Spirulina platensis improves insulin sensitivity and reduces hyperglycemia-mediated oxidative stress in fructose-fed rats
Abstract
Oxidative stress, hyperglycemia and insulin resistance are hallmarks of diabetes mellitus. The present study aimed to assess the antidiabetic activity of a local strain of Spirulina platensis produced at Pahou (Benin), known as “Spiruline Dou Bogan” (SPD), in fructose-fed rats. Glucose metabolism impairment was induced by feeding 8g/kg, body weight (bw), fructose solution orally to Sprague Dawley rats (n = 8) for 56 days, treated with SPD (18.75; 37.5 and 75 mg/kg, bw), and analyzed for plasma blood glucose, serum biochemistry and the markers of oxidative stress (Ferric Reducing Antioxidant Power Assay (FRAP), Malondialdehyde (MDA), Reduced glutathione (GSH), DPPH radical scavenging assay. SPD concentrations, given orally for 42 days, significantly reversed the elevations in plasma blood glucose, MDA, and the reduction in kidneys glutathione activity. Oral administration of 18.75, 37.5, and 75 mg/kg doses of SPD also lowered serum Aspartate Aminotransferase (ASAT), Alanine Aminotransferase (ALAT), Triglycerides and Creatinine levels. SPD 75 mg/kg treatment in particular has significantly decreased serum Triglycerides level and increased HDL-Cholesterol levels, reversing the atherogenic potential of 56 days fructose administration. The consumption of S. platensis produced locally in Benin as a food supplement, easily accessible for low-income populations, may be helpful in the prevention and management of type 2 diabetes.
Keywords: Oxidative stress; Spirulina platensis; hyperglycemia; insulin resistance, fructose diet
Keywords:
Oxidative stress, Spirulina platensis, hyperglycemia, insulin resistance, fructose diet
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[6] M. Khan, J.C. Shobha, I.K. Mohan, M.U. Rao Naidu, A. Prayag, V.K. Kutala, Spirulina attenuates cyclosporine-induced nephrotoxicity in rats, J. Appl. Toxicol. 26 (2006) 444-451. DOI : https://doi.org/10.1002/jat.1159
[7] A. Karadeniz, M. Cemek, N. Simsek, The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats, Ecotoxicol. Environ. Saf. 72 (2009) 231-235. DOI : https://doi.org/10.1155/2013/742859
[8] M.M. Abdel-Daim, S.M. Abuzead, S.M. Halawa, Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats, PLoS One 8 (2013) e72991. DOI : https://doi.org/10.1371/journal.pone.0072991
[9] P. Parikh, U. Mani, U. Iyer, Role of Spirulina in the control of glycemia and lipidemia in type 2 diabetes mellitus, J. Med. Food 4 (2001) 193-199. DOI : https://doi.org/10.1089/10966200152744463
[10] R. Holman, R. Turner, Oral agents and insulin in the treatment of NIDDM, Textbook of Diabetes, Oxford: Blackwell 9 (1991) 467-469
[11] J.T. Manandhar Shrestha, H. Shrestha, M. Prajapati, A. Karkee, A. Maharjan, Adverse Effects of Oral Hypoglycemic Agents and Adherence to them among Patients with Type 2 Diabetes Mellitus in Nepal, J. Lumbini Med. Coll. 5 (2017) 34-40. DOI : https://doi.org/10.22502/jlmc.v5i1.126
[12] T. Xu, S. Qin, Y. Hu, Z. Song J. Ying, P. Li, W. Dong, F. Zhao, H. Yang, Q. Bao, Whole genomic DNA sequencing and comparative genomic analysis of Arthrospira platensis: high genome plasticity and genetic diversity, DNA Res. 23 (2016) 325-338. DOI : https://doi.org/10.1093/dnares/dsw023
