Effect of Sechium edule var. nigrum spinosum (Chayote) on Oxidative Stress and Pro-Inflammatory Markers in Older Adults with Metabolic Syndrome: An Exploratory Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Design and Subjects
2.2. Anthropometric Measurements
2.3. Blood Pressure
2.4. Blood Sampling and Biochemical Analyses
2.5. Plasma Thiobarbituric Acid Reactive Substances (TBARS)
2.6. Plasma Total Antioxidant Status
2.7. Red Blood Cell Superoxide Dismutase
2.8. Red Blood Cell Glutathione Peroxidase
2.9. Oxidative Stress Score
2.10. Inflammatory Cytokines and C-Reactive Protein (CRP)
2.11. Treatment
3. Statistical Analysis
4. Results
5. Discussion
6. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Han, T.S.; Lean, M.E. A clinical perspective of obesity, metabolic syndrome and cardiovascular disease. JRSM Cardiovasc. Dis. 2016, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Samson, S.L.; Garber, A.J. Metabolic syndrome. Endocrinol. Metab. Clin. N. Am. 2014, 43, 1–23. [Google Scholar] [CrossRef] [PubMed]
- Sherling, D.H.; Perumareddi, P.; Hennekens, C.H. Metabolic syndrome. J. Cardiovasc. Pharmacol. Ther. 2017, 22, 365–367. [Google Scholar] [CrossRef] [PubMed]
- Yaffe, K.; Haan, M.; Blackwell, T.; Cherkasova, E.; Whitmer, R.A.; West, N. Metabolic syndrome and cognitive decline in elderly Latinos: Findings from the Sacramento Area Latino Study of Aging study. J. Am. Geriatr. Soc. 2007, 55, 758–762. [Google Scholar] [CrossRef] [PubMed]
- Feinkohl, I.; Janke, J.; Hadzidiakos, D.; Slooter, A.; Winterer, G.; Spies, C.; Pischon, T. Associations of the metabolic syndrome and its components with cognitive impairment in older adults. BMC Geriatr. 2019, 19, 77. [Google Scholar] [CrossRef] [PubMed]
- Dommermuth, R.; Ewing, K. Metabolic syndrome: Systems thinking in heart disease. Prim. Care 2018, 45, 109–129. [Google Scholar] [CrossRef]
- Eckel, R.H.; Alberti, K.G.; Grundy, S.M.; Zimmet, P.Z. The metabolic syndrome. Lancet 2010, 375, 181–183. [Google Scholar] [CrossRef]
- McCracken, E.; Monaghan, M.; Sreenivasan, S. Pathophysiology of the metabolic syndrome. Clin. Dermatol. 2018, 36, 14–20. [Google Scholar] [CrossRef]
- Furukawa, S.; Fujita, T.; Shimabukuro, M.; Iwaki, M.; Yamada, Y.; Nakajima, Y.; Nakayama, O.; Makishima, M.; Matsuda, M.; Shimomura, I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Investig. 2004, 114, 1752–1761. [Google Scholar] [CrossRef]
- Holvoet, P. Relations between metabolic syndrome, oxidative stress and inflammation and cardiovascular disease. Verh K Acad. Geneeskd. Belg. 2008, 70, 193–219. [Google Scholar]
- Mopuri, R.; Islam, M.S. Medicinal plants and phytochemicals with anti-obesogenic potentials: A review. Biomed. Pharmacother. 2017, 89, 1442–1452. [Google Scholar] [CrossRef] [PubMed]
