Korean Journal of Biological Psychiatry (생물정신의학)

The Korean Society of Biological Psychiatry (대한생물정신의학회)
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Effects of the Combination Herbal Extract on Working Memory and White Matter Integrity in Healthy Individuals with Subjective Memory Complaints : A Randomized, Double-Blind, Placebo-Controlled Clinical Trial

  • Kwon, Oran (Ewha Brain Institute, Ewha Womans University) ;
  • Lee, Sunho (Ewha Brain Institute, Ewha Womans University) ;
  • Ban, Soonhyun (Ewha Brain Institute, Ewha Womans University) ;
  • Im, Jooyeon J. (Ewha Brain Institute, Ewha Womans University) ;
  • Lee, Doo Suk (School of Biological Sciences, Seoul National University) ;
  • Lee, Eun Hee (Green Cross Laboratories) ;
  • Kim, Joohee (Department of Nutritional Science and Food Management, College of Health Sciences, Ewha Womans University) ;
  • Lim, Soo Mee (Ewha Brain Institute, Ewha Womans University) ;
  • Lee, Sang Gon (Green Cross Laboratories) ;
  • Kang, Ilhyang (Ewha Brain Institute, Ewha Womans University) ;
  • Kim, Kyung-Hee (Division of Cardiology, Department of Internal Medicine, Sejong General Hospital) ;
  • Yoon, Sujung (Ewha Brain Institute, Ewha Womans University) ;
  • Lee, Sun Hea (Ewha Brain Institute, Ewha Womans University)
  • Received : 2015.02.23
  • Accepted : 2015.02.26
  • Published : 2015.05.31
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Abstract

Objectives The combination extract of four kinds of herbs, Gastrodia elata, Liriope platyphylla, Dimocarpus longan, and Salvia miltiorrhiza, has shown to have memory improving effects in mice. The aim of this study was to investigate the efficacy and safety of the herbal mixture for improving working memory as well as microstructural changes in white matter integrity in individuals with subjective memory complaints. Methods Seventy-five individuals with subjective memory complaints were assigned to receive either placebo (n = 15) or herbal mixture (low-dose group, n = 30 and high-dose group, n = 30) supplementation in an 8-week, randomized, double-blind, placebo-controlled clinical trial. Changes in working memory performance and fractional anisotropy (FA) values reflecting white matter integrity from baseline to 8-week endpoint were assessed. Results The herbal mixture group showed an increase in working memory performance compared to the placebo group (p for interaction = 0.001). In addition, the herbal mixture group showed an increase in FA values in the temporo-parietal regions (corrected p < 0.05), which are crucially involved in working memory function and are among the most affected regions in patients with cognitive impairments. Conclusions Findings from this study indicate that the herbal mixture may be a promising therapeutic option for individuals with subjective memory complaints.

Keywords

References

  1. Stewart R. Subjective cognitive impairment. Curr Opin Psychiatry 2012;25:445-450. https://doi.org/10.1097/YCO.0b013e3283586fd8
  2. von Gunten A, Giannakopoulos P, Duc R. Cognitive and demographic determinants of dementia in depressed patients with subjective memory complaints. Eur Neurol 2005;54:154-158. https://doi.org/10.1159/000090104
  3. Waldorff FB, Siersma V, Vogel A, Waldemar G. Subjective memory complaints in general practice predicts future dementia: a 4-year follow-up study. Int J Geriatr Psychiatry 2012;27:1180-1188. https://doi.org/10.1002/gps.3765
  4. Reid LM, Maclullich AM. Subjective memory complaints and cognitive impairment in older people. Dement Geriatr Cogn Disord 2006; 22:471-485. https://doi.org/10.1159/000096295
  5. Schofield PW, Marder K, Dooneief G, Jacobs DM, Sano M, Stern Y. Association of subjective memory complaints with subsequent cognitive decline in community-dwelling elderly individuals with baseline cognitive impairment. Am J Psychiatry 1997;154:609-615. https://doi.org/10.1176/ajp.154.5.609
  6. Bassel C, Rourke SB, Halman MH, Smith ML. Working memory performance predicts subjective cognitive complaints in HIV infection. Neuropsychology 2002;16:400-410. https://doi.org/10.1037/0894-4105.16.3.400
