Euterpe Oleracea Martius (Açaí) Extract and Resistance Exercise Modulate Cardiac Parameters of Hypertensive Rats
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Acquisition, Preparation, and Administration of Açai Pulp
2.3. Centesimal Composition of Açai
2.4. Antioxidant Capacity
2.5. Systolic Blood Pressure
2.6. Physical Test and Resistance Exercise Training Protocol
2.7. Echocardiographic Analysis
2.8. Histological Analysis of the Heart
2.9. Analysis of Oxidative Stress
2.10. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Meissner, A. Hypertension and the Brain: A Risk Factor for More Than Heart Disease. Cerebrovasc. Dis. 2016, 42, 255–262. [Google Scholar] [CrossRef]
- Whelton, P.K.; Carey, R.M.; Aronow, W.S.; Casey, D.E., Jr.; Collins, K.J.; Dennison Himmelfarb, C.; DePalma, S.M.; Gidding, S.; Jamerson, K.A.; Jones, D.W.; et al. 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for the Prevention, Detection, Evaluation, and Management of High Blood Pressure in Adults: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Hypertension 2018, 71, e13–e115. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.; Hu, G.; Qiu, J.; Miura, T.; Yamakoshi, S.; Namai-Takahashi, A.; Kohzuki, M.; Ito, O. Exercise Training Prevents High Fructose-Induced Hypertension and Renal Damages in Male Dahl Salt-Sensitive Rats. Med. Sci. Sports Exerc. 2023, 55, 803–812. [Google Scholar] [CrossRef]
- Okamoto, K.; Aoki, K. Development of a strain of spontaneously hypertensive rats. Jpn. Circ. J. 1963, 27, 282–293. [Google Scholar] [CrossRef]
- Silva, A.K.N.; Beckman, J.C.; Rodrigues, A.M.C.; Silva, L.H.M. Avaliação da composição nutricional e capacidade antioxidante de compostos bioativos da polpa de açaí. Rev. Bras. Tecnol. Agroind. 2017, 11, 11. [Google Scholar]
- Oliveira, A.G.; Costa, M.C.D.; Rocha, S.M.B.M. Benefícios funcionais do açaí na prevenção das doenças cardiovasculares. J. Amaz. Health Sci. 2015, 1, 1–10. [Google Scholar]
- Rosner, W.M.; Liberali, R.; Navarro, F. Os efeitos do treinamento de força para hipertensos: Revisão. Rev. Bras. Prescrição Fisiol. Exerc. 2020, 14, 7. [Google Scholar]
- Tan, Z.; Zhao, Y.; Zheng, Y.; Pan, Y. The Effect of Blood Flow-Restricted Low Resistance Training on Microvascular Circulation of Myocardium in Spontaneously Hypertensive Rats. Front. Physiol. 2022, 13, 829718. [Google Scholar] [CrossRef]
- Miguel-dos-Santos, R.; Santos, J.F.D.; Macedo, F.N.; Marçal, A.C.; Santana Filho, V.J.; Wichi, R.B.; Lauton-Santos, S. Strength Training Reduces Cardiac and Renal Oxidative Stress in Rats with Renovascular Hypertension. Arq. Bras. Cardiol. 2021, 116, 4–11. [Google Scholar] [CrossRef]
- da Costa Guerra, J.F.; Maciel, P.S.; de Abreu, I.C.M.E.; Pereira, R.R.; Silva, M.; de Morais Cardoso, L.; Pinheiro-Sant’Ana, H.M.; de Lima, W.G.; Silva, M.E.; Pedrosa, M.L. Dietary açai attenuates hepatic steatosis via adiponectin-mediated effects on lipid metabolism in high-fat diet mice. J. Funct. Foods 2015, 14, 192–202. [Google Scholar] [CrossRef]