- Agbabiaka, T.; Wider, B.; Watson, L.K.; Goodman, C. Concurrent use of prescription drugs and herbal medicinal products in older adults: A systematic review. Drugs Aging 2017, 34, s40017–s40266. [Google Scholar] [CrossRef] [PubMed]
- Cadena-Iñiguez, J.; Arévalo-Galarza, L.; Avendaño-Arrazate, C.H.; Soto-Hernández, M.; Ruiz-Posadas, L.M.; Santiago-Osorio, E.; Acosta-Ramos, M.; Cisneros-Solano, V.M.; Aguirre-Medina, J.F.; Ochoa-Martinez, D. Production, genetics, postharvest management and pharmacological characteristics of Sechium edule (Jacq.) Sw. Fresh Prod. 2007, 1, 41–53. [Google Scholar]
- Newstrom, L.E. Evidence for the origin of chayote, Sechium edule (Cucurbitaceae). Econ. Botan. 1991, 45, 410–428. [Google Scholar] [CrossRef]
- Siciliano, T.; De Tommasi, N.; Morelli, I.; Braca, A. Study of flavonoids of Sechium edule (Jacq) Swartz (Cucurbitaceae) different edible organs by liquid chromatography photodiode array mass spectrometry. J. Agric. Food Chem. 2004, 52, 6510–6515. [Google Scholar] [CrossRef]
- Dhiman, K.; Gupta, A.; Sharma, D.K.; Gil, N.S.; Goyal, A. A review on the medicinally important plants of the family Cucurbitaceae. Asian. J. Clin. Nutr. 2012, 4, 16–26. [Google Scholar] [CrossRef]
- Sulaiman, S.F.; Ooi, K.L.; Supriatno. Antioxidant and α-glucosidase inhibitory activities of cucurbit fruit vegetables and identification of active and major constituents from phenolic-rich extracts of Lagenaria siceraria and Sechium edule. J. Agric. Food Chem. 2013, 61, 10080–10090. [Google Scholar] [CrossRef]
- Rosado-Pérez, J.; Aguiñiga-Sánchez, I.; Arista-Ugalde, T.L.; Santiago-Osorio, E.; Mendoza-Núñez, V.M. The biological significance of oxidative stress, effects of fruits as natural edible antioxidants. Curr. Pharm. Des. 2018, 24, 4807–4824. [Google Scholar] [CrossRef]
- Vieira, E.F.; Pinho, O.; Ferreira, I.M.P.L.V.O.; Delerue-Matos, C. Chayote (Sechium edule): A review of nutritional composition, bioactivities and potential applications. Food Chem. 2019, 275, 557–568. [Google Scholar] [CrossRef]
- Expert Panel on Detection. Evaluation, and treatment of high blood cholesterol in adults. Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel detection, evaluation, and treatment of high blood cholesterol adults (Adult Treatment Panel III). J. Am. Med. Assoc. 2001, 285, 2486e–2497e. [Google Scholar]
- Mendoza-Núñez, V.M.; Arista-Ugalde, T.L.; Rosado-Pérez, J.; Ruiz-Ramos, M.; Santiago-Osorio, E. Hypoglycemic and antioxidant effect of Tai chi exercise training in older adults with metabolic syndrome. Clin. Interv. Aging 2018, 13, 523–531. [Google Scholar] [CrossRef]
- Secretaría de Salud. Norma Oficial Mexicana NOM-030-SSA-1999, para la Prevención, Tratamiento y Control de la Hipertensión Arterial; Secretaría de Salud: Mexico City, Mexico, 1999.