  7. Gray JR, Chabris CF, Braver TS. Neural mechanisms of general fluid intelligence. Nat Neurosci 2003;6:316-322. https://doi.org/10.1038/nn1014
  8. Johansson B, Tornmalm M. Working memory training for patients with acquired brain injury: effects in daily life. Scand J Occup Ther 2012;19:176-183. https://doi.org/10.3109/11038128.2011.603352
  9. Westerberg H, Jacobaeus H, Hirvikoski T, Clevberger P, Ostensson ML, Bartfai A, et al. Computerized working memory training after stroke--a pilot study. Brain Inj 2007;21:21-29. https://doi.org/10.1080/02699050601148726
  10. Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, et al. Temporal dynamics of brain activation during a working memory task. Nature 1997;386:604-608. https://doi.org/10.1038/386604a0
  11. Laroche S, Davis S, Jay TM. Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus 2000;10:438-446. https://doi.org/10.1002/1098-1063(2000)10:4<438::AID-HIPO10>3.0.CO;2-3
  12. Serby MJ, Yhap C, Landron EY. A study of herbal remedies for memory complaints. J Neuropsychiatry Clin Neurosci 2010;22:345-347. https://doi.org/10.1176/jnp.2010.22.3.345
  13. Lee DS, Choi J, Kim SH, Kim S. Ameliorating effects of HX106N, a water-soluble botanical formulation, on A${\beta}$25-35-induced memory impairment and oxidative stress in mice. Biol Pharm Bull 2014;37: 954-960. https://doi.org/10.1248/bpb.b13-00906
  14. Choi SI, Go J, Kim JE, Lee YJ, Kwak MH, Jung YJ, et al. Precautionary effects of Red Liriope platyphylla on NGF secretion and $A{\beta}42$ deposition under the preclinical stage of Alzheimer's disease in Tg2576 mice. Lab Anim Res 2013;29:212-220. https://doi.org/10.5625/lar.2013.29.4.212
  15. Lee YK, Kim JE, Nam SH, Goo JS, Choi SI, Choi YH, et al. Differential regulation of the biosynthesis of glucose transporters by the PI3-K and MAPK pathways of insulin signaling by treatment with novel compounds from Liriope platyphylla. Int J Mol Med 2011;27: 319-327.
  16. Lee YW, Kim DH, Jeon SJ, Park SJ, Kim JM, Jung JM, et al. Neuroprotective effects of salvianolic acid B on an $A{\beta}25-35$ peptide-induced mouse model of Alzheimer's disease. Eur J Pharmacol 2013; 704:70-77. https://doi.org/10.1016/j.ejphar.2013.02.015
  17. Lin AM, Wu LY, Hung KC, Huang HJ, Lei YP, Lu WC, et al. Neuroprotective effects of longan (Dimocarpus longan Lour.) flower water extract on MPP+-induced neurotoxicity in rat brain. J Agric Food Chem 2012;60:9188-9194. https://doi.org/10.1021/jf302792t
  18. Tsai CF, Huang CL, Lin YL, Lee YC, Yang YC, Huang NK. The neuroprotective effects of an extract of Gastrodia elata. J Ethnopharmacol 2011;138:119-125. https://doi.org/10.1016/j.jep.2011.08.064
  19. Tsai YC, Chiang SY, El-Shazly M, Wu CC, Beerhues L, Lai WC, et al. The oestrogenic and anti-platelet activities of dihydrobenzofuroisocoumarins and homoisoflavonoids from Liriope platyphylla roots. Food Chem 2013;140:305-314. https://doi.org/10.1016/j.foodchem.2013.02.069
  20. Ho SC, Hwang LS, Shen YJ, Lin CC. Suppressive effect of a proanthocyanidin-rich extract from longan (Dimocarpus longan Lour.) flowers on nitric oxide production in LPS-stimulated macrophage cells. J Agric Food Chem 2007;55:10664-10670. https://doi.org/10.1021/jf0721186
  21. Yu SJ, Kim JR, Lee CK, Han JE, Lee JH, Kim HS, et al. Gastrodia elata blume and an active component, p-hydroxybenzyl alcohol reduce focal ischemic brain injury through antioxidant related gene expressions. Biol Pharm Bull 2005;28:1016-1020. https://doi.org/10.1248/bpb.28.1016
  22. Bartzokis G, Beckson M, Lu PH, Nuechterlein KH, Edwards N, Mintz J. Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. Arch Gen Psychiatry 2001; 58:461-465. https://doi.org/10.1001/archpsyc.58.5.461
  23. Kane MJ, Engle RW. The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychon Bull Rev 2002;9:637-671. https://doi.org/10.3758/BF03196323
  24. Choi SH, Na DL, Lee BH, Halm D, Jeong JH, Jeong Y, et al. The validity of the Korean version of Global Deter iorat ion Scale. J Korean Neurol Assoc 2002;20:612-617.
