Evaluation of Brain Activity Using Near-infrared Spectroscopy in Inflammatory Bowel Disease Patients

Tatsuo Fujiwara, Soichi Kono, Kyoko Katakura, Kazumichi Abe, Atsushi Takahashi, Naohiko Gunji, Aki Yokokawa, Kazumasa Kawashima, Rieko Suzuki, Akira Wada, Itaru Miura, Hirooki Yabe, Hiromasa Ohira, Tatsuo Fujiwara, Soichi Kono, Kyoko Katakura, Kazumichi Abe, Atsushi Takahashi, Naohiko Gunji, Aki Yokokawa, Kazumasa Kawashima, Rieko Suzuki, Akira Wada, Itaru Miura, Hirooki Yabe, Hiromasa Ohira

Abstract

Depression is implicated as a risk factor for the recurrence of inflammatory bowel disease (IBD). Near-infrared spectroscopy (NIRS) and brain-derived neurotrophic factor (BDNF) are useful tools for evaluation of brain activity and a depressive state, respectively. The aim of this study was to clarify the association between brain activity or depressive symptoms and IBD using NIRS and BDNF. This study included 36 ulcerative colitis (UC) patients, 32 Crohn's disease (CD) patients, and 17 healthy controls (HC). Center for Epidemiologic Studies Depression Scale (CES-D) scores were determined, NIRS was performed, and serum BDNF levels were measured in all subjects. NIRS showed that the mean oxygenated hemoglobin concentration was significantly lower in the frontal lobe in the UC group than in the HC group (HC 167 ± 106 vs. UC 83.1 ± 85.3, p < 0.05). No significant difference was seen between the HC and CD groups. There were also no significant differences in CED-D scores and BDNF levels among the groups. Changes in the NIRS values of the UC group may indicate decreased brain activity and a fundamental difference between UC and CD, which are often lumped together as two types of IBD.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Comparisons of CES-D scores among the HC, UC, and CD groups; HC, active UC, and UC in remission groups; and HC, active CD, and CD in remission groups. (a) Scores in the UC and CD groups do not differ significantly from HC group scores. (b) Scores in the active UC group are significantly higher compared with the HC group. (c) Scores in the active CD and remission CD groups do not differ significantly from HC group scores.
Figure 2
Figure 2
Measurement points of 52 channels for near-infrared spectroscopy. The measuring positions of the device are superimposed on the 3D-reconstructed cerebral surface, based on magnetic resonance imaging, in the right temporal (a), frontal (b), and left temporal (c) brain regions. The 52 measuring positions are labeled channel (ch) 1 to 52, from the right posterior to the left posterior.
Figure 3
Figure 3
(a) Comparison of changes in mean oxy-Hb concentration in the HC (green) and UC (red) groups. (b) Topographic map of the differences in mean oxy-Hb concentration changes between the UC and HC groups. THE mean oxy-Hb concentration is significantly decreased in the UC group (p < 0.05 in channels 4, 8, 14, 15, 17, 18, 25 to 29, 37, 46, 47, 49, and 50 (yellow) and p < 0.01 in channels 9, 19, 35, 36, 38, 39, 45, and 48 (red)).
Figure 4
Figure 4
(a) Comparison of changes in mean oxy-Hb concentrations in the HC (green) and CD (blue) groups. (b) Topographic map of the differences in mean oxy-Hb concentration changes between the CD and HC groups. No significant differences are noted in any channel.
Figure 5
Figure 5
(a) Comparison of changes in the mean oxy-Hb concentration in the HC (green) and active UC (purple) groups. The mean oxy-Hb concentration is significantly decreased in the active UC patients (p < 0.05 in channels 3, 9, 24, 35, 36, 38, 39, 46 and 47 (yellow) and p < 0.01 in channel 49 (red)). (b) Comparison of changes in the mean oxy-Hb concentration in the HC (green) and UC in remission (red) groups. The mean oxy-Hb concentration is significantly decreased in the patients with UC in remission (p < 0.05 in channels 8, 9, 14, 15, 18, 23, 28, 29, 35, 37, 39, 46 to 48, and 50 (yellow) and p < 0.01 in channels 19, 36, 38, and 45 (red)).
Figure 6
Figure 6
Time-dependent changes in oxy-hemoglobin (oxy-Hb) concentration in an NIRS signal waveform (sample). The average waveforms of time-dependent changes in mean oxy-Hb concentrations in the channels. (1) 10-s pre-task baseline period (2) 60-s activation period (3) in the 55-s post-task baseline period.