- Jentzsch, A.M.; Bachmann, H.; Fürst, P.; Biesalski, H.K. Improved analysis of malondialdehyde in human body fluids. Free Radic. Biol. Med. 1996, 20, 251–256. [Google Scholar] [CrossRef]
- Miller, N.J. Nonvitamin plasma antioxidants. In Free Radical and Antioxidant Protocols; Armstrong, D., Ed.; Humana Press: Totowa, NJ, USA, 1998; pp. 285–297. [Google Scholar]
- Sánchez-Rodríguez, M.A.; Ruiz-Ramos, M.; Mendoza-Núñez, V.M. Proposal of a construct to measure severity of oxidative stress. Free Radic. Biol. Med. 2006, 41, S29. [Google Scholar]
- Salazar-Aguilar, S.; Ruiz-Posadas, L.D.M.; Cadena-Iñiguez, J.; Soto-Hernández, M.; Santiago-Osorio, E.; Aguiñiga-Sánchez, I.; Rivera-Martínez, A.R.; Aguirre-Medina, J.F. Sechium edule (Jacq.) Swartz, a New Cultivar with Antiproliferative Potential in a Human Cervical Cancer HeLa Cell Line. Nutrients 2017, 9, 798. [Google Scholar] [CrossRef] [PubMed]
- St Sauver, J.L.; Boyd, C.M.; Grossardt, B.R.; Bobo, W.V.; Finney Rutten, L.J.; Roger, V.L.; Ebbert, J.O.; Therneau, T.M.; Yawn, B.P.; Rocca, W.A. Risk of developing multimorbidity across all ages in an historical cohort study: Differences by sex and ethnicity. BMJ Open 2015, 5, e006413. [Google Scholar] [CrossRef]
- Forti, P.; Pirazzoli, G.L.; Maltoni, B.; Bianchi, G.; Magalotti, D.; Muscari, A.; Mariani, E.; Ravaglia, G.; Zoli, M. Metabolic syndrome and all-cause mortality in older men and women. Eur. J. Clin. Investig. 2012, 42, 1000–1009. [Google Scholar] [CrossRef]
- Koskinen, J.; Kahonen, M.; Viikari, J.S.; Taittonen, L.; Laitinen, T.; Rönnemaa, T.; Lehtimäki, T.; Hutri-Kähönen, N.; Pietikäinen, M.; Jokinen, E.; et al. Conventional cardiovascular risk factors and metabolic syndrome in predicting carotid intima-media thickness progression in young adults: The cardiovascular risk in young Finns study. Circulation 2009, 120, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Ford, E.S.; Li, C.; Sattar, N. Metabolic syndrome and incident diabetes: Current state of the evidence. Diabetes Care 2008, 31, 1898–1904. [Google Scholar] [CrossRef]
- Tiwari, A.K.; Anusha, I.; Sumangali, M.; Kumar, D.A.; Madhusudana, K.; Agawane, S.B. Preventive and therapeutic efficacies of Benincasa hispida and Sechium edule fruit’s juice on sweet-beverages induced impaired glucose tolerance and oxidative stress. Pharmacologia 2013, 4, 197–207. [Google Scholar] [CrossRef]
- Hii, C.S.T.; Howell, S.L. Effects of flavonoids on insulin secretion and 45Ca2+ handling in rat islets of Langerhans. J. Endocrinol. 1985, 107, 1–8. [Google Scholar] [CrossRef]
- Yang, M.Y.; Chan, K.C.; Lee, Y.J. Sechium edule shoot extracts and active components improve obesity and a fatty liver that involved reducing hepatic lipogenesis and adipogenesis in high-fat-diet-fed rats. J. Agric. Food Chem. 2015, 63, 4587–4596. [Google Scholar] [CrossRef]
- Wu, C.H.; Ou, T.T.; Chang, C.H.; Chang, X.Z.; Yang, M.Y.; Wang, C.J. The polyphenol extract from Sechium edule shoots inhibits lipogenesis and stimulates lipolysis via activation of AMPK signals in HepG2 cells. J. Agric. Food Chem. 2014, 62, 750–759. [Google Scholar] [CrossRef]
