Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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The influence of obesity on the effects of spirulina supplementation in the human metabolic response of Korean elderly

  • Received : 2015.12.04
  • Accepted : 2016.02.19
  • Published : 2016.08.01
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Abstract

BACKGROUND/OBJECTIVES: Spirulina, a blue-green alga, is widely produced and commercialized as a dietary supplement with bio- and immune-modulatory functions. We have previously shown that spirulina had favorable effects on lipid profiles, immune functions, and antioxidant capacity in healthy Korean elderly. Despite favorable effect of spirulina supplementation, some sub-populations have shown a poor response to supplementation. Obesity is a factor related to poor-response. Therefore, the purpose of this study was to determine the immuno-modulation, antioxidant capacity, and lipid-lowering effect of spirulina in obese and non-obese Korean elderly. SUBJECTS/METHODS: The subjects were 78 elderly aged 60-87 years. In a randomized double blind, placebo-controlled study, subjects were fed either placebo or spirulina daily, at 8 g for 12 weeks. Subjects were divided into the non-obese group and the obese group based on body mass index (BMI) criteria for Asians suggested by the International Obesity Task Force: $BMI<25kg/m^2$ (non-obese) and $BMI{\geq}25kg/m^2$ (obese). RESULTS: In the non-obese group, spirulina supplementation showed a significant lowering effect on plasma concentration of total cholesterol and LDL-cholesterol, a significant increase in interleukin (IL)-2 concentration (P < 0.01) and a significant increment (P < 0.05) in IL-2/IL-6 ratio, and a significant increase in total antioxidant status level and a significant decrease in thiobarbituric acid reactive substances level. However, these effects were not observed in the obese group. CONCLUSION: These results demonstrated that blood lipid lowering and immune and antioxidant improving response for spirulina supplement was affected by obesity in Korean elderly.

