In recent years, there has been a tremendous expansion in medical and dental research concerned with free radicals, reactive oxygen species, and anti-oxidant defense mechanisms. This review is intended to provide a critical, up-to-date summary of the field, with particular emphasis on its implications for the application of "anti-oxidant therapy" in periodontal disease. We have reviewed the nomenclature, mechanisms of actions, features, and sources of most common free radicals and reactive oxygen species, as well as analyzed the typical biological targets for oxidative damage. Based on a review of direct and indirect anti-oxidant host defenses, particularly in relation to the key role of polymorphonuclear neutrophils in periodontitis, we review current evidence for oxidative damage in chronic inflammatory periodontal disease, and the possible therapeutic effects of anti-oxidants in treating and/or preventing such pathology, with special attention to vitamin E and Co-enzyme Q.
References
1.
Allison AC (1997). Antioxidant drug targeting. In: Antioxidants in disease mechanisms and therapy. Sies H, editor. Advances in pharmacology. Vol. 38. San Diego: Academic Press, pp. 273-291.
2.
Altman LC, Baker C., Fleckman P., Luchtel D., Oda D. (1992). Neutrophil-mediated damage to human gingival epithelial cells. J Periodont Res27:70-79.
3.
Armeni T., Tomasetti M., Svegliati Baroni S., Saccucci F., Marra M., Pieri C., et al. (1997). Dietary restriction affects antioxidant levels in rat liver mitochondria during ageing. Molec Aspects Med18(Suppl):241-245.
4.
Ashkenazi M., White RR, Dennison DK (1992). Neutrophil modulation by A. actinomycetemcomitans. II. Phagocytosis and development of respiratory burst. J Periodont Res27:457-465.
5.
Asman B. (1988). Peripheral PMN cells in juvenile periodontitis. Increased release of elastase and oxygen radicals after stimulation with opsonized bacteria. J Clin Periodontol153:360-364.
6.
Asman B., Engstrom PE, Olsson T., Bergstrom K. (1984). Increased luminol enhanced chemiluminescence from peripheral granulocytes in juvenile periodontitis. Scand J Dent Res92:218-233.
7.
Asman B., Wijkander P., Hjerpe A. (1994). Reduction of collagen degradation in experimental granulation tissue by vitamin E and selenium. J Clin Periodontol21:45-47.
8.
Atleva R., Tomasetti M., Battino M., Curatola G., Littarru GP, Folkers K. (1995). The roles of CoQ10 in preventing peroxidation of LDL subfractions. Proc Natl Acad Sci USA92:9388-9391.
9.
Battino M., Ferri E., Girotti S., Lenaz G. (1991a). Free radical scavenging activity of coenzyme Q measured by a chemiluminescent assay. Anal Chim Acta255:367-371.
10.
Battino M., Ferri E., Gattavecchia E., Sassi S., Lenaz G. ( 1991b). Coenzyme Q as a possible membrane protecting agent against γ-irradiation damages. In: Biomedical and clinical aspects of Coenzyme Q. Vol. 6. Folkers K, Littarru GP, Yamagami T, editors. Amsterdam: Elsevier, pp. 181-190.
11.
Battino M., Lenaz G., Littarru GP (1993). Evidences for long chain CoQ homologs involvement in free radical scavenging activity. In: Free radicals and antioxidants in nutrition. Corongiu F, Banni S, Dessi MA, Rice-Evans C, editors. London: Richelieu Press, pp. 37-49.
12.
Battino M., Gorini A., Villa RF, Genova ML, Bovina C., Sassi S., et al. ( 1995). Coenzyme Q content in synaptic and non-synaptic mitochondria from different brain regions in the ageing rat. Mech Ageing Dev78:173-187.
13.
Battino M., Littarru GP, Gorini A., Villa RF (1996). Coenzyme Q, peroxidation and cytochrome oxidase features after Parkinson's-like disease by MPTP toxicity in intra-synaptic and non-synaptic mitochondria from Macaca fascicularis cerebral cortex and hippocampus: action of dihydroergocriptine. Neurochem Res21:1505-1514.
14.
Battino M., Ferri E., Gattavecchia E., Breccia A., Genova ML, Littarru GP, et al. (1997a). Mitochondrial respiratory chain features after γ-irradiation. Free Rad Res26:431-438.
15.
