Fatty Acid Supplementation Affects Skin Wound Healing in a Rat Model
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Protocol
2.2. Analysis of Wound Closure Using Digital Planimetry
2.3. Sample Collection
2.4. Hematological Analyses
2.5. Biochemical Analyses
2.6. Tissue Sample Analyses
2.6.1. Fluorescence Microscopy
2.6.2. Electron Microscopy
2.7. Statistical Analyses
3. Results
3.1. Wound Closure Level
3.2. Blood and Plasma Parameters
3.3. Wound Tissue Samples
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pokorná, A.; Benešová, K.; Mužík, J.; Jarkovský, J. Data sources for monitoring of non-healing wounds in a national health information system-epidemiology of non-healing wounds-Analysis of the national register of hospitalized patients in 2007–2015. Ceska Slov. Neurol. Neurochir. 2017, 80, S8–S17. [Google Scholar] [CrossRef]
- Middleton, J.E. Wound Healing: Process, Phases, and Promoting (Human Anatomy and Physiology); Nova Science Publishers Incorporated: Hauppauge, NY, USA, 2011. [Google Scholar]
- Kavalukas, S.L.; Barbul, A. Nutrition and wound healing: An update. Plast. Reconstr. Surg. 2011, 127 (Suppl. 1), 38S–43S. [Google Scholar] [CrossRef] [PubMed]
- Alexander, J.W.; Supp, D.M. Role of Arginine and Omega-3 Fatty Acids in Wound Healing and Infection. Adv. Wound Care 2014, 3, 682–690. [Google Scholar] [CrossRef] [PubMed]
- Armstrong, D.G.; Hanft, J.R.; Driver, V.R.; Smith, A.P.; Lazaro-Martinez, J.L.; Reyzelman, A.M.; Furst, G.J.; Vayser, D.J.; Cervantes, H.L.; Snyder, R.J.; et al. Effect of oral nutritional supplementation on wound healing in diabetic foot ulcers: A prospective randomized controlled trial. Diabet. Med. 2014, 31, 1069–1077. [Google Scholar] [CrossRef]
- Mohammed, B.M.; Fisher, B.J.; Kraskauskas, D.; Ward, S.; Wayne, J.S.; Brophy, D.F.; Fowler, A.A.; Yager, D.R.; Natarajan, R. Vitamin C promotes wound healing through novel pleiotropic mechanisms. Int. Wound J. 2016, 13, 572–584. [Google Scholar] [CrossRef]
- McDaniel, J.C.; Belury, M.; Ahijevych, K.; Blakely, W. Omega-3 fatty acids effect on wound healing. Wound Repair Regen. 2008, 16, 337–345. [Google Scholar] [CrossRef] [Green Version]
- Calder, P.C. Omega-3 fatty acids and inflammatory processes: From molecules to man. Biochem. Soc. Trans. 2017, 45, 1105–1115. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.R.; Burger, B.; Kuhl, C.M.C.; Candreva, T.; dos Anjos, M.B.P.; Rodrigues, H.G. Wound Healing and Omega-6 Fatty Acids: From Inflammation to Repair. Mediat. Inflamm. 2018, 2018, 2503950. [Google Scholar] [CrossRef] [Green Version]
- Jain, A.P.; Aggarwal, K.K.; Zhang, P.Y. Omega-3 fatty acids and cardiovascular disease. Eur. Rev. Med. Pharmacol. Sci. 2015, 19, 441–445. [Google Scholar]
- De Caterina, R.; Zampolli, A. Omega-3 fatty acids, atherogenesis, and endothelial activation. J. Cardiovasc. Med. 2007, 8 (Suppl. 1), S11–S14. [Google Scholar] [CrossRef]
- Wu, S.; Ding, Y.; Wu, F.; Li, R.; Hou, J.; Mao, P. Omega-3 fatty acids intake and risks of dementia and Alzheimer’s disease: A meta-analysis. Neurosci. Biobehav. Rev. 2015, 48, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Cardoso, C.R.; Souza, M.A.; Ferro, E.A.; Favoreto, S.; Pena, J.D. Influence of topical administration of n-3 and n-6 essential and n-9 nonessential fatty acids on the healing of cutaneous wounds. Wound Repair Regen. 2004, 12, 235–243. [Google Scholar] [CrossRef] [PubMed]
- Lania, B.G.; Morari, J.; Almeida, A.R.; Silva, M.N.D.; Vieira-Damiani, G.; Lins, K.A.; César, C.L.; Velloso, L.A.; Maia, N.B.; Cintra, M.L.; et al. Topical essential fatty acid oil on wounds: Local and systemic effects. PLoS ONE 2019, 14, e0210059. [Google Scholar] [CrossRef] [Green Version]