References

    1. Porcelli P, Zaka S, Tarantino S, Sisto G. [Body Image Index in the Rorschach test in ulcerative proctocolitis] Minerva Psichiatr. 1993;34:25–28.
    1. Calvet X, et al. Remission on thiopurinic immunomodulators normalizes quality of life and psychological status in patients with Crohn’s disease. Inflamm Bowel Dis. 2006;12:692–696. doi: 10.1097/00054725-200608000-00004.
    1. Levenstein S, et al. Psychological stress and disease activity in ulcerative colitis: a multidimensional cross-sectional study. Am J Gastroenterol. 1994;89:1219–1225.
    1. Maunder RG, et al. Psychobiological subtypes of ulcerative colitis: pANCA status moderates the relationship between disease activity and psychological distress. Am J Gastroenterol. 2006;101:2546–2551. doi: 10.1111/j.1572-0241.2006.00798.x.
    1. Porcelli P, Leoci C, Guerra V. A prospective study of the relationship between disease activity and psychologic distress in patients with inflammatory bowel disease. Scand J Gastroenterol. 1996;31:792–796. doi: 10.3109/00365529609010354.
    1. Mardini HE, Kip KE, Wilson JW. Crohn’s disease: a two-year prospective study of the association between psychological distress and disease activity. Dig Dis Sci. 2004;49:492–497. doi: 10.1023/B:.
    1. Mikocka-Walus AA, et al. Does psychological status influence clinical outcomes in patients with inflammatory bowel disease (IBD) and other chronic gastroenterological diseases: an observational cohort prospective study. Biopsychosoc Med. 2008;2:11. doi: 10.1186/1751-0759-2-11.
    1. Mittermaier C, et al. Impact of depressive mood on relapse in patients with inflammatory bowel disease: a prospective 18-month follow-up study. Psychosom Med. 2004;66:79–84. doi: 10.1097/01.PSY.0000106907.24881.F2.
    1. Klumpp H, Deldin P. Review of brain functioning in depression for semantic processing and verbal fluency. Int J Psychophysiol. 2010;75:77–85. doi: 10.1016/j.ijpsycho.2009.10.003.
    1. Suto T, Fukuda M, Ito M, Uehara T, Mikuni M. Multichannel near-infrared spectroscopy in depression and schizophrenia: cognitive brain activation study. Biol Psychiatry. 2004;55:501–511. doi: 10.1016/j.biopsych.2003.09.008.
    1. Takizawa R, et al. Reduced frontopolar activation during verbal fluency task in schizophrenia: a multi-channel near-infrared spectroscopy study. Schizophr Res. 2008;99:250–262. doi: 10.1016/j.schres.2007.10.025.
    1. Irani F, Platek SM, Bunce S, Ruocco AC, Chute D. Functional near infrared spectroscopy (fNIRS): an emerging neuroimaging technology with important applications for the study of brain disorders. Clin Neuropsychol. 2007;21:9–37. doi: 10.1080/13854040600910018.
    1. Dwivedi Y, et al. Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch Gen Psychiatry. 2003;60:804–815. doi: 10.1001/archpsyc.60.8.804.
    1. Brunoni AR, Lopes M, Fregni F. A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int J Neuropsychopharmacol. 2008;11:1169–1180. doi: 10.1017/S1461145708009309.
    1. Bocchio-Chiavetto L, et al. Serum and plasma BDNF levels in major depression: a replication study and meta-analyses. World J Biol Psychiatry. 2010;11:763–773. doi: 10.3109/15622971003611319.
    1. Sen S, Duman R, Sanacora G. Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol Psychiatry. 2008;64:527–532. doi: 10.1016/j.biopsych.2008.05.005.
    1. Mitoma M, et al. Stress at work alters serum brain-derived neurotrophic factor (BDNF) levels and plasma 3-methoxy-4-hydroxyphenylglycol (MHPG) levels in healthy volunteers: BDNF and MHPG as possible biological markers of mental stress? Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:679–685. doi: 10.1016/j.pnpbp.2007.11.011.