Battino M., Svegliati Baroni S., Littarru GP, Bompadre S., Leone L., Gorini A., et al. (1997b). Coenzyme Q homologs and vitamin E in synaptic and non-synaptic occipital cerebral cortex mitochondria in the ageing rat. Molec Aspects Med18(Suppl):279-282.
Berlett BS, Stadtman ER ( 1997). Protein oxidation in aging, disease and oxidative stress. J Biol Chem272:20313-20316.
18.
Bimstein E., Lustmann J., Sela MN, Ben Neriah Z., Soskolne WA (1990). Periodontitis associated with Papillon-Lefevre syndrome. J Periodontol61:373-377.
19.
Bobyrev VN, Rozkolupa NV, Skripnikova TP (1994a). Experimental and clinical bases for the use of antioxidants as agents for treating and preventing periodontitis. Stomatologiia73(3):11-18.
20.
Bobyrev VN, Kovalev EV, Rozkolupa NV, Eremina NF, Voskresenskii ON (1994b). Biochemical and ultrastructural changes in the periodontium during the chronic administration of pro-oxidant xenobiotics. Stomatologiia73(4):57-61.
21.
Bors W., Heller W., Michel C., Stettmaier K. (1996). Flavonoids and polyphenols: chemistry and biology. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 409-466.
22.
Bowry VW, Stocker R. (1993). Tocopherol-mediated peroxidation. The prooxidant effect of vitamin E on the radical initiated oxidation of human low density lipoprotein. J Am Chem Soc115:6029-6040.
23.
Bowry VW, Ingold KU, Stocker R. (1992). Vitamin E in human low density lipoprotein. When and how this antioxidant becomes pro-oxidant. Biochem J288:341-344.
24.
Brown LAS, Jones DP (1996). The biology of ascorbic acid. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 117-154.
25.
Buettner GR, Jurkiewicz BA (1996). Chemistry and biochemistry of ascorbic acid. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 91-115.
26.
Bullon P., Pascual A., Fernandez-Novoa MC, Borobio MV, Muniain MA, Camacho F. (1993). Late onset Papillon-Lefevre syndrome? A chromosomic, neutrophil function and microbiological study. J Clin Periodontol20:662-667.
27.
Cadenas E. (1989). Biochemistry of oxygen toxicity. Ann Rev Biochem58:79-110.
28.
Carlsson J., Larsen IT, Edlund MB (1993). Peptostreptococcus micros has a uniquely high capacity to form hydrogen sulfide from glutathione. Oral Microbiol Immunol8:42-45.
29.
Cerna H., Vesely J. Fingerova H., Pohanska J. (1988). Blood serum vitamin E and A levels during peroral therapy of periodontal disease with zinc sulphate. Acta Univ Palacki Olomuc Fac Med119:187-193.
30.
Cerna H., Vesely J., Nastoupilova E., Lechner J., Fingerova H., Pohanka J. (1990). Periodontium and vitamin E and A in pregnancy. Acta Univ Palacki Olomuc Fac Med125:173-179.
31.
Cerna H., Vesely J., Krikal Z. (1992). Vitamin E and A and periodontium in pregnant diabetics. Acta Univ Palacki Olomuc Fac Med134:93-95.
32.
Chapple IL (1997). Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodont24:287-296.
33.
Charon JA, Joachim F., Champagne C., Torpier G., Capron A. (1987). Effect of dental plaque on the oxidative metabolism of normal neutrophils. Oral Microbiol Immunol2:92-96.
34.
Cohen ME, Meyer DM (1993). Effect of dietary vitamin E supplementation and rotational stress on alveolar bone loss in rice rats. Arch Oral Biol38:601-606.
35.
Cohen RE, Ciancio SG, Mather ML, Curro FA (1991). Effect of vitamin E gel, placebo gel and chlorhexidine on periodontal disease. Clin Prev Dent13:20-24.
36.
Deguchi S., Hori T., Creamer H., Gabler W. (1990). Neutrophil-mediated damage to human periodontal ligament-derived fibroblast: role of lipopolysaccharide. J Periodont Res25:293-299.
37.
Deviatkina TA, Tarasenko LM, Kovalenko EG (1989). Antioxidant deficiency and reaction of tissues on the acute emotional-pain stress. Vopr Med Khim35:45-49.
38.
Diplock AT (1994). Antioxidants and disease prevention. Molec Aspects Med15:293-376.
39.
Ellegaard B., Borregaard N., Ellegaard J. (1984). Neutrophil chemotaxis and phagocytosis in juvenile peridontitis. J Periodont Res19:261-268.
