Effects of Phenols from Olive Vegetation Water on Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties
Abstract
:1. Introduction
2. Materials and Methods
2.1. Phenolic Extract (PE)
2.2. Preparation of the Beef Patties
2.3. Phenols Analysis
2.4. Lipid Extraction
2.5. Determination of Cholesterol Oxidation Products (COPs)
2.6. Determination of HCAs
2.7. Isolation of Mononuclear Cells from Peripheral Blood
2.8. Treatment of PBMCs with Meat Extracts and Cytotoxicity Analysis
2.9. Single-Cell Gel Electrophoresis (SCGE or Comet Assay)
2.10. Comet Detection
2.11. Ames Test
2.12. Statistical Analysis
3. Results and Discussion
3.1. Impact on Total Phenols in Stored-Cooked Beef Patties
3.2. Formation of COPs in Stored-Cooked Beef Patties
3.3. Formation of HCAs in Stored-Cooked Beef Patties
3.4. Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties
3.5. Principal Component Analysis (PCA)
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Neuhouser, M.L.; Prentice, R.L.; Tinker, L.F.; Lampe, J.W. Enhancing capacity for food and nutrient intake assessment in population sciences research. Annu. Rev. Public Health 2023, 44, 37–54. [Google Scholar] [CrossRef] [PubMed]
- Collatuzzo, G.; Boffetta, P. Cancers attributable to modifiable risk factors: A road map for prevention. Annu. Rev. Public Health 2023, 3, 279–300. [Google Scholar] [CrossRef] [PubMed]
- Domingo, J.L.; Nadal, M. Carcinogenicity of consumption of red meat and processed meat: A review of scientific news since the IARC decision. Food Chem. Toxicol. 2017, 105, 256–261. [Google Scholar] [CrossRef] [PubMed]
- International Agency for Research on Cancer—IARC. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Red Meat and Processed Meat—Volume 114. Lyon, France. Available online: https://publications.iarc.fr/Book-And-Report-Series/Iarc-Monographs-On-The-Identification-Of-Carcinogenic-Hazards-To-Humans/Red-Meat-And-Processed-Meat-2018 (accessed on 30 April 2024).
- Bouvard, V.; Loomis, D.; Guyton, K.Z.; Grosse, Y.; Ghissassi, F.E.; Benbrahim-Tallaa, L.; Guha, N.; Mattock, H.; Straif, K. International Agency for Research on Cancer Monograph Working Group. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 2015, 16, 1599–1600. [Google Scholar] [CrossRef]
- Canzoneri, F.; Leoni, V.; Rosso, G.; Risso, D.; Menta, R.; Poli, G. Oxysterols as reliable markers of quality and safety in cholesterol containing food ingredients and products. Front. Nutri. 2022, 9, 853460. [Google Scholar] [CrossRef]
- Sawada, M.I.; Ferreira, G.D.S.; Passarelli, M. Cholesterol derivatives and breast cancer: Oxysterols driving tumor growth and metastasis. Biomark. Med. 2020, 14, 1299–1302. [Google Scholar] [CrossRef] [PubMed]
- Staurenghi, E.; Giannelli, S.; Testa, G.; Sottero, B.; Leonarduzzi, G.; Gamba, P. Cholesterol dysmetabolism in Alzheimer’s disease: A starring role for astrocytes? Antioxidants 2021, 10, 1890. [Google Scholar] [CrossRef] [PubMed]
- Poli, G.; Leoni, V.; Biasi, F.; Canzoneri, F.; Risso, D.; Menta, R. Oxysterols: From redox bench to industry. Redox Biol. 2022, 49, 102220. [Google Scholar] [CrossRef]
- Malaguti, M.; Cardenia, V.; Rodriguez-Estrada, M.T.; Hrelia, S. Nutraceuticals and physical activity: Their role on oxysterols-mediated neurodegeneration. J. Steroid Biochem. Mol. Biol. 2019, 193, 105430. [Google Scholar] [CrossRef]