- Firdous, S.M.; Shounak, P.; Bag, A.K. Effect of Sechium edule on chemical induced kidney damage in experimental animals. Bangladesh J. Pharmacol. 2013, 8, 28–35. [Google Scholar] [CrossRef]
- Trujillo, J.; Chirino, Y.I.; Martínez-Tagueña, N.; Pedraza-Chaverri, J. Renal damage in the metabolic syndrome (MetSx): Disorders implicated. Eur. J. Pharmacol. 2017, 818, 554–568. [Google Scholar] [CrossRef]
- La Russa, D.; Brunelli, E.; Pellegrino, D. Oxidative imbalance and kidney damage in spontaneously hypertensive rats: Activation of extrinsic apoptotic pathways. Clin. Sci. (Lond.) 2017, 131, 1419–1428. [Google Scholar] [CrossRef]
- La Russa, D.; Giordano, F.; Marrone, A.; Parafati, M.; Janda, E.; Pellegrino, D. Oxidative Imbalance and Kidney Damage in Cafeteria Diet-Induced Rat Model of Metabolic Syndrome: Effect of Bergamot Polyphenolic Fraction. Antioxidants 2019, 8, 66. [Google Scholar] [CrossRef]
- Firdous, S.; Sravanthi, K.; Debnath, R.; Neeraja, K. Protective effect of ethanolic extract and its ethylacetate and n-butanol fractions of Sechium edule fruits against carbon tetrachloride induced hepatic injury in rats. Int. J. Pharm. Pharm. Sci. 2012, 4, 354–359. [Google Scholar]
- Firdous, S.; Sravanthi, K.; Debnath, R.; Neeraja, K. Protective effect of ethanolic extract and its ethylacetate and n-butanol fractions of Sechium edule fruits against paracetamol induced hepatic injury in mice. Asian J. Pharm. Clin. Res. 2012, 5, 10–14. [Google Scholar]
- Scevola, D.; Bacbacini, G.; Grosso, A.; Bona, S.; Perissoud, D. Flavonoids and hepatic cyclic monophasphates in liver injury. Boll. dell’Istituto Sieroter. Milan. 1984, 63, 77–82. [Google Scholar]
- Raja, K.S.; Mohd, R.E.S.; Abdul, N.N.A.; Ismail, N.H.M.; Mohd, F.N.A. Preventive Effect of Naringin on Metabolic Syndrome and Its Mechanism of Action: A Systematic Review. Evid. Based Complement Altern. Med. 2019, 2019, 9752826. [Google Scholar] [CrossRef]
- Parafati, M.; Lascala, A.; La Russa, D.; Mignogna, C.; Trimboli, F.; Morittu, V.M.; Riillo, C.; Macirella, R.; Mollace, V.; Brunelli, E.; et al. Bergamot Polyphenols Boost Therapeutic Effects of the Diet on Non-Alcoholic Steatohepatitis (NASH) Induced by “Junk Food”: Evidence for Anti-Inflammatory Activity. Nutrients 2018, 10, 1604. [Google Scholar] [CrossRef] [PubMed]
- Parafati, M.; Lascala, A.; Morittu, V.M.; Trimboli, F.; Rizzuto, A.; Brunelli, E.; Coscarelli, F.; Costa, N.; Britti, D.; Ehrlich, J.; et al. Bergamot polyphenol fraction prevents nonalcoholic fatty liver disease via stimulation of lipophagy in cafeteria diet-induced rat model of metabolic syndrome. J. Nutr. Biochem. 2015, 26, 938–948. [Google Scholar] [CrossRef] [PubMed]
- Aguiñiga-Sánchez, I.; Cadena-Iñiguez, J.; Santiago-Osorio, E.; Gómez-García, G.; Mendoza-Núñez, V.M.; Rosado-Pérez, J.; Ruíz-Ramos, M.; Cisneros-Solano, V.M.; Ledesma-Martínez, E.; Delgado-Bordonave, A.J.; et al. Chemical analyses and in vitro and in vivo toxicity of fruit methanol extract of Sechium edule var. nigrum spinosum. Pharm. Biol. 2017, 55, 1638–1645. [Google Scholar] [CrossRef] [PubMed]