40.
Enwonwu CO (1994). Cellular and molecular effects of malnutrition and their relevance to periodontal disease. J Clin Periodontol21:643-657.
41.
Enwonwu CO (1995). Interface of malnutrition and periodontal disease. Am J Clin Nutr61(Suppl):430-436.
42.
Esterbauer H. (1993). Cytotoxicity and genotoxicity of lipid-oxidation products. Am J Clin Nutr57(Suppl):779-786.
43.
Esterbauer H., Schaur RJ, Zollner H. (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Rad Biol Med11:81-128.
44.
Ferri E., Gattavecchia E., Feroci G., Battino M. (1994). Interaction between reactive oxygen species and coenzyme Q10 in an aprotic medium: a cyclic voltammetry study. Molec Aspects Med15(Suppl):83-88.
45.
Firatli E., Unal T., Onan U., Sandalli P. (1994). Anti-oxidative activities of some chemotherapeutics. A possible mechanism in reducing gingival inflammation. J Clin Periodontol21:680-683.
46.
Folkers K., Watanabe T. (1977). Bioenergetics in clinical medicine. X. Survey of the adjunctive use of Coenzyme Q with oral therapy in treating periodontal disease. J Med8:333-348.
47.
Frei B., Kim MC, Ames BN ( 1990). Ubiquinol-10 is an effective lipid-soluble antioxidant at physiological concentrations. Proc Natl Acad Sci USA87:4879-4883.
48.
Fujikawa K. (1983). Alpha-tocopherol content in the human gingiva in chronic marginal periodontitis. Nippon Shishubyo Gakkai Kaishi25:178-184 [in Japanese].
49.
Gomez RS, Da Costa JE, Lorentz TM, Almeida Garrocho A., Nogueira-Machado JA (1994). Chemoluminescence generation and MTT dye reduction by polymorphonuclear leukocytes from periodontal disease patients. I Periodont Res29:109-112.
50.
Goultschin J., Levy H. ( 1986). Inhibition of superoxide generation by human polymorphonuclear leukocytes with chlorhexidine. Its possible relation to periodontal disease. J Periodontol57:422-425.
51.
Guarnieri C., Zucchelli G., Bernardi F., Scheda M., Valentini AF, Calandriello M. (1991). Enhanced superoxide production with no change of the antioxidant activity in gingival fluid of patients with chronic adult periodontitis. Free Rad Res Commun15:11-16.
52.
Gustafsson A., Asman B. (1996). Increased release of free oxygen radicals from peripheral neutrophils in adult periodontitis after Fcy-receptor stimulation. J Clin Periodontol23:38-44.
53.
Gutteridge JMC, Halliwell B. (1994). Antioxidants in nutrition, health, and disease. New York: Oxford University Press.
54.
Halliwell B. (1994). Free radicals, antioxidants and human disease: curiosity, cause or consequence. Lancet344:721-724.
55.
Halliwell B. (1996). Uric acid: an example of antioxidant evaluation. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 243-256.
56.
Halliwell B. (1997). Antioxidants: the basics-what they are and how to evaluate them. In: Antioxidants in disease mechanisms and therapy. Advances in pharmacology. Vol. 38. San Diego: Academic Press, pp. 3-20.
57.
Halliwell B., Gutteridge JMC (1985). Free radicals in biology and medicine. New York: Oxford University Press.
58.
Halliwell B., Gutteridge JM (1990). Role of free radicals and catalytic metal ions in human disease: an overview. Meth Enzymol186:1-85.
59.
Handelman GJ (1996). Carotenoids as scavengers of active oxygen species. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 259-314.
60.
Hanioka T., McRee JT, Xia L.-J, Shizukuishi S., Folkers K. (1993). Therapy with Coenzyme Q10 for patients with periodontal disease.2. Effect of Coenzyme Q10 on the immune systemI Dent Health43:667-672.
61.
Hanioka T., Tanaka M., Ojima M., Shizukuishi S., Folkers K. (1994). Effect of topical application of Coenzyme Q10 on adult periodontitis. Molec Aspects Med15(Suppl):241-248.
62.
Hansen IL, Iwamoto Y., Kishi T., Folkers K., Thompson LE (1976). Bioenergetics in clinical medicine. IX. Gingival and leucocytic deficiencies of Coenzyme Q10 in patients with periodontal disease. Res Commun Chem Pathol Pharmacol14:729-738.