- Biasi, F.; Chiarpotto, E.; Sottero, B.; Maina, M.; Mascia, C.; Guina, T.; Gamba, P.; Gargiulo, S.; Testa, G.; Leonarduzzi, G.; et al. Evidence of cell damage induced by major components of a diet-compatible mixture of oxysterols in human colon cancer CaCo-2 cell line. Biochimie 2013, 95, 632–640. [Google Scholar] [CrossRef]
- Barriuso, B.; Ansorena, D.; Astiasarán, I. Oxysterols formation: A review of a multifactorial process. J. Steroid Biochem. Mol. Biol. 2017, 169, 39–45. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Yang, X.; Xiao, F.; Jie, F.; Zhang, Q.; Liu, Y.; Xiao, H.; Lu, B. Dietary cholesterol oxidation products: Perspectives linking food processing and storage with health implications. Compr. Rev. Food Sci. Food Saf. 2022, 21, 738–779. [Google Scholar] [CrossRef] [PubMed]
- Broncano, J.M.; Petrón, M.J.; Parra, V.; Timón, M.L. Effect of different cooking methods on lipid oxidation and formation of free cholesterol oxidation products (COPs) in Latissimus dorsi of Iberian pigs. Meat Sci. 2009, 83, 431–437. [Google Scholar] [CrossRef] [PubMed]
- Straif, K.; Baan, R.; Grosse, Y.; Secretan, B.; El Ghissassi, F.; Cogliano, V. Carcinogenicity of polycyclic aromatic hydrocarbons. Lancet Oncol. 2005, 6, 931–932. [Google Scholar] [CrossRef] [PubMed]
- IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Some heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr. Eval. Carcinog. Risks Hum. 2010, 92, 1–853. [Google Scholar]
- Ni, W.; McNaughton, L.; LeMaster, D.M.; Sinha, R.; Turesky, R.J. Quantitation of 13 heterocyclic aromatic amines in cooked beef, pork, and chicken by liquid chromatography− electrospray ionization/tandem mass spectrometry. J. Agric. Food Chem. 2008, 56, 68–78. [Google Scholar] [CrossRef] [PubMed]
- Hsu, K.Y.; Chen, B.H. Analysis and reduction of heterocyclic amines and cholesterol oxidation products in chicken by controlling flavorings and roasting condition. Food Res. Int. 2020, 131, 109004. [Google Scholar] [CrossRef] [PubMed]
- Sugimura, T.; Wakabayashi, K.; Nakagama, H.; Nagao, M. Heterocyclic amines: Mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci. 2004, 95, 290–299. [Google Scholar] [CrossRef] [PubMed]
- Khan, I.A.; Khan, A.; Zou, Y.; Zhu, Z.; Xu, W.; Wang, D.; Huang, M. Heterocyclic amines in cooked meat products, shortcomings during evaluation, factors influencing formation, risk assessment and mitigation strategies. Meat Sci. 2022, 184, 108693. [Google Scholar] [CrossRef]
- Marrero, A.D.; Quesada, A.R.; Martínez-Poveda, B.; Medina, M.Á. Anti-Cancer, Anti-Angiogenic, and Anti-Atherogenic Potential of Key Phenolic Compounds from Virgin Olive Oil. Nutrients 2024, 16, 1283. [Google Scholar] [CrossRef]
- Castejón, M.L.; Montoya, T.; Alarcón-de-la-Lastra, C.; Sánchez-Hidalgo, M. Potential protective role exerted by secoiridoids from Olea europaea L. in cancer, cardiovascular, neurodegenerative, aging-related, and immunoinflammatory diseases. Antioxidants 2020, 9, 149. [Google Scholar] [CrossRef] [PubMed]
- Fuccelli, R.; Sepporta, M.V.; Rosignoli, P.; Morozzi, G.; Servili, M.; Fabiani, R. Preventive activity of olive oil phenolic compounds on alkene epoxides induced oxidative DNA damage on human peripheral blood mononuclear cells. Nutr. Cancer 2014, 66, 1322–1330. [Google Scholar] [CrossRef] [PubMed]
