Spirulina platensis (SPI) is a microalga with a high content of functional compounds, such as phenolics, phycocyanins and polysaccharides that has been shown to have antioxidant, anti-inflammatory, hypoglycemic, neuro-protective and immunomodulatory effects. The objectives of the present work were to study the possible effects of SPI treatment on the glycemic-lipid profile, oxidative stress, lipid peroxidation and cardiac performance in diabetic rats. Diabetes was induced by streptozotocin (STZ) in male Wistar rats. In diabetic animals SPI, at a dose of 50 mg/kg/day, reduced lipid peroxidation, nitrite levels and lipids in plasma and tissues. SPI exhibited an effective improvement on +dP/dT and − d P/ dT in non-diabetic rats. This study showed that SPI significantly suppressed nitrite generation and lipoperoxidation in the hearts of diabetic animals, as well as an improvement in the cardiac function in control SPI-treated rats which is consistent with several studies that demonstrated the protective effect of antioxidants on oxidative stress-mediated injury caused by reactive oxygen species (ROS) produced in diabetic myocardial tissues.
Tietze, H.W. (2004) Spirulina Micro Food Macro Blessing. 4th Edition, Harald W. Tietze Publishing, Australia.
Kay, R.A (1991) Microalgae as Food and Supplement. Critical Reviews in Food Science and Nutrition, 30, 555-573. https://doi.org/10.1080/10408399109527556
Piñero Estrada, J.E., Bermejo Bescós, P. and Villar del Fresno, A.M. (2001) Antioxidant Activity of Different Fractions of Spirulina Protean Extract. Farmaco, 56, 497-500. https://doi.org/10.1016/S0014-827X(01)01084-9
Chen, J.C., Liu, K.S., Yang, T.J., Hwang, J.H., Chan, Y.C. and Lee, I.T. (2012) Spirulina and C-Phycocyanin Reduce Cytotoxicity and Inflammation-Related Genes Expression of Microglial Cells. Nutritional Neuroscience, 15, 252-256. https://doi.org/10.1179/1476830512Y.0000000020
Joventino, I.P., Alves, H.G., Neves. L.C., Pinheiro-Joventino, F., Leal, L.K., Neves, S.A., et al. (2012) The Microalga SPI Presents Anti-Inflammatory Action as Well as Hypoglycemic and Hypolipidemic Properties in Diabetic Rats. Journal of Complementary and Integrative Medicine, 9, 1553-3840. https://doi.org/10.1515/1553-3840.1534
Lima, F.A.V., Joventino, I.P., Joventino, F.P., de Almeida A.C., Neves. K.R.T., do Carmo, M.R., et al. (2017) Neuroprotective Activities of Spirulina platensis in the 6-OHDA Model of Parkinson’s Disease Are Related to Its Anti-Inflammatory Effects. Neurochemical Research, 42, 3390-3400. https://doi.org/10.1007/s11064-017-2379-5
Pentón-Rol, G., Martínez-Sánchez, G., Cervantes-Llanos, M., Lagumersindez-Denis, N., Acosta-Medina, E.F., Falcón-Cama, V., et al. (2011) C-Phycocyanin Ameliorates Experimental Autoimmune Encephalomyelitis and Induces Regulatory T Cells. International Immunopharmacology, 11, 29-38. https://doi.org/10.1016/j.intimp.2010.10.001
Lee, J., Park, A., Kim, M.J., Lim, H.J., Rha, Y.A. and Kang, H.G. (2017) Spirulina Extract Enhanced a Protective Effect in Type 1 Diabetes by Anti-Apoptosis and Anti-ROS Production. Nutrients, 9, E1363. https://doi.org/10.3390/nu9121363
Farouk, K., El-Baz, F., Hanan Aly., El-Sayed A.B. and Amal, A. (2013) Mohamed. Role of Spirulina platensis in the Control of Glycemia in DM2 Rats. International Journal of Scientific & Engineering Research, 4, 1731-1740.