63.
Henle ES, Linn S. ( 1997). Formation, prevention and repair of DNA damage by iron/hydrogen peroxide. J Biol Chem272:19095-19098.
64.
Hsieh C., Inoshita E., Hanioka T., Tamagawa H., Takagaki M., Shizukuishi S. (1983). Changes in coenzyme Q-dependent enzyme activities in the inflamed gingiva of dogs. J Osaka Univ Dent Sch23:93-98.
65.
Huertas JR, Battino M., Lenaz G., Mataix FJ (1991). Changes in mitochondrial and microsomal rat liver coenzyme Q9 and Q10 content induced by dietary fat and endogenous lipid peroxidation. FEBS Lett287:89-92.
66.
Ignarro L, Murad F, editors (1995). Nitric oxide. Biochemistry, molecular biology, and therapeutic implications. In: Advances in pharmacology. Vol. 34. San Diego: Academic Press.
67.
Iwamoto Y., Nakamura R., Folkers K., Morrison RF (1975). Study of periodontal disease and Coenzyme Q. Res Commun Chem Pathol Pharmacol11:265-271.
68.
Iwamoto Y., Watanabe T., Okamoto H., Ohata N., Folkers K. (1981). Clinical effect of Coenzyme Q10 on periodontal disease. In: Biomedical and clinical aspects of Coenzyme Q. Vol. 3. Folkers K, Yamamura Y, editors. Amsterdam: Elsevier, pp. 109-119.
69.
Jacob RA, Omaye ST, Skala JH, Leggott PJ, Rothman DL, Murray PA (1987). Experimental vitamin C depletion and supplementation in young men. Nutrient interactions and dental health effects. Ann NY Acad Sci498:333-346.
70.
lacobson MD (1996). Reactive oxygen species and programmed cell death. TIBS21:83-86.
71.
Kagan VE, Serbinova EA, Packer L. (1990). Antioxidant effects of ubiquinones in microsomes and mitochondria are mediated by tocopherol recycling. Biochem Biophys Res Commun169:851-857.
72.
Kagan VE, Serbinova EA, Fore T., Scita G., Packer L. (1992). Recycling of vitamin E in human low density lipoprotein. J Lipid Res33:385-397.
73.
Kagan VE, Nohl H., Quinn PJ (1996). Coenzyme Q: its role in scavenging and generation of radicals in membranes. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 157-201.
74.
Katsuragi H., Hasegawa A., Saito K. (1997). Distribution of metallothionein in cigarette smokers and non smokers in advanced periodontitis patients. J Periodontol68:1005-1009.
75.
Kettle AJ (1996). Neutrophils convert tyrosyl residues in albumin to chlorotyrosine. FEBS Lett379:103-106.
76.
Khmelevskii IUV, Danilevskii NF, Borisenko AV, Poberezkina NV ( 1985). Effect of vitamin A, E and K on the indices of the glutathione antiperoxide system in gingival tissues in periodontitis. Vopr Pitan4:54-56.
77.
Kimura S., Yonemura T., Kaya H. ( 1993). Increased oxidative product formation by peripheral blood polymorphonuclear leukocytes in human periodontal disease. J Periodont Res28:197-203.
78.
Kontush A., Meyer S., Finckh B., Kohlschütter A., Beisiegel U. (1996). a-tocopherol as a reductant for Cu(II) in human lipoproteins. J Biol Chem271:11106-11112.
79.
Lala A., Amano A., Sojar HT, Radel SJ, De Nardin E. (1994). P. gingivalis trypsin-like protease: a possible natural ligand for the neutrophil formyl peptide receptor. Biochem Biophys Res Commun199:1489-1496.
80.
Leino L., Hurttia HM, Sorvajarvi K., Sewon LA (1994). Increased respiratory burst activity is associated with normal expression of IgG-Fc-receptors and complement receptors in peripheral neutrophils from patients with juvenile periodontitis. J Periodont Res29:179-184.
81.
Levitskii AP, Kozlianina NP, Skliar VE (1987). Lipid peroxidation and antioxidant systems in cat periodontal tissue. Vopr Med Khim33:107-111.
82.
Li KL, Vogel R., Jeffcoat MK, Alfano MC, Smith MA, Collins JG, et al. (1996). The effect of ketoprofen creams on periodontal disease in rhesus monkey. J Periodont Res31:525-532.
83.