- European Commission Regulation EC No. 432/2012. Establishing a list of permitted health claims made on foods, other than those referring to the reduction of disease risk and to children’s development and health. Off. J. Eur. Union. 2012, L136, 1–40. [Google Scholar]
- Klen, T.J.; Vodopivec, B.M. The fate of olive fruit phenols during commercial olive oil processing: Traditional press versus continuous two-and three-phase centrifuge. LWT-Food Sci. Technol. 2012, 49, 267–274. [Google Scholar] [CrossRef]
- Romani, A.; Ieri, F.; Urciuoli, S.; Noce, A.; Marrone, G.; Nediani, C.; Bernini, R. Health effects of phenolic compounds found in extra-virgin olive oil, by-products, and leaf of Olea europaea L. Nutrients 2019, 11, 1776. [Google Scholar] [CrossRef] [PubMed]
- Balzan, S.; Taticchi, A.; Cardazzo, B.; Urbani, S.; Servili, M.; Di Lecce, G.; Berasategi Zabalza, I.; Rodriguez-Estrada, M.T.; Novelli, E.; Fasolato, L. Effect of phenols extracted from a by-product of the oil mill on the shelf-life of raw and cooked fresh pork sausage in the absence of chemical additives. LWT-Food Sci. Technol. 2017, 85, 89–95. [Google Scholar] [CrossRef]
- Barbieri, S.; Mercatante, D.; Balzan, S.; Esposto, S.; Cardenia, V.; Servili, M.; Novelli, E.; Taticchi, A.; Rodriguez-Estrada, M.T. Improved oxidative stability and sensory evaluation of beef hamburgers enriched with phenol extracts from olive vegetation water. Antioxidants 2021, 10, 1969. [Google Scholar] [CrossRef] [PubMed]
- Hawashin, M.D.; Al-Juhaimi, F.; Ahmed, I.A.M.; Ghafoor, K.; Babiker, E.E. Physicochemical, microbiological and sensory evaluation of beef patties incorporated with destoned olive cake powder. Meat Sci. 2016, 122, 32–39. [Google Scholar] [CrossRef]
- Nieto, G.; Martínez, L.; Castillo, J.; Ros, G. Hydroxytyrosol extracts, olive oil and walnuts as functional components in chicken sausages. J. Sci. Food Agric. 2017, 97, 3761–3771. [Google Scholar] [CrossRef]
- Munekata, P.E.S.; Nieto, G.; Pateiro, M.; Lorenzo, J.M. Phenolic compounds obtained from Olea europaea by-products and their use to improve the quality and shelf life of meat and meat products—A Review. Antioxidants 2020, 9, 1061. [Google Scholar] [CrossRef]
- Galanakis, C.M. Phenols recovered from olive mill wastewater as additives in meat products. Trends Food Sci. Technol. 2018, 79, 98–105. [Google Scholar] [CrossRef]
- Nardella, S.; Conte, A.; Del Nobile, M.A. State-of-Art on the recycling of by-products from fruits and vegetables of mediterranean countries to prolong food shelf life. Foods 2022, 11, 665. [Google Scholar] [CrossRef] [PubMed]
- Mercatante, D.; Ansorena, D.; Taticchi, A.; Astiasarán, I.; Servili, M.; Rodriguez-Estrada, M.T. Effects of in vitro digestion on the antioxidant activity of three phenolic extracts from olive mill wastewaters. Antioxidants 2023, 12, 22. [Google Scholar] [CrossRef] [PubMed]
- Miraglia, D.; Castrica, M.; Menchetti, L.; Esposto, S.; Branciari, R.; Ranucci, D.; Urbani, S.; Sordini, B.; Veneziani, G.; Servili, M. Effect of an olive vegetation water phenolic extract on the physico-chemical, microbiological and sensory traits of shrimp (Parapenaeus longirostris) during the shelf-life. Foods 2020, 9, 1647. [Google Scholar] [CrossRef] [PubMed]
