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Carmona Hernández, J. C., Ángel Isaza, J., Restrepo López, J. P., Narváez Solarte, W., & González Correa, C. H. (2022). Effect of the extract of Passiflora ligularis Juss 1805 (Malpighiales: Passifloraceae) as a reducing agent of chronic inflammation markers. Boletín Científico. Centro De Museos, 26(2), 53–64. https://doi.org/10.17151/bccm.2022.26.2.3
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Authors
Juan C. Carmona Hernández
Perfil Google Scholar
Jaime Ángel Isaza
Juan P. Restrepo López
William Narváez Solarte
Clara H. González Correa
Abstract
Objective: The objective of this study was to determine the effect of the supplementation with Passiflora ligularis (granadilla) extract on some low-grade chronic inflammation markers associated with overweight in a model of albino mice fed a high-fat diet. Materials and methods: thirty-six albino mice were used, distributed in an unrestrictedly random design in 3 treatments and 12 repetitions. The treatments represented a group with a control diet, a second
treatment with a high-fat diet, and a group that received high-fat food and supplementation with 3g/L of Passiflora ligularis extract in the drinking water. After 49 days, the variables food consumption, water consumption, and weight gain were evaluated, in addition to the serum concentration of the inflammation markers IL-6 and TNF-α. Results: Supplementation with Passiflora ligularis extract reduced (p <0.05) the weight gain of mice compared to animals that received the high-fat diet without supplementation. Serum levels of TNF-α on supplemented mice did not show differences with neither of both control groups while the amounts of IL-6 were not affected by the treatments. Conclusion: The concentration of 3g/L in the drinking water of the of Passiflora ligularis extract decreased the weight gain produced by the increase fat in diet and reduced the measurement of the serum inflammation marker TNF-α indicating a beneficial effect on the risk associated with chronic low-grade inflammation.
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References
Bak. M. J., Truong, V. L., Kang, H. S. & Jun, M. (2013). Jeong WS. Anti-inflammatory effect of procyanidins from wild grape (Vitis amurensis) seeds in LPS-induced RAW 264.7 cells. Oxidative Medicine and Cellular Longevity. https://doi.org/10.1155/2013/409321
Cao, Y. J., Zhang, Y. M., Qi, J. P., Liu, R., Zhang, H. & He, L. C. (2015). Ferulic acid inhibits H2O2-induced oxidative stress and inflammation in rat vascular smooth muscle cells via inhibition of the NADPH oxidase and NF-κB pathway. International immunopharmacology, 28(2): 1018-1025. https://doi.org/10.1016/j.intimp.2015.07.037
Carmona-Hernández, J. C., Ángel-Isaza, J., González-Correa, C. H. & Narváez-Solarte, W. (2017). Anti-inflammatory effects of flavonoids evaluated in murine models: a descriptive review. Animal Science Papers & Reports, 35(4).
Carmona-Hernández, J. C., Taborda-Ocampo, G., Valdez, J. C., Bolling, B. W. & González-Correa, C. H. (2019). polyphenol extracts from three colombian passifloras (passion fruits) prevent inflammation-induced barrier dysfunction of caco-2 cells. Molecules, 24(24). https://doi.org/10.3390/molecules24244614
Chaparro, D. C., Maldonado, M. E., Franco, M. C. & Urango, L. A. (2015). Nutritional and antioxidant characteristics of banana passion fruit (Passiflora mollisima Bailey). Biotecnología en el Sector Agropecuario y Agroindustrial, 13(1): 120-128. https://doi.org/10.17533/udea.penh.v16n2a07
Chen, N., Bezzina, R., Hinch, E., Lewandowski, P. A., Cameron-Smith, D., Mathai, M. L. & Weisinger, R. S. (2009). Green tea, black tea, and epigallocatechin modify body composition, improve glucose tolerance, and differentially alter metabolic gene expression in rats fed a high-fat diet. Nutrition Research, 29(11): 784-793. https://doi.org/10.1016/j.nutres.2009.10.003
DANE. (2016). Encuesta Nacional Agropecuaria ENA. Boletín Técnico. Comunicación informativa.