[13] K. Adounkpe, P. Lawson-Evi, B. Bakoma, M. Gbéassor, Effect of Spirulina platensis powder on metabolic syndrome in sprague dawley rats, J. rech. sci. Univ. Lomé 17 (2015) 9-19
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[15] J. Zhishen, W. Jianming, La determinación del contenido de flavonoides en la morera y sus efectos depuradores sobre los radicales superóxidos, Food Chem. 64 (1999) 555-559. DOI : https://doi.org/10.1016/S0308-8146(98)00102-2
[16] R.B. Broadhurst, W.T. Jones, Analysis of condensed tannins using acidified vanillin, J. Sci. Food Agric. 29 (1978) 788-794
[17] S. Boussiba, A.E. Richmond, Isolation and characterization of phycocyanins from the blue-green alga Spirulina platensis, Arch. Microbiol. 120 (1979) 155-159. DOI : https://doi.org/10.1007/BF00409102
[18] W.T. Friedewald, R.I. Levy, D.S. Fredrickson, Estimation of the Concentration of Low-Density Lipoprotein Cholesterol in Plasma, Without Use of the Preparative Ultracentrifuge, Clin. Chem. 18 (1972) 499-502. DOI : https://doi.org/10.1093/clinchem/18.6.499
[19] I. Benzie, J. Strain, The ferric reducing ability of plasma as a measure of “antioxidant power”: The FRAP Assay, Analyt. Biochem. 239 (1996) 70-76. DOI : https://doi.org/10.1006/abio.1996.0292
[20] J. Sedlak, R.H. Lindsay, Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent, Anal. Biochem. 25 (1968) 192-205. DOI : https://doi.org/10.1016/0003-2697(68)90092-4
[21] A.K. Patlolla, C. Barnes, C. Yedjou, V. Velma, P.B. Tchounwou, Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague‐Dawley rats, Environ. Toxicol. 24 (2009) 66-73. DOI : https://doi.org/10.1002/tox.20395
[22] M.M. Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Analyt. Biochem. 72 (1976) 248-254. DOI : https://doi.org/10.1006/abio.1976.9999
[23] K. Shimada, K. Fujikawa, K. Yahara, T. Nakamura, Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion, J. Agric. Food Chem. 40 (1992) 945-948. DOI : https://doi.org/10.1021/jf00018a005
[24] H. Yaribeygi, F.R. Farrokhi, A.E. Butler, A. Sahebkar, Insulin resistance: Review of the underlying molecular mechanisms, J. Cell. Physiol. 234 (2019) 8152-8161. DOI : https://doi.org/10.1002/jcp.27603
[25] I. Zavaroni, S. Sander, S. Scott, G.M. Reaven, Effect of fructose feeding on insulin secretion and insulin action in the rat, Metabolism 29 (1980) 970-973. DOI : https://doi.org/10.1016/0026-0495(80)90041-4
[26] I.S. Hwang, H. Ho, B.B. Hoffman, G.M. Reaven, Fructose-induced insulin resistance and hypertension in rats, Hypertension 10 (1987) 512-516. DOI : https://doi.org/10.1161/01.hyp.10.5.512
[27] H. Basciano, L. Federico, K. Adeli, Fructose, insulin resistance, and metabolic dyslipidemia, Nutr. Metab. 2 (2005) 5. DOI : https://doi.org/10.1186/1743-7075-2-5
[28] W.C. Dornas, W.G. de Lima, M.L. Pedrosa, M.E. Silva, Health Implications of High-Fructose Intake and Current Research, Adv. Nutr., 6 (2015) 729-737. DOI : https://doi.org/10.3945/an.114.008144
[29] U. Jarouliya, Z.J. Anish, P. Kumar, P. Bisen, G. Prasad, Alleviation of metabolic abnormalities induced by excessive fructose administration in Wistar rats by Spirulina maxima, Indian J. Med. Res. 135 (2012) 422-428.