Lister RE (1995). Coenzyme Q10 and periodontal disease (letter). Br Dent J179:200-201.
84.
Littarru GP, Nakamura R., Ho L., Folkers K., Kuzell WC (1971). Deficiency of coenzyme Q10 in gingival tissue from patients with periodontal disease. Proc Natl Acad Sci USA68:2332-2335.
85.
Littarru GP, Battino M., Folkers K. (1996). Clinical aspects of coenzyme Q: improvement of cellular bioenergetics or antioxidant protection? In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 203-239.
86.
Livrea MA, Tesoriere L., Freisleben HJ (1996). Vitamin A as an antioxidant. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 371-405.
87.
Lodi R., Rinaldi R., Gaddi A., Iotti S., D'Alessandro R., Scoz N., et al. (1997). Brain and skeletal muscle bioenergetics failure in familial hypobetalipoproteinemia. J Neurol Neurosurg Psychiatry62:574-580.
88.
Loesche WJ, Robinson JP, Flynn M., Hudson JL, Duque RE (1988). Reduced oxidative function in gingival crevicular neutrophils in periodontal diseases. Infect Immun56:156-160.
89.
Marton IJ, Balla G., Hegedus C., Redi P., Szilagyi Z., Karmazsin L., et al. (1993). The role of reactive oxygen intermediates in the pathogenesis of chronic apical periodontitis. Oral Microbiol Immunol8:254-257.
90.
Mataix J., Manas M., Quiles JL, Battino M., Cassinello M., Lopez-Frias M., et al. (1997). Coenzyme 0 content depends upon oxidative stress and dietary fat unsaturation. Molec Aspects Med18(Suppl):129-135.
91.
Matsumura T., Kimata M., Tsunemitsu A., Akiyoshi M. (1969a). Effect of coenzyme Q administration on the periodontal lesions in citrated rats. Koku Eisei Gakkai Zasshi19:134-142.
92.
Matsumura T., Kimata M., Tsunemitsu A., Akiyoshi M. (1969b). Effect of coenzyme Q on blood-citrate and calcium levels and on the periodontium of citrated rats. J Dent Res48:1264-1267.
93.
Matsumura T., Saji S., Nakamura R., Folkers K. (1973). Evidence for enhanced treatment of periodontal disease by therapy with Coenzyme Q. Int J Vitam Nutr Res43:537-538.
94.
McCord JM (1993). Human disease, free radicals, and the oxidant/antioxidant balance. Clin Biochem26:351-357.
95.
McRee JT, Hanioka T., Shizukuishi S., Folkers K. (1993). Therapy with Coenzyme Q10 for patients with periodontal disease. 1. Effect of Coenzyme Q10 on subgingival micro-organisms. J Dent Health43:659-666.
96.
Meyer MR, Schreck R., Baeuerle PA (1993). Hydrogen peroxide and antioxidants have opposite effects on activation of NF-KB and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J12:2005-2015.
97.
Mishchenko VP, Silenko IUL, VKH Khavinson, Tokar' DL (1991). The effect of periodontal cytomedin on lipid peroxidation and hemostasis in spontaneous periodontitis in rats. Stomatologiia70(5):12-14.
98.
Miyasaki KT (1991). The neutrophil: mechanisms of controlling periodontal bacteria. J Periodontol62:761-774.
99.
Moore S., Calder KA, Miller NJ, Rice-Evans CA (1994). Antioxidant activity of saliva and periodontal disease. Free Rad Res21:417-425.
100.
Morimoto RI (1993). Cells in stress: transcriptional activation of heat shock genes. Science259:1409-1410.
101.
Mouynet P., Delamaire M., Legoff MC, Genetet B., Yardin M., Michel IF (1994). Ex vivo studies of polymorphonuclear neutrophils from patients with early onset periodontitis. (II). Chemiluminescence response analysis. J Clin Periodontol21:533-539.
102.
Nakamura R., Littarru GP, Folkers K., Wilkinson EG (1973). Deficiency of coenzyme Q in gingiva of patients with periodontal disease. Int J Vitam Nutr Res43:84-92.
103.
Niki E. ( 1996). α-Tocopherol. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 3-25.
104.
Nohl H., Jordan W. (1986). The mitochondrial site of superoxide formation. Biochem Biophys Res Commun138:533-539.
105.
Pabst MJ, Pabst KM, Collier JA, Coleman TC, Lemons-Prince ML, Godat MS, et al. (1995). Inhibition of neutrophil and monocyte defensive functions by nicotine. J Periodontol66:1047-1055.
