B, Mark Davis J, Eckert S, Miller AL: Trail making test errors and executive function in schizophrenia and depression. Clin Neuropsychol 2006, 20(2):271-288.
• [21]Shinkai T, Ohmori O, Hori H, Nakamura J: Genetic approaches to polydipsia in schizophrenia: a preliminary report of a family study and an association study of an angiotensin-converting enzyme gene polymorphism. Am J Med Genet B Neuropsychiatr Genet 2003, 119B(1):7-12.
• [22]Van Amelsvoort T, Bakshi R, Devaux CB, Schwabe S: Hyponatremia associated with carbamazepine and oxcarbazepine therapy: a review. Epilepsia 1994, 35(1):181-188.
• [23]Kay SR, Opler LA, Lindenmayer JP: The Positive and Negative Syndrome Scale (PANSS): rationale and standardisation. Br J Psychiatry Suppl 1989, 7:59-67.
• [24]Leadbetter RA, Shutty MS Jr, Elkashef AM, Kirch DG, Spraggins T, Cail WS, Wu H, Bilder RM, Lieberman JA, Wyatt RJ: MRI changes during water loading in patients with polydipsia and intermittent hyponatremia. Am J Psychiatry 1999, 156(6):958-960.
• [25]Ashburner J, Friston KJ: Unified segmentation. NeuroImage 2005, 26(3):839-851.
• [26]Keefe RS, Goldberg TE, Harvey PD, Gold JM, Poe MP, Coughenour L: The Brief Assessment of Cognition in Schizophrenia: reliability, sensitivity, and comparison with a standard neurocognitive battery. Schizophr Res 2004, 68(2–3):283-297.
• [27]Kaneda Y, Sumiyoshi T, Keefe R, Ishimoto Y, Numata S, Ohmori T: Brief assessment of cognition in schizophrenia: validation of the Japanese version. Psychiatry Clin Neurosci 2007, 61(6):602-609.
• [28]Wylie KP, Tregellas JR: The role of the insula in schizophrenia. Schizophr Res 2010, 123(2–3):93-104.
• [29]Poirier S, Legris G, Tremblay P, Michea R, Viau-Guay L, Merette C, Bouchard RH, Maziade M, Roy MA: Schizophrenia patients with polydipsia and water intoxication are characterized by greater severity of psychotic illness and a more frequent history of alcohol abuse. Schizophr Res 2010, 118(1–3):285-291.
• [30]Augustine JR: Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996, 22(3):229-244.
• [31]Jones CL, Ward J, Critchley HD: The neuropsychological impact of insular cortex lesions. J Neurol Neurosurg Psychiatry 2010, 81(6):611-618.
• [32]Ture U, Yasargil DC, Al-Mefty O, Yasargil MG: Topographic anatomy of the insular region. J Neurosurg 1999, 90(4):720-733.
• [33]Josiassen RC, Filmyer DM, Geboy AG, Martin DM, Curtis JL, Shaughnessy RA, Salzman A, Orlandi C: Psychomotor deficits associated with hyponatremia: a retrospective analysis. Clin Neuropsychol 2012, 26(1):74-87.
• [34]Renneboog B, Musch W, Vandemergel X, Manto MU, Decaux G: Mild chronic hyponatremia is associated with falls, unsteadiness, and attention deficits. Am J Med 2006, 119(1):71e71-71e78.
• [35]Ragland JD, Yoon J, Minzenberg MJ, Carter CS: Neuroimaging of cognitive disability in schizophrenia: search for a pathophysiological mechanism. Int Rev Psychiatry 2007, 19(4):417-427.
• [36]Weiss AP, Ellis CB, Roffman JL, Stufflebeam S, Hamalainen MS, Duff M, Goff DC, Schacter DL: Aberrant frontoparietal function during recognition memory in schizophrenia: a multimodal neuroimaging investigation. J Neurosci 2009, 29(36):11347-11359.
• [37]Neuner I, Stocker T, Kellermann T, Kircher T, Zilles K, Schneider F, Shah NJ: Wechsler Memory Scale Revised Edition: neural correlates of the visual paired associates subtest adapted for fMRI. Brain Res 2007, 1177:66-78.
• [38]Andreasen NC, Nopoulos P, O’Leary DS, Miller DD, Wassink T, Flaum M: Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol Psychiatry 1999, 46(7):908-920.
• [39]Weiss AP, Dewitt I, Goff D, Ditman T, Heckers S: Anterior and posterior hippocampal volumes in schizophrenia. Schizophr Res 2005, 73(1):103-112.
• [40]Gloor P: The Temporal Lobe and Limbic System. New York: Oxford University Press; 1997.
• [41]Duvernoy HM: The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI. New York: Springer Verlag; 1998.
• [42]Chan WY, Chia MY, Yang GL, Woon PS, Sitoh YY, Collinson SL, Nowinski WL, Sim K: Duration of illness, regional brain morphology and neurocognitive correlates in schizophrenia. Ann Acad Med Singap 2009, 38(5):388-395.
• [43]Puri BK: Brain tissue changes and antipsychotic medication. Expert Rev Neurother 2011, 11(7):943-946.