De Melo, T. S., Lima, P. R., Carvalho, K. M. M. B., Fontenele, T. M., Solon, F. R. N., Tomé, A. R. & De Queiroz, M. G. R. (2017). Ferulic acid lowers body weight and visceral fat accumulation via modulation of enzymatic, hormonal and inflammatory changes in a mouse model of high-fat diet-induced obesity. Brazilian Journal of Medical and Biological Research, 50(1). https://doi.org/10.1590/1414-431x20165630
Esser, N., Legrand-Poels, S., Piette, J., Scheen, A.J. & Paquot, N. (2014). Inflammation As A Link Between Obesity, Metabolic Syndrome and Type 2 Diabetes. Diabetes Research and Clinical Practice, 105(2): 141-150. https://doi.org/10.1016/j.diabres.2014.04.006
Faam, B., Zarkesh, M., Daneshpour, M. S., Azizi, F. & Hedayati, M. (2014). The association between inflammatory markers and obesity-related factors in Tehranian adults: Tehran lipid and glucose study. Iranian Journal of Basic Medical Sciences, 17(8): 577-82.
Hariri, N. & Thibault, L. (2010). High-fat diet-induced obesity in animal models. Nutrition Research Reviews, 23(2): 270-299.
https://doi.org/10.1017/S0954422410000168
He, X., Luan, F., Yang, Y., Wang, Z., Zhao, Z., Fang, J., ... & Li, Y. (2020). Passiflora edulis: an insight into current researches on phytochemistry and pharmacology. Frontiers in Pharmacology, 11, 617. https://doi.org/10.3389/fphar.2020.00617
Ibitoye, O. B. & Ajiboye, T. O. (2018). Dietary phenolic acids reverse insulin resistance, hyperglycaemia, dyslipidaemia, inflammation and oxidative stress in high-fructose diet-induced metabolic syndrome rats. Archives of Physiology and Biochemistry, 124(5), 410-417. https://doi.org/10.1080/13813455.2017.1415938
Kim, J. A., & Choi, K. M. (2020). Newly discovered adipokines: pathophysiological link between obesity and cardiometabolic disorders. Frontiers in Physiology, 11. https://doi.org/10.3389/fphys.2020.568800
Lu, C., Zhu, W., Shen, C. L. & Gao, W. (2012). Green tea polyphenols reduce body weight in rats by modulating obesity-related genes. PLoS ONE, 7(6). https://doi.org/10.1371/journal.pone.0038332
Mattila, P., Hellström, J. & Törrönen, R. (2006). Phenolic acids in berries, fruits, and beverages. Journal of Agricultural and Food Chemistry, 54(19): 7193-7199. https://doi.org/10.1021/jf0615247
Mattila, P., Pihlava, J. M., & Hellström, J., (2005). Contents of phenolic acids, alkyl-and alkenylresorcinols, and avenanthramides in commercial grain products. Journal of Agricultural and Food Chemistry, 53(21), 8290-8295. https://doi.org/10.1021/jf051437z
Nani, A., Murtaza, B., Khan, A. S., Khan, N. A., & Hichami, A. (2021). Antioxidant and Anti-Inflammatory Potential of Polyphenols Contained in Mediterranean Diet in Obesity: Molecular Mechanisms. Molecules, 26(4): 985. https://doi.org/10.3390/MOLECULES26040985
National Research Council. (2010). Guide for the Care and Use of Laboratory Animals. The National Academies Press.