[30] W.G. Hozayen, A.M. Mahmoud, H.A. Soliman, S.R. Mostafa, Spirulina versicolor improves insulin sensitivity and attenuates hyperglycemia-mediated oxidative stress in fructose-fed rats, J. Intercult. Ethnopharmacol. 5 (2016) 57. DOI : https://doi.org/10.5455/jice.20151230055930
[31] M. Gargouri, H. Hamed, A. Akrouti, X. Dauvergne, C. Magné, A. El Feki, Effects of Spirulina platensis on lipid peroxidation, antioxidant defenses, and tissue damage in kidney of alloxan-induced diabetic rats, Appl Physiol Nutr Metab. 43 (2018) 345-354. DOI : https://doi.org/10.1139/apnm-2017-0461
[32] M.A. Herman, V.T. Samuel, The sweet path to metabolic demise: fructose and lipid synthesis, Trends Endocrinol. Metab. 27 (2016) 719-730. DOI : https://doi.org/10.1016/j.tem.2016.06.00
[33] C. Taghibiglou, A. Carpentier, S.C. Van Iderstine, B. Chen, D. Rudy, A. Aiton, G.F. Lewis, K. Adeli, Mechanisms of Hepatic Very Low Density Lipoprotein Overproduction in Insulin Resistance: evidence for enhanced lipoprotein assembly, reduced intracellular ApoB degradation, and increased microsomal triglyceride transfer protein in a fructose-fed hamster model, J. Biol. Chem. 275 (2000) 8416-8425. DOI : https://doi.org/10.1074/jbc.275.12.8416
[34] P.V. Torres-Duran, A. Ferreira-Hermosillo, M.A. Juarez-Oropeza, Antihyperlipemic and antihypertensive effects of Spirulina maxima in an open sample of Mexican population: a preliminary report, Lipids Health Dis. 6 (2007) 1-8. DOI : https://doi.org/10.1186/1476-511X-6-33
[35] S. Nagaoka, K. Shimizu, H. Kaneko, F. Shibayama, K. Morikawa, Y. Kanamaru, A. Otsuka, T. Hirahashi, T. Kato, A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats, J. Nutr. 135 (2005) 2425-2430. DOI : https://doi.org/10.1093/jn/135.10.2425
[36] O. Aissaoui, M. Amiali, N. Bouzid, K. Belkacemi, A. Bitam, Effect of Spirulina platensis ingestion on the abnormal biochemical and oxidative stress parameters in the pancreas and liver of alloxan-induced diabetic rats, Pharm. Biol. 55 (2017) 1304-1312. DOI : https://doi.org/10.1080/13880209.2017.1300820
[37] F. Nasirian, M. Dadkhah, N. Moradi-Kor, Z. Obeidavi, Effects of Spirulina platensis microalgae on antioxidant and anti-inflammatory factors in diabetic rats, Diabetes Metab. Syndr. Obes. 11 (2018) 375-380. DOI : https://doi.org/10.2147/DMSO.S172104
[38] U. Jarouliya, A. Zacharia, R.K. Keservani, G.B.K.S. Prasad, Spirulina maxima and its effect on antioxidant activity in fructose induced oxidative stress with histopathological observations, Eur. Pharm. J. 62 (2015) 13-19. DOI : https://doi.org/10.1515/afpuc-2015-0027
[39] J. Dupas, C. Goanvec, A. Feray, A. Guernec, C. Alain, F. Guerrero, J. Mansourati, Progressive Induction of Type 2 Diabetes: Effects of a Reality–Like Fructose Enriched Diet in Young Wistar Rats, PLoS One 11 (2016) e0146821. DOI : https://doi.org/10.1371/journal.pone.0146821
[40] M.G. Heo, S.Y. Choung , Anti-obesity effects of Spirulina maxima in high fat diet induced obese rats via the activation of AMPK pathway and SIRT1, Food Funct. (2018) 9(9) 4906-4915. DOI : DOI : https://doi.org/10.1039/C8FO00986D