American Diabetes Association (2012) Diagnosis and Classification of Diabetes Mellitus. Diabetes Care, 35, 564-571.
Bugger, H. and Abel, E.D. (2014) Molecular Mechanisms of Diabetic Cardiomyopathy. Diabetologia, 57, 660-671. https://doi.org/10.1007/s00125-014-3171-6
Secrest, A.M., Becker, D.J., Kelsey, S.F., LaPorte, R.E. and Orchard, T.J. (2010) All-Cause Mortality Trends in a Large Population-Based Cohort with Long-Standing Childhood-Onset Type 1 Diabetes: The Allegheny County Type 1 Diabetes Registry. Diabetes Care, 33, 2573-2579. https://doi.org/10.2337/dc10-1170
Dobrin, J.S. and Lebeche, D. (2010) Diabetic Cardiomyopathy: Signaling Defects and Therapeutic Approaches. Expert Review of Cardiovascular Therapy, 8, 373-391. https://doi.org/10.1586/erc.10.17
Cai, H. and Harrison, D.G. (2000) Endothelial Dysfunction in Cardiovascular Diseases: The Role of Oxidant Stress. Circulation Research, 87, 840-844. https://doi.org/10.1161/01.RES.87.10.840
Guzik T.J., Mussa, S., Gastaldi, D., Sadowski, J., Ratnatunga, C., Pillai, R. and Channon, K.M. (2002) Mechanisms of Increased Vascular Superoxide Production in Human Diabetes Mellitus: Role of NAD(P)H Oxidase and Endothelial Nitric Oxide Synthase. Circulation, 105, 1656-1662. https://doi.org/10.1161/01.CIR.0000012748.58444.08
Suzuki, H., Kayama, Y., Sakamoto, M., Iuchi, H., Shimizu, I., Yoshino, T., et al. (2015) Arachidonate 12/15-Lipoxygenase-Induced Inflammation and Oxidative Stress Are Involved in the Development of Diabetic Cardiomyopathy. Diabetes, 64, 618-630. https://doi.org/10.2337/db13-1896
Kayama, Y., Raaz, U., Jagger, A., Adam, M., Schellinger, I.N, Sakamoto, M., et al. (2015) Diabetic Cardiovascular Disease Induced by Oxidative Stress. International Journal of Molecular Sciences, 16, 25234-25263. https://doi.org/10.3390/ijms161025234
Zarrouk, C. (1996) Contribution to the Study of a Cyanophycea: Influence of Various Physical and Chemical Factors on the Growth and Photosynthesis of Spirulina Maxima. PhD Thesis, Fac. Sci., University of Paris, Paris.
Rodrigues, B., Xiang, H. and McNeill, J.H. (1988) Effect of Lcarnitine Treatment on Lipid Metabolism and Cardiac Performance in Chronically Diabetic Rats. Diabetes, 37, 1358-1364. https://doi.org/10.2337/diab.37.10.1358
Rodrigues, B., Goyal, R.K. and McNeill, J.H. (1986) Effects of Hydralazine on STZ-Induced Diabetes Rats-Prevention of Hyperlipidemia and Improvement in Cardiac Function. The Journal of Pharmacology and Experimental Therapeutics, 237, 292-299.
Deng, R. and Chow, T.J. (2010) Hypolipidemic, Antioxidant, and Antiinflammatory Activities of Microalgae Spirulina. Cardiovascular Therapeutics, 28, 33-45. https://doi.org/10.1111/j.1755-5922.2010.00200.x
Lee, E.H., Park, J.E., Choi, Y.J., Huh, K.B. and Kim, W.Y. (2008) A Randomized Study to Establish the Effects of Spirulina in Type 2 Diabetes Mellitus Patients. Nutrition Research and Practice, 2, 295-300. https://doi.org/10.4162/nrp.2008.2.4.295
Mani, U.V., Desai, U.V.S. and Iyer, U. (2000) Studies on the Long-Term Effect of Spirulina Supplementation on Serum Lipid Profile and Glycated Proteins in NIDDM Patients. Journal of Nutraceuticals, Functional and Medical Foods, 2, 25-32. https://doi.org/10.1300/J133v02n03_03
Park, J.Y. and Kim, W.Y. (2003) The Effect of Spirulina on Lipid Metabolism, Antioxidant Capacity and Immune Function in Korean Elderly. The Korean Journal of Nutrition, 36, 287-297.