- Selvaggini, R.; Esposto, S.; Taticchi, A.; Urbani, S.; Veneziani, G.; Di Maio, I.; Sordini, B.; Servili, M. Optimization of the temperature and oxygen concentration conditions in the malaxation during the oil mechanical extraction process of four Italian olive cultivars. J. Agric. Food. Chem. 2014, 62, 3813–3822. [Google Scholar] [CrossRef] [PubMed]
- Boselli, E.; Velazco, V.; Caboni, M.F.; Lercker, G. Pressurized liquid extraction of lipids for the determination of oxysterols in egg-containing food. J. Chromatogr. A 2001, 917, 239–244. [Google Scholar] [CrossRef] [PubMed]
- Turesky, R.J.; Taylor, J.; Schnackenberg, L.; Freeman, J.P.; Holland, R.D. Quantitation of carcinogenic heterocyclic aromatic amines and detection of novel heterocyclic aromatic amines in cooked meats and grill scrapings by HPLC/ESI-MS. J. Agric. Food Chem. 2005, 53, 3248–3258. [Google Scholar] [CrossRef] [PubMed]
- Rosignoli, P.; Fuccelli, R.; Sepporta, M.V.; Fabiani, R. In vitro chemo-preventive activities of hydroxytyrosol: The main phenolic compound present in extra-virgin olive oil. Food Funct. 2016, 7, 301–307. [Google Scholar] [CrossRef]
- Collins, A.; Dusinská, M.; Franklin, M.; Somorovská, M.; Petrovská, H.; Duthie, S.; Fillion, L.; Panayiotidis, M.; Raslová, K.; Vaughan, N. Comet assay in human biomonitoring studies: Reliability, validation, and applications. Environ. Mol. Mutagen. 1997, 30, 139–146. [Google Scholar] [CrossRef]
- Collins, A. The comet assay. Principles, applications, and limitations. Methods Mol. Biol. 2002, 203, 163–177. [Google Scholar]
- Wahab, N.F.A.C.; Kannan, T.P.; Mahmood, Z.; Rahman, I.A.; Ismail, H. Genotoxicity assessment of biphasic calcium phosphate of modified porosity on human dental pulp cells using Ames and comet assays. Toxicol. In Vitro 2018, 47, 207–212. [Google Scholar] [CrossRef] [PubMed]
- Lu, P.; Parrella, J.A.; Xu, Z.; Kogut, A. A scoping review of the literature examining consumer acceptance of upcycled foods. Food Qual. Pref. 2024, 114, 105098. [Google Scholar] [CrossRef]
- Thorsen, M.; Skeaff, S.; Goodman-Smith, F.; Thong, B.; Bremer, P.; Mirosa, M. Upcycled foods: A nudge toward nutrition. Front. Nutr. 2022, 9, 1071829. [Google Scholar] [CrossRef] [PubMed]
- Obied, H.K.; Prenzler, P.D.; Ryan, D.; Servili, M.; Taticchi, A.; Esposto, S.; Robards, K. Biosynthesis and biotransformations of phenol-conjugated oleosidic secoiridoids from Olea europaea L. Nat. Prod. Rep. 2008, 25, 1167–1179. [Google Scholar] [CrossRef] [PubMed]
- Ruíz-Delgado, A.; Roccamante, M.A.; Oller, I.; Agüera, A.; Malato, S. Natural chelating agents from olive mill wastewater to enable photo-Fenton-like reactions at natural pH. Catal. Today 2019, 328, 281–285. [Google Scholar] [CrossRef]
- Barriuso, B.; Ansorena, D.; Calvo, M.I.; Cavero, R.Y.; Astiasarán, I. Role of Melissa officinalis in cholesterol oxidation: Antioxidant effect in model systems and application in beef patties. Food Res. Int. 2015, 69, 133–140. [Google Scholar] [CrossRef]
- Rodriguez-Estrada, M.T.; Garcia-Llatas, G.; Lagarda, M.J. 7-Ketocholesterol as marker of cholesterol oxidation in model and food systems: When and how. Biochem. Biophys. Res. Commun. 2014, 446, 792–797. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Llatas, G.; Mercatante, D.; López-García, G.; Rodríguez-Estrada, M.T. Oxysterols–how much do we know about food occurrence, dietary intake and absorption? Curr. Opin. Food Sci. 2021, 41, 231–239. [Google Scholar] [CrossRef]
