Fisheries and Aquatic Sciences

한국수산과학회 (The Korean Society of Fisheries and Aquatic Science)
권호 표지
DOI QR코드

DOI QR Code

Fermented Laminaria japonica improves working memory and antioxidant defense mechanism in healthy adults: a randomized, double-blind, and placebo-controlled clinical study

  • Kim, Young-Sang (Department of Marine Life Science, Jeju National University) ;
  • Reid, Storm N.S. (Department of Sports and Health Science, Kyungsung University) ;
  • Ryu, Jeh-Kwang (Institute for Cognitive Science, College of Humanities, Seoul National University) ;
  • Lee, Bae-Jin (Marine Bio-Industry Development Center, Marine Bioprocess Co., Ltd.) ;
  • Jeon, Byeong Hwan (Department of Sports and Health Science, Kyungsung University)
  • 투고 : 2022.07.16
  • 심사 : 2022.07.27
  • 발행 : 2022.08.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

A randomized, double-blind, and placebo-controlled clinical study was used to determine the cognitive functions related to working memory (WM) and antioxidant properties of fermented Laminaria japonica (FLJ) on healthy volunteers. Eighty participants were divided into a placebo group (n = 40) and FLJ group (n = 40) that received FLJ (1.5 g/day) for 6 weeks. Memory-related blood indices (brain-derived neurotrophic factor, BDNF; angiotensin-converting enzyme; human growth hormone, HGH; insulin-like growth factor-1, IGF-1) and antioxidant function-related indices (catalase, CAT; malondialdehyde, MDA; 8-oxo-2'-deoxyguanosine, 8-oxo-dG; thiobarbituric acid reactive substances, TBARS) were determined before and after the trial. In addition, standardized cognitive tests were conducted using the Cambridge Neuropsychological Test Automated Batteries. Furthermore, the Korean Wechsler Adult Intelligence Scale (K-WAIS)-IV, and the Korean version of the Montreal Cognitive Assessment (MoCA-K) were used to assess the pre and post intake changes on WM-related properties. According to the results, FLJ significantly increased the level of CAT, BDNF, HGH, and IGF-1. FLJ reduced the level of TBARS, MDA, and 8-oxo-dG in serum. Furthermore, FLJ improved physical activities related to cognitive functions such as K-WAIS-IV, MoCA-K, Paired Associates Learning, and Spatial Working Memory compared to the placebo group. Our results suggest that FLJ is a potential candidate to develop functional materials reflecting its capability to induce antioxidant mechanisms together with WM-related indices.