Parikh, P., Mani, U. and Iyer, U. (2001) Role of Spirulina in the Control of Glycemia and Lipidemia in Type 2 Diabetes Mellitus. Journal of Medicinal Food, 4, 193-199. https://doi.org/10.1089/10966200152744463
Nagaoka, S., Shimizu, K., Kaneko, H., Shibayama, F., Morikawa, K., Kanamaru, Y., et al. (2005) A Novel Protein C-Phycocyanin Plays a Crucial Role in the Hypocholesterolemic Action of Spirulina platensis Concentrate in Rats. Journal of Nutrition, 135, 2425-2430. https://doi.org/10.1093/jn/135.10.2425
Li-Kun, H., Dong-Xia, L., Lan, X., Xiao-Jie, G., Yasumasa, K., Isao, S. and Hiromichi, O. (2006) Isolation of Pancreatic Lipase Activity-Inhibitory Component of Spirulina platensis and It Reduce Postprandial Triacylglycerolemia. Yakugaku Zasshi, 126, 43-49. https://doi.org/10.1248/yakushi.126.43
Iwata, K., Inayama, T. and Kato, T. (1990) Effects of Spirulina platensis on Plasma Lipoprotein Lipase Activity in Fructose-Induced Hyperlipidemic Rats. Journal of Nutritional Science and Vitaminology, 36, 165-171. https://doi.org/10.3177/jnsv.36.165
Miczke, A.A., SzulInska, M., Hansdorfer-Korzon, R., Kregielsk-Narozna, M., Suliburska, J., Walkowiak, J., et al. (2016) Effects of Spirulina Consumption on Body Weight, Blood Pressure, and Endothelial Function in Overweight Hypertensive Caucasians: A Double Blind, Placebo-Controlled, Randomized Trial. European Review for Medical and Pharmacological Sciences, 20, 150-156.
Zeinalian, R., Farhangi, M.A., Shariat, A. and Saghafi-Asl, M. (2017) The Effects of Spirulina Platensis on Anthropometric Indices, Appetite, Lipid Profile and Serum Vascular Endothelial Growth Factor (VEGF) in Obese Individuals: A Randomized Double Blinded Placebo Controlled Trial. BMC Complementary and Alternative Medicine, 17, 225. https://doi.org/10.1186/s12906-017-1670-y
Fromenty, B. and Pessayre, D. (1995) Inhibition of Mitochondrial Beta-Oxidation as a Mechanism of Hepatotoxicity. Pharmacology & Therapeutics, 67, 101-154. https://doi.org/10.1016/0163-7258(95)00012-6
Bertolin, T.E., Pilatti, D., Giacomini, A.C.V.V., Bavaresco, C.S., Colla, L.M. and Costa, J.A.V. (2009) Effect of Microalga Spirulina platensis (Arthrospira platensis) on Hippocampus Lipoperoxidation and Lipid Profile in Rats with Induced Hypercholesterolemia. Brazilian Archives of Biology and Technology, 52, 1253-1259. https://doi.org/10.1590/S1516-89132009000500024
Malik, Z.A., Tabassum, N. and Sharma, P.L. (2013) Attenuation of Experimentally Induced Diabetic Neuropathy in Association with Reduced Oxidative-Nitrosative Stress by Chronic Administration of Momordica charantia. Advances in Bioscience and Biotechnology, 4, 356-363. https://doi.org/10.4236/abb.2013.43047
Lee, J., Park, A., Kim, M.J., Lim, H.J., Rha, Y.A. and Kang, H.G. (2017) Spirulina Extract Enhanced a Protective Effect in Type 1 Diabetes by Anti-Apoptosis and Anti-ROS Production. Nutrients, 9, 1363. https://doi.org/10.3390/nu9121363
Romay, C., Delgado, R., Remirez, D., González, R. and Rojas, A. (2001) Effects of Phycocyanin Extract on Tumor Necrosis Factor-Alpha and Nitrite Levels in Serum of Mice Treated with Endotoxin. Arzneimittelforschung, 51, 733-736.