- Hornberger, T.A., Jr.; Farrar, R.P. Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can. J. Appl. Physiol. 2004, 29, 16–31. [Google Scholar] [CrossRef] [PubMed]
- Leite, L.B.; Soares, L.L.; Portes, A.M.O.; Soares, T.I.; da Silva, B.A.F.; Dias, T.R.; Costa, S.F.F.; Guimarães-Ervilha, L.O.; Assis, M.Q.; Lavorato, V.N.; et al. Combined physical training protects the left ventricle from structural and functional damages in experimental pulmonary arterial hypertension. Clin. Hypertens. 2024, 30, 12. [Google Scholar] [CrossRef]
- Perilhao, M.S.; Krause Neto, W.; da Silva, A.A.; Alves, L.L.S.; Antonio, E.L.; Medeiros, A.; Rica, R.L.; Serra, A.J.; Tucci, P.J.F.; Bocalini, D.S. Linear periodization of strength training in blocks attenuates hypertension and diastolic dysfunction with normalization of myocardial collagen content in spontaneously hypertensive rats. J. Hypertens. 2020, 38, 73–81. [Google Scholar] [CrossRef]
- Lavorato, V.N.; Del Carlo, R.J.; da Cunha, D.N.Q.; Okano, B.S.; Belfort, F.G.; de Freitas, J.S.; Mota, G.d.F.A.d.; Quintão-Júnior, J.F.; Silame-Gomes, L.H.L.; Drummond, F.R.; et al. Mesenchymal stem cell therapy associated with endurance exercise training: Effects on the structural and functional remodeling of infarcted rat hearts. J. Mol. Cell. Cardiol. 2016, 90, 111–119. [Google Scholar] [CrossRef]
- Sahn, D.J.; Allen, H.D.; Anderson, R.; Goldberg, S.J. echocardiographic diagnosis of atrial septal aneurysm in an infant with hypoplastic right heart syndrome. Chest 1978, 73, 227–230. [Google Scholar] [CrossRef] [PubMed]
- Aebi, H. Catalase in vitro. Methods Enzymol. 1984, 105, 121–126. [Google Scholar] [CrossRef]
- Dieterich, S.; Bieligk, U.; Beulich, K.; Hasenfuss, G.; Prestle, J. Gene expression of antioxidative enzymes in the human heart: Increased expression of catalase in the end-stage failing heart. Circulation 2000, 101, 33–39. [Google Scholar] [CrossRef]
- Wallin, B.; Rosengren, B.; Shertzer, H.G.; Camejo, G. Lipoprotein oxidation and measurement of thiobarbituric acid reacting substances formation in a single microtiter plate: Its use for evaluation of antioxidants. Anal. Biochem. 1993, 208, 10–15. [Google Scholar] [CrossRef] [PubMed]
- Griffith, O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106, 207–212. [Google Scholar] [CrossRef]
- Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265–275. [Google Scholar] [CrossRef]
- Kenchaiah, S.; Pfeffer, M.A. Cardiac remodeling in systemic hypertension. Med. Clin. N. Am. 2004, 88, 115–130. [Google Scholar] [CrossRef]
- Liu, Y.-W.; Lee, W.-H.; Lin, C.-C.; Huang, Y.-Y.; Lee, W.-T.; Lee, C.-H.; Tsai, L.-M.; Chen, J.-H.; Tsai, W.-C. Left ventricular diastolic wall strain and myocardial fibrosis in treated hypertension. Int. J. Cardiol. 2014, 172, e304–e306. [Google Scholar] [CrossRef] [PubMed]