106.
Packer L., Witt EH, Tritschler HJ (1996). Antioxidant properties and clinical applications of a-lipoic acid and dihydrolipoic acid. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 545-591.
107.
Page RC, Kornman KS, editors (1997). The pathogenesis of human periodontitis: an introduction. Periodontol200014:9-11.
108.
Palozza P., Krinsky NI (1992). Antioxidant effects of carotenoids in vivo and in vitro: an overview. Meth Enzymol213:403-420.
109.
Park EM, Shigenaga MK, Degan P., Korn TS, Kitzler JW, Wehr CM, et al. (1992). Assay of excised oxidative DNA lesions: isolation of 8-oxoguanine and its nucleoside derivatives from biological fluids with a monoclonal antibody column. Proc Natl Acad Sci USA89:3375-3379.
110.
Parrish JH Jr, De Marco T.), Bissada NF (1977). Vitamin E and periodontitis in the rat. Oral Surg Oral Med Oral Pathol44:210-218.
111.
Petrovich Tua, Podorozhanaia RP, Genesina TI, Beloklitskaia GF (1996). Iron in oral cavity fluid in gingival inflammation. Patol Fiziol Eksp Ter3:22-24.
112.
Primiano T., Sutter TR, Kensler TW (1997). Antioxidant-inducible genes. In: Antioxidants in disease mechanisms and therapy. Sies H, editor. Advances in pharmacology. Vol. 38. San Diego: Academic Press, pp. 293-328.
113.
Pryor WA (1986). Oxy-radicals and related species: their formation, lifetimes and reactions. Ann Rev Physiol48:657-667.
114.
Quiles JL, Huertas JR, Manas M., Battino M., Cassinello M., Littarru GP, et al. (1994). Peroxidative extent and coenzyme Q levels in the rat: influence of physical training and dietary fats. Molec Aspects Med15(Suppl):89-95.
115.
Roberfroid M., Buc Calderon P. (1995). Free radicals and oxidation phenomena in biological systems. New York: Marcel Dekker, Inc.
116.
Rice-Evans C., Burdon R. (1993). Free radical-lipid interactions and their pathological consequences. Prog Lipid Res32:71-110.
117.
Sato K., Niki E., Shimasaki H. (1990). Free radical mediated chain oxidation of low density lipoprotein and its synergistic inhibition by vitamin E and C. Arch Biochem Biophys279:402-405.
118.
Schmidt AM, Weidman E., Lalla E., Yan SD, Hori O, Cao R., et al. (1996). Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodont Res31:508-515.
119.
Schneider HG, Pose G. ( 1968). The effect of oral vitamin A supply on periodontal alterations due to prolonged hypovitaminosis A. Dtsch Stomatol18:408-423.
120.
Schneider HG, Pose G. ( 1969). Influence of tocopherol on the periodontium of molars in rats fed a diet lacking in vitamin E. Arch Oral Biol14:431-433.
121.
Schreck R., Alberman K., Bauerle PA (1992). Nuclear factor KB: an oxidative stress-responsive transcription factor of eucaryotic cells. Free Rad Res Commun17:221-237.
122.
Sela MN, Weinberg A., Borinsky R., Holt SC, Dishon T. (1988). Inhibition of superoxide production in human polymorphonuclear leukocytes by oral treponemal factors. Infect Immun56:589-594.
123.
Sevanian A., Hochstein P. (1985). Mechanisms and consequences of lipid peroxidation in biological systems. Ann Rev Nutr5:365-390.
124.
Sevanian A., Peterson AR (1984). Cholesterol epoxide is a direct-acting mutagen. Proc Natl Acad Sci USA81:4198-4202.
125.
Sevanian A., Peterson AR (1986). The cytotoxic and mutagenic properties of cholesterol oxidation products. Food Chem Toxicol24:1103-1010.
126.
Sevanian A., Hodis HN, Hwang J., Peterson H. (1995). Involvement of cholesterol oxides in the atherogenic action of oxidised LDL. In: Free radicals, lipoprotein oxidation and atherosclerosis. Bellomo G, Finardi G, Maggi E, Rice-Evans C, editors. London: Richelieu Press, pp. 139-161.
127.
Seymour GJ, Whyte GJ, Powell RN (1986). Chemiluminescence in the assessment of polymorphonuclear leukocyte function in chronic inflammatory periodontal disease. J Oral Pathol15:125-131.
