Antioxidant potential of wine polyphenols on hematological indices and apical periodontitis in male rats

Authors

DOI:

https://doi.org/10.1590/1678-7757-2025-0229

Keywords:

Apical periodontitis, Dealcoholized Red Wine, Blood, Oxidative stress, Rats

Abstract

Objective:  To investigate the effects of dealcoholized red wine supplementation on blood cells and the redox state in male rats with established apical periodontitis (AP). Methodology:  Thirty-two male Wistar rats were assigned to one of four groups: control (C), dealcoholized red wine (DRW), red wine (RW), and alcohol (AL). AP was induced, and supplementation was administered for 30 days, starting 30 days after AP induction. At the end of the 60th day, the maxillae were removed for AP radiographic analysis and blood was collected for blood cell and redox state analysis. Statistical tests were applied (p<0.05). Results:  The C and DRW groups showed higher weight gain percentages (p<0.05). The DRW and AL groups exhibited the smallest and the largest periapical lesion areas, respectively (p<0.05). The RW and DRW groups showed similar red blood cell parameters to the C group but different from the AL group (p<0.05). Lymphocyte counts were smaller in the DRW and RW groups compared to the AL and C groups (p<0.05), and the neutrophil count was lower in the AL group (p<0.05). No significant differences were found in monocytes and in lipid and protein oxidative damage. Superoxide dismutase activity was lower in the AL group (p<0.05). The DRW group presented a higher glutathione concentration compared to the RW and AL groups (p<0.05). Conclusion:  DRW reduced periapical lesion size and altered the blood profile by reducing the lymphocyte count and increasing the concentration of endogenous antioxidants such as GSH in male rats with established AP.

Downloads

Download data is not yet available.

References

Kakehashi S, Stanley HR, Fitzgerald RJ. The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol. 1965;20(3):340-9. doi: 10.1016/0030-4220(65)90166-0

» https://doi.org/10.1016/0030-4220(65)90166-0

Cintra LT, Estrela C, Azuma MM, Queiroz ÍO, Kawai T, Gomes-Filho JE. Endodontic medicine: interrelationships among apical periodontitis, systemic disorders, and tissue responses of dental materials. Braz Oral Res. 2018;32(Suppl 1):e68. doi: 10.1590/1807-3107bor-2018.vol32.0068

» https://doi.org/10.1590/1807-3107bor-2018.vol32.0068

Samuel RO, Gomes-Filho JE, Azuma MM, Sumida DH, Oliveira SH, Chiba FY, et al. Endodontic infections increase leukocyte and lymphocyte levels in the blood. Clin Oral Investig. 2018;22(1):343-8. doi: 10.1007/s00784-017-2222-z

» https://doi.org/10.1007/s00784-017-2222-z

Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 5th ed. Oxford: Oxford University Press; 2015.

Hernández-Ríos P, Pussinen PJ, Vernal R, Hernández M. Oxidative stress in the local and systemic events of apical periodontitis. Front Physiol. 2017;8:869. doi: 10.3389/fphys.2017.00869

» https://doi.org/10.3389/fphys.2017.00869

Vejarano R, Luján-Corro M. Red wine and health: approaches to improve the phenolic content during winemaking. Front Nutr. 2022;9:890066. doi: 10.3389/fnut.2022.890066

» https://doi.org/10.3389/fnut.2022.890066

Castaldo L, Narváez A, Izzo L, Graziani G, Gaspari A, Di MG, et al. Red wine consumption and cardiovascular health. Molecules. 2019;24(19):3626. doi: 10.3390/molecules24193626

» https://doi.org/10.3390/molecules24193626

Hu C, Huang C, Li J, Liu F, Huang K, Liu Z, et al. Causal associations of alcohol consumption with cardiovascular diseases and all-cause mortality among Chinese males. Am J Clin Nutr. 2022;116(3):771-9. doi: 10.1093/ajcn/nqac159

» https://doi.org/10.1093/ajcn/nqac159

Malherbe DC, Messaoudi I. Transcriptional and epigenetic regulation of monocyte and macrophage dysfunction by chronic alcohol consumption. Front Immunol. 2022;13:911951. doi:10.3389/fimmu.2022.911951

» https://doi.org/10.3389/fimmu.2022.911951

Sam FE, Ma TZ, Salifu R, Wang J, Jiang YM, Zhang B, et al. Techniques for dealcoholization of wines: their impact on wine phenolic composition, volatile composition, and sensory characteristics. Foods. 2021;10(10):2498. doi: 10.3390/foods10102498

» https://doi.org/10.3390/foods10102498

Vinson JA, Teufel K, Wu N. Red wine, dealcoholized red wine, and especially grape juice, inhibit atherosclerosis in a hamster model. Atherosclerosis. 2001;156(1):67-72. doi: 10.1016/S0021-9150(00)00625-0