키워드

참고문헌

  1. Alloway TP, Alloway RG. Investigating the predictive roles of working memory and IQ in academic attainment. J Exp Child Psychol. 2010;106:20-9. https://doi.org/10.1016/j.jecp.2009.11.003
  2. Asanka Sanjeewa KK, Jeon YJ. Edible brown seaweeds: a review. J Food Bioact. 2018;2:37-50.
  3. Asanka Sanjeewa KK, Kim EA, Son KT, Jeon YJ. Bioactive properties and potentials cosmeceutical applications of phlorotannins isolated from brown seaweeds: a review. J Photochem Photobiol B Biol. 2016;162:100-5. https://doi.org/10.1016/j.jphotobiol.2016.06.027
  4. Asanka Sanjeewa KK, Lee WW, Kim JI, Jeon YJ. Exploiting biological activities of brown seaweed Ishige okamurae Yendo for potential industrial applications: a review. J Appl Phycol. 2017;29:3109-19. https://doi.org/10.1007/s10811-017-1213-4
  5. Baddeley A. Working memory. Science. 1992;255:556-9. https://doi.org/10.1126/science.1736359
  6. Barnett JH, Blackwell AD, Sahakian BJ, Robbins TW. The paired associates learning (PAL) test: 30 years of CANTAB translational neuroscience from laboratory to bedside in dementia research. Curr Top Behav Neurosci. 2016;28:449-74.
  7. Cha JY, Lee BJ, Je JY, Kang YM, Kim YM, Cho YS. GABA-enriched fermented Laminaria japonica protects against alcoholic hepatotoxicity in Sprague-Dawley rats. Fish Aquat Sci. 2011;14:79-88.
  8. Chen YC, Cheng CY, Liu CT, Sue YM, Chen TH, Hsu YH, et al. Alleviative effect of fucoxanthin-containing extract from brown seaweed Laminaria japonica on renal tubular cell apoptosis through upregulating Na+/H+ exchanger NHE1 in chronic kidney disease mice. J Ethnopharmacol. 2018;224:391-9. https://doi.org/10.1016/j.jep.2018.06.023
  9. Choi YS, Choi JH, Han DJ, Kim HY, Kim HW, Lee MA, et al. Effects of Laminaria japonica on the physico-chemical and sensory characteristics of reduced-fat pork patties. Meat Sci. 2012;91:1-7. https://doi.org/10.1016/j.meatsci.2011.11.011
  10. Cirulli F, Berry A, Chiarotti F, Alleva E. Intrahippocampal administration of BDNF in adult rats affects shortterm behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus. 2004;14:802-7. https://doi.org/10.1002/hipo.10220
  11. Cowan N. The many faces of working memory and short-term storage. Psychon Bull Rev. 2017;24:1158-70. https://doi.org/10.3758/s13423-016-1191-6
  12. Fang Q, Wang JF, Zha XQ, Cui SH, Cao L, Luo JP. Immunomodulatory activity on macrophage of a purified polysaccharide extracted from Laminaria japonica. Carbohydr Polym. 2015;134:66-73. https://doi.org/10.1016/j.carbpol.2015.07.070
  13. Head E. Oxidative damage and cognitive dysfunction: antioxidant treatments to promote healthy brain aging. Neurochem Res. 2009;34:670-8. https://doi.org/10.1007/s11064-008-9808-4
  14. Kadam SU, Tiwari BK, O'Donnell CP. Application of novel extraction technologies for bioactives from marine algae. J Agric Food Chem. 2013;61:4667-75. https://doi.org/10.1021/jf400819p
  15. Kang MC, Wijesinghe WAJP, Lee SH, Kang SM, Ko SC, Yang X, et al. Dieckol isolated from brown seaweed Ecklonia cava attenuates type II diabetes in db/db mouse model. Food Chem Toxicol. 2013;53:294-8. https://doi.org/10.1016/j.fct.2012.12.012
  16. Kang SY, Kim E, Kang I, Lee M, Lee Y. Anti-diabetic effects and anti-inflammatory effects of Laminaria japonica and Hizikia fusiforme in skeletal muscle: in vitro and in vivo model. Nutrients. 2018;10:491.
  17. Kang YM, Lee BJ, Kim JI, Nam BH, Cha JY, Kim YM, et al. Antioxidant effects of fermented sea tangle (Laminaria japonica) by Lactobacillus brevis BJ20 in individuals with high level of γ-GT: a randomized, double-blind, and placebo-controlled clinical study. Food Chem Toxicol. 2012;50:1166-9. https://doi.org/10.1016/j.fct.2011.11.026
  18. Kaser M, Deakin JB, Michael A, Zapata C, Bansal R, Ryan D, et al. Modafinil improves episodic memory and working memory cognition in patients with remitted depression: a double-blind, randomized, placebo-controlled study. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2:115-22.
  19. Khan Z, Ali SA. Oxidative stress-related biomarkers in Parkinson's disease: a systematic review and meta-analysis. Iran J Neurol. 2018;17:137-44.
  20. Kim SK, Bhatnagar I. Physical, chemical, and biological properties of wonder kelp-Laminaria. In: Kim SK, editor. Marine medicinal foods: implications and applications, macro and microalgae. Waltham, MA: Academic Press; 2011. p. 85-96.
  21. Lee A, Archer J, Wong CKY, Chen SHA, Qiu A. Age-related decline in associative learning in healthy Chinese adults. PLOS ONE. 2013;8:e80648.
  22. Lee BJ, Kim JS, Kang YM, Lim JH, Kim YM, Lee MS, et al. Antioxidant activity and γ-aminobutyric acid (GABA) content in sea tangle fermented by Lactobacillus brevis BJ20 isolated from traditional fermented foods. Food Chem. 2010;122:271-6. https://doi.org/10.1016/j.foodchem.2010.02.071
