Oxidative Stress and Dietary Fat Type in Relation to Periodontal Disease
Abstract
:1. Introduction
2. Periodontal Disease and Oxidative Stress
3. Dietary Fat and Oxidative Stress
4. Dietary Lipids and Periodontitis
Study Type (Duration) | Subjects | Age (n) | Main Clinical Outcomes/Periodontitis Definition | Main Results/Conclusions | Reference |
---|---|---|---|---|---|
Cross-sectional | NHANES 1999–2004 participants (USA) | ≥20 years (9182) | Periodontitis: PPD ≥ 4 mm & AL ≥ 3 mm in any mid-facial or mesial tooth | Inverse association of n-3 PUFA, DHA, EPA & GLA intake with periodontitis prevalence | [96] |
Cross-sectional | Patients attended the Sevilla University Dental School (Spain) | ≥35 years (56) | Periodontitis: AL ≥ 6 mm in ≥ 2 teeth & ≥ 1 sites with PPD 5 ≥ mm | Serum levels of n-6 PUFA, SFA and MUFA were higher in the periodontitis group compared to subjects without periodontitis which also occurred with peroxida bility index | [97] |
Cross-sectional | Patient form dental school of the Rio de Janeiro State University (Brazil). | 46.0 ± 8.8/31.5 ± 7.5 years (37) | chronic generalized periodontitis & gingivitis were diagnosed according to criteria described by the American Academy of Periodontology | Higher serum levels of DHA, DPA, EPA, & AA were observed in patients with chronic generalized periodontitis when compared with patients with gingivitis | [98] |
Cohort (5 years) | Niigata study participants (Japan). | 74 years (55) | Periodontal disease events: n° of teeth with AL ≥ 3mm/year | Negative association of DHA intake with risk of periodontal disease events | [99] |
Cohort (3 years) | Niigata study participants (Japan) | 75 years (235) | Periodontal disease events: n° of teeth with AL ≥ 3mm/ year | Positive association of n-6/n-3 PUFA ratio with risk of periodontal disease events | [100] |
Cohort (3 years) | Niigata study participants (Japan) | 75 years (264) | Periodontal disease events: n° of teeth with AL ≥ 3mm/year | Positive association of SFA intakes ratio with risk of periodontal disease events in non-smokers | [101] |
Randomized controlled trial (DB) (12 weeks) | Subjects with periodontitis (USA) | 18–60 years (30) | MGI, PI, PPD | Supplementation with borage oil (a GLA source) or EPA improved PPD, but only the first was statistical significant respect to the placebo (an olive & corn oil mixture). Additionally, it was the only that also improved MGI. | [102] |
Randomized controlled trial (DB) (3/6 months) | Subjects with advanced untreated chronic periodontitis (Egypt) | 30–70 years (80) | PI, MGI, BOP, PPD & CAL | Dietary supplementation with a combination of fish oil (EPA & DHA-rich) & aspirin after SRP, reduced PPD & salivary levels of RANKL & MMP-8 & increased CAL | [103] |
Animal Model | Gender Age/Weight (n) | Dietary Treatments (Duration) | Periodontal Intervention (Duration) | Main Results/Conclusions | Reference |
---|---|---|---|---|---|
New Zealand rabbits with dietary-induced atherosclerosis | Male 2.5 kg (48) | CoQ10, squalene, or hydroxytyrosol supplements after atherosclerosis induction (30 days) | None | Hydroxytyrosol reduced endothelial activation of gums & squalene additionally decreased fibrosis | [7] |
Obese (by diet) & non-obese Wistar rats | Male 8 weeks (42) | High-fat diet combined with exercise training or not (4/8 weeks) | None | Rats fed a high-fat diet showed higher serum ROM & gingival 8-OHdG levels, & gingival GSH/GSSG ratio than rats fed a regular diet that were reduced by exercise training | [83] |
Obese (by diet) & non-obese C57BL/6J mice | Both 4 weeks (80) | High-fat or standard diet with or without moderate exercise after obesity development (4 weeks) | P. gingivalis-soaked or sterile ligatures (last week) | High-fat diet increased P. gingivalis-induced ABL which associated to higher serum levels of TNFα, MCP-1, IL-1β & lower of IL-6 & IL-12p70. However moderate daily exercise decreased ABL & restores cytokines normal levels. | [87] |
Wistar rats | Male 8 weeks (24) | high-cholesterol or regular diet (12 weeks) | None | High-cholesterol diet decreased alveolar bone density & increased TRAP–positive osteoclasts & the expression of 8-OHdG in the periodontal tissue | [85] |
Wistar rats with & without induced periodontitis | Male 8 weeks (32) | high-cholesterol or regular diet (8 weeks) | Application of LPS & proteases or pyrogen free water (last 4 weeks) | High-cholesterol diet increased proliferation of the junctional epithelium with increasing bone resorption & cell-proliferative activity of the junctional epithelium induced by LPS & proteases. | [86] |