Navarrete, S., Alarcón, M. & Palomo, I. (2015). Aqueous extract of tomato (Solanum lycopersicum L.) and ferulic acid reduce the expression of TNF-α and IL-1β in LPS- activated macrophages. Molecules, 20(8), 15319-15329. https://doi.org/10.3390/molecules200815319
Pan, M. H., Yang, G., Li, S., Li, M. Y., Tsai, M. L., Wu, J. C. & Lai, C. S. (2017). Combination of citrus polymethoxyflavones, green tea polyphenols, and Lychee extracts suppresses obesity and hepatic steatosis in high-fat diet induced obese mice. Molecular Nutrition and Food Research, 61(11): 1-29. https://doi.org/10.1002/mnfr.201601104
Peluso, I., Raguzzini, A. & Serafini, M. (2013). Effect of flavonoids on circulating levels of TNF-α and IL-6 in humans: A systematic review and meta-analysis. Molecular Nutrition and Food Research, 57(5): 784-801. https://doi.org/10.1002/mnfr.201200721
Rani, V., Deep, G., Singh, R. K., Palle, K. & Yadav, U. C. S. (2016). Oxidative stress and metabolic disorders: Pathogenesis and therapeutic strategies. Life Sciences, 148: 183-193. https://doi.org/10.1016/j.lfs.2016.02.002
Rivera, L., Morón, R., Sánchez, M., Zarzuelo, A. & Galisteo, M. (2008). Quercetin ameliorates metabolic syndrome and improves the inflammatory status in obese Zucker rats. Obesity, 16(9): 2081-2087. https://doi.org/10.1038/oby.2008.315
Romier, B., Van De Walle, J., During, A., Larondelle, Y. & Schneider, Y. J. (2008). Modulation of signalling nuclear factor-kB activation pathway by polyphenols in human intestinal Caco-2 cells. British Journal of Nutrition, 100(3): 542-551. https://doi.org/10.1017/S0007114508966666
Sabogal-Palma, A., Chávez-Marín, J., Oliveros-Gómez, D., Murillo-Perea, E. & Méndez-Arteaga, J. J. (2016). Funcionalidades Biológicas de Passiflora Maliformis del Sur Macizo Colombiano. Bioagro, 28(1): 3-12.
Sae-Tan, S., Grove, K. A., Kennett, M. J. & Lambert, J. D. (2011). (−)-Epigallocatechin-3- gallate increases the expression of genes related to fat oxidation in the skeletal muscle of high fat-fed mice. Food & Function, 2(2): 111. https://doi.org/10.1039/C0FO00155D
Senaphan, K., Kukongviriyapan, U., Sangartit, W., Pakdeechote, P., Pannangpetch, P., Prachaney, P. & Kukongviriyapan, V. (2015). Ferulic acid alleviates changes in a rat model of metabolic syndrome induced by high-carbohydrate, high-fat diet. Nutrients, 7(8): 6446-6464. https://doi.org/10.3390/nu7085283
Shishikura, Y., Khokhar, S. & Murray, B. S. (2006). Effects of tea polyphenols on emulsification of olive oil in a small intestine model system. Journal of Agricultural and Food Chemistry, 54(5): 1906-1913. https://doi.org/10.1021/jf051988p
Sun, C., Zhao, C., Guven, E. C., Paoli, P., Simal‐Gandara, J., Ramkumar, K. M., ... & Xiao, J. (2020). Dietary polyphenols as antidiabetic agents: Advances and opportunities. Food Frontiers, 1(1): 18-44. https://doi.org/10.1002/FFT2.15
Torres, A. (2012). Caracterización Física, Química y Compuestos Bioactivos de Pulpa Madura de Tomate de Árbol (Cyphomandra Betacea) (Cav.) Sendtn. Archivos Latinoamericanos de Nutrición, 62(4): 381-388.