- Maatouk, M.; Elgueder, D.; Mustapha, N.; Chaaban, H.; Bzéouich, I.M.; Loannou, I.; Kilani, S.; Ghoul, M.; Ghedira, K.; Chekir-Ghedira, L. Effect of heated naringeninon immunomodulatory properties and cellular antioxidant activity. Cell Stress Chaperones 2016, 21, 1101–1109. [Google Scholar] [CrossRef] [PubMed]
- Heim, K.E.; Tagliaferro, A.R.; Bobilya, D.J. Flavonoid antioxidants: Chemistry, metabolism and structure-activity relationships. J. Nutr. Biochem. 2002, 13, 572–584. [Google Scholar] [CrossRef]
- Rice-Evans, C.A.; Miller, N.J.; Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 1996, 20, 933–956. [Google Scholar] [CrossRef]
- Kaneko, T.; Kaji, K.; Matsuo, M. Protection of linoleic acid hydroperoxide- induced cytotoxicity by phenolic antioxidants. Free Radic. Biol. Med. 1994, 16, 405–409. [Google Scholar] [CrossRef]
- Shakeel, S.; Rehman, M.U.; Tabassum, N.; Amin, U.M.; Mir, R. Effect of Naringenin (a naturally occurring flavanone) against pilocarpine- induced status epilepticus and oxidative stress in mice. Pharmacogn. Mag. 2017, 13, S154–S160. [Google Scholar] [PubMed]
- Dong, D.; Xu, L.; Yin, L.; Qi, Y.; Peng, J. Naringenin prevents carbon tetrachloride-induced acute liver injury in mice. J. Funct. Foods 2015, 12, 179–191. [Google Scholar] [CrossRef]
- Lou, H.; Jing, X.; Wei, X.; Shi, H.; Ren, D.; Zhang, X. Naringenin protects against 6-OHDA-induced neurotoxicity via activation of the Nrf2/ARE signaling pathway. Neuropharmacology 2014, 79, 380–388. [Google Scholar] [CrossRef] [PubMed]
- Han, X.; Pan, J.; Ren, D.; Cheng, Y.; Fan, P.; Lou, H. Naringenin-7-Oglucoside protects against doxorubicin-induced toxicity in H9c2 cardiomyocytes by induction of endogenous antioxidant enzymes. Food Chem. Toxicol. 2008, 46, 3140–3146. [Google Scholar] [CrossRef]
- Yu, J.; Bi, X.; Yu, B.; Chen, D. Isoflavones: Anti-Inflammatory benefit and possible caveats. Nutrients 2016, 10, 361. [Google Scholar] [CrossRef] [PubMed]
- Yahfoufi, N.; Alsadi, N.; Jambi, M.; Matar, C. The Immunomodulatory and Anti-Inflammatory role of polyphenols. Nutrients 2018, 2, 1618. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Cano, F.J.; Castell, M. Flavonoids, inflammation and immune system. Nutrients 2016, 8, 659. [Google Scholar]
- Rakhshandehroo, M.; Knoch, B.; Müller, M.; Kersten, S. Peroxisome proliferator-activated receptor alpha target genes. PPAR Res. 2010, 2010, 612089. [Google Scholar] [CrossRef] [PubMed]
- Esmaeili, M.A.; Alilou, M. Naringenin attenuates CCl4 -induced hepatic inflammation by the activation of an Nrf2-mediated pathway in rats. Clin. Exp. Pharmacol. Physiol. 2014, 41, 416–422. [Google Scholar] [CrossRef] [PubMed]
- Martinez, R.M.; Pinho-Ribeiro, F.A.; Steffen, V.S.; Silva, T.C.; Caviglione, C.V.; Bottura, C.; Fonseca, M.J.; Vicentini, F.T.; Vignoli, J.A.; Baracat, M.M.; et al. Topical formulation containing naringenin: Efficacy against ultraviolet B irradiation-induced skin inflammation and oxidative stress in mice. PLoS ONE 2016, 11, e0146296. [Google Scholar] [CrossRef]