Wistar rats with & without induced periodontitis | Male 8 weeks (32) | high-cholesterol or regular diet (8 weeks) | Application of LPS & proteases or pyrogen free water (last 4 weeks) | High-cholesterol diet augmented the induced production of pro-inflammatory cytokines by bacterial products & mitochondrial 8-OHdG in periodontal tissues | [95] |
Sprague-Dawley rats with induced periodontitis | Female 8–9 weeks (95) | Diets containing 17% fish oil & 3% corn oil or 5% corn oil only (22 weeks) | Infection with P. gingivalis (last 12 weeks) | Rat fed on diets containing fish oil had less ABL | [104] |
Sprague-Dawley rats with induced periodontitis | Female 8–9 weeks (82) | Diets containing 17% fish oil & 3% corn oil or 5% corn oil only (22 weeks) | Infection with P. gingivalis 381 or A7A1-28 (last 12 weeks) | Diet containing fish oil led to decreased IL-1β, TNF-α & enhanced IFN-γ, CAT & SOD gingival mRNA levels | [105] |
BALB/c mice with & without induced periodontitis | Female 6–8 weeks (70) | Diet containing 10% tuna oil or sunola oil (57 days) | Orally inoculation with P. gingivalis, with a mixture of P. gingivalis & F. nucleatum or none (last 43 days) | Diet containing 10% tuna oil decreased ABL in inoculated mice | [106] |
Wistar rats | Not given 4 weeks (60) | Diet containing 10% refined fish oil or corn oil (6–8 weeks) | Tooth movement by 20 g continuous force on the lingual side of 1st maxillary molars with a lateral expansion spring (0/3/7/14 from the sixth week) | The diet containing 10% fish oil reduced tooth movement, n° osteoclasts & bone resorption | [107] |
Sprague-Dawley rats with & without induced periodontitis | Male Adults (39) | Orally gavaged with n-3 PUFA (EPA + DHA) or saline supplements (15 days) | LPS or saline injections | n-3 PUFA supplements increased IL-1β & OC serum levels in LPS-treated rats | [108] |
Aged & young Wistar rats | Male 80–90 g (72) | Virgin olive, sunflower or fish oil, as life-long dietary fat sources (6/24 months) | None | At endpoint, virgin olive oil fed rats showed the lowest age-related ABL, followed by those fed on fish oil. Additionally, sunflower oil fed rats showed a high degree of fibrosis & a moderate degree of inflammation | [109] |
Wistar rats | Male 60 days (28) | Hyperlipidic or standard diet (17 weeks) | None | The hyperlipidic diet consumption led to development of more periodontal disease sites defined by an ABL > 0.51 mm (75th percentile) | [84] |
5. Conclusions
Acknowledgments
Conflicts of Interest
References
- DeStefano, F.; Anda, R.F.; Kahn, H.S.; Williamson, D.F.; Russell, C.M. Dental disease and risk of coronary heart disease and mortality. BMJ 1993, 306, 688–691. [Google Scholar] [CrossRef] [PubMed]
- Garcia, R.I.; Krall, E.A.; Vokonas, P.S. Periodontal disease and mortality from all causes in the VA Dental Longitudinal Study. Ann. Periodontol. 1998, 3, 339–349. [Google Scholar] [CrossRef] [PubMed]
- Linden, G.J.; Linden, K.; Yarnell, J.; Evans, A.; Kee, F.; Patterson, C.C. All-cause mortality and periodontitis in 60–70-year-old men: A prospective cohort study. J. Clin. Periodontol. 2012, 39, 940–946. [Google Scholar] [CrossRef] [PubMed]
- Van der Velden, U.; Kuzmanova, D.; Chapple, I.L.C. Micronutritional approaches to periodontal therapy. J. Clin. Periodontol. 2011, 38, 142–158. [Google Scholar] [CrossRef]
- Kaye, E.K. n-3 Fatty acid intake and periodontal disease. J. Am. Diet Assoc. 2010, 110, 1650–1652. [Google Scholar] [CrossRef] [PubMed]
- Halliwell, B. Reactive oxygen species in living systems: Source, biochemistry, and role in human disease. Am. J. Med. 1991, 91, 14–22. [Google Scholar] [CrossRef]
- Bullon, P.; Morillo, J.M.; Ramirez-Tortosa, M.C.; Quiles, J.L.; Newman, H.N.; Battino, M. Metabolic syndrome and periodontitis: Is oxidative stress a common link? J. Dent Res. 2009, 88, 503–518. [Google Scholar] [CrossRef] [PubMed]
- Chapple, I.L.; Matthews, J.B. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontology 2000 2007, 43, 160–232. [Google Scholar] [CrossRef] [PubMed]
- Brock, G.R.; Matthews, J.B.; Butterworth, C.J.; Chapple, I.L.C. Local and systemic antioxidant capacity in periodontitis and health. J. Clin. Periodontol. 2004, 31, 515–521. [Google Scholar] [CrossRef] [PubMed]
- Palmer, R.M.; Wilson, R.F.; Hasan, A.S.; Scott, D.A. Mechanisms of action of environmental factors-tobacco smoking. J. Clin. Periodontol. 2005, 32 (Suppl. 6), 180–195. [Google Scholar] [CrossRef] [PubMed]
- Panjamurthy, K.; Manoharan, S.; Ramachandran, C.R. Lipid peroxidation and antioxidant status n patients with periodontitis. Cell Mol. Biol. Lett. 2005, 10, 255–264. [Google Scholar] [PubMed]
- Chapple, I.L. Reactive oxygen species and antioxidants in inflammatory diseases. J. Clin. Periodontol. 1997, 24, 287–296. [Google Scholar] [CrossRef] [PubMed]