Wang, J. Q., Li, J., Zou, Y. H., Cheng, W. M., Lu. C., Zhang, L., Ge, J. F., Huang, C., Jin, Y., Lv, X. W., Hu, C. M. & Liu, L. P. (2009). Preventive effects of total flavonoids of Litsea coreana leve on hepatic steatosis in rats fed with high fat diet. Journal of Ethnopharmacology, 121(1): 54-60. https://doi.org/10.1016/j.jep.2008.09.029
Wang, O., Liu, J., Cheng, Q., Guo, X., Wang, Y., Zhao, L., ... y Ji, B. (2015). Effects of ferulic acid and γ-oryzanol on high-fat and highfructose diet-induced metabolic syndrome in rats. PloS one, 10(2): e0118135. https://doi.org/10.1371/journal.pone.0118135
Xu, Y., Zhang, M., Wu, T., Dai, S., Xu, J. & Zhou, Z. (2015). The anti-obesity effect of green tea polysaccharides, polyphenols and caffeine in rats fed with a high-fat diet. Food Funct, 6(1): 296-303. https://doi.org/10.1039/C4FO00970C
Zapata, K., Cortes, F. B. & Rojano, B. A. (2013). Polifenoles y actividad antioxidante del fruto de guayaba agria (Psidium Araca). Información Tecnológica, 24(5): 103.112. http://dx.doi.org/10.4067/S0718-07642013000500012
Zatterale, F., Longo, M., Naderi, J., Raciti, G. A., Desiderio, A., Miele, C., & Beguinot, F. (2020). Chronic adipose tissue inflammation linking obesity to insulin resistance and type 2 diabetes. Frontiers in Physiology, 10, 1607. https://doi.org/10.3389/FPHYS.2019.01607
Zhang, H. & Tsao, R. (2016). Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Current Opinion in Food Science, 8: 33-42. https://doi.org/10.1016/j.cofs.2016.02.002
Zhao, Z. & Moghadasian, M. H. (2008). Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: A review. Food Chemistry, 109(4): 691-702. https://doi.org/10.1016/j.foodchem.2008.02.039
Cao, Y. J., Zhang, Y. M., Qi, J. P., Liu, R., Zhang, H. & He, L. C. (2015). Ferulic acid inhibits H2O2-induced oxidative stress and inflammation in rat vascular smooth muscle cells via inhibition of the NADPH oxidase and NF-κB pathway. International immunopharmacology, 28(2): 1018-1025. https://doi.org/10.1016/j.intimp.2015.07.037
Carmona-Hernández, J. C., Ángel-Isaza, J., González-Correa, C. H. & Narváez-Solarte, W. (2017). Anti-inflammatory effects of flavonoids evaluated in murine models: a descriptive review. Animal Science Papers & Reports, 35(4).
Carmona-Hernández, J. C., Taborda-Ocampo, G., Valdez, J. C., Bolling, B. W. & González-Correa, C. H. (2019). polyphenol extracts from three colombian passifloras (passion fruits) prevent inflammation-induced barrier dysfunction of caco-2 cells. Molecules, 24(24). https://doi.org/10.3390/molecules24244614
Chaparro, D. C., Maldonado, M. E., Franco, M. C. & Urango, L. A. (2015). Nutritional and antioxidant characteristics of banana passion fruit (Passiflora mollisima Bailey). Biotecnología en el Sector Agropecuario y Agroindustrial, 13(1): 120-128. https://doi.org/10.17533/udea.penh.v16n2a07
Chen, N., Bezzina, R., Hinch, E., Lewandowski, P. A., Cameron-Smith, D., Mathai, M. L. & Weisinger, R. S. (2009). Green tea, black tea, and epigallocatechin modify body composition, improve glucose tolerance, and differentially alter metabolic gene expression in rats fed a high-fat diet. Nutrition Research, 29(11): 784-793. https://doi.org/10.1016/j.nutres.2009.10.003
DANE. (2016). Encuesta Nacional Agropecuaria ENA. Boletín Técnico. Comunicación informativa.
De Melo, T. S., Lima, P. R., Carvalho, K. M. M. B., Fontenele, T. M., Solon, F. R. N., Tomé, A. R. & De Queiroz, M. G. R. (2017). Ferulic acid lowers body weight and visceral fat accumulation via modulation of enzymatic, hormonal and inflammatory changes in a mouse model of high-fat diet-induced obesity. Brazilian Journal of Medical and Biological Research, 50(1). https://doi.org/10.1590/1414-431x20165630
Esser, N., Legrand-Poels, S., Piette, J., Scheen, A.J. & Paquot, N. (2014). Inflammation As A Link Between Obesity, Metabolic Syndrome and Type 2 Diabetes. Diabetes Research and Clinical Practice, 105(2): 141-150. https://doi.org/10.1016/j.diabres.2014.04.006
Faam, B., Zarkesh, M., Daneshpour, M. S., Azizi, F. & Hedayati, M. (2014). The association between inflammatory markers and obesity-related factors in Tehranian adults: Tehran lipid and glucose study. Iranian Journal of Basic Medical Sciences, 17(8): 577-82.