    1. Matsuo K, Kato T, Fukuda M, Kato N. Alteration of hemoglobin oxygenation in the frontal region in elderly depressed patients as measured by near-infrared spectroscopy. J Neuropsychiatry Clin Neurosci. 2000;12:465–471. doi: 10.1176/jnp.12.4.465.
    1. Matsuo K, Kato N, Kato T. Decreased cerebral haemodynamic response to cognitive and physiological tasks in mood disorders as shown by near-infrared spectroscopy. Psychol Med. 2002;32:1029–1037. doi: 10.1017/S0033291702005974.
    1. Abe K, et al. Reduced frontal activation during verbal fluency task in chronic hepatitis C patients with interferon-based therapy as measured by near-infrared spectroscopy. Hepatol Res. 2017;47:E55–E63. doi: 10.1111/hepr.12721.
    1. Takahashi A, et al. Reduced brain activity in female patients with non-alcoholic fatty liver disease as measured by near-infrared spectroscopy. PLoS One. 2017;12:e0174169. doi: 10.1371/journal.pone.0174169.
    1. Castaneda AE, Tuulio-Henriksson A, Marttunen M, Suvisaari J, Lonnqvist J. A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J Affect Disord. 2008;106:1–27. doi: 10.1016/j.jad.2007.06.006.
    1. Gualtieri CT, Johnson LG, Benedict KB. Neurocognition in depression: patients on and off medication versus healthy comparison subjects. J Neuropsychiatry Clin Neurosci. 2006;18:217–225. doi: 10.1176/jnp.2006.18.2.217.
    1. Castaneda AE, et al. Cognitive functioning in a population-based sample of young adults with a history of non-psychotic unipolar depressive disorders without psychiatric comorbidity. J Affect Disord. 2008;110:36–45. doi: 10.1016/j.jad.2007.12.239.
    1. Gunther T, Holtkamp K, Jolles J, Herpertz-Dahlmann B, Konrad K. Verbal memory and aspects of attentional control in children and adolescents with anxiety disorders or depressive disorders. J Affect Disord. 2004;82:265–269. doi: 10.1016/j.jad.2003.11.004.
    1. Thaler JP, et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest. 2012;122:153–162. doi: 10.1172/JCI59660.
    1. Daly M. The relationship of C-reactive protein to obesity-related depressive symptoms: a longitudinal study. Obesity (Silver Spring) 2013;21:248–250. doi: 10.1002/oby.20051.
    1. Paulley JW. Psychological management of Crohn’s disease. Practitioner. 1974;213:59–64.
    1. Mawdsley JE, Rampton DS. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut. 2005;54:1481–1491. doi: 10.1136/gut.2005.064261.
    1. Suda M, et al. Decreased cortical reactivity underlies subjective daytime light sleepiness in healthy subjects: a multichannel near-infrared spectroscopy study. Neurosci Res. 2008;60:319–326. doi: 10.1016/j.neures.2007.12.001.
    1. Kakimoto Y, et al. Intrasubject reproducibility of prefrontal cortex activities during a verbal fluency task over two repeated sessions using multi-channel near-infrared spectroscopy. Psychiatry Clin Neurosci. 2009;63:491–499. doi: 10.1111/j.1440-1819.2009.01988.x.
    1. Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med. 1987;317:1625–1629. doi: 10.1056/NEJM198712243172603.
    1. Best WR, Becktel JM, Singleton JW. Rederived values of the eight coefficients of the Crohn’s Disease Activity Index (CDAI) Gastroenterology. 1979;77:843–846.
    1. Weissman MM, Sholomskas D, Pottenger M, Prusoff BA, Locke BZ. Assessing depressive symptoms in five psychiatric populations: a validation study. Am J Epidemiol. 1977;106:203–214. doi: 10.1093/oxfordjournals.aje.a112455.
    1. Tsuzuki D, et al. Virtual spatial registration of stand-alone fNIRS data to MNI space. Neuroimage. 2007;34:1506–1518. doi: 10.1016/j.neuroimage.2006.10.043.
    1. Okamoto M, et al. Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. Neuroimage. 2004;21:99–111. doi: 10.1016/j.neuroimage.2003.08.026.

Source: PubMed

3
订阅