- Janssen-Heininger, Y.M.W.; Poynter, M.E.; Baeuerle, P.A. Recent advances towards understanding redox mechanisms in the activation of nuclear factor κB. Free Radic Biol. Med. 2000, 28, 1317–1327. [Google Scholar] [CrossRef] [PubMed]
- Matthews, J.B.; Wright, H.J.; Ling-Mountford, N.; Cooper, P.R.; Chapple, I.L.C. Neutrophil hyper-responsiveness in periodontitis. J. Dent Res. 2007, 86, 718–722. [Google Scholar] [CrossRef] [PubMed]
- Matthews, J.B.; Wright, H.J.; Roberts, A.; Cooper, P.R.; Chapple, I.L.C. Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clin. Exp. Immunol. 2007, 147, 255–264. [Google Scholar] [CrossRef] [PubMed]
- Gustafsson, A.; Asman, B. Increased release of free oxygen radicals from peripheral neutrophils in adult periodontitis after Fcgamma-receptor stimulation. J. Clin. Periodontol. 1996, 23, 38–44. [Google Scholar] [CrossRef] [PubMed]
- Gustafsson, A.; Asman, B.; Bergström, K. Priming response to inflammatory mediators in hyperreactive peripheral neutrophils from adult periodontitis. Oral Dis. 1997, 3, 167–171. [Google Scholar] [CrossRef] [PubMed]
- Fredriksson, M.; Gustafsson, A.; Bergström, K.; Asman, B. Hyper-reactive peripheral neutrophils in adult periodontitis: generation of chemiluminescence and intracellular hydrogen peroxide after in vitro priming and FcgammaR-stimulation. J. Clin. Periodontol. 1998, 25, 395–398. [Google Scholar] [CrossRef]
- Battino, M.; Ferreiro, M.S.; Bompadre, S.; Leone, L.; Mosca, F.; Bullon, P. Elevated hydroperoxide levels and antioxidant patterns in Papillon-Lefèvre syndrome. J. Periodontol. 2001, 72, 1760–1766. [Google Scholar] [CrossRef] [PubMed]
- Holman, R.T. Autoxidation of fats and related substances. In Progress in Chemistry of Fats and other Lipids; Holman, R.T., Lundberg, W.O., Malkin, T., Eds.; Pergamon Press: London, UK, 1954; pp. 51–98. [Google Scholar] [CrossRef]
- Montebugnoli, L.; Servidio, D.; Miaton, R.A.; Prati, C.; Tricoci, P.; Melloni, C. Poor oral health is associated with coronary heart disease and elevated systemic inflammatory and haemostatic factors. J. Clin. Periodontol. 2004, 31, 25–29. [Google Scholar] [CrossRef] [PubMed]
- Baltacioglu, E.; Akalin, F.A.; Alver, A.; Deger, O.; Karabulut, E. Protein carbonyl levels in serum and gingival crevicular fluid in patients with chronic periodontitis. Arch. Oral Biol. 2008, 53, 716–722. [Google Scholar] [CrossRef] [PubMed]
- Chapple, I.L.; Brock, G.; Eftimiadi, C.; Matthews, J.B. Glutathione in gingival crevicular fluid and its relation to local antioxidant capacity in periodontal health and disease. In Mol. Pathol.; 2002; 55, pp. 367–373. Available online: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1187272 (accessed on 21 February 2015). [Google Scholar]
- Chapple, I.L.; Milward, M.R.; Dietrich, T. The prevalence of inflammatory periodontitis is negatively associated with serum antioxidant concentrations. J. Nutr. 2007, 137, 657–664. [Google Scholar] [PubMed]
- Battino, M.; Ferreiro, M.S.; Quiles, J.L.; Bompadre, S.; Leone, L.; Bullon, P. Alterations in the oxidation products, antioxidant markers, antioxidant capacity and lipid patterns in plasma of patients affected by Papillon-Lefèvre syndrome. Free Radic. Res. 2003, 37, 603–609. [Google Scholar] [CrossRef] [PubMed]
- Baltacioglu, E.; Akalin, F.A.; Alver, A.; Balaban, F.; Unsal, M.; Karabulut, E. Total antioxidant capacity and superoxide dismutase activity levels in serum and gingival crevicular fluid in post-menopausal women with chronic periodontitis. J. Clin. Periodontol. 2006, 33, 385–392. [Google Scholar] [CrossRef] [PubMed]
- Akalin, F.A.; Baltacioglu, E.; Alver, A.; Karabulut, E. Lipid peroxidation levels and total oxidant status in serum, saliva and gingival crevicular fluid in patients with chronic periodontitis. J. Clin. Periodontol. 2007, 34, 558–565. [Google Scholar] [CrossRef] [PubMed]
- Konopka, T.; Król, K.; Kopec, W.; Gerber, H. Total antioxidant status and 8-hydroxy-2′-deoxyguanosine levels in gingival and peripheral blood of periodontitis patients. In Arch. Immunol. Ther. Exp.; 2007; 55, pp. 417–422. Available online: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2766448/ (accessed on 21 February 2015). [Google Scholar]
- Zilinskas, J.; Zekonis, J.; Zekonis, G.; Valantiejiene, A.; Periokaite, R. The reduction of nitroblue tetrazolium by total blood in periodontitis patients and the aged. Stomatologija 2007, 9, 105–108. [Google Scholar] [CrossRef] [PubMed]
- Tonetti, M.S.; van Dyke, T.E.; Working group 1 of the joint EFP/AAP workshop. Periodontitis and atherosclerotic cardiovascular disease: Consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J. Periodontol. 2013, 84, S24–S29. [Google Scholar] [CrossRef] [PubMed]