  25. Roth M, Tym E, Mountjoy CQ, Huppert FA, Hendrie H, Verma S, et al. CAMDEX. A standardised instrument for the diagnosis of mental disorder in the elderly with special reference to the early detection of dementia. Br J Psychiatry 1986;149:698-709. https://doi.org/10.1192/bjp.149.6.698
  26. Zandi T. Relationship between subjective memory complaints, objective memory performance, and depression among older adults. Am J Alzheimers Dis Other Demen 2004;19:353-360. https://doi.org/10.1177/153331750401900610
  27. Choi SH, Na DL, Lee BH, Hahm D, Jeong JH, Yoon SJ, et al. Dementia Research Group. Estimating the validity of the Korean version of Expanded Clinical Dementia Rating (CDR) scale. J Korean Neurol Assoc 2001;19:585-591.
  28. Reay JL, Scholey AB, Kennedy DO. Panax ginseng (G115) improves aspects of working memory performance and subjective ratings of calmness in healthy young adults. Hum Psychopharmacol 2010;25: 462-471. https://doi.org/10.1002/hup.1138
  29. Dumville JC, Torgerson DJ, Hewitt CE. Reporting attrition in randomised controlled trials. BMJ 2006;332:969-971. https://doi.org/10.1136/bmj.332.7547.969
  30. Ministry of Food and Drug Safety [homepage on the Internet]. Korea: Regulation on Approval of Functional ingredient and of Standard/Specification for Health Functional Food [undated 2013 Oct 7; cited 2015 Feb 17]. Available from: http://www.mfds.go.kr/index.do?mid=687&pageNo=4&seq=7102&cmd=v.
  31. Schmand B, Jonker C, Hooijer C, Lindeboom J. Subjective memory complaints may announce dementia. Neurology 1996;46:121-125. https://doi.org/10.1212/WNL.46.1.121
  32. Wechsler D. Wechsler Memory Scale-Fourth Edition (WMS-IV): technical and interpretive manual. San Antonio, TX: Pearson;2009.
  33. Strauss E, Sherman EM, Spreen OA. Compendium of Neuropsychological Tests: administration, norms, and commentary. 3rd ed. New York: Oxford University Press;2006.
  34. Beglinger LJ, Gaydos B, Tangphao-Daniels O, Duff K, Kareken DA, Crawford J, et al. Practice effects and the use of alternate forms in serial neuropsychological testing. Arch Clin Neuropsychol 2005;20: 517-529. https://doi.org/10.1016/j.acn.2004.12.003
  35. Gregoire J, Van der Linden M. Effects of age on forward and backward digit spans. Aging Neuropsychol Cogn 1997;4:140-149. https://doi.org/10.1080/13825589708256642
  36. Levine AJ, Miller EN, Becker JT, Selnes OA, Cohen BA. Normative data for determining significance of test-retest differences on eight common neuropsychological instruments. Clin Neuropsychol 2004; 18:373-384. https://doi.org/10.1080/1385404049052420
  37. Iwasaki K, Kobayashi S, Chimura Y, Taguchi M, Inoue K, Cho S, et al. A randomized, double-blind, placebo-controlled clinical trial of the Chinese herbal medicine "ba wei di huang wan" in the treatment of dementia. J Am Geriatr Soc 2004;52:1518-1521. https://doi.org/10.1111/j.1532-5415.2004.52415.x
  38. Kim J, Chung SY, Park S, Park JH, Byun S, Hwang M, et al. Enhancing effect of HT008-1 on cognitive function and quality of life in cognitively declined healthy adults: a randomized, double-blind, placebo-controlled, trial. Pharmacol Biochem Behav 2008;90:517-524. https://doi.org/10.1016/j.pbb.2008.03.033
  39. Unsworth N, Engle RW. On the division of short-term and working memory: an examination of simple and complex span and their relation to higher order abilities. Psychol Bull 2007;133:1038-1066. https://doi.org/10.1037/0033-2909.133.6.1038
  40. Hoelzle JB, Nelson NW, Smith CA. Comparison of Wechsler Memory Scale-Fourth Edition (WMS-IV) and Third Edition (WMS-III) dimensional structures: improved ability to evaluate auditory and visual constructs. J Clin Exp Neuropsychol 2011;33:283-291. https://doi.org/10.1080/13803395.2010.511603