[41] A.F.A. Diniz, B.F. de Oliveira Claudino, M.V. Duvirgens, P.P. da Silva Souza, P.B. Ferreira, F.F.L. Júnior, A.F. Alves, B.A. da Silva, Spirulina platensis Consumption Prevents Obesity and Improves the Deleterious Effects on Intestinal Reactivity in Rats Fed a Hypercaloric Diet, Oxid Med Cell Longev. (2021) 3260789. DOI: https://doi.org/10.1155/2021/3260789
[42] R.J. Johnson, M.S. Segal, Y. Sautin, T. Nakagawa, D.I. Feig, D.H. Kang, L.G. Sánchez-Lozada, Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease, Am. J. Clin. Nutr. 86 (2007) 899-906. DOI : https://doi.org/10.1093/ajcn/86.4.899
[43] M.A. Herman, V.T. Samuel, The sweet path to metabolic demise: Fructose and lipid synthesis, Trends Endrocrinol. Metab. 27 (2016) 719–730. DOI : https://doi.org/10.1016/j.tem.2016.06.005
[2] S.M Hoseini, K. Khosravi-Darani, M.R. Mozafari, Nutritional and medical applications of spirulina microalgae, Mini-Rev. Med. Chem. 13 (2013) 1231-1237. DOI: https://doi.org/10.2174/1389557511313080009
[3] M.C. Ruiz-Domínguez, M. Jáuregui, E. Medina, C. Jaime, P. Cerezal, Rapid green extractions of C-phycocyanin from Arthrospira maxima for functional applications, Appl. Sci. 9 (2019) 1987. DOI: https://doi.org/10.3390/app9101987
[4] U. Jarouliya, A. Zacharia, R.K. Keservani, G. Prasad, Spirulina maxima and its effect on antioxidant activity in fructose induced oxidative stress with histopathological observations, Acta Fac. Pharm. Univ. Comen. 62 (2015) 13-9. DOI: https://doi.org/10.1515/afpuc-2015-0027
[5] A. Parodi, A. Leip, I. De Boer, P. Slegers, F. Ziegler, E.H. Temme, M. Herrero, H. Tuomisto, H. Valin, C. Van Middelaar, The potential of future foods for sustainable and healthy diets, Nat. Sustain. 1 (2018) 782-789. DOI: https://doi.org/10.1038/s41893-018-0189-7
[6] M. Khan, J.C. Shobha, I.K. Mohan, M.U. Rao Naidu, A. Prayag, V.K. Kutala, Spirulina attenuates cyclosporine-induced nephrotoxicity in rats, J. Appl. Toxicol. 26 (2006) 444-451. DOI : https://doi.org/10.1002/jat.1159
[7] A. Karadeniz, M. Cemek, N. Simsek, The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats, Ecotoxicol. Environ. Saf. 72 (2009) 231-235. DOI : https://doi.org/10.1155/2013/742859
[8] M.M. Abdel-Daim, S.M. Abuzead, S.M. Halawa, Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats, PLoS One 8 (2013) e72991. DOI : https://doi.org/10.1371/journal.pone.0072991
[9] P. Parikh, U. Mani, U. Iyer, Role of Spirulina in the control of glycemia and lipidemia in type 2 diabetes mellitus, J. Med. Food 4 (2001) 193-199. DOI : https://doi.org/10.1089/10966200152744463
[10] R. Holman, R. Turner, Oral agents and insulin in the treatment of NIDDM, Textbook of Diabetes, Oxford: Blackwell 9 (1991) 467-469
[11] J.T. Manandhar Shrestha, H. Shrestha, M. Prajapati, A. Karkee, A. Maharjan, Adverse Effects of Oral Hypoglycemic Agents and Adherence to them among Patients with Type 2 Diabetes Mellitus in Nepal, J. Lumbini Med. Coll. 5 (2017) 34-40. DOI : https://doi.org/10.22502/jlmc.v5i1.126
[12] T. Xu, S. Qin, Y. Hu, Z. Song J. Ying, P. Li, W. Dong, F. Zhao, H. Yang, Q. Bao, Whole genomic DNA sequencing and comparative genomic analysis of Arthrospira platensis: high genome plasticity and genetic diversity, DNA Res. 23 (2016) 325-338. DOI : https://doi.org/10.1093/dnares/dsw023