- Randriamboavonjy, J.I.; Loirand, G.; Vaillant, N.; Lauzier, B.; Derbré, S.; Michalet, S.; Pacaud, P.; Tesse, A. Cardiac Protective Effects of Moringa oleifera Seeds in Spontaneous Hypertensive Rats. Am. J. Hypertens. 2016, 29, 873–881. [Google Scholar] [CrossRef] [PubMed]
- Roman-Campos, D.; Carneiro-Júnior, M.A.; Prímola-Gomes, T.N.; Silva, K.A.; Quintão-Júnior, J.F.; Gondim, A.N.; Duarte, H.L.; Cruz, J.S.; Natali, A.J.; Roman-Campos, D.; et al. Chronic exercise partially restores the transmural heterogeneity of action potential duration in left ventricular myocytes of spontaneous hypertensive rats. Clin. Exp. Pharmacol. Physiol. 2012, 39, 155–157. [Google Scholar] [CrossRef] [PubMed]
- Carneiro-Júnior, M.A.; Quintão-Júnior, J.F.; Drummond, L.R.; Lavorato, V.N.; Drummond, F.R.; da Cunha, D.N.Q.; Amadeu, M.A.; Felix, L.B.; de Oliveira, E.M.; Cruz, J.S.; et al. The benefits of endurance training in cardiomyocyte function in hypertensive rats are reversed within four weeks of detraining. J. Mol. Cell. Cardiol. 2013, 57, 119–128. [Google Scholar] [CrossRef] [PubMed]
- da Costa, C.A.; Ognibene, D.T.; Cordeiro, V.S.C.; de Bem, G.F.; Santos, I.B.; Soares, R.A.; de Melo Cunha, L.L.; Carvalho, L.C.R.; de Moura, R.S.; Resende, A.C. Effect of Euterpe oleracea Mart. Seeds Extract on Chronic Ischemic Renal Injury in Renovascular Hypertensive Rats. J. Med. Food 2017, 20, 1002–1010. [Google Scholar] [CrossRef]
- Schauss, A.G.; Wu, X.; Prior, R.L.; Ou, B.; Huang, D.; Owens, J.; Agarwal, A.; Jensen, G.S.; Hart, A.N.; Shanbrom, E. Antioxidant capacity and other bioactivities of the freeze-dried amazonian palm berry, Euterpe oleraceae Mart. (Acai). J. Agric. Food Chem. 2006, 54, 8604–8610. [Google Scholar] [CrossRef]
- Mink, P.J.; Scrafford, C.G.; Barraj, L.M.; Harnack, L.; Hong, C.P.; Nettleton, J.A.; Jacobs, D.R., Jr. Flavonoid intake and mortality from cardiovascular diseases: A prospective study in postmenopausal women. Am. J. Clin. Nutr. 2007, 85, 14. [Google Scholar] [CrossRef]
- Ognibene, D.; Cordeiro, V.; Carvalho, L.; Costa, C.; Bem, G.; Souza, M.A.; Sousa, P.J.; Daleprane, J.; Moura, R.S.; Resende, A. Effects of the Euterpe Oleracea Mart. (Açai) Extract on Cardiovascular Changes and Oxidative Stress in Spontaneously Hypertensive Rats. FASEB J. 2015, 29. [Google Scholar] [CrossRef]
- Figueiredo, A.M.; Cardoso, A.C.; Pereira, B.L.B.; Silva, R.A.C.; Della Ripa, A.F.G.; Pinelli, T.F.B.; Oliveira, B.C.; Rafacho, B.P.M.; Ishikawa, L.L.W.; Azevedo, P.S.; et al. Açai supplementation (Euterpe oleracea Mart.) attenuates cardiac remodeling after myocardial infarction in rats through different mechanistic pathways. PLoS ONE 2022, 17, e0264854. [Google Scholar] [CrossRef]
