Effect of different contraceptive methods on the oxidative stress status in women aged 40-48 years from the ELAN study in the province of Liege, Belgium
oxidative stress; antioxidants; oral contraception; ELAN study
Abstract :
[en] Oxidative stress is associated with the development of several disorders including cardiovascular disease and cancer. Among conditions known to influence oxidative stress, the use of oral contraception (OC) in women has been a matter of ongoing discussion. METHODS: A total of 897 eligible and healthy volunteers were recruited from among the patients of 50 general practitioners participating in the ELAN study (Etude Liegeoise sur les ANtioxydants). A subsample consisting of 209 women aged 40-48 years was studied for a comprehensive oxidative stress status (OSS), including the analysis of antioxidants, trace elements and three markers of oxidative damage to lipids. Among 209 subsample, 49 (23%) were OC users (OCU), 119 (57%) non-contraception users (NCU) and 41 (20%) were intrauterine (hormonal and copper) devices users (IUD). RESULTS: After adjustment for smoking, systolic and diastolic blood pressure and BMI (or waist circumference), a marked and significant increase in lipid peroxides was observed among OCU women when compared with NCU and IUD users. A cut-off value of 660 mu M in lipid peroxides allowed the discrimination of OCU from the two other groups. In contrast, no difference was observed in the plasma concentration of both oxidized low-density lipoprotein (LDL) and their related antibodies. The increased level in lipid peroxides was strongly related to higher concentrations of copper (r < 0.84; P < 0.0001, cut-off value 1.2 mg/1). When compared with NCU and IUD users, plasma antioxidant defences were significantly altered in OCU women as shown by lower levels of beta-carotene (decrease of 39%; P < 0.01) andytocopherol (decrease by 22%; P < 0.01). In contrast, higher concentrations of selenium (increased by 11.8%; P < 0.01) were observed in OCU women. Blood concentrations of vitamin C, alpha-tocopherol and zinc were unaffected by OC use. CONCLUSIONS: The intake of OC significantly increases the lipid peroxidation in women aged 40-48 years. This may represent a potential cardiovascular risk factor for these women.
Disciplines :
Reproductive medicine (gynecology, andrology, obstetrics)
Author, co-author :
Pincemail, Joël ; Centre Hospitalier Universitaire de Liège - CHU > Chirurgie cardio-vasculaire
Vanbelle, Sophie ; Université de Liège - ULiège > Département des sciences de la santé publique > Informatique médicale et biostatistique
Gaspard, Ulysse ; Université de Liège - ULiège > Services généraux (Faculté de médecine) > Relations académiques et scientifiques (Médecine)
Collette, Georges ; Université de Liège - ULiège > Département des sciences cliniques > Médecine générale
Haleng, Jeanine ; Centre Hospitalier Universitaire de Liège - CHU > Chimie médicale
Cheramy-Bien, J. P.
Charlier, Corinne ; Université de Liège - ULiège > Département de pharmacie > Chimie toxicologique
Chapelle, Jean-Paul ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale
Albert, Adelin ; Université de Liège - ULiège > Département des sciences de la santé publique > Informatique médicale et biostatistique
Limet, Raymond ; Université de Liège - ULiège > Département des sciences cliniques > Chirurgie cardio-vasculaire et thoracique
Defraigne, Jean-Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie générale
Language :
English
Title :
Effect of different contraceptive methods on the oxidative stress status in women aged 40-48 years from the ELAN study in the province of Liege, Belgium
Ageno W, Squizzato A, Garcia D, Imberti D. Epidemiology and risk factors of venous thromboembolism. Semin Thromb Hemost 2006;32 651-658.
Ahotupa M, Rauramo, I, Vasankari TJ, Skouby SO, Hakonen T. Estrogen replacement therapy in combination with continuous intrauterine progestin administration reduces the amount of circulating oxidized LDL in postmenopausal women: Dependence on the dose of progestin. Ann Med 2004;36:278-284.
Arab L, Schellenberg B, Schlierf G. Nutrition and Health - A survey of young men and women in Heidelberg. Ann Nutr Metal 1982;26 S1-S244.
Baker H, Handelman GJ, Short S, Machlin LJ, Bhagavan HN, Dratz EA, Frank O. Comparison of plasma alpha and gamma tocopherol levels following chronic oral administration of either all-rac-alpha-tocopheryl acetate or RRR-alpha tocopheryl acetate in normal adult male subjects. Am J Clin Nutr. 1986;43:382-387.
Bednarek-Tupikowska G, Tworowska U, Jedrychowska I, Radomska B, Tupikowski K, Bidzinska - Speichert B, Milewicz A. Effets of oestradiol and oestroprogestin on erythrocyte antioxidative enzyme system activity in posmenopausal women. Clin Endocrinol 2006;64:463-468.
Behall KM, Moser PB, Kelsay JL, Prather ES. The effect of kind of carbohydrate in the diet and the use of oral contraception on metabolism of young women. Am J Clin Nutr 1980;33:825-831.
Benes B, Spevackova V, Smid J, Batariova A, Cejchanova M, Zitkova L. Effects of age, BMI, smoking and contraception levels of Cu, Se, Zn in the blood of the population in the Czech Republic. Cent Eur J Public Health 2003;13:202-207.
Berg G, Kohlmeier L, Brenner H. Use of oral contraceptives and serum beta-carotene. Eur J Clin Nutr 1997a;51:181-187.
Berg G, Kohlmeier L, Brenner H. Effect of oral contraceptive progestins on serum copper concentration. Eur J Clin Nutr 1998b;52 711-715.
Brown L, Hoong I, Doggrell SA. The heart as a target for oestrogens. Heart Lung Circ 2000;9:113-125.
Bureau I, Laporte F, Favier M, Faure H, Fields M, Favier A, Roussel AM. No antioxidant effect of combined HRT on LDL oxidizability and oxidative stress biomarkers in treated post - menopausal women. J Am Coll Nutr 2002;21:333-338.
Butterworth PH, Baum H, Porter JW, Ellman GL. A modification of the Ellman procedure for the estimation of protein sulfhydryl groups. Arch Biochem Biophys. 1967;118:716-723.
Capel ID, Jenner M, Williams DC, Donaldson D, Nath A. The effect of prolonged oral contraceptive steroid use on erythrocyte glutathione peroxidase activity. J Ster Biochem 1981;14:729-732.
Carr BR, Ory H. Estrogen and progestin components of oral contraceptives: Relationship to vascular disease. Contraception 1997;55:267-272.
Chang MC, Hafez ES, Merrilla A, Pincus G. Effect of certain 19-nor steroids on reproductive process in animal. Science 1956;124 890-891.
Chiang K, Parthasarathy S, Santanam N. Estrogen, neutrophils and oxidation. Life Sci 2004;75:2425-2428.
Ciavatti M, Blache D, Renaud S. Hormonal contraceptive increases plasma lipid peroxides in females rats. Relationship to platelet aggregation and lipid biosynthesis. Arteriosclerosis 1989;9:84-89.
Ciavatti M, Renaud S. Oxidative status and oral contraception. Its relevance to platelet abnormalities and cardiovascular risk. Free Rad Biol Med 1991;10:325-338.
Chilvers DC, Jones MM, Selby PL, Dawson JB, Hodgkinson A. Effect of oral ethinyl oestradiol and norethisterone on plasma copper and zinc complexes in post - menopausal women. Horm Metab Res 1985;17 532-535.
Clemente C, Caruso MG, Berloco P, Notarnicola M, D'Attoma B, Osella AR, Guerra V, Buonsante A, Giannandrea B, Di Leo A et al. Antioxidant effect of short - term hormonal treatement in postmenopausal women. Maturitas 1999;31:137-142.
Crews MG, Taper LG, Ritchey SJ. Effects of oral contraceptive agents on copper and zinc balance in young women. Am J Clin Nutr 1980;33 1940-1945.
Cutler RG. Oxidative stress profiling: Part I. Its potential importance in the optimization of human health. Ann NY Acad Sci 2005;1055 93-135.
Dantas AP, Tostes RCA, Fortes ZB, Costa SG, Nigro D, Carvalho MH. In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats. Hypertension 2002;39 405-411.
Falkeborn M, Lithell H, Persson I, Vessby B, Naessen T. Lipids and antioxidative effects of estradiol and sequential norethisterone acetate treatment in a 3-month randomized controlled trial. Climacteric 2002;5:240-258.
Galan P, Viteri FE, Bertrais S, Czernichow S, Faure H, Arnaud J, Ruffleux D Chenal S, Arnault N, Favier A et al. Serum concentrations of beta-carotene, vitamins C and E, zinc and selenium are influenced by sex, age, diet, smoking status, alcohol consumption and corpulence in a general French adult population. Eur J Clin Nutr. 2005;59:1181-1190.
Gey KF. Optimum plasma levels of antioxidant micronutrient - ten years of antioxidant hypothesis on atherosclerosis. Bibli Nutr Diet 1994;51:84-89.
Gey KF. Vitamins E plus C and interacting conutrients required for optimal health. A critical and constructive review of epidemiology and supplementation data regarding cardiovascular disease and cancer. Biofactors. 1998;7:113-174.
Ha EJ, Smith AM. Plasma selenium and plasma and erythrocyte glutathione peroxidase activity increase with estrogen during the menstrual cycle. J Am Coll Nutr 2003;22:45-51.
Heikkinen AM, Niskanen L, Yla-Herttuala S, Luoma J, Tuppurainen MT, Komulainen M, Saarikosi S. Postmenopausal hormone replacement therapy and antibodies against oxidized LDL. Maturitas 1998,29 155-161.
Hernandez I, Delgado JL, Diaz J, Quesada T, Teruel MJ, Llanos MC, Carbonell LF. 17 β - estradiol prevents oxidative stress and decreases blood pressure in ovariectomized rats. Am J Physiol Regul Interg Comp Physiol 2000;279:R1599-R1605.
Holvoet P, Vanhaecke J, Janssens S, Van de Werf F, Collen D. Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 1998; 98:1487-1494.
Horwitt MK, Harvey CC, Dahm CH. Relationship between levels of blood lipids, vitamins C, A, E, serum copper compounds, and urinary excretions of tryptophan metabolites in women taking oral contraceptive therapy. Am J Clin Nutr 1975;28:403-412.
Hwang J, Peterson H, Hodis HN, Choi B, Sevanian A. Ascorbic acid enhances 17 β-estradiol-mediated inhibition of oxidized low density lipoprotein formation. Atheroscl 2000;150:275-284.
Karbownik M, Reiter RJ, Burkhardt S, Gitto E, Tan DX, Lewinski A. Melatonin attenuates estradiol induced oxidative damage to DNA: relevance for cancer prevention. Exp Biol Med 2001;226 707-712.
Kluft C, Leuven JA, Helmerhorst FM, Krans HM. Pro-inflammatory effects of estrogens during use of oral contraceptives and hormone replacement therapy. Vascul Pharmacol 2002;39:149-154.
Kose K, Dogan P, Ozesmi C. Contraceptive steroids increase erythrocyte lipid peroxidation in female rats. Contraception 1993;47 421-425.
Leone N, Courbon D, Ducimetiere P, Zureik M. Zinc, copper, and magnesium and risks for all-cause cancer, and cardiovascular mortality. Epidemiol 2006;17:308-314.
Limpongsanurak S, Jenkins N, Fotherby K. Effect of contraceptive steroids on serum levels of sex hormone binding globulin and caerulopasmin. Curr Med Res Opin 1981;7:185-191.
Ling S, Komesaroff P, Sudhir K. Cellular mechanisms underlying the cardiovascular actions of estrogens. Clin Sci 2006;111 107-118.
Markides CS, Roy D, Liehr JG. Concentration dependence of prooxidant and antioxidant properties of catecholestrogens. Arch Biochem Biophys 1998;360:105-112.
Massafra C, Buonocore G, Berni S, Gioia D, Giuliani A, Vezzosi P. Antioxidant erythrocyte enzyme activities during oral contraception. Contraception 1993;47:591-596.
McManus J, McEneny J, Young IS, Thompson W. The effect of various oestrogens and progestogens on the susceptibility of low density lipoproteins to oxidation in vivo. Maturitas 1996;25:125-131.
McManus J, McEnemy J, Thompson W, Young IS. The effect of hormone replacement therapy on the oxidation of low density lipoprotein in Postmenopausal women. Atherosclerosis 1997;135:73-81.
Mezzetti A, Pierdomenico SD, Costantini F, Romano F, De Cesare D, Cuccurullo F, Imbastara T, Riario-Sforza G, Di Giacomo F, Zuliani G et al. Copper/zinc ratio and systemic oxidant load: Effect of aging and aging - related degenerative diseases. Free Rad Biol Med 1998;25:676-681.
Misra R, Mangi S, Joshi S, Mittal S, Gupta SK, Pandey RM. LycoRed as an alternative to hormone replacement therapy in lowering serum lipids and oxidative stress markers: A randomized controlled clinical trial. J Obstet Gynaecol Res 2006;32:299-304.
Miura T, Muraoka S, Fujimoto Y. Effect of estrogens on the oxidative damage induced by ferrylmyoglobin. J Steroid Biochem Mol Biol 1998;67:57-62.
Mooij P, Thomas C, Doesburt W, Eskes T. Multivitamin supplementation in oral contraceptive users. Contraception 1991;44:277-288.
Mueck AO, Seeger H, Wallwiener D. Fluvastatin combined with 17 β - estradiol: Effect on the oxidation of human low density lipoprotein. Exp Clin Endocrinol Diabetes 2000;108:316-317.
Nessa A, Latif SA, Siddiqui NI. Risk of cardiovascular diseases with oral contraception. Mymensingh Med J 2006;15:220-224.
Omaye ST, Tumbull JD, Sauerlich HE. Selected methods for the determination of ascorbic acid in animal cells, tissues and fluids. Methods Enzymol 1979;62:3-11.
Palan PR, Rommey SL, Vermund SH, Mikhail MG, Basu J. Effects of smoking and oral contraception on plasma beta-carotene levels in healthy women. Am J Obstet Gynecol 1989;161:881-885.
Palan PR, Magneson AT, Castillo M, Dunne J, Mikhail MS. Effects of menstrual cycle and oral contraceptive use on serum levels of lipid-soluble antioxidants. Am J Obstetrics Gynecology 2006;194 e35-e38.
Plaa GL, Wittchi H. Chemical drugs and lipid peroxidation. Ann Rev Pharmacol 1976;16:125-141.
Prasad AS, Lei KY, Oberleas D, Moghissi KS, Stryker JC. Effect of oral contraceptive agents on nutrients: II- vitamins. Am J Clin Nutr 1975a;28:385-391.
Prasad AS, Oberleas D, Moghissi KS, Ley KY, Stryker JC. Effect of oral contraceptive agents on nutrients: I. Minerals. Am J Clin Nutr 1975b;28:377-384.
Prema K, Ramalakshmi BA, Babu S. Serum copper and zinc in hormonal contraceptive users. Fertil Steril 1980;33:267-271.
Rosenberg L, Palmer JR, Sands MI, Grimes D, Bergman U, Daling J, Mills A. Modern oral contraceptives and cardiovascular diseases. Am J Obstet Gynecol 1997;177:707-715.
Russ EM, Raymund J. Influence of oestrogen on total serum copper and ceruloplasmin. Proc Soc Exp Biol Med 1956;92:465-466.
Saha A, De AU, Sengupta C. Ethinyl estradiol: Its interaction on blood-lipid. Indian J Exp Biol 2000;38:906-911.
Seeger H, Wallwiener D, Mueck AO. Additive antioxidative effect of hormone replacement therapy combined with a statin. Clin Exp Obstet Gynecol 2000;27:179-181.
Sher PP. Drug interference with laboratory tests: Oral contraceptives. Drug Ther 1977;2:61-63.