» https://doi.org/10.1016/S0021-9150(00)00625-0

Chiva-Blanch G, Urpi-Sarda M, Ros E, Arranz S, Valderas-Martínez P, Casas R, et al. Dealcoholized red wine decreases systolic and diastolic blood pressure and increases plasma nitric oxide: short communication. Circ Res. 2012;111(8):1065-8. doi: 10.1161/CIRCRESAHA.112.275636

» https://doi.org/10.1161/CIRCRESAHA.112.275636

Dal-Fabbro R, Cosme-Silva L, Rezende SM, Capaldo LC, Plazza FA, Ervolino E, et al. Effect of red wine or its polyphenols on induced apical periodontitis in rats. Int Endod J. 2021;54(12):2276-89. doi: 10.1111/iej.13633

» https://doi.org/10.1111/iej.13633

Ricci R, Pereira BM, Alvarado JD, Sales RO Junior, Machado NE, Santos DC, et al. Impact of wine polyphenols on the inflammatory profile of induced apical periodontitis in rats. J Endod. 2025:S0099-2399(25)00065-2. doi: 10.1016/j.joen.2025.01.023

» https://doi.org/10.1016/j.joen.2025.01.023

Sales-Junior RO, Pereira BM, Ricci R, Machado NE, Alvarado JD, Carreto AB, et al Systemic administration of polyphenols from dealcoholized red wine reduces inflammation and bone resorption in established apical periodontitis in male rats. Arch Oral Biol. 2025;173:106206. doi: 10.1016/j.archoralbio.2025.106206

» https://doi.org/10.1016/j.archoralbio.2025.106206

Dal-Fabbro R, Marques-de-Almeida M, Cosme-Silva L, Capalbo LC, Ervolino E, Cintra LTA, Gomes-Filho JE. Effects of different alcohol concentrations on the development of apical periodontitis in rats. Arch Oral Biol. 2019;108:104538. doi: 10.1016/j.archoralbio.2019.104538

» https://doi.org/10.1016/j.archoralbio.2019.104538

Verhave PS, van Eenige R, Tiebosch I. Methods for applying blinding and randomisation in animal experiments. Lab Anim. 2024;58(5):419-26. doi: 10.1177/00236772241272991

» https://doi.org/10.1177/00236772241272991

Tsosura TV, Santos RM, Chaves Neto AH, Chiba FY, Carnevali AC, et al. Maternal apical periodontitis increases insulin resistance and modulates the antioxidant defense system in the gastrocnemius muscle of adult offspring. J Endod. 2021;47(7):1126-31. doi: 10.1016/j.joen.2021.04.003

» https://doi.org/10.1016/j.joen.2021.04.003

Frazão DR, Mendes PF, Baia-da-Silva DC, Moura JD, Santos VR, et al. Modulation of blood redox status by the progression of induced apical periodontitis in rats. Front Physiol. 2023;14:1214990. doi: 10.3389/fphys.2023

» https://doi.org/10.3389/fphys.2023

Sarıtekin E, Üreyen Kaya B, Aşcı H, Özmen Ö. Anti-inflammatory and antiresorptive functions of melatonin on experimentally induced periapical lesions. Int Endod J. 2019;52(10):1466-78. doi: 10.1111/iej.13138

» https://doi.org/10.1111/iej.13138

Hartree E. Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem. 1972;48(2):422-7. doi: 10.1016/0003-2697(72)90094-2

» https://doi.org/10.1016/0003-2697(72)90094-2

Buege JA, Aust SD. Microsomal lipid peroxidation. In: Methods Enzymol. Academic Press; 1978; 302-10. doi: 10.1016/s0076-6879(78)52032-6

» https://doi.org/10.1016/s0076-6879(78)52032-6

Mesquita CS, Santos L, Farias MF, Santos DC, Santos MF. Simplified 2, 4-dinitrophenylhydrazine spectrophotometric assay for quantification of carbonyls in oxidized proteins. Anal Biochem. 2014;458:69-71. doi: 10.1016/j.ab.2014.04.034

» https://doi.org/10.1016/j.ab.2014.04.034

Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem. 1996;239(1):70-76. doi: 10.1006/abio.1996.0292

» https://doi.org/10.1006/abio.1996.0292

Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882-8.

Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974;47(3):469-74. doi: 10.1111/j.1432-1033.1974.tb03714.x

» https://doi.org/10.1111/j.1432-1033.1974.tb03714.x

He Q, Su G, Liu K, Zhang F, Jiang Y, Gao J, et al. Sex-specific reference intervals of hematologic and biochemical analytes in Sprague-Dawley rats using the nonparametric rank percentile method. PLoS One. 2017;12(12):e0189837. doi: 10.1371/journal.pone.0189837

» https://doi.org/10.1371/journal.pone.0189837

Nelson NG, Suhaidi FA, DeAngelis RS, Liang NC. Appetite and weight gain suppression effects of alcohol depend on the route and pattern of administration in Long Evans rats. Pharmacol Biochem Behav. 2016;150-151:124-33. doi: 10.1016/j.pbb.2016.10.006

» https://doi.org/10.1016/j.pbb.2016.10.006

World MJ, Ryle PR, Thomson AD. Alcoholic malnutrition and the small intestine. Alcohol Alcohol. 1985;20(2):89-124

Rabai M, Toth A, Kenyeres P, Mark L, Marton Z, Juricskay I, et al. In vitro hemorheological effects of red wine and alcohol-free red wine extract. Clin Hemorheol Microcirc. 2010;44(3):227-36. doi: 10.3233/CH-2010-1267

» https://doi.org/10.3233/CH-2010-1267

Ballard HS. The hematological complications of alcoholism. Alcohol Health Res World. 1997;21(1):42-52.

Wu D, Cederbaum AI. Alcohol, oxidative stress, and free radical damage. Alcohol Res Health. 2003;27(4):277-84.

Pavanello S, Snenghi R, Nalesso A, Sartore D, Ferrara SD, Montisci M. Alcohol drinking, mean corpuscular volume of erythrocytes, and alcohol metabolic genotypes in drunk drivers. Alcohol. 2012;46(1):61-8. doi: 10.1016/j.alcohol.2011.08.009

» https://doi.org/10.1016/j.alcohol.2011.08.009

Milman N, Pedersen AN. Blood haemoglobin concentrations are higher in smokers and heavy alcohol consumers than in non-smokers and abstainers: should we adjust the reference range? Ann Hematol. 2009;88(7):687-94. doi: 10.1007/s00277-008-0647-9

» https://doi.org/10.1007/s00277-008-0647-9

Watzl B, Bub A, Pretzer G, Roser S, Barth SW, Rechkemmer G. Daily moderate amounts of red wine or alcohol have no effect on the immune system of healthy men. Eur J Clin Nutr. 2004;58(1):40-5. doi: 10.1038/sj.ejcn.1601742

» https://doi.org/10.1038/sj.ejcn.1601742

Percival SS, Sims CA. Wine modifies the effects of alcohol on immune cells of mice. J Nutr. 2000;130(5):1091-4. doi:10.1093/jn/130.5.1091

» https://doi.org/10.1093/jn/130.5.1091

Rothenberg EV, Kueh HY, Yui MA, Zhang JA. Hematopoiesis and T-cell specification as a model developmental system. Immunol Rev. 2016;271(1):72-97. doi:10.1111/imr.12417

» https://doi.org/10.1111/imr.12417

Zhang H, Meadows GG. Chronic alcohol consumption in mice increases the proportion of peripheral memory T cells by homeostatic proliferation. J Leukoc Biol. 2005;78(5):1070-80. doi: 10.1189/jlb.0605317

» https://doi.org/10.1189/jlb.0605317

Márton IJ, Kiss C. Overlapping protective and destructive regulatory pathways in apical periodontitis. J Endod. 2014;40(2):155-63. doi: 10.1016/j.joen.2013.10.036

» https://doi.org/10.1016/j.joen.2013.10.036

Molina PE, Happel KI, Zhang P, Kolls JK, Nelson S. Focus on: Alcohol and the immune system. Alcohol Res Health. 2010;33(1-2):97-108

Zhu R, Wang Y, Zhang L, Guo Q. Oxidative stress and liver disease. Hepatol Res. 2012;42(8):741-9. doi: 10.1111/j.1872-034X.2012.00996.x

» https://doi.org/10.1111/j.1872-034X.2012.00996.x

Tedesco I, Spagnuolo C, Russo GL, Russo M, Cervellera C, Moccia S. The pro-oxidant activity of red wine polyphenols induces an adaptive antioxidant response in human erythrocytes. Antioxidants (Basel). 2021;10(5):800. doi: 10.3390/antiox10050800

» https://doi.org/10.3390/antiox10050800

Kado A, Moriya K, Inoue Y, Yanagimoto S, Tsutsumi T, Koike K, et al. Decreased antioxidant-related superoxide dismutase 1 expression in peripheral immune cells indicates early ethanol exposure. Sci Rep. 2024;14(1):25091. doi: 10.1038/s41598-024-76084-8

» https://doi.org/10.1038/s41598-024-76084-8

Downloads

Published

2025-08-12

Issue

Section

Original Articles

How to Cite

Sales-Junior, R. de O., Alvarado, J. D. A., Pereira, B. de M., Ricci, R., Machado, N. E. da S., Ferraz, M. C., Freitas, R. N. de, Barzotti, R. J., Chaves-Neto, A. H., Cintra, L. T. Ângelo, & Gomes-Filho, J. E. (2025). Antioxidant potential of wine polyphenols on hematological indices and apical periodontitis in male rats. Journal of Applied Oral Science, 33, e20250229. https://doi.org/10.1590/1678-7757-2025-0229