[13] K. Adounkpe, P. Lawson-Evi, B. Bakoma, M. Gbéassor, Effect of Spirulina platensis powder on metabolic syndrome in sprague dawley rats, J. rech. sci. Univ. Lomé 17 (2015) 9-19
[14] K. Slinkard, V.L. Singleton, Total phenol analysis: automation and comparison with manual methods, Am. J. Enol. Vitic. 28 (1977) 49-55
[15] J. Zhishen, W. Jianming, La determinación del contenido de flavonoides en la morera y sus efectos depuradores sobre los radicales superóxidos, Food Chem. 64 (1999) 555-559. DOI : https://doi.org/10.1016/S0308-8146(98)00102-2
[16] R.B. Broadhurst, W.T. Jones, Analysis of condensed tannins using acidified vanillin, J. Sci. Food Agric. 29 (1978) 788-794
[17] S. Boussiba, A.E. Richmond, Isolation and characterization of phycocyanins from the blue-green alga Spirulina platensis, Arch. Microbiol. 120 (1979) 155-159. DOI : https://doi.org/10.1007/BF00409102
[18] W.T. Friedewald, R.I. Levy, D.S. Fredrickson, Estimation of the Concentration of Low-Density Lipoprotein Cholesterol in Plasma, Without Use of the Preparative Ultracentrifuge, Clin. Chem. 18 (1972) 499-502. DOI : https://doi.org/10.1093/clinchem/18.6.499
[19] I. Benzie, J. Strain, The ferric reducing ability of plasma as a measure of “antioxidant power”: The FRAP Assay, Analyt. Biochem. 239 (1996) 70-76. DOI : https://doi.org/10.1006/abio.1996.0292
[20] J. Sedlak, R.H. Lindsay, Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent, Anal. Biochem. 25 (1968) 192-205. DOI : https://doi.org/10.1016/0003-2697(68)90092-4
[21] A.K. Patlolla, C. Barnes, C. Yedjou, V. Velma, P.B. Tchounwou, Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague‐Dawley rats, Environ. Toxicol. 24 (2009) 66-73. DOI : https://doi.org/10.1002/tox.20395
[22] M.M. Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Analyt. Biochem. 72 (1976) 248-254. DOI : https://doi.org/10.1006/abio.1976.9999
[23] K. Shimada, K. Fujikawa, K. Yahara, T. Nakamura, Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion, J. Agric. Food Chem. 40 (1992) 945-948. DOI : https://doi.org/10.1021/jf00018a005
[24] H. Yaribeygi, F.R. Farrokhi, A.E. Butler, A. Sahebkar, Insulin resistance: Review of the underlying molecular mechanisms, J. Cell. Physiol. 234 (2019) 8152-8161. DOI : https://doi.org/10.1002/jcp.27603
[25] I. Zavaroni, S. Sander, S. Scott, G.M. Reaven, Effect of fructose feeding on insulin secretion and insulin action in the rat, Metabolism 29 (1980) 970-973. DOI : https://doi.org/10.1016/0026-0495(80)90041-4
[26] I.S. Hwang, H. Ho, B.B. Hoffman, G.M. Reaven, Fructose-induced insulin resistance and hypertension in rats, Hypertension 10 (1987) 512-516. DOI : https://doi.org/10.1161/01.hyp.10.5.512
[27] H. Basciano, L. Federico, K. Adeli, Fructose, insulin resistance, and metabolic dyslipidemia, Nutr. Metab. 2 (2005) 5. DOI : https://doi.org/10.1186/1743-7075-2-5
[28] W.C. Dornas, W.G. de Lima, M.L. Pedrosa, M.E. Silva, Health Implications of High-Fructose Intake and Current Research, Adv. Nutr., 6 (2015) 729-737. DOI : https://doi.org/10.3945/an.114.008144
[29] U. Jarouliya, Z.J. Anish, P. Kumar, P. Bisen, G. Prasad, Alleviation of metabolic abnormalities induced by excessive fructose administration in Wistar rats by Spirulina maxima, Indian J. Med. Res. 135 (2012) 422-428.