128.
Shapira L., Borinski R., Sela MN, Soskolne A. (1991). Superoxide formation and chemiluminescence of peripheral polymorphonuclear leukocytes in rapidly progressive periodontitis. ) Clin Periodontol18:44-48.
129.
Shapira L., Gordon B., Warbington M., Van Dyke TE (1994). Priming effect of P. gingivalis lipopolysaccharide on superoxide production by neutrophils from healthy and rapidly progressive periodontitis subjects. ) J Periodontol65:129-133.
130.
Shapira L., Schatzker Y., Gedalia I., Borinski R., Sela MN ( 1997). Effects of amine and stannous fluoride on human neutrophil functions in vitro. J Dent Res76:1381-1386.
131.
Shizukuishi S., Inoshita E., Tsunemitsu A., Takahashi K., Kishi T., Folkers K. (1984). Therapy by Coenzyme Q10 of experimental periodontitis in a dog-model supports results of human periodontitis therapy. In: Biomedical and clinical aspects of Coenzyme Q. Vol. 4. Folkers K, Yamamura Y, editors. Amsterdam: Elsevier, pp. 153-162.
132.
Shizukuishi S., Hanioka T., Tsunemitsu A., Fukunaga Y., Kishi T., Sato N. ( 1986). Clinical effect of Coenzyme Q10 on periodontal disease; evaluation of oxygen utilisation in gingiva by tissue reflectance spectrophotometry. In: Biomedical and clinical aspects of Coenzyme Q. Vol. 5. Folkers K, Yamamura Y, editors. Amsterdam: Elsevier, pp. 359-368.
133.
Sies H. ( 1986). Biochemistry of oxidative stress. Angew Chem Int Ed Engl25:1058-1071.
134.
Sies H, editor (1997). Antioxidants in disease mechanisms and therapy. In: Advances in pharmacology. Vol. 38. San Diego: Academic Press.
135.
Silenko lul, Mishchenko VP, Tokar' DL, Khavinson VKH, Zhukova MU (1991). The mechanism of the therapeutic effect of periodontal cytomedin on the course of experimental periodontitis. Stomatologiia70(4): 13-15.
136.
Silenko lul, Tsebrzhinskii OI, Mishchenko VP (1992). The mechanisms of the action of fluorine on periodontal tissue. Fiziol Zh38:85-90.
137.
Silenko lul, Vesnina LE, Mishchenko VP (1994a). Effect of paradentium polypeptide on the lipid peroxidation of the membranes and coagulation of erythrocytes in rats with spontaneous paradentitis. Fiziol Zh40:88-91.
138.
IUI Silenko, Mishchenko VP, Tokar' DL, VKH Khavinson, Popsuiko GI (1994b). The effect of periodontal cytomedin on free-radical lipid oxidation and on anti-aggregation activity in the periodontium in chronic stress. Stomatologiia73(4):6-8.
139.
Simic MG (1990). Pulse radiolysis in study of oxygen radicals. Meth Enzymol186:89-100.
140.
Slade EW Jr, Bartuska D., Rose LF, Cohen DW (1976). Vitamin E and periodontal disease. J Periodontol47:352-354.
141.
Speirs RL, Beeley JA (1992). Food and oral health: 2. Periodontium and oral mucosa. Dent Update19:161-167.
142.
Stadtman ER (1992). Protein oxidation and ageing. Science257:1220-1224.
143.
Stocker R., Bowry VW (1996). Tocopherol-mediated peroxidation of lipoprotein lipids and its inhibition by co-antioxidants. In: Handbook of antioxidants. Cadenas E, Packer L, editors. New York: Marcel Dekker, Inc., pp. 27-41.
144.
Stocker R., Bowry VW, Frei B. ( 1991). Ubiquinol-10 protects human low density lipoprotein more efficiently against lipid peroxidation than does a-tocopherol. Proc Natl Acad Sci USA88:1646-1650.
145.
Storz G., Tartaglia LA (1992). OxyR: a regulator of antioxidant genes. J Nutr122:627-630.
146.
Suomalainen K., Sorsa T., Lindy O., Saari H., Konttinen YT, Uitto VJ (1991). Hypochlorous acid induced activation of human neutrophil and gingival crevicular fluid collagenase can be inhibited by ascorbate. Scand J Dent Res99:397-405.
147.