  23. Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, et al. Oxidative stress, aging, and diseases. Clin Interv Aging. 2018;13:757-72. https://doi.org/10.2147/CIA.S158513
  24. Lin HTV, Lu WJ, Tsai GJ, Chou CT, Hsiao HI, Hwang PA. Enhanced anti-inflammatory activity of brown seaweed Laminaria japonica by fermentation using Bacillus subtilis. Process Biochem. 2016;51:1945-53. https://doi.org/10.1016/j.procbio.2016.08.024
  25. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, et al. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging. 2005;26:115-23. https://doi.org/10.1016/j.neurobiolaging.2004.03.002
  26. Lu J, You L, Lin Z, Zhao M, Cui C. The antioxidant capacity of polysaccharide from Laminaria japonica by citric acid extraction. Int J Food Sci Technol. 2013;48:1352-8. https://doi.org/10.1111/ijfs.12072
  27. Ma L, Chang L, Chen X, Zhou R. Working memory test battery for young adults: computerized working memory assessment. PLOS ONE. 2017;12:e0175047.
  28. Mahadevan K. Seaweeds: a sustainable food source. In: Tiwari BK, Troy DJ, editors. Seaweed sustainability: food and nonfood applications. San Diego, CA: Academic Press; 2015. p. 347-64.
  29. Markowska AL, Mooney M, Sonntag WE. Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience. 1998;87:559-69. https://doi.org/10.1016/S0306-4522(98)00143-2
  30. Martins S, Mussatto SI, Martinez-Avila G, Montanez-Saenz J, Aguilar CN, Teixeira JA. Bioactive phenolic compounds: production and extraction by solid-state fermentation. A review. Biotechnol Adv. 2011;29:365-73. https://doi.org/10.1016/j.biotechadv.2011.01.008
  31. Mecocci P, Polidori MC. Antioxidant clinical trials in mild cognitive impairment and Alzheimer's disease. Biochim Bio-phys Acta. 2012;1822:631-8. https://doi.org/10.1016/j.bbadis.2011.10.006
  32. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695-9. https://doi.org/10.1111/j.1532-5415.2005.53221.x
  33. Ossoukhova A, Owen L, Savage K, Meyer M, Ibarra A, Roller M, et al. Improved working memory performance following administration of a single dose of American ginseng (Panax quinquefolius L.) to healthy middle-age adults. Hum Psychopharmacol Clin Exp. 2015;30:108-22. https://doi.org/10.1002/hup.2463
  34. Ozer J, Ratner M, Shaw M, Bailey W, Schomaker S. The current state of serum biomarkers of hepatotoxicity. Toxicology. 2008;245:194-205. https://doi.org/10.1016/j.tox.2007.11.021
  35. Park MJ, Han JS. Radical scavenging and antioxidant activities of fermented Laminaria japonica extracts. Prev Nutr Food Sci. 2006;11:10-6. https://doi.org/10.3746/jfn.2006.11.1.010
  36. Reid SNS, Ryu JK, Kim Y, Jeon BH. The effects of fermented Laminaria japonica on short-term working memory and physical fitness in the elderly. Evid Based Complement Alternat Med. 2018;2018:8109621.
  37. Socci V, Tempesta D, Desideri G, De Gennaro L, Ferrara M. Enhancing human cognition with cocoa flavonoids. Front Nutr. 2017;4:19.
  38. Spellman T, Rigotti M, Ahmari SE, Fusi S, Gogos JA, Gordon JA. Hippocampal-prefrontal input supports spatial encoding in working memory. Nature. 2015;522:309-14. https://doi.org/10.1038/nature14445
  39. Sytze van Dam P, Aleman A. Insulin-like growth factor-I, cognition and brain aging. Eur J Pharmacol. 2004;490:87-95. https://doi.org/10.1016/j.ejphar.2004.02.047
  40. Um MY, Lim DW, Son HJ, Cho S, Lee C. Phlorotannin-rich fraction from Ishige foliacea brown seaweed prevents the scopolamine-induced memory impairment via regulation of ERKCREB-BDNF pathway. J Funct Foods. 2018;40:110-6. https://doi.org/10.1016/j.jff.2017.10.014
  41. Wang J, Zhang Q, Zhang Z, Li Z. Antioxidant activity of sulfated polysaccharide fractions extracted from Laminaria japonica. Int J Biol Macromol. 2008;42:127-32. https://doi.org/10.1016/j.ijbiomac.2007.10.003
  42. Wojtunik-Kulesza KA, Oniszczuk A, Oniszczuk T, Waksmundzka-Hajnos M. The influence of common free radicals and antioxidants on development of Alzheimer's disease. Biomed Pharmacother. 2016;78:39-49. https://doi.org/10.1016/j.biopha.2015.12.024
  43. Yang H, Zeng M, Dong S, Liu Z, Li R. Anti-proliferative activity of phlorotannin extracts from brown algae Laminaria japonica Aresch. Chin J Oceanol Limnolgy. 2010;28:122-30. https://doi.org/10.1007/s00343-010-9054-x
  44. Yeom TH, Park YS, Oh KJ, Lee YH. Korean version Wechsler Adult Intelligence Scale. Seoul: Korean Guidance; 1992. p. 13-28.
  45. Zha XQ, Xiao JJ, Zhang HN, Wang JH, Pan LH, Yang XF, et al. Polysaccharides in Laminaria japonica (LP): extraction, physicochemical properties and their hypolipidemic activities in diet-induced mouse model of atherosclerosis. Food Chem. 2012;134:244-52. https://doi.org/10.1016/j.foodchem.2012.02.129
  46. Zhang Z, Deng L, Bai F, Shi Y, Yu H, Yuan Y, et al. ACE I/D polymorphism affects cognitive function and gray-matter volume in amnestic mild cognitive impairment. Behav Brain Res. 2011;218:114-20. https://doi.org/10.1016/j.bbr.2010.11.032