- Zong, J.; Jiang, J.; Shi, P.; Liu, J.; Wang, W.; Li, B.; Zhao, T.; Pan, T.; Zhang, Z.; Bi, L.; et al. Fatty acid extracts facilitate cutaneous wound healing through activating AKT, ERK, and TGF-β/Smad3 signaling and promoting angiogenesis. Am. J. Transl. Res. 2020, 12, 478–492. [Google Scholar]
- Komprda, T.; Sladek, Z.; Sevcikova, Z.; Svehlova, V.; Wijacki, J.; Guran, R.; Do, T.; Lackova, Z.; Polanska, H.; Vrlikova, L.; et al. Comparison of Dietary Oils with Different Polyunsaturated Fatty Acid n-3 and n-6 Content in the Rat Model of Cutaneous Wound Healing. Int. J. Mol. Sci. 2020, 21, 7911. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, H.G.; Vinolo, M.A.; Magdalon, J.; Vitzel, K.; Nachbar, R.T.; Pessoa, A.F.; dos Santos, M.F.; Hatanaka, E.; Calder, P.C.; Curi, R. Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J. Investig. Dermatol. 2012, 132, 208–215. [Google Scholar] [CrossRef]
- Horman, T.; Fernandes, M.F.; Tache, M.C.; Hucik, B.; Mutch, D.M.; Leri, F. Dietary n-6/n-3 Ratio Influences Brain Fatty Acid Composition in Adult Rats. Nutrients 2020, 12, 1847. [Google Scholar] [CrossRef]
- Lepczynski, A.; Ozgo, M.; Michalek, K.; Dratwa-Chalupnik, A.; Grabowska, M.; Herosimczyk, A.; Liput, K.P.; Polawska, E.; Kram, A.; Pierzchala, M. Effects of Three-Month Feeding High Fat Diets with Different Fatty Acid Composition on Myocardial Proteome in Mice. Nutrients 2021, 13, 330. [Google Scholar] [CrossRef]
- Novak, F.; Borovska, J.; Vecka, M.; Rychlikova, J.; Vavrova, L.; Petraskova, H.; Zak, A.; Novakova, O. Plasma Phospholipid Fatty Acid Profile is Altered in Both Septic and Non-Septic Critically Ill: A Correlation with Inflammatory Markers and Albumin. Lipids 2017, 52, 245–254. [Google Scholar] [CrossRef]
- Tvrzická, E.; Vecka, M.; Staňková, B.; Žák, A. Analysis of fatty acids in plasma lipoproteins by gas chromatography–flame ionization detection: Quantitative aspects. Anal. Chim. Acta 2002, 465, 337–350. [Google Scholar] [CrossRef]
- Hlaváčová, M.; Gumulec, J.; Stračina, T.; Fojtů, M.; Raudenská, M.; Masařík, M.; Nováková, M.; Paulová, H. Different doxorubicin formulations affect plasma 4-hydroxy-2-nonenal and gene expression of aldehyde dehydrogenase 3A1 and thioredoxin reductase 2 in rat. Physiol. Res. 2015, 64 (Suppl. 5), S653–S660. [Google Scholar] [CrossRef] [PubMed]
- Rao, A.M.; Dogan, A.; Hatcher, J.F.; Dempsey, R.J. Fluorometric assay of nitrite and nitrate in brain tissue after traumatic brain injury and cerebral ischemia. Brain Res. 1998, 793, 265–270. [Google Scholar] [CrossRef]
- Orozco-Ibarra, M.; Medina-Campos, O.N.; Sánchez-González, D.J.; Martínez-Martínez, C.M.; Floriano-Sánchez, E.; Santamaría, A.; Ramirez, V.; Bobadilla, N.A.; Pedraza-Chaverri, J. Evaluation of oxidative stress in D-serine induced nephrotoxicity. Toxicology 2007, 229, 123–135. [Google Scholar] [CrossRef] [PubMed]
- Jimenez, P.C.; Wilke, D.V.; Takeara, R.; Lotufo, T.M.; Pessoa, C.; de Moraes, M.O.; Lopes, N.P.; Costa-Lotufo, L.V. Cytotoxic activity of a dichloromethane extract and fractions obtained from Eudistoma vannamei (Tunicata: Ascidiacea). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2008, 151, 391–398. [Google Scholar] [CrossRef]
- Mihalj, M.; Stupin, A.; Kolobaric, N.; Bujak, I.T.; Matic, A.; Kralik, Z.; Jukic, I.; Stupin, M.; Drenjancevic, I. Leukocyte Activation and Antioxidative Defense Are Interrelated and Moderately Modified by n-3 Polyunsaturated Fatty Acid-Enriched Eggs Consumption-Double-Blind Controlled Randomized Clinical Study. Nutrients 2020, 12, 3122. [Google Scholar] [CrossRef]
- Meng, F.X.; Qiu, J.Y.; Chen, H.J.; Shi, X.J.; Yin, M.F.; Zhu, M.S.; Yang, G. Dietary supplementation with N-3 polyunsaturated fatty acid-enriched fish oil promotes wound healing after ultraviolet B-induced sunburn in mice. Food Sci. Nutr. 2021, 9, 3693–3700. [Google Scholar] [CrossRef]