- de Moura, R.S.; Ferreira, T.S.; Lopes, A.A.; Pires, K.M.P.; Nesi, R.T.; Resende, A.C.; Souza, P.J.C.; da Silva, A.J.R.; Borges, R.M.; Porto, L.C.; et al. Effects of Euterpe oleracea Mart. (AÇAÍ) extract in acute lung inflammation induced by cigarette smoke in the mouse. Phytomedicine 2012, 19, 262–269. [Google Scholar] [CrossRef]
- da Costa, C.A.; de Oliveira, P.R.B.; de Bem, G.F.; de Cavalho, L.C.R.M.; Ognibene, D.T.; da Silva, A.F.E.; dos Santos Valença, S.; Pires, K.M.P.; da Cunha Sousa, P.J.; de Moura, R.S.; et al. Euterpe oleracea Mart.-derived polyphenols prevent endothelial dysfunction and vascular structural changes in renovascular hypertensive rats: Role of oxidative stress. Naunyn-Schmiedeberg’s Arch. Pharmacol. 2012, 385, 1199–1209. [Google Scholar] [CrossRef] [PubMed]
- Patil, P.D.; Melo, A.C.; Westwood, B.M.; Tallant, E.A.; Gallagher, P.E. A Polyphenol-Rich Extract from Muscadine Grapes Prevents Hypertension-Induced Diastolic Dysfunction and Oxidative Stress. Antioxidants 2022, 11, 2026. [Google Scholar] [CrossRef]
- Joyner, M.J.; Green, D.J. Exercise protects the cardiovascular system: Effects beyond traditional risk factors. J. Physiol. 2009, 587, 5551–5558. [Google Scholar] [CrossRef]
- Lino, A.D.d.S.; Vianna, D.; Oishi, J.C.; Souza, M.V.C.; Ruffoni, L.D.; Marin, C.T.; de Avó, L.R.d.S.; Perez, S.E.d.A.; Rodrigues, G.J.; Tirapegui, J.; et al. Resistance training and caloric restriction prevent systolic blood pressure rise by improving the nitric oxide effect on smooth muscle and morphological changes in the aorta of ovariectomized rats. PLoS ONE 2018, 13, e0201843. [Google Scholar] [CrossRef] [PubMed]
- Neves, R.V.P.; Rosa, T.S.; Souza, M.K.; Passos, C.S.; Carbonel, A.A.F.; Teixeira, C.P.; Navarro, F.; Simões, R.S.; Soares, B.R.A.; Franco, M.C.P.; et al. Moderate Resistance Training Attenuates the Increase in Blood Pressure and Decreases the Cardiomyocyte Nuclei Number in Hypertensive Rats. Int. J. Cardiovasc. Sci. 2016, 29, 492–499. [Google Scholar] [CrossRef]
- Myers, M.G. Kaplan’s Clinical Hypertension. Can. J. Cardiol. 2017, 13, 1–2. [Google Scholar]
Compounds | Values |
---|---|
Proteins (%) | 12.68 ± 1.27 |
Lipids (%) | 50.70 ± 0.28 |
Fibers (%) | 21.47 ± 1.12 |
Ashes (%) | 3.78 ± 0.02 |
Carbohydrates (%) | 11.37 |
Phenolics (mg GAE/g) | 8.02 ± 0.11 |
Antioxidant capacity (µM Trolox/g) | 18.19 ± 0.90 |
C | H | HA | HT | HAT | |
---|---|---|---|---|---|
Initial Body Mass (g) | 403.1 ± 41.82 Ω**** | 289.5 ± 11.67 | 303.7 ± 19.74 | 302.2 ± 38.50 | 294.8 ± 27.50 |
Final Body Mass (g) | 432.7 ± 43.06 #***Ω**** | 349.4 ± 26.12 #**** | 355.1 ± 30.96 #**** | 349.9 ± 37.79 #*** | 348.6 ± 18.51 #**** |
Initial SBP (mmHg) | 116.1 ± 12.44 Ω**** | 199.0 ± 17.29 | 197.5 ± 11.97 | 199.5 ± 10.92 | 200.0 ± 10.95 |
Final SBP (mmHg) | 117.0 ± 4.07 Ω**** | 209.4 ± 12.04 Ω**** | 180.2 ± 13.83 #*** | 171.4 ± 14.12 #*** | 166.2 ± 14.20 #*** |
Initial MCL (g) | 361.5 ± 55.99 | 316.3 ± 51.28 | 347.4 ± 49.79 | 325.5 ± 44.29 | 306.8 ± 33.58 |