Romay, C., González, R., Ledón, N., Remirez, D. and Rimbau, V. (2003) C-Phycocyanin: A Biliprotein with Antioxidant, Anti-Inflammatory and Neuroprotective Effects. Current Protein & Peptide Science, 4, 207-216. https://doi.org/10.2174/1389203033487216
Riss, J., Décordé, K., Sutra, T., Delage, M., Baccou, J.C., Jouy, N., et al. (2007) Phycobiliprotein C-Phycocyanin from Spirulina platensis Is Powerfully Responsible for Reducing Oxidative Stress and NADPH Oxidase Expression Induced by an Atherogenic Diet in Hamsters. Journal of Agricultural and Food Chemistry, 55, 7962-7967. https://doi.org/10.1021/jf070529g
Lanone, S., Bloc, S., Foresti, R., Almolki, A., Taillé, C., Callebert, J., et al. (2005) Bilirubin Decreases nos2 Expression via Inhibition of NAD(P)H Oxidase: Implication for Protection against Endotoxic Shock in Rats. FASEB Journal, 19, 1890-1892. https://doi.org/10.1096/fj.04-2368fje
Inoguchi, T., Li, P., Umeda, F., Yu, H.Y., Kakimoto, M., Imamura, M., et al. (2000) High Glucose Level and Free Fatty Acid Stimulate Reactive Oxygen Species Production through Protein Kinase C-Dependent Activation of NAD(P)H Oxidase in Cultured Vascular Cells. Diabetes, 49, 1939-1945. https://doi.org/10.2337/diabetes.49.11.1939
Inoguchi, T. and Nawata, H. (2005) NAD(P)H Oxidase Activation: A Potential Target Mechanism for Diabetic Vascular Complications, Progressive Beta-Cell Dysfunction and Metabolic Syndrome. Current Drug Targets, 6, 495-501. https://doi.org/10.2174/1389450054021927
Bayeva, M., Sawicki, K.T. and Ardehali, H. (2013) Taking Diabetes to Heart-Deregulation of Myocardial Lipid Metabolism in Diabetic Cardiomyopathy. Journal of the American Heart Association, 2, e000433. https://doi.org/10.1161/JAHA.113.000433
Khan, M., Varadharaj, S., Ganesan, L.P., Shobha, J.C. and Naidu, M.U. (2005) C-Phycocyanin Protects against Ischemia-Reperfusion Injury of Heart through Involvement of p38 MAPK and ERK Signaling. American Journal of Physiology. Heart and Circulatory Physiology, 290, 2136-2145. https://doi.org/10.1152/ajpheart.01072.2005
Khan, M., Shobha, J.C., Mohan, I.K., Naidu, M.U., Sundaram, C., Singh, S., et al. (2005) Protective Effect of SPI against Doxorubicin-Induced Cardiotoxicity. Phytotherapy Research, 19, 1030-1037. https://doi.org/10.1002/ptr.1783
Khan, M., Varadharaj, S., Shobba, J.C., Naidu, M.U., Parinandi, N.L., Kutala, V.K., et al. (2006) C-Phycocyanin Ameliorates Doxorubicin-Induced Oxidative Stress and Apoptosis in Adult Rat Cardiomyocytes. Journal of Cardiovascular Pharmacology, 47, 9-20. https://doi.org/10.1097/01.fjc.0000191520.48404.27