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References

  1. Thengodkar RR, Sivakami S. Degradation of Chlorpyrifos by an alkaline phosphatase from the cyanobacterium Spirulina platensis. Biodegradation 2010;21:637-44. https://doi.org/10.1007/s10532-010-9331-6
  2. Hasler CM. Functional foods: benefits, concerns and challenges-a position paper from the American Council on Science and Health. J Nutr 2002;132:3772-81. https://doi.org/10.1093/jn/132.12.3772
  3. Bhavisha R, Parula P. Spirulina: potential clinical therapeutic application. J Pharm Res 2010;3:1726-32.
  4. Savranoglu S, Tumer TB. Inhibitory effects of spirulina platensis on carcinogen-activating cytochrome p450 I for drug interactions. Int J Toxicol 2013;32:376-84. https://doi.org/10.1177/1091581813503887
  5. Serban MC, Sahebkar A, Dragan S, Stoichescu-Hogea G, Ursoniu S, Andrica F, Banach M. A systematic review and meta-analysis of the impact of Spirulina supplementation on plasma lipid concentrations. Clin Nutr. Forthcoming 2015.
  6. Joventino IP, Alves HG, Neves LC, Pinheiro-Joventino F, Leal LK, Neves SA, Ferreira FV, Brito GA, Viana GB. The microalga spirulina platensis presents anti-inflammatory action as well as hypoglycemic and hypolipidemic properties in diabetic rats. J Complement Integr Med 2012;9:Article 17.
  7. Torres-Duran PV, Ferreira-Hermosillo A, Juarez-Oropeza MA. Antihyperlipemic and antihypertensive effects of Spirulina maxima in an open sample of Mexican population: a preliminary report. Lipids Health Dis 2007;6:33. https://doi.org/10.1186/1476-511X-6-33
  8. Marcel AK, Ekali LG, Eugene S, Arnold OE, Sandrine ED, von der Weid D, Gbaguidi E, Ngogang J, Mbanya JC. The effect of Spirulina platensis versus soybean on insulin resistance in HIV-infected patients: a randomized pilot study. Nutrients 2011;3:712-24. https://doi.org/10.3390/nu3070712
  9. Derosa G, Limas CP, Macias PC, Estrella A, Maffioli P. Dietary and nutraceutical approach to type 2 diabetes. Arch Med Sci 2014;10:336-44.
  10. Moura LP, Puga GM, Beck WR, Teixeira IP, Ghezzi AC, Silva GA, Mello MA. Exercise and spirulina control non-alcoholic hepatic steatosis and lipid profile in diabetic Wistar rats. Lipids Health Dis 2011;10:77. https://doi.org/10.1186/1476-511X-10-77
  11. Martinez-Galero E, Perez-Pasten R, Perez-Juarez A, Fabila-Castillo L, Gutierrez-Salmean G, Chamorro G. Preclinical antitoxic properties of Spirulina (Arthrospira). Pharm Biol 2015;6:1-9.
  12. Watanuki H, Ota K, Tassakka AC, Kato T, Sakai M. Immunostimulant effects of dietary spirulina platensis on carp, Cyprinus carpio. Aquaculture 2006;258:157-63. https://doi.org/10.1016/j.aquaculture.2006.05.003
  13. Balachandran P, Pugh ND, Ma G, Pasco DS. Toll-like receptor 2-dependent activation of monocytes by Spirulina polysaccharide and its immune enhancing action in mice. Int Immunopharmacol 2006;6:1808-14. https://doi.org/10.1016/j.intimp.2006.08.001
  14. Park HJ, Lee YJ, Ryu HK, Kim MH, Chung HW, Kim WY. A randomized double-blind, placebo-controlled study to establish the effects of spirulina in elderly Koreans. Ann Nutr Metab 2008;52:322-8. https://doi.org/10.1159/000151486
  15. Keaney JF Jr, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA, Benjamin EJ; Framingham Study. Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 2003;23:434-9. https://doi.org/10.1161/01.ATV.0000058402.34138.11
  16. Steffes MW, Gross MD, Lee DH, Schreiner PJ, Jacobs DR Jr. Adiponectin, visceral fat, oxidative stress, and early macrovascular disease: the Coronary Artery Risk Development in Young Adults Study. Obesity (Silver Spring) 2006;14:319-26. https://doi.org/10.1038/oby.2006.41
  17. Painter SD, Ovsyannikova IG, Poland GA. The weight of obesity on the human immune response to vaccination. Vaccine 2015;33:4422-9. https://doi.org/10.1016/j.vaccine.2015.06.101
  18. Bozaoglu K, Attard C, Kulkarni H, Cummings N, Diego VP, Carless MA, Shields KA, Johnson MP, Kowlessur S, Dyer TD, Comuzzie AG, Almasy L, Zimmet P, Moses EK, Goring HH, Curran JE, Blangero J, Jowett JB. Plasma levels of soluble interleukin 1 receptor accessory protein are reduced in obesity. J Clin Endocrinol Metab 2014;99:3435-43. https://doi.org/10.1210/jc.2013-4475
  19. O'Brien KB, Vogel P, Duan S, Govorkova EA, Webby RJ, McCullers JA, Schultz-Cherry S. Impaired wound healing predisposes obese mice to severe influenza virus infection. J Infect Dis 2012;205:252-61. https://doi.org/10.1093/infdis/jir729
  20. Kim IY, Williams RH, Schutzler SE, Lasley CJ, Bodenner DL, Wolfe RR, Coker RH . Acute lysine supplementation does not improve hepatic or peripheral insulin sensitivity in older, overweight individuals. Nutr Metab (Lond) 2014;11:49. https://doi.org/10.1186/1743-7075-11-49
  21. Korean Nutrition Society. CAN-Pro: computer aided nutritional analysis program. Version 3.0. Seoul: Korean Nutrition Society; 2006.
  22. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.
  23. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: the Muscatine Study. Pediatrics 1988;82:309-18.
  24. Yagi K. Assay for blood plasma or serum. Methods Enzymol 1984;105:328-31.
  25. Hwang JH, Lee IT, Jeng KC, Wang MF, Hou RC, Wu SM, Chan YC. Spirulina prevents memory dysfunction, reduces oxidative stress damage and augments antioxidant activity in senescence-accelerated mice. J Nutr Sci Vitaminol (Tokyo) 2011;57:186-91. https://doi.org/10.3177/jnsv.57.186
  26. Kurd F, Samavati V. Water soluble polysaccharides from Spirulina platensis: extraction and in vitro anti-cancer activity. Int J Biol Macromol 2015;74:498-506. https://doi.org/10.1016/j.ijbiomac.2015.01.005
  27. Yang Y, Kim B, Park YK, Lee JY. Effects of long-term supplementation of blue-green algae on Lipid Metabolism in C57BL/6J mice. J Nutrit Health Food Sci 2014;1.
  28. Muga MA, Chao JC. Effects of fish oil and spirulina on oxidative stress and inflammation in hypercholesterolemic hamsters. BMC Complement Altern Med 2014;14:470-9. https://doi.org/10.1186/1472-6882-14-470
  29. Weber DJ, Rutala WA, Samsa GP, Santimaw JE, Lemon SM. Obesity as a predictor of poor antibody response to hepatitis B plasma vaccine. JAMA 1985;254:3187-9. https://doi.org/10.1001/jama.1985.03360220053027
  30. Magrone T, Jirillo E. Childhood obesity: immune response and nutritional approaches. Front Immunol 2015;6:76.
  31. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 2012;18:363-74. https://doi.org/10.1038/nm.2627
  32. Stowe DF, Camara AK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 2009;11:1373-414. https://doi.org/10.1089/ars.2008.2331
  33. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW 3rd, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD. Mitochondrial $H_2O_2$ emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009;119:573-81. https://doi.org/10.1172/JCI37048
  34. Paich HA, Sheridan PA, Handy J, Karlsson EA, Schultz-Cherry S, Hudgens MG, Noah TL, Weir SS, Beck MA. Overweight and obese adult humans have a defective cellular immune response to pandemic H1N1 influenza A virus. Obesity (Silver Spring) 2013;21:2377-86. https://doi.org/10.1002/oby.20383
  35. Scott EM. Circadian clocks, obesity and cardiometabolic function. Diabetes Obes Metab 2015;17 Suppl 1:84-9. https://doi.org/10.1111/dom.12518
  36. Adler WH 3rd. Immune function in the elderly. Geriatrics 1989;44 Suppl A:7-10.
  37. Rabinowich H, Goses Y, Reshef T, Klajman A. Interleukin-2 production and activity in aged humans. Mech Ageing Dev 1985;32:213-26. https://doi.org/10.1016/0047-6374(85)90081-8
  38. Galloway SD, Craig TP, Cleland SJ. Effects of oral L-carnitine supplementation on insulin sensitivity indices in response to glucose feeding in lean and overweight/obese males. Amino Acids 2011;41:507-15. https://doi.org/10.1007/s00726-010-0770-5
  39. Sahebkar A, Mohammadi A, Atabati A, Rahiman S, Tavallaie S, Iranshahi M, Akhlaghi S, Ferns GA, Ghayour-Mobarhan M. Curcuminoids modulate pro-oxidant-antioxidant balance but not the immune response to heat shock protein 27 and oxidized LDL in obese individuals. Phytother Res 2013;27:1883-8. https://doi.org/10.1002/ptr.4952

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