Final MCL (g) | 379.5 ± 54.24 | 344.2 ± 96.05 †**** | 295.3 ± 41.22 #*§**** | 584.4 ± 34.03 #**** | 533.8 ± 32.32 #**** |
C | H | HA | HT | HAT | p | |
---|---|---|---|---|---|---|
Heart mass (g) | 1.535 ± 0.4090 | 1.541 ± 0.1142 | 1.559 ± 0.1355 | 1.753 ± 0.2794 | 1.562 ± 0.1356 | 0.2519 |
Ventricle mass (g) | 0.966 ± 0.1476 | 1.102 ± 0.1402 | 1.144 ± 0.0846 | 1.183 ± 0.2054 * | 1.100 ± 0.1047 | 0.0267 |
LV mass (g) | 0.583 ± 0.3927 | 0.774 ± 0.1389 | 0.795 ± 0.0639 | 0.840 ± 0.1587 | 0.794 ± 0.0512 | 0.0666 |
Heart/Body mass (g) | 0.003 ± 0.0012 | 0.004 ± 0.0003 | 0.004 ± 0.0003 | 0.005 ± 0.0013 * | 0.004 ± 0.0002 | 0.0093 |
Ventricle/Body mass (g) | 0.002 ± 0.0003 Ω | 0.0031 ± 0.0003 | 0.0031 ± 0.0002 | 0.0034 ± 0.0008 | 0.0031 ± 0.0002 | <0.0001 |
LV/Body mass (g) | 0.001 ± 0.0005 | 0.0022 ± 0.0004 | 0.0021 ± 0.0001 | 0.0024 ± 0.0006 * | 0.0022 ± 0.0001 | 0.0276 |
C | H | HA | HT | HAT | p | |
---|---|---|---|---|---|---|
RVID-d (mm) | 1.60 ± 0.49 | 2.08 ± 0.43 | 1.73 ± 0.39 | 2.01 ± 0.38 | 2.03 ± 0.57 | 0.3057 |
IVS-d (mm) | 1.83 ± 0.35 | 2.08 ± 0.24 | 2.06 ± 0.31 | 2.21 ± 0.29 | 2.15 ± 0.41 | 0.3555 |
LVID-d (mm) | 7.80 ± 1.24 | 7.88 ± 0.42 | 7.71 ± 0.77 | 7.75 ± 1.20 | 7.58 ± 0.87 | 0.9874 |
LVFW-d (mm) | 1.70 ± 0.40 | 2.16 ± 0.30 | 2.20 ± 0.20 | 2.13 ± 0.52 | 2.31 ± 0.50 | 0.1242 |
IVS-s (mm) | 2.81 ± 0.54 | 2.91 ± 1.03 | 2.38 ± 0.34 | 2.66 ± 0.28 | 2.46 ± 0.30 | 0.4631 |
LVID-s (mm) | 4.68 ± 0.77 | 5.68 ± 0.33 | 5.25 ± 0.61 | 5.20 ± 0.93 | 5.05 ± 0.49 | 0.1654 |
LVFW-s (mm) | 2.48 ± 0.26 | 2.85 ± 0.23 * | 2.70 ± 0.18 | 2.81 ± 0.14 | 2.78 ± 0.16 | 0.0328 |
EF (%) | 76.00 ± 2.82 | 59.67 ± 2.06 * | 65.67 ± 4.63 | 67.33 ± 4.54 ᴪ | 67.50 ± 3.27 ᴪ | <0.0001 |
FS (%) | 39.83 ± 2.71 | 27.83 ± 1.47 * | 32.00 ± 3.28 | 32.83 ± 3.43 ᴪ | 32.83 ± 2.63 ᴪ | <0.0001 |
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de Meireles, P.B.; de Miranda, D.C.; de Moura, A.G.; Ribeiro, W.C.; Oliveira, Â.Q.; Leite, L.B.; Forte, P.; Ribeiro, L.; Encarnação, S.G.; Guimarães-Ervilha, L.O.; et al. Euterpe Oleracea Martius (Açaí) Extract and Resistance Exercise Modulate Cardiac Parameters of Hypertensive Rats. Life 2024, 14, 1101. https://doi.org/10.3390/life14091101
de Meireles PB, de Miranda DC, de Moura AG, Ribeiro WC, Oliveira ÂQ, Leite LB, Forte P, Ribeiro L, Encarnação SG, Guimarães-Ervilha LO, et al. Euterpe Oleracea Martius (Açaí) Extract and Resistance Exercise Modulate Cardiac Parameters of Hypertensive Rats. Life. 2024; 14(9):1101. https://doi.org/10.3390/life14091101
Chicago/Turabian Stylede Meireles, Pilar Barbosa, Denise Coutinho de Miranda, Anselmo Gomes de Moura, Willian Cruz Ribeiro, Ângela Quinelato Oliveira, Luciano Bernardes Leite, Pedro Forte, Lúcia Ribeiro, Samuel G. Encarnação, Luiz Otávio Guimarães-Ervilha, and et al. 2024. "Euterpe Oleracea Martius (Açaí) Extract and Resistance Exercise Modulate Cardiac Parameters of Hypertensive Rats" Life 14, no. 9: 1101. https://doi.org/10.3390/life14091101