[30] W.G. Hozayen, A.M. Mahmoud, H.A. Soliman, S.R. Mostafa, Spirulina versicolor improves insulin sensitivity and attenuates hyperglycemia-mediated oxidative stress in fructose-fed rats, J. Intercult. Ethnopharmacol. 5 (2016) 57. DOI : https://doi.org/10.5455/jice.20151230055930
[31] M. Gargouri, H. Hamed, A. Akrouti, X. Dauvergne, C. Magné, A. El Feki, Effects of Spirulina platensis on lipid peroxidation, antioxidant defenses, and tissue damage in kidney of alloxan-induced diabetic rats, Appl Physiol Nutr Metab. 43 (2018) 345-354. DOI : https://doi.org/10.1139/apnm-2017-0461
[32] M.A. Herman, V.T. Samuel, The sweet path to metabolic demise: fructose and lipid synthesis, Trends Endocrinol. Metab. 27 (2016) 719-730. DOI : https://doi.org/10.1016/j.tem.2016.06.00
[33] C. Taghibiglou, A. Carpentier, S.C. Van Iderstine, B. Chen, D. Rudy, A. Aiton, G.F. Lewis, K. Adeli, Mechanisms of Hepatic Very Low Density Lipoprotein Overproduction in Insulin Resistance: evidence for enhanced lipoprotein assembly, reduced intracellular ApoB degradation, and increased microsomal triglyceride transfer protein in a fructose-fed hamster model, J. Biol. Chem. 275 (2000) 8416-8425. DOI : https://doi.org/10.1074/jbc.275.12.8416
[34] P.V. Torres-Duran, A. Ferreira-Hermosillo, M.A. Juarez-Oropeza, Antihyperlipemic and antihypertensive effects of Spirulina maxima in an open sample of Mexican population: a preliminary report, Lipids Health Dis. 6 (2007) 1-8. DOI : https://doi.org/10.1186/1476-511X-6-33
[35] S. Nagaoka, K. Shimizu, H. Kaneko, F. Shibayama, K. Morikawa, Y. Kanamaru, A. Otsuka, T. Hirahashi, T. Kato, A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats, J. Nutr. 135 (2005) 2425-2430. DOI : https://doi.org/10.1093/jn/135.10.2425
[36] O. Aissaoui, M. Amiali, N. Bouzid, K. Belkacemi, A. Bitam, Effect of Spirulina platensis ingestion on the abnormal biochemical and oxidative stress parameters in the pancreas and liver of alloxan-induced diabetic rats, Pharm. Biol. 55 (2017) 1304-1312. DOI : https://doi.org/10.1080/13880209.2017.1300820
[37] F. Nasirian, M. Dadkhah, N. Moradi-Kor, Z. Obeidavi, Effects of Spirulina platensis microalgae on antioxidant and anti-inflammatory factors in diabetic rats, Diabetes Metab. Syndr. Obes. 11 (2018) 375-380. DOI : https://doi.org/10.2147/DMSO.S172104
[38] U. Jarouliya, A. Zacharia, R.K. Keservani, G.B.K.S. Prasad, Spirulina maxima and its effect on antioxidant activity in fructose induced oxidative stress with histopathological observations, Eur. Pharm. J. 62 (2015) 13-19. DOI : https://doi.org/10.1515/afpuc-2015-0027
[39] J. Dupas, C. Goanvec, A. Feray, A. Guernec, C. Alain, F. Guerrero, J. Mansourati, Progressive Induction of Type 2 Diabetes: Effects of a Reality–Like Fructose Enriched Diet in Young Wistar Rats, PLoS One 11 (2016) e0146821. DOI : https://doi.org/10.1371/journal.pone.0146821
[40] M.G. Heo, S.Y. Choung , Anti-obesity effects of Spirulina maxima in high fat diet induced obese rats via the activation of AMPK pathway and SIRT1, Food Funct. (2018) 9(9) 4906-4915. DOI : DOI : https://doi.org/10.1039/C8FO00986D
[41] A.F.A. Diniz, B.F. de Oliveira Claudino, M.V. Duvirgens, P.P. da Silva Souza, P.B. Ferreira, F.F.L. Júnior, A.F. Alves, B.A. da Silva, Spirulina platensis Consumption Prevents Obesity and Improves the Deleterious Effects on Intestinal Reactivity in Rats Fed a Hypercaloric Diet, Oxid Med Cell Longev. (2021) 3260789. DOI: https://doi.org/10.1155/2021/3260789
[42] R.J. Johnson, M.S. Segal, Y. Sautin, T. Nakagawa, D.I. Feig, D.H. Kang, L.G. Sánchez-Lozada, Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease, Am. J. Clin. Nutr. 86 (2007) 899-906. DOI : https://doi.org/10.1093/ajcn/86.4.899
[43] M.A. Herman, V.T. Samuel, The sweet path to metabolic demise: Fructose and lipid synthesis, Trends Endrocrinol. Metab. 27 (2016) 719–730. DOI : https://doi.org/10.1016/j.tem.2016.06.005
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Kougblenou KR, Kantati Y, Dossou-Yovo K, Lawson-Evi P, Eklu-Gadegbeku K. Spirulina platensis improves insulin sensitivity and reduces hyperglycemia-mediated oxidative stress in fructose-fed rats. JDDT [Internet]. 15Sep.2023 [cited 2Oct.2023];13(9):78-0. Available from: https://jddtonline.info/index.php/jddt/article/view/6205
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