Hariri, N. & Thibault, L. (2010). High-fat diet-induced obesity in animal models. Nutrition Research Reviews, 23(2): 270-299.
https://doi.org/10.1017/S0954422410000168
He, X., Luan, F., Yang, Y., Wang, Z., Zhao, Z., Fang, J., ... & Li, Y. (2020). Passiflora edulis: an insight into current researches on phytochemistry and pharmacology. Frontiers in Pharmacology, 11, 617. https://doi.org/10.3389/fphar.2020.00617
Ibitoye, O. B. & Ajiboye, T. O. (2018). Dietary phenolic acids reverse insulin resistance, hyperglycaemia, dyslipidaemia, inflammation and oxidative stress in high-fructose diet-induced metabolic syndrome rats. Archives of Physiology and Biochemistry, 124(5), 410-417. https://doi.org/10.1080/13813455.2017.1415938
Kim, J. A., & Choi, K. M. (2020). Newly discovered adipokines: pathophysiological link between obesity and cardiometabolic disorders. Frontiers in Physiology, 11. https://doi.org/10.3389/fphys.2020.568800
Lu, C., Zhu, W., Shen, C. L. & Gao, W. (2012). Green tea polyphenols reduce body weight in rats by modulating obesity-related genes. PLoS ONE, 7(6). https://doi.org/10.1371/journal.pone.0038332
Mattila, P., Hellström, J. & Törrönen, R. (2006). Phenolic acids in berries, fruits, and beverages. Journal of Agricultural and Food Chemistry, 54(19): 7193-7199. https://doi.org/10.1021/jf0615247
Mattila, P., Pihlava, J. M., & Hellström, J., (2005). Contents of phenolic acids, alkyl-and alkenylresorcinols, and avenanthramides in commercial grain products. Journal of Agricultural and Food Chemistry, 53(21), 8290-8295. https://doi.org/10.1021/jf051437z
Nani, A., Murtaza, B., Khan, A. S., Khan, N. A., & Hichami, A. (2021). Antioxidant and Anti-Inflammatory Potential of Polyphenols Contained in Mediterranean Diet in Obesity: Molecular Mechanisms. Molecules, 26(4): 985. https://doi.org/10.3390/MOLECULES26040985
National Research Council. (2010). Guide for the Care and Use of Laboratory Animals. The National Academies Press.
Navarrete, S., Alarcón, M. & Palomo, I. (2015). Aqueous extract of tomato (Solanum lycopersicum L.) and ferulic acid reduce the expression of TNF-α and IL-1β in LPS- activated macrophages. Molecules, 20(8), 15319-15329. https://doi.org/10.3390/molecules200815319
Pan, M. H., Yang, G., Li, S., Li, M. Y., Tsai, M. L., Wu, J. C. & Lai, C. S. (2017). Combination of citrus polymethoxyflavones, green tea polyphenols, and Lychee extracts suppresses obesity and hepatic steatosis in high-fat diet induced obese mice. Molecular Nutrition and Food Research, 61(11): 1-29. https://doi.org/10.1002/mnfr.201601104
Peluso, I., Raguzzini, A. & Serafini, M. (2013). Effect of flavonoids on circulating levels of TNF-α and IL-6 in humans: A systematic review and meta-analysis. Molecular Nutrition and Food Research, 57(5): 784-801. https://doi.org/10.1002/mnfr.201200721
Rani, V., Deep, G., Singh, R. K., Palle, K. & Yadav, U. C. S. (2016). Oxidative stress and metabolic disorders: Pathogenesis and therapeutic strategies. Life Sciences, 148: 183-193. https://doi.org/10.1016/j.lfs.2016.02.002
Rivera, L., Morón, R., Sánchez, M., Zarzuelo, A. & Galisteo, M. (2008). Quercetin ameliorates metabolic syndrome and improves the inflammatory status in obese Zucker rats. Obesity, 16(9): 2081-2087. https://doi.org/10.1038/oby.2008.315
Romier, B., Van De Walle, J., During, A., Larondelle, Y. & Schneider, Y. J. (2008). Modulation of signalling nuclear factor-kB activation pathway by polyphenols in human intestinal Caco-2 cells. British Journal of Nutrition, 100(3): 542-551. https://doi.org/10.1017/S0007114508966666
Sabogal-Palma, A., Chávez-Marín, J., Oliveros-Gómez, D., Murillo-Perea, E. & Méndez-Arteaga, J. J. (2016). Funcionalidades Biológicas de Passiflora Maliformis del Sur Macizo Colombiano. Bioagro, 28(1): 3-12.