- Katz, J.; Bhattacharyya, I.; Farkhondeh-Kish, F.; Perez, F.M.; Caudle, R.M.; Heft, M.W. Expression of the receptor of advanced glycation end products in gingival tissues of type 2 diabetes patients with chronic periodontal disease: A study utilizing immunohistochemistry and RT-PCR. J. Clin. Periodontol. 2005, 32, 40–44. [Google Scholar] [CrossRef] [PubMed]
- Koyama, H.; Shoji, T.; Yokoyama, H.; Motoyama, K.; Mori, K.; Fukumoto, S.; Emoto, M.; Shoji, T.; Tamei, H.; Matsuki, H.; et al. Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis. Arterioscler Thromb. Vasc. Biol. 2005, 25, 2587–2593. [Google Scholar] [CrossRef] [PubMed]
- Alikhani, M.; Alikhani, Z.; Boyd, C.; MacLellan, C.M.; Raptis, M.; Liu, R.; Pischona, N.; Trackmana, P.C.; Gerstenfeldb, L.; Graves, D.T. Advanced glycation endproducts stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 2007, 40, 345–353. [Google Scholar] [CrossRef] [PubMed]
- Alikhani, M.; Maclellan, C.M.; Raptis, M.; Vora, S.; Trackman, P.C.; Graves, D.T. Advanced glycation end products induce apoptosis in fibroblasts through activation of ROS, MAP kinases, and the FOXO1 transcription factor. Am. J. Physiol. Cell Physiol. 2007, 292, C850–C856. [Google Scholar] [CrossRef] [PubMed]
- Fahy, E.; Subramaniam, S.; Brown, H.A.; Glass, C.K.; Merrill, A.H., Jr.; Murphy, R.C.; Raetz, C.R.; Russell, D.W.; Seyama, Y.; Shaw, W.; et al. A comprehensive classification system for lipids. J. Lipid Res. 2005, 46, 839–861. [Google Scholar] [CrossRef] [PubMed]
- Rohrbach, S. Effects of dietary polyunsaturated fatty acids on mitochondria. Curr. Pharm. 2009, 15, 4103–4116. [Google Scholar] [CrossRef]
- Aoun, M.; Fouret, G.; Michel, F.; Bonafos, B.; Ramos, J.; Cristol, J.P.; Carbonneau, M.A.; Coudray, C.; Feillet-Coudray, C. Dietary fatty acids modulate liver mitochondrial cardiolipin content and its fatty acid composition in rats with non alcoholic fatty liver disease. J. Bioenerg. Biomembr. 2012, 44, 439–452. [Google Scholar] [CrossRef] [PubMed]
- Lobb, K.; Chow, C.K. Fatty acid classification and nomenclature. In Fatty Acids in Foods and Their Health Implications; Chow, C.K., Ed.; CRC Press: Boca Raton, FL, USA, 2008; pp. 1–15. [Google Scholar]
- Pamplona, R. Membrane phospholipids, lipoxidative damage and molecular integrity: A causal role in aging and longevity. Biochim. Biophys. Acta 2008, 1777, 1249–1262. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. n–3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006, 83, 1505S–1519S. [Google Scholar] [PubMed]
- Zevenbergen, H.; de Bree, A.; Zeelenberg, M.; Laitinen, K.; van Duijn, G.; Flöter, E. Foods with a high fat quality are essential for healthy diets. Ann. Nutr. MeTable 2009, 54, 15–24. [Google Scholar] [CrossRef]
- Uauy, R.; Mena, P.; Valenzuela, A. Essential fatty acids as determinants of lipid requirements in infants, children and adults. Eur. J. Clin. Nutr. 1999, 53, S66–S77. [Google Scholar] [CrossRef] [PubMed]
- Mataix, J.; Quiles, J.L.; Huertas, J.R.; Battino, M.; Mañas, M. Tissue specific interactions of exercise, dietary fatty acids, and vitamin E in lipid peroxidation. Free Radic. Biol. Med. 1998, 24, 511–521. [Google Scholar] [CrossRef] [PubMed]
- Quiles, J.L.; Huertas, J.R.; Mañas, M.; Battino, M.; Mataix, J. Physical exercise affects the lipid profile of mitochondrial membranes in rats fed with virgin olive oil or sunflower oil. Br. J. Nutr. 1999, 81, 21–24. [Google Scholar] [CrossRef] [PubMed]
- Simkiss, K. Cell membranes; barriers, regulators and transducers? Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1998, 120, 17–22. [Google Scholar] [CrossRef] [PubMed]
- Gamliel, A.; Afri, M.; Frimer, A.A. Determining radical penetration of lipid bilayers with new lipophilic spin traps. Free Radic. Biol. Med. 2008, 44, 1394–1405. [Google Scholar] [CrossRef] [PubMed]
- Milatovic, D.; Montine, T.J.; Aschner, M. Measurement of isoprostanes as markers of oxidative stress. Methods Mol. Biol. 2011, 758, 195–204. [Google Scholar] [CrossRef] [PubMed]
- Bielski, B.H.; Arudi, R.L.; Sutherland, M.W. A study of the reactivity of HO2/O2-with unsaturated fatty acids. J. Biol. Chem. 1983, 258, 4759–4761. [Google Scholar] [PubMed]
- Halliwell, B.; Gutteridge, J.M.C. Free radicals in Biology and Medicine, 3rd ed.; Oxford University Press: Oxford, UK, 1999; p. 980. [Google Scholar]
- Pamplona, R.; Barja, G. An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology 2011, 12, 409–435. [Google Scholar] [CrossRef] [PubMed]
- Esterbauer, H.; Schaur, R.J.; Zollner, H. Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11, 81–128. [Google Scholar] [CrossRef] [PubMed]
- Pamplona, R.; Barja, G.; Portero-Otín, M. Membrane fatty acid unsaturation, protection against oxidative stress, and máximum life span: A homeoviscous-longevity adaptation? Ann. N. Y. Acad. Sci. 2002, 959, 475–490. [Google Scholar] [CrossRef] [PubMed]