- Lorente-Cebrián, S.; Costa, A.G.; Navas-Carretero, S.; Zabala, M.; Martínez, J.A.; Moreno-Aliaga, M.J. Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: A review of the evidence. J. Physiol. Biochem. 2013, 69, 633–651. [Google Scholar] [CrossRef]
- Arterburn, L.M.; Hall, E.B.; Oken, H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am. J. Clin. Nutr. 2006, 83, 1467S–1476S. [Google Scholar] [CrossRef]
- Huo, Y.; Qiu, W.Y.; Pan, Q.; Yao, Y.F.; Xing, K.; Lou, M.F. Reactive oxygen species (ROS) are essential mediators in epidermal growth factor (EGF)-stimulated corneal epithelial cell proliferation, adhesion, migration, and wound healing. Exp. Eye Res. 2009, 89, 876–886. [Google Scholar] [CrossRef]
- Janda, J.; Nfonsam, V.; Calienes, F.; Sligh, J.E.; Jandova, J. Modulation of ROS levels in fibroblasts by altering mitochondria regulates the process of wound healing. Arch Dermatol. Res. 2016, 308, 239–248. [Google Scholar] [CrossRef]
- Ayala, A.; Muñoz, M.F.; Argüelles, S. Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell. Longev. 2014, 2014, 360438. [Google Scholar] [CrossRef] [PubMed]
- Leonarduzzi, G.; Arkan, M.C.; Başağa, H.; Chiarpotto, E.; Sevanian, A.; Poli, G. Lipid oxidation products in cell signaling. Free Radic. Biol. Med. 2000, 28, 1370–1378. [Google Scholar] [CrossRef]
- Hankenson, K.D.; Watkins, B.A.; Schoenlein, I.A.; Allen, K.G.; Turek, J.J. Omega-3 fatty acids enhance ligament fibroblast collagen formation in association with changes in interleukin-6 production. Proc. Soc. Exp. Biol. Med. 2000, 223, 88–95. [Google Scholar] [CrossRef] [PubMed]
- Magalhes, M.S.F.; Fechine, F.V.; de Macedo, R.N.; Monteiro, D.L.S.; Oliveira, C.C.; Brito, G.A.D.; de Moraes, M.E.A.; de Moraes, M.O. Effect of a combination of medium chain triglycerides, linoleic acid, soy lecithin and vitamins A and E on wound healing in rats. Acta Cir. Bras. 2008, 23, 262–269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Lipid Emulsion | Emulsion A | Emulsion B |
---|---|---|
Palmitic acid | 14.62 | 15.08 |
Stearic acid | 3.07 | 2.73 |
Oleic acid | 31.99 | 39.37 |
Linoleic acid (LA) | 18.36 | 6.72 |
α-Linolenic acid (ALA) | 15.32 | 16.74 |
Docosahexaenoic acid (DHA) | 10.12 | 12.24 |
PUFA | Kruskal-Wallis ANOVA | Multiple Comparisons | |||
---|---|---|---|---|---|
C vs. A | C vs. B | A vs. B | |||
Dihomo-γ-linolenic acid | 20:3n-6 | 0.047 * | 0.052 | 0.260 | 1.000 |
Osbond acid | 22:5n-6 | 0.008 * | 0.037 * | 0.014 * | 1.000 |
Eicosapentaenoic acid (EPA) | 20:5n-3 | <0.0001 *** | 0.008 * | 0.0001 *** | 0.898 |
PUFA | Kruskal-Wallis ANOVA | Multiple Comparisons | |||
---|---|---|---|---|---|
C vs. A | C vs. B | A vs. B | |||
Linoleic acid (LA) | 18:2n-6 | 0.0345 * | 0.060 | 1.000 | 0.074 |
Osbond acid | 22:5n-6 | 0.0267 * | 0.176 | 0.029 * | 1.000 |
Docosahexaenoic acid (DHA) | 22:6n-3 | 0.048 * | 1.000 | 0.047 * | 0.368 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Hokynková, A.; Nováková, M.; Babula, P.; Sedláčková, M.; Paulová, H.; Hlaváčová, M.; Charwátová, D.; Stračina, T. Fatty Acid Supplementation Affects Skin Wound Healing in a Rat Model. Nutrients 2022, 14, 2245. https://doi.org/10.3390/nu14112245
Hokynková A, Nováková M, Babula P, Sedláčková M, Paulová H, Hlaváčová M, Charwátová D, Stračina T. Fatty Acid Supplementation Affects Skin Wound Healing in a Rat Model. Nutrients. 2022; 14(11):2245. https://doi.org/10.3390/nu14112245
Chicago/Turabian StyleHokynková, Alica, Marie Nováková, Petr Babula, Miroslava Sedláčková, Hana Paulová, Miroslava Hlaváčová, Daniela Charwátová, and Tibor Stračina. 2022. "Fatty Acid Supplementation Affects Skin Wound Healing in a Rat Model" Nutrients 14, no. 11: 2245. https://doi.org/10.3390/nu14112245