  41. Lu PH, Boone KB, Cozolino L, Mitchell C. Effectiveness of the Rey-Osterrieth Complex Figure Test and the Meyers and Meyers recognition trial in the detection of suspect effort. Clin Neuropsychol 2003; 17:426-440. https://doi.org/10.1076/clin.17.3.426.18083
  42. Engle RW, Tuholski SW, Laughlin JE, Conway AR. Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. J Exp Psychol Gen 1999;128:309-331. https://doi.org/10.1037/0096-3445.128.3.309
  43. Johnson MK, McMahon RP, Robinson BM, Harvey AN, Hahn B, Leonard CJ, et al. The relationship between working memory capacity and broad measures of cognitive ability in healthy adults and people with schizophrenia. Neuropsychology 2013;27:220-229. https://doi.org/10.1037/a0032060
  44. Nouchi R, Taki Y, Takeuchi H, Hashizume H, Nozawa T, Sekiguchi A, et al. Beneficial effects of short-term combination exercise training on diverse cognitive functions in healthy older people: study protocol for a randomized controlled trial. Trials 2012;13:200. https://doi.org/10.1186/1745-6215-13-200
  45. Wroolie TE, Kenna HA, Williams KE, Powers BN, Holcomb M, Khaylis A, et al. Differences in verbal memory performance in postmenopausal women receiving hormone therapy: $17{\beta}$-estradiol versus conjugated equine estrogens. Am J Geriatr Psychiatry 2011;19: 792-802. https://doi.org/10.1097/JGP.0b013e3181ff678a
  46. Dobbs AR, Rule BG. Adult age differences in working memory. Psychol Aging 1989;4:500-503. https://doi.org/10.1037/0882-7974.4.4.500
  47. Salthouse TA. Mediation of adult age differences in cognition by reductions in working memory and speed of processing. Psychol Sci 1991;2:179-183. https://doi.org/10.1111/j.1467-9280.1991.tb00127.x
  48. Keefe RS, Sweeney JA, Gu H, Hamer RM, Perkins DO, McEvoy JP, et al. Effects of olanzapine, quetiapine, and risperidone on neurocognitive function in early psychosis: a randomized, double-blind 52-week comparison. Am J Psychiatry 2007;164:1061-1071. https://doi.org/10.1176/ajp.2007.164.7.1061
  49. Milbury K, Chaoul A, Biegler K, Wangyal T, Spelman A, Meyers CA, et al. Tibetan sound meditation for cognitive dysfunction: results of a randomized controlled pilot trial. Psychooncology 2013;22: 2354-2363.
  50. Duff SJ, Hampson E. A sex difference on a novel spatial working memory task in humans. Brain Cogn 2001;47:470-493. https://doi.org/10.1006/brcg.2001.1326
  51. Kaufman SB. Sex differences in mental rotation and spatial visualization ability: can they be accounted for by differences in working memory capacity? Intell 2007;35:211-223. https://doi.org/10.1016/j.intell.2006.07.009
  52. Shelton JT, Elliott EM, Hill BD, Calamia MR, Gouvier WD. A Comparison of Laboratory and Clinical Working Memory Tests and Their Prediction of Fluid Intelligence. Intelligence 2009;37:283. https://doi.org/10.1016/j.intell.2008.11.005
  53. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Study Research Group, Jacobson AM, Musen G, Ryan CM, Silvers N, Cleary P, et al. Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med 2007;356:1842-1852. https://doi.org/10.1056/NEJMoa066397
  54. Kennedy DO, Scholey AB. Ginseng: potential for the enhancement of cognitive performance and mood. Pharmacol Biochem Behav 2003;75:687-700. https://doi.org/10.1016/S0091-3057(03)00126-6
  55. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003;6:750-757. https://doi.org/10.1038/nn1075
  56. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505. https://doi.org/10.1016/j.neuroimage.2006.02.024
  57. Lingjaerde O, Ahlfors UG, Bech P, Dencker SJ, Elgen K. The UKU side effect rating scale. A new comprehensive rating scale for psychotropic drugs and a cross-sectional study of side effects in neuroleptic-treated patients. Acta Psychiatr Scand Suppl 1987;334:1-100.