- Huertas, J.R.; Battino, M.; Lenaz, G.; Mataix, F.J. Changes in mitochondrial and microsomal rat liver coenzyme Q9 and Q10 content induced by dietary fat and endogenous lipid peroxidation. FEBS Lett. 1991, 287, 89–92. [Google Scholar] [CrossRef] [PubMed]
- Huertas, J.R.; Martínez-Velasco, E.; Ibáñez, S.; López-Frías, M.; Ochoa, J.J.; Quiles, J.L.; Parenti-Castelli, G.; Mataix, J.; Lenaz, G. Virgin olive oil protect heart mitochondria from peroxidative damage during aging. BioFactors 1999, 9, 337–343. [Google Scholar] [CrossRef] [PubMed]
- Ochoa-Herrera, J.J.; Huertas, J.R.; Quiles, J.L.; Mataix, J. Dietary oils high in oleic acid, but with different non-glyceride contents, have different effects on lipid profiles and peroxidation in rabbit hepatic mitochondria. J. Nutr. Biochem. 2001, 12, 357–364. [Google Scholar] [CrossRef] [PubMed]
- Huertas, J.R.; Battino, M.; Mataix, F.J.; Lenaz, G. Cytochrome oxidase induction after oxidative stress induced by adriamycin in liver of rats fed with dietary olive oil. Biochem. Biophys. Res. Commun. 1991, 181, 375–382. [Google Scholar] [CrossRef] [PubMed]
- Quiles, J.L.; Huertas, J.R.; Mañas, M.; Ochoa, J.J.; Battino, M.; Mataix, J. Dietary fat type and regular exercise affect mitochondrial composition and function depending on specific tissue in rat. J. Bioenerg. Biomembr. 2001, 33, 127–143. [Google Scholar] [CrossRef] [PubMed]
- Battino, M.; Ferreiro, M.S.; Littarru, G.; Quiles, J.L.; Ramírez-Tortosa, M.C.; Huertas, J.R.; Mataix, J.; Villa, R.F.; Gorini, A. Structural damages induced by peroxidation could account for functional impairment of heavy synaptic mitochondria. Free Radic. Res. 2002, 36, 479–484. [Google Scholar] [CrossRef] [PubMed]
- Pamplona, R.; Portero-Otín, M.; Sanz, A.; Requena, J.; Barja, G. Modification of the longevity-related degree of fatty acid unsaturation modulates oxidative damage to proteins and mitocondrial DNA in liver and brain. Exp. Gerontol. 2004, 39, 725–733. [Google Scholar] [CrossRef] [PubMed]
- Quiles, J.L.; Huertas, J.R.; Mañas, M.; Ochoa, J.J.; Battino, M.; Mataix, J. Oxidative stress induced by exercise and dietary fat modulates the coenzyme Q and vitamin A balance between plasma and mitochondria. Int. J. Vitam. Nutr. Res. 1999, 69, 243–249. [Google Scholar] [CrossRef] [PubMed]
- Quiles, J.L.; Martínez, E.; Ibáñez, S.; Ochoa, J.J.; Martín, Y.; López-Frías, M.; Huertas, J.R.; Mataix, J. Ageing-related tissue-specific alterations in mitochondrial composition and function are modulated by dietary fat type in the rat. J. Bioenerg. Biomembr. 2002, 34, 517–524. [Google Scholar] [CrossRef] [PubMed]
- Ramírez-Tortosa, M.C.; López-Pedrosa, J.M.; Suarez, A.; Ros, E.; Mataix, J.; Gil, A. Olive oil and fish oil enriched diets modify plasma lipids and susceptibility of low density lipoprotein to oxidative modification in free-living male patients with peripheral vascular disease: The Spanish Nutrition Study. Br. J. Nutr. 1999, 82, 31–39. [Google Scholar] [CrossRef] [PubMed]
- Battino, M.; Quiles, J.L.; Huertas, J.R.; RamírezTortosa, M.C.; Cassinello, M.; Mañas, M.; López-Frías, M.; Mataix, J. Feeding fried oil changes antioxidant and fatty acid pattern of rat and affects rat liver mitochondrial respiratory chain components. J. Bioenerg. Biomembr. 2002, 34, 127–134. [Google Scholar] [CrossRef] [PubMed]
- Ochoa, J.J.; Quiles, J.L.; RamirezTortosa, M.C.; Mataix, J.; Huertas, J.R. Dietary oils high in oleic acid but with different unsaponifiable fraction contens have different effects in lipid profile and peroxidation in rabbit-LDL. Nutrition 2002, 18, 60–65. [Google Scholar] [CrossRef] [PubMed]
- Carluccio, M.A.; Massaro, M.; Scoditti, E.; de Caterina, R. Vasculoprotective potential of olive oil components. Mol. Nutr. Food Res. 2007, 51, 1225–1234. [Google Scholar] [CrossRef] [PubMed]
- Astrup, A.; Dyerberg, J.; Elwood, P.; Hermansen, K.; Hu, F.B.; Jakobsen, M.U.; Kok, F.J.; Krauss, R.M.; Lecerf, J.M.; LeGrand, P.; et al. The role of reducing intakes of saturated fat in the prevention of cardiovascular disease: Where does the evidence stand in 2010. Am. J. Clin. Nutr. 2011, 93, 684–688. [Google Scholar] [CrossRef] [PubMed]
- Vance, D.E.; Vance, J.E. Biochemistry of Lipids, Lipoproteins and Membranes; Elsevier Science BV: Amsterdam, The Netherlands, 1996; pp. 1–553. [Google Scholar]
- Wallis, J.G.; Watts, J.L.; Browse, J. Polyunsaturated fatty acid synthesis: What will they think of next? Trends Biochem. Sci. 2002, 27, 467–473. [Google Scholar] [CrossRef] [PubMed]
- Sanz, A.; Caro, P.; Sánchez, J.G.; Barja, G. Effect of lipid restriction on mitocondrial free radical production and oxidative DNA damage. Ann. N. Y. Acad. Sci. 2006, 1067, 200–209. [Google Scholar] [CrossRef] [PubMed]