- Meurillon, M.; Engel, E. Mitigation strategies to reduce the impact of heterocyclic aromatic amines in proteinaceous foods. Trends Food Sci. Technol. 2016, 50, 70–84. [Google Scholar] [CrossRef]
- Gibis, M.; Weiss, J. Antioxidant capacity and inhibitory effect of grape seed and rosemary extract in marinades on the formation of heterocyclic amines in fried beef patties. Food Chem. 2012, 134, 766–774. [Google Scholar] [CrossRef]
- Günal-Köroğlu, D.; Turan, S.Y.; Kıralan, M.; Ramadan, M.F. Enhancement of sunflower oil stability during deep-frying using extracts from olive oil by-products and soy lecithin. Int. Food Res. J. 2019, 26, 1269–1277. [Google Scholar]
- Sepahpour, S.; Selamat, J.; Khatib, A.; Manap, M.Y.A.; Razis, A.F.A.; Hajeb, P. Inhibitory effect of mixture herbs/spices on formation of heterocyclic amines and mutagenic activity of grilled beef. Food Addit. Contam. A 2018, 35, 1911–1927. [Google Scholar] [CrossRef] [PubMed]
- Biasi, F.; Guina, T.; Maina, M.; Cabboi, B.; Deiana, M.; Tuberoso, C.I.; Calfapietra, S.; Chiarpotto, E.; Sottero, B.; Gamba, P.; et al. Phenolic compounds present in Sardinian wine extracts protect against the production of inflammatory cytokines induced by oxysterols in CaCo-2 human enterocyte-like cells. Biochem. Pharmacol. 2013, 86, 138–145. [Google Scholar] [CrossRef]
- Kurzawa-Zegota, M.; Najafzadeh, M.; Baumgartner, A.; Anderson, D. The protective effect of the flavonoids on food-mutagen-induced DNA damage in peripheral blood lymphocytes from colon cancer patients. Food Chem. Toxicol. 2012, 50, 124–129. [Google Scholar] [CrossRef] [PubMed]
- Fuccelli, R.; Rosignoli, P.; Servili, M.; Veneziani, G.; Taticchi, A.; Fabiani, R. Genotoxicity of heterocyclic amines (HCAs) on freshly isolated human peripheral blood mononuclear cells (PBMC) and prevention by phenolic extracts derived from olive, olive oil and olive leaves. Food Chem. Toxicol. 2018, 122, 234–241. [Google Scholar] [CrossRef] [PubMed]
- Shaughnessy, D.T.; Gangarosa, L.M.; Schliebe, B.; Umbach, D.M.; Xu, Z.; MacIntosh, B.; Mark, G.Z.; Matthews, P.P.; Swank, A.E.; Sandler, R.S.; et al. Inhibition of fried meat-induced colorectal DNA damage and altered systemic genotoxicity in humans by crucifera, chlorophyllin, and yogurt. PLoS ONE 2011, 6, e18707. [Google Scholar] [CrossRef] [PubMed]
- Kulig, W.; Cwiklik, L.; Jurkiewicz, P.; Rog, T.; Vattulainen, I. Cholesterol oxidation products and their biological importance. Chem. Phys Lipids 2016, 199, 144–160. [Google Scholar] [CrossRef] [PubMed]
- de Freitas, F.A.; Levy, D.; Zarrouk, A.; Lizard, G.; Bydlowski, S.P. Impact of oxysterols on cell death, proliferation, and differentiation induction: Current status. Cells 2021, 10, 2301. [Google Scholar] [CrossRef] [PubMed]
- Hodson, D.; Mistry, H.; Yates, J.; Guzzetti, S.; Davies, M.; Aarons, L.; Ogungbenro, K. Hierarchical cluster analysis and nonlinear mixed-effects modelling for candidate biomarker detection in preclinical models of cancer. Eur. J. Pharm. Sci. 2024, 197, 106774. [Google Scholar] [CrossRef]
- Carvalho, A.M.; Miranda, A.M.; Santos, F.A.; Loureiro, A.P.D.M.; Fisberg, R.M.; Marchioni, D.M. High intake of heterocyclic amines from meat is associated with oxidative stress. Br. J. Nutr. 2015, 113, 1301–1307. [Google Scholar] [CrossRef]
Storage Time (Days) | SEM | p | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Samples | 0 | 6 | 9 | F | S | F × S | |||||