  58. West BT, Welch KB, Galecki AT. Linear mixed models: a practical guide using statistical software. Boca Raton, FL: Chapman & Hall/CRC;2007.
  59. Gildengers AG, Mulsant BH, Begley A, Mazumdar S, Hyams AV, Reynolds Iii CF, et al. The longitudinal course of cognition in older adults with bipolar disorder. Bipolar Disord 2009;11:744-752. https://doi.org/10.1111/j.1399-5618.2009.00739.x
  60. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002; 15:1-25. https://doi.org/10.1002/hbm.1058
  61. Avery AJ, Rodgers S, Cantrill JA, Armstrong S, Cresswell K, Eden M, et al. A pharmacist-led information technology intervention for medication errors (PINCER): a multicentre, cluster randomised, controlled trial and cost-effectiveness analysis. Lancet 2012;379: 1310-1319. https://doi.org/10.1016/S0140-6736(11)61817-5
  62. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O. Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: an in vivo study with TBSS and VBM. Hum Brain Mapp 2009;30:2852-2861. https://doi.org/10.1002/hbm.20713
  63. Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci 2004;27:279-306. https://doi.org/10.1146/annurev.neuro.27.070203.144130
  64. Stewart R, Dufouil C, Godin O, Ritchie K, Maillard P, Delcroix N, et al. Neuroimaging correlates of subjective memory deficits in a community population. Neurology 2008;70:1601-1607. https://doi.org/10.1212/01.wnl.0000310982.99438.54
  65. Karlsgodt KH, van Erp TG, Poldrack RA, Bearden CE, Nuechterlein KH, Cannon TD. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol Psychiatry 2008;63:512-518. https://doi.org/10.1016/j.biopsych.2007.06.017
  66. Vestergaard M, Madsen KS, Baare WF, Skimminge A, Ejersbo LR, Ramsoy TZ, et al. White matter microstructure in superior longitudinal fasciculus associated with spatial working memory performance in children. J Cogn Neurosci 2011;23:2135-2146. https://doi.org/10.1162/jocn.2010.21592
  67. Medina D, DeToledo-Morrell L, Urresta F, Gabrieli JD, Moseley M, Fleischman D, et al. White matter changes in mild cognitive impairment and AD: a diffusion tensor imaging study. Neurobiol Aging 2006;27:663-672. https://doi.org/10.1016/j.neurobiolaging.2005.03.026
  68. Head D, Buckner RL, Shimony JS, Williams LE, Akbudak E, Conturo TE, et al. Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. Cereb Cortex 2004;14:410-423. https://doi.org/10.1093/cercor/bhh003
  69. Malik R, Sangwan A, Saihgal R, Jindal DP, Piplani P. Towards better brain management: nootropics. Curr Med Chem 2007;14:123-131. https://doi.org/10.2174/092986707779313408
  70. Kim HJ, Moon KD, Lee DS, Lee SH. Ethyl ether fraction of Gastrodia elata Blume protects amyloid beta peptide-induced cell death. J Ethnopharmacol 2003;84:95-98. https://doi.org/10.1016/S0378-8741(02)00290-8
  71. Mun JH, Lee SG, Kim DH, Jung JW, Lee S, Yoon BH, et al. Neurotrophic factors mediate memory enhancing property of ethanolic extract of liriope platyphylla in mice. J Appl Pharmacol 2007;15:83-88. https://doi.org/10.4062/biomolther.2007.15.2.083
  72. Pan YM, Wang K, Huang SQ, Wang HS, Mu XM, He CH, et al. Antioxidant activity of microwave-assisted extract of longan (Dimocarpus Longan Lour.) peel. Food Chem 2008;106:1264-1270. https://doi.org/10.1016/j.foodchem.2007.07.033
  73. Ribnicky DM, Poulev A, Schmidt B, Cefalu WT, Raskin I. Evaluation of botanicals for improving human health. Am J Clin Nutr 2008; 87:472S-475S. https://doi.org/10.1093/ajcn/87.2.472S
  74. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 2007;36:630-644. https://doi.org/10.1016/j.neuroimage.2007.02.049