- Navarro, M.D.; Periago, J.L.; Pita, M.L.; Hortelano, P. The n-3 polyinsaturates fatty acid levels in rat tissue lipids increase in response of dietary olive oil relative to sunflower oil. Lipids 1994, 29, 845–849. [Google Scholar] [CrossRef] [PubMed]
- Escudero, A.; Montilla, J.C.; García, J.M.; Sánchez Quevedo, M.C.; Periago, J.L.; Hortelano, P.; Suárez, M.D. Effect of dietary n-6, n-3, n-9 fatty acids on membranae lipid composicion and morphology of rat erythrocytes. Bioquem Biophys. Acta 1998, 1394, 65–73. [Google Scholar] [CrossRef]
- Ayre, K.J.; Hulbert, A.J. Dietary fatty acid profiles affect indurance in rats. Lipids 1997, 32, 1265–1270. [Google Scholar] [CrossRef] [PubMed]
- Pamplona, R.; Barja, G. Aging rate, free radical production, and constitutive sensitivity to lipid peroxidation: insights from comparative studies. In Biology of Aging and Its Modulation Series. Aging at the Molecular Level; van Zglinicki, T., Ed.; Kluwer Academic Publisher: New York, NY, USA, 2003; Volume 1, pp. 47–64. [Google Scholar]
- Gibson, R.A.; McMurchie, E.J.; Charnock, J.S.; Kneebone, G.M. Homeostatic control of membrane fatty acid composition in the rat after dietary lipid treatment. Lipids 1984, 19, 942–951. [Google Scholar] [CrossRef] [PubMed]
- Giron, M.D.; Mataix, J.; Suárez, M.D. Long term effects of dietary monounsaturated and polyunsaturated fatty acid of lipid composition of erythrocyte membrane in dog. Comp. Biochem. Fisiol. 1992, 102, 197–201. [Google Scholar] [CrossRef]
- Quiles, J.L.; Pamplona, R.; Ramírez-Tortosa, M.C.; Naudí, A.; Araujo-Nepomuceno, E.; Portero-Otín, M.; López-Frías, M.; Battino, M.; Ochoa, J.J. Coenzyme Q addition to an n-6 PUFA-rich diet resermbles benefits on age-related mitocondrial DNA deletion and oxidative stress of a MUFA-rich diet in rat heart. Mech. Aging Dev. 2010, 131, 38–47. [Google Scholar] [CrossRef] [PubMed]
- Martin, F. Efecto de la Adaptación al Tipo de Grasa Dietética y del Ejercicio Físico Sobre la Composición Lipídica de Membranas Microsomales y Mitocondriales de Distintos Órganos. Doctor’s Thesis, University of Granada, Granada, Spain, 2002. [Google Scholar]
- Simopoulos, A.P. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp. Biol. Med. 2008, 233, 674–688. [Google Scholar] [CrossRef]
- Arab, L. Biomarkers of fat and fatty acid intake. J. Nutr. 2003, 133, 925S–932S. [Google Scholar] [PubMed]
- Maddux, B.A.; See, W.; Lawrence, J.C., Jr.; Goldfine, A.L.; Goldfine, I.D.; Evans, J.L. Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolar concentrations of α-lipoic acid. Diabetes 2001, 50, 404–410. [Google Scholar] [CrossRef] [PubMed]
- Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M. Are oxidative stress activated signaling pathways mediators of insulin resistance and β-cell dysfunction? Diabetes 2003, 52, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Matsuzawa-Nagata, N.; Takamura, T.; Ando, H.; Nakamura, S.; Kurita, S.; Misu, H.; Ota, T.; Yokoyama, M.; Honda, M.; Miyamoto, K.; et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 2008, 57, 1071–1077. [Google Scholar] [CrossRef] [PubMed]
- Azuma, T.; Tomofuji, T.; Endo, Y.; Tamaki, N.; Ekuni, D.; Irie, K.; Kasuyama, K.; Kato, T.; Morita, M. Effects of exercise training on gingival oxidative stress in obese rats. Arch. Oral Biol. 2011, 56, 768–774. [Google Scholar] [CrossRef] [PubMed]
- Cavagni, J.; Wagner, T.; Gaio, E.; Rego, R.; Torres, I.; Rosing, C. Obesity may increase the occurrence of spontaneous periodontal disease in Wistar rats. Arch. Oral Biol. 2013, 58, 1034–1039. [Google Scholar] [CrossRef] [PubMed]
- Sanbe, T.; Tomofuji, T.; Ekuni, D.; Azuma, T.; Tamaki, N.; Yamamoto, T. Oral administration of vitamin C prevents alveolar bone resorption induced by high dietary cholesterol in rats. J. Periodontol. 2007, 78, 2165–2170. [Google Scholar] [CrossRef] [PubMed]
- Tomofuji, T.; Kusano, H.; Azuma, T.; Ekuni, D.; Yamamoto, T.; Watanabe, T. Effects of a high-cholesterol diet on cell behavior in rat periodontitis. J. Dent Res. 2005, 84, 752–756. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Q.; Leeman, S.; Amar, S. Signaling mechanisms in the restoration of impaired immune function due to diet-induced obesity. Proc. Natl. Acad. Sci. USA 2011, 108, 2867–2872. [Google Scholar] [CrossRef] [PubMed]
- Bullon, P.; Quiles, J.L.; Morillo, J.M.; Rubini, C.; Goteri, G.; Granados-Principal, S.; Battino, M.; Ramirez-Tortosa, M. Gingival vascular damage in atherosclerotic rabbits: Hydroxytyrosol and squalene benefits. Food Chem. Toxicol. 2009, 47, 2327–2331. [Google Scholar] [CrossRef] [PubMed]
- Cascio, G.; Schiera, G.; di Liegro, I. Dietary fatty acids in metabolic syndrome, diabetes and cardiovascular diseases. Curr. Diabetes Rev. 2012, 8, 2–17. [Google Scholar] [CrossRef] [PubMed]