Parameter | Baseline | Post-Treatment |
---|---|---|
BMI | 29.3 ± 4.4 | 29.4 ± 4.4 |
SBP (mmHg) | 127 ± 12 | 127 ± 16 |
DBP (mmHg) | 82 ± 7 | 81 ± 9 |
Circumference of the waist (cm) | 99.5 ± 9 | 99 ± 7 |
Parameter | Baseline | Post-Treatment |
---|---|---|
Glucose (mg/dL) | 107 ± 38 | 95 ± 5 |
Total Cholesterol (mg/dL) | 204 ± 34 | 200 ± 28 |
Triglycerides (mg/dL) | 170 ± 76 | 153 ± 66 |
HDL-C (mg/dL) | 49 ± 7 | 50 ± 9 |
Uricacid (mg/dL) | 5.1 ± 1.2 | 4.2 ± 1.2 * |
Urea (mg/dL) | 38 ± 22 | 35 ± 18 |
Creatinine (mg/dL) | 1.1 ± 0.26 | 0.85 ± 0.2 * |
Albumin (mg/dL) | 4.2 ± 0.2 | 4.2 ± 0.15 |
AST (U/L) | 30.9 ± 11 | 24.8 ± 10 * |
ALT (U/L) | 36 ± 18 | 28 ± 12 * |
Total Bilirubin (mg/dL) | 0.61 ± 0.27 | 0.62 ± 0.22 |
Direct Bilirubin (mg/dL) | 0.22 ± 0.098 | 0.26 ± 0.08 |
HbA1c (%) | 5.9 ± 2.7 | 6.0 ± 2.7 |
Parameter | Baseline | Post-Treatment |
---|---|---|
Lipoperoxides (µmol/L) | 0.289 ± 0.04 | 0.234 ± 0.06 * |
SOD (U/mL) | 190 ± 3.4 | 190 ± 8 |
GPx (U/L) | 7542 ± 2651 | 8113 ± 3477 |
TAS (mmol/L) | 0.97 ± 0.18 | 1.2 ± 0.12 * |
SOD/GPx | 0.27 ± 0.013 | 0.28 ± 0.011 |
AOGAP (µmol/L) | 188 ± 258 | 497 ± 83 * |
OxS-Score | 1.7 ± 0.78 | 0.75 ± 0.87 * |
Parameter | Baseline | Post-Treatment |
---|---|---|
IL-12p70 (pg/dL) | 1.8 ± 0.9 | 1.2 ± 1.1 |
TNF-α (pg/dL) | 5.3 ± 1.4 | 3.5 ± 1.3 * |
IL-10 (pg/dL) | 1.7 ± 0.65 | 1.3 ± 0.86 |
IL-6 (pg/dL) | 4.2 ± 0.8 | 3.3 ± 1.6 |
IL-1β (pg/dL) | 8.5 ± 1.4 | 9.5 ± 2.7 |
IL-8 (pg/dL) | 11.5 ± 3.9 | 11.8 ± 3.6 |
CRP (mg/dL) | 0.36 ± 0.31 | 0.30 ± 0.32 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rosado-Pérez, J.; Aguiñiga-Sánchez, I.; Santiago-Osorio, E.; Mendoza-Núñez, V.M. Effect of Sechium edule var. nigrum spinosum (Chayote) on Oxidative Stress and Pro-Inflammatory Markers in Older Adults with Metabolic Syndrome: An Exploratory Study. Antioxidants 2019, 8, 146. https://doi.org/10.3390/antiox8050146
Rosado-Pérez J, Aguiñiga-Sánchez I, Santiago-Osorio E, Mendoza-Núñez VM. Effect of Sechium edule var. nigrum spinosum (Chayote) on Oxidative Stress and Pro-Inflammatory Markers in Older Adults with Metabolic Syndrome: An Exploratory Study. Antioxidants. 2019; 8(5):146. https://doi.org/10.3390/antiox8050146
Chicago/Turabian StyleRosado-Pérez, Juana, Itzen Aguiñiga-Sánchez, Edelmiro Santiago-Osorio, and Víctor Manuel Mendoza-Núñez. 2019. "Effect of Sechium edule var. nigrum spinosum (Chayote) on Oxidative Stress and Pro-Inflammatory Markers in Older Adults with Metabolic Syndrome: An Exploratory Study" Antioxidants 8, no. 5: 146. https://doi.org/10.3390/antiox8050146
APA StyleRosado-Pérez, J., Aguiñiga-Sánchez, I., Santiago-Osorio, E., & Mendoza-Núñez, V. M. (2019). Effect of Sechium edule var. nigrum spinosum (Chayote) on Oxidative Stress and Pro-Inflammatory Markers in Older Adults with Metabolic Syndrome: An Exploratory Study. Antioxidants, 8(5), 146. https://doi.org/10.3390/antiox8050146