Tang-Larsen J., Claesson R., Edlund MB, Carlsson J. (1995). Competition for peptides and amino acids among periodontal bacteria. J Periodont Res30:390-395.
148.
Tarasenko LM, Voskresenskii ON (1986). Role of lipid peroxidation in the pathogenesis of periodontal damage in stress. Patol Fiziol Eksp Ter6:12-14.
149.
Thomas SR, Neuzil J., Stocker R. (1997). Inhibition of LDL oxidation by ubiquinol-10. A protective mechanism for coenzyme Q in atherogenesis? Molec Aspects Med18(Suppl):85-103.
150.
Trykowsky J. Patalias B., Senator M. (1994). The use of toothpaste with vitamin A in treating periodontitis. Stomatologiia73(1): 11-13.
151.
Tsunemitsu A., Matsumura T. (1967). Effect of Coenzyme Q administration on hypercitricemia of patients with periodontal disease. J Dent Res46:1382-1384.
152.
Tsunemitsu A., Honjo K., Nakamura R., Kani M., Matsumura T. (1968). Effect of ubiquinone 35 on hypercitricemia. J Periodontol39:215-218.
153.
Van Dyke TE, Zinney W., Winkel K., Taufiq A., Offenbacher S., Arnold RR (1986). Neutrophil function in localized juvenile periodontitis: phagocytosis, superoxide production and specific granule release. J Periodontol57:703-708.
154.
Villa RF, Gorini A. (1997). Pharmacology of lazaroids and brain energy metabolism: a review. Pharmacol Rev49:99-136.
155.
von Sonntag C. (1987). The chemical basis of radiation biology. London: Taylor & Francis.
156.
Voskresenskii ON, Tkachenko EK (1991). The role of lipid peroxidation in the pathogenesis of periodontitis. Stomatologiia70(4):5-10.
157.
Waerhaug J. (1967) Prevalence of periodontal disease in Ceylon. Association with age, sex, oral hygiene, socio-economic factors, vitamin deficiencies, malnutrition, betel and tobacco consumption and ethnic group. Final report. Acta Odontol Scand25:205-231.
158.
Watts TL (1995). Coenzyme Q10 and periodontal treatment: is there any beneficial effect? Br Dent J178:209-213.
159.
Whyte GJ, Seymour GJ, Cheung K., Robinson MF (1989). Chemiluminescence of peripheral polymorphonuclear leukocytes from adult periodontitis. J Clin Periodontol16:69-74.
160.
Wilkinson EG, Arnold RM, Folkers K., Hansen I., Kishi H. (1975). Bioenergetics in clinical medicine. II. Adjunctive treatment with Coenzyme Q in periodontal disease. Res Commun Chem Pathol Pharmacol12:111-123.
161.
Wilkinson EG, Arnold RM, Folkers K. (1976). Bioenergetics in clinical medicine. VI. Adjunctive treatment of periodontal disease with Coenzyme Q10. Res Commun Chem Pathol Pharmacol14:715-719.
162.
Wilkinson EG, Arnold RM, Folkers K. (1977). Treatment of periodontal and other soft tissue diseases of the oral cavity with Coenzyme Q. In: Biomedical and clinical aspects of Coenzyme Q. Vol. 1. Folkers K, Yamamura Y, editors. Amsterdam: Elsevier, pp. 251-265.
163.
Winrow VR, Winyard PG, Morris CJ, Blake DR (1993). Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull49:506-522.
164.
Winyard PG, Blake DR (1997). Antioxidants, redox-regulated transcription factors, and inflammation. In: Antioxidants in disease mechanisms and therapy. Sies H, editor. Advances in pharmacology. Vol. 38. San Diego: Academic Press, pp. 403-421.
165.
Yamamoto Y., Komuro E., Niki E. ( 1990). Antioxidant activity of ubiquinol in solution and phosphatidylcholine liposome. J Nutr Sci Vitaminol36:505-511.
166.
Zafiropoulos GG, Flores-De-Jacoby L., Czerch W., Kolb G., Markitziu A., Havemann K. (1988). Neutrophil function in patients with localised juvenile periodontitis and with rapidly progressive periodontitis. J Biol Buccale16:151-156.
167.
Zafiropoulos GG, Flores-de-Jacoby L., Plate VM, Eckle I., Kolb G. ( 1991). Polymorphonuclear neutrophil chemiluminescence in periodontal disease. J Clin Periodontol18:634-639.