- Amar, S.; Leeman, S. Periodontal innate immune mechanisms relevant to obesity. Mol. Oral Microbiol. 2013, 28, 331–341. [Google Scholar] [CrossRef] [PubMed]
- Bullon, P.; Newman, H.N.; Battino, M. Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: A shared pathology via oxidative stress and mitochondrial dysfunction? Periodontology 2000 2014, 64, 139–153. [Google Scholar] [CrossRef] [PubMed]
- Genco, R.J.; Borgnake, W.S. Risk factors for periodontal disease. Periodontology 2000 2013, 62, 59–94. [Google Scholar] [CrossRef] [PubMed]
- Iacopino, A.M. Periodontitis and diabetes interrelationships: Role of inflammation. Ann. Periodontol. 2001, 6, 125–137. [Google Scholar] [CrossRef] [PubMed]
- Soskolne, W.A.; Klinger, A. The Relationship between periodontal diseases and diabetes: An Overview. Ann. Periodontol. 2001, 6, 91–98. [Google Scholar] [CrossRef] [PubMed]
- Tomofuji, T.; Azuma, T.; Kusano, H.; Sanbe, T.; Ekuni, D.; Tamaki, N.; Yamamoto, T.; Watanabe, T. Oxidative damage of periodontal tissue in the rat periodontitis model: Effects of a high-cholesterol diet. FEBS Lett. 2006, 580, 3601–3604. [Google Scholar] [CrossRef] [PubMed]
- Naqvi, A.; Buettner, C.; Phillips, R.; Davis, R.; Mukamal, K. n-3 Fatty acids and periodontitis in US adults. J. Am. Diet Assoc. 2010, 110, 1669–1675. [Google Scholar] [CrossRef] [PubMed]
- Ramirez-Tortosa, M.C.; Quiles, J.L.; Battino, M.; Granados, S.; Morillo, J.M.; Bompadree, S.; Newman, H.N.; Bullon, P. Periodontitis is associated with altered plasma fatty acids and cardiovascular risk markers. Nutr. Metab. Cardiovasc. Dis. 2010, 20, 133–139. [Google Scholar] [CrossRef] [PubMed]
- Figueredo, C.M.; Martinez, G.L.; Koury, J.C.; Fischer, R.G.; Gustafsson, A. Serum levels of long chain polyunsaturated fatty acids in patients with periodontal disease. J. Periodontol. 2013, 84, 675–682. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, M.; Yoshihara, A.; Moynihan, P.; Watanabe, R.; Taylor, G.W.; Miyazaki, H. Longitudinal relationship between dietary ω-3 fatty acids and periodontal disease. Nutrition 2010, 26, 1105–1109. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, M.; Taylor, G.W.; Moynihan, P.; Yoshihara, A.; Muramatsu, K.; Watanabe, R.; Miyazaki, H. Dietary ratio of n-6 to n-3 polyunsaturated fatty acids and periodonta ldisease in community-based older Japanese: A 3-year follow-up study. Prostaglandins Leukot. Essent. Fatty Acids 2011, 85, 107–112. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, M.; Manz, M.; Moynihan, P.; Yoshihara, A.; Muramatsu, K.; Watanabe, R.; Miyazaki, H. Relationship between saturated fatty acids and periodontal disease. J. Dent Res. 2011, 90, 861–867. [Google Scholar] [CrossRef] [PubMed]
- Rosenstein, E.D.; Kushner, L.J.; Kramer, N.; Kazandjian, G. Pilot study of dietary fatty acid supplementation in the treatment of adult periodontitis. Prostaglandins Leukot. Essent. Fatty Acids 2003, 68, 213–218. [Google Scholar] [CrossRef] [PubMed]
- El-Sharkawy, H.; Aboelsaad, N.; Eliwa, M.; Darweesh, M.; Alshahat, M.; Kantarci, A.; Hasturk, H.; van Dyke, T. Adjunctive treatment of chronic periodontitis with daily dietary supplementation with omega-3 Fatty acids and low-dose aspirin. J. Periodontol. 2010, 81, 1635–1643. [Google Scholar] [CrossRef] [PubMed]
- Kesavalu, L.; Vasudevan, B.; Raghu, B.; Browning, E.; Dawson, D.; Novak, J.M.; Correll, M.C.; Steffen, M.J.; Bhattacharya, A.; Fernandes, G.; et al. Omega-3 fatty acid effect on alveolar bone loss in rat. J. Dent Res. 2006, 85, 648–652. [Google Scholar] [CrossRef] [PubMed]
- Kesavalu, L.; Bakthavatchalu, V.; Rahman, M.M.; Su, J.; Raghu, B.; Dawson, D.; Fernandes, G.; Ebersole, J.L. Omega-3 fatty acid regulates inflammatory cytokine/mediator messenger RNA expression in Porphyromonas gingivalis-induced experimental periodontal disease. Oral Microbiol. Immunol. 2007, 22, 232–239. [Google Scholar] [CrossRef] [PubMed]
- Bendyk, A.; Marino, V.; Zilm, P.S.; Howe, P.; Bartold, P.M. Effect of dietary omega-3 polyunsaturated fatty acids on experimental periodontitis in the mouse. J. Periodontol. Res. 2009, 44, 211–216. [Google Scholar] [CrossRef]
- Iwamati-Miromoto, Y.; Yamaguchi, K.; Tanne, K. Influence of dietary n-3 polyunsaturated acids fatty acid on experimental tooth movement in rats. Angle Orthodontist. 1999, 64, 365–371. [Google Scholar]
- Vardar-Sengul, S.; Buduneli, N.; Buduneli, E.; Kardeşler, L.; Baylas, H.; Atilla, G.; Lappin, D.; Kinane, D. Dietary supplementation of omega-3 fatty acid and circulating levels of interleukin-1beta, osteocalcin, and C-reactive protein in rats. J. Periodontol. 2006, 77, 814–820. [Google Scholar] [CrossRef] [PubMed]