Sae-Tan, S., Grove, K. A., Kennett, M. J. & Lambert, J. D. (2011). (−)-Epigallocatechin-3- gallate increases the expression of genes related to fat oxidation in the skeletal muscle of high fat-fed mice. Food & Function, 2(2): 111. https://doi.org/10.1039/C0FO00155D
Senaphan, K., Kukongviriyapan, U., Sangartit, W., Pakdeechote, P., Pannangpetch, P., Prachaney, P. & Kukongviriyapan, V. (2015). Ferulic acid alleviates changes in a rat model of metabolic syndrome induced by high-carbohydrate, high-fat diet. Nutrients, 7(8): 6446-6464. https://doi.org/10.3390/nu7085283
Shishikura, Y., Khokhar, S. & Murray, B. S. (2006). Effects of tea polyphenols on emulsification of olive oil in a small intestine model system. Journal of Agricultural and Food Chemistry, 54(5): 1906-1913. https://doi.org/10.1021/jf051988p
Sun, C., Zhao, C., Guven, E. C., Paoli, P., Simal‐Gandara, J., Ramkumar, K. M., ... & Xiao, J. (2020). Dietary polyphenols as antidiabetic agents: Advances and opportunities. Food Frontiers, 1(1): 18-44. https://doi.org/10.1002/FFT2.15
Torres, A. (2012). Caracterización Física, Química y Compuestos Bioactivos de Pulpa Madura de Tomate de Árbol (Cyphomandra Betacea) (Cav.) Sendtn. Archivos Latinoamericanos de Nutrición, 62(4): 381-388.
Wang, J. Q., Li, J., Zou, Y. H., Cheng, W. M., Lu. C., Zhang, L., Ge, J. F., Huang, C., Jin, Y., Lv, X. W., Hu, C. M. & Liu, L. P. (2009). Preventive effects of total flavonoids of Litsea coreana leve on hepatic steatosis in rats fed with high fat diet. Journal of Ethnopharmacology, 121(1): 54-60. https://doi.org/10.1016/j.jep.2008.09.029
Wang, O., Liu, J., Cheng, Q., Guo, X., Wang, Y., Zhao, L., ... y Ji, B. (2015). Effects of ferulic acid and γ-oryzanol on high-fat and highfructose diet-induced metabolic syndrome in rats. PloS one, 10(2): e0118135. https://doi.org/10.1371/journal.pone.0118135
Xu, Y., Zhang, M., Wu, T., Dai, S., Xu, J. & Zhou, Z. (2015). The anti-obesity effect of green tea polysaccharides, polyphenols and caffeine in rats fed with a high-fat diet. Food Funct, 6(1): 296-303. https://doi.org/10.1039/C4FO00970C
Zapata, K., Cortes, F. B. & Rojano, B. A. (2013). Polifenoles y actividad antioxidante del fruto de guayaba agria (Psidium Araca). Información Tecnológica, 24(5): 103.112. http://dx.doi.org/10.4067/S0718-07642013000500012
Zatterale, F., Longo, M., Naderi, J., Raciti, G. A., Desiderio, A., Miele, C., & Beguinot, F. (2020). Chronic adipose tissue inflammation linking obesity to insulin resistance and type 2 diabetes. Frontiers in Physiology, 10, 1607. https://doi.org/10.3389/FPHYS.2019.01607
Zhang, H. & Tsao, R. (2016). Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Current Opinion in Food Science, 8: 33-42. https://doi.org/10.1016/j.cofs.2016.02.002
Zhao, Z. & Moghadasian, M. H. (2008). Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: A review. Food Chemistry, 109(4): 691-702. https://doi.org/10.1016/j.foodchem.2008.02.039