Total phenols | C | - | B | - | B | - | B | 0.52 | *** | *** | *** |
P1 | 1.62 | a,A | 0.92 | b,A | 0.48 | c,A | |||||
7β-HC | C | 76.29 | c,B | 323.27 | b,A | 428.64 | a,A | 0.35 | *** | *** | *** |
P1 | 115.11 | b,A | 156.12 | a,B | 117.45 | b, | |||||
5β,6β-EC | C | 51.55 | c,B | 172.47 | b,A | 283.72 | a,A | 0.34 | *** | *** | *** |
P1 | 67.75 | b,A | 84.59 | a,B | 67.66 | c,B | |||||
5α,6α-EC | C | 17.00 | c,B | 101.29 | a,A | 77.98 | b,A | 0.22 | ** | N.S. | N.S. |
P1 | 18.96 | b,A | 27.26 | a,B | 30.84 | a,B | |||||
CT | C | 8.73 | c | 24.75 | a,A | 21.38 | b,A | 0.12 | ** | N.S. | N.S. |
P1 | 8.35 | b | 10.64 | a,B | 9.07 | b,B | |||||
7-KC | C | 76.15 | c,B | 324.02 | b,A | 547.61 | a,A | 0.63 | *** | *** | *** |
P1 | 109.03 | b,A | 116.14 | a,B | 80.78 | c,B | |||||
Total COPs | C | 229.72 | c,B | 945.80 | b,A | 1359.33 | a,A | 0.82 | *** | *** | *** |
P1 | 319.20 | b,A | 394.74 | a,B | 295.80 | c,B | |||||
IQ | C | n.d. | n.d. | n.d. | |||||||
P1 | n.d. | n.d. | n.d. | ||||||||
8-MeIQx | C | 20.21 | N.S. | 26.21 | N.S. | 24.54 | N.S. | 0.01 | N.S. | N.S. | N.S. |
P1 | 22.87 | N.S. | 24.86 | N.S. | 26.04 | N.S. | |||||
4,8-DiMeIQx | C | 11.31 | N.S. | 9.80 | N.S. | 10.58 | N.S. | 0.00 | N.S. | N.S. | N.S. |
P1 | 9.91 | N.S. | 10.06 | N.S. | 10.27 | N.S. | |||||
PhIP | C | n.d. | n.d. | n.d. | |||||||
P1 | n.d. | n.d. | n.d. | ||||||||
Total HCAs | C | 31.51 | N.S. | 36.01 | N.S. | 35.11 | N.S. | 0.01 | N.S. | N.S. | N.S. |
P1 | 32.78 | N.S. | 34.92 | N.S. | 36.31 | N.S. |
Storage Time (Days) | SEM | p | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Samples | 0 | 6 | 9 | F | S | F × S | |||||
Comet Assay | DMSO | 2.8 | C | 2.5 | B | 2.4 | B | 0.52 | ** | N.S. | N.S. |
C | 5.8 | A | 5.7 | A | 6.1 | A | |||||
P1 | 4.1 | a,B | 1.9 | b,B | 3.0 | ab,B | |||||
Ames Test | Spontaneous revertants | 12.2 | N.S. | 12.2 | N.S. | 12.2 | N.S. | 1.32 | N.S. | N.S. | N.S. |
C | 20.5 | N.S. | 21.0 | N.S. | 13.5 | N.S. | |||||
P1 | 13.5 | N.S. | 15.5 | N.S. | 11.5 | N.S. |
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Mercatante, D.; Curró, S.; Rosignoli, P.; Cardenia, V.; Sordini, B.; Taticchi, A.; Rodriguez-Estrada, M.T.; Fabiani, R. Effects of Phenols from Olive Vegetation Water on Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties. Antioxidants 2024, 13, 695. https://doi.org/10.3390/antiox13060695
Mercatante D, Curró S, Rosignoli P, Cardenia V, Sordini B, Taticchi A, Rodriguez-Estrada MT, Fabiani R. Effects of Phenols from Olive Vegetation Water on Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties. Antioxidants. 2024; 13(6):695. https://doi.org/10.3390/antiox13060695
Chicago/Turabian StyleMercatante, Dario, Sarah Curró, Patrizia Rosignoli, Vladimiro Cardenia, Beatrice Sordini, Agnese Taticchi, Maria Teresa Rodriguez-Estrada, and Roberto Fabiani. 2024. "Effects of Phenols from Olive Vegetation Water on Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties" Antioxidants 13, no. 6: 695. https://doi.org/10.3390/antiox13060695
APA StyleMercatante, D., Curró, S., Rosignoli, P., Cardenia, V., Sordini, B., Taticchi, A., Rodriguez-Estrada, M. T., & Fabiani, R. (2024). Effects of Phenols from Olive Vegetation Water on Mutagenicity and Genotoxicity of Stored-Cooked Beef Patties. Antioxidants, 13(6), 695. https://doi.org/10.3390/antiox13060695