- Bullon, P.; Battino, M.; Varela-Lopez, A.; Perez-Lopez, P.; Granados-Principal, S.; Ochoa, J.J.; Ramirez-Tortosa, M.C.; Cordero, M.; Gonzalez-Alonso, A.; Ramirez-Tortosa, C.L.; et al. Diets based on virgin olive oil or fish oil but not on sunflower oil prevent age-related alveolar bone resorption by mitochondrial-related mechanisms. PLoS ONE 2013, 8, e74234. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, M.; Yoshihara, A.; Hirotomi, T.; Ogawa, H.; Hanada, N.; Miyazaki, H. Longitudinal study on the relationship between serum albumin and periodontal disease. J. Clin. Periodontol. 2008, 35, 291–296. [Google Scholar] [CrossRef] [PubMed]
- Vardar, S.; Buduneli, E.; Turkoğlu, O.; Berdeli, A.; Baylas, H.; Başkesen, A.; Atilla, G. Therapeutic versus prophylactic plus therapeutic administration of omega-3 fatty acid on endotoxin-induced periodontitis in rats. J. Periodontol. 2004, 75, 1640–1646. [Google Scholar] [CrossRef] [PubMed]
- Campan, P.; Planchand, P.O.; Duran, D. Pilot study on n-3 polyunsaturated fatty acids in the treatment of human experimental gingivitis. J. Clin. Periodontol. 1997, 24, 907–913. [Google Scholar] [CrossRef] [PubMed]
- Granados-Principal, S.; Quiles, J.L.; Ramirez-Tortosa, C.L.; Ramirez-Tortosa, M.C.; Sanchez-Rovira, P. Hydroxytyrosol: From laboratory investigations to future clinical trials. Nutr. Rev. 2010, 68, 191–206. [Google Scholar] [CrossRef] [PubMed]
- Salami, M.; Galli, C.; de Angelis, L.; Visioli, F. Formation of F2-isoprostanes in oxidized low density lipoprotein: Inhibitory effect of hydroxytyrosol. Pharmacol. Res. 1995, 31, 275–279. [Google Scholar] [CrossRef] [PubMed]
- Leenen, R.; Roodenburg, A.J.; Vissers, M.N.; Schuurbiers, J.A.; van Putte, K.P.; Wiseman, S.A.; van de Put, F.H. Supplementation of plasma with olive oil phenols and extracts: influence on LDL oxidation. J. Agric. Food Chem. 2002, 50, 1290–1297. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez-Santiago, M.; Martin-Bautista, E.; Carrero, J.J.; Fonolla, J.; Baro, L.; Bartolome, M.V.; Gil-Loyzaga, P.; Lopez-Huertas, E. One-month administration of hydroxytyrosol, a phenolic antioxidant present in olive oil, to hyperlipemic rabbits improves blood lipid profile, antioxidant status and reduces atherosclerosis development. Atherosclerosis 2006, 188, 35–42. [Google Scholar] [CrossRef] [PubMed]
- Marrugat, J.; Covas, M.-I.; Fitó, M.; Schröder, H.; Miró-Casas, E.; Gimeno, E.; López-Sabater, M.C.; de la Torre, R.; Farré, M.; SOLOS Investigators. Effects of differing phenolic content in dietary olive oils on lipids and LDL oxidation. Eur. J. Nutr. 2004, 43, 140–147. [Google Scholar] [CrossRef] [PubMed]
- Maiuri, M.C.; de Stefano, D.; di Meglio, P.; Irace, C.; Savarese, M.; Sacchi, R.; Cinelli, M.P.; Carnuccio, R. Hydroxytyrosol, a phenolic compound from virgin olive oil, prevents macrophage activation. Naunyn-Schmiedeberg’s Arch. Pharmacol. 2005, 371, 457–465. [Google Scholar] [CrossRef]
- Newmark, H.L. Is oleic acid or squalene the important preventive agent? Am. J. Clin. Nutr. 2000, 72, 502–502. [Google Scholar] [PubMed]
- Kohno, Y.; Egawa, Y.; Itoh, S.; Nagaoka, S.; Takahashi, M.; Mukai, K. Kinetic study of quenching reaction of singlet oxygen and scavenging reaction of free radical by squalene in n-butanol. Biochim. Biophys. Acta 1995, 1256, 52–56. [Google Scholar] [CrossRef] [PubMed]
- Aioi, A.; Shimizu, T.; Kuriyama, K. Effect of squalene on superoxide anion generation induced by a skin irritant, lauroylsarcosine. Int. J. Pharm. 1995, 113, 159–164. [Google Scholar] [CrossRef]
- Huang, Z.-R.; Lin, Y.-K.; Fang, J.-Y. Biological and Pharmacological Activities of Squalene and Related Compounds: Potential Uses in Cosmetic Dermatology. Molecules 2009, 14, 540–554. [Google Scholar] [CrossRef] [PubMed]
- Passi, S.; de Pità, O.; Puddu, P.; Littarru, G.P. Lipophilic Antioxidants in Human Sebum and Aging. Free Radic. Res. 2002, 36, 471–477. [Google Scholar] [CrossRef] [PubMed]
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Varela-López, A.; Quiles, J.L.; Cordero, M.; Giampieri, F.; Bullón, P. Oxidative Stress and Dietary Fat Type in Relation to Periodontal Disease. Antioxidants 2015, 4, 322-344. https://doi.org/10.3390/antiox4020322
Varela-López A, Quiles JL, Cordero M, Giampieri F, Bullón P. Oxidative Stress and Dietary Fat Type in Relation to Periodontal Disease. Antioxidants. 2015; 4(2):322-344. https://doi.org/10.3390/antiox4020322
Chicago/Turabian StyleVarela-López, Alfonso, José L. Quiles, Mario Cordero, Francesca Giampieri, and Pedro Bullón. 2015. "Oxidative Stress and Dietary Fat Type in Relation to Periodontal Disease" Antioxidants 4, no. 2: 322-344. https://doi.org/10.3390/antiox4020322
APA StyleVarela-López, A., Quiles, J. L., Cordero, M., Giampieri, F., & Bullón, P. (2015). Oxidative Stress and Dietary Fat Type in Relation to Periodontal Disease. Antioxidants, 4(2), 322-344. https://doi.org/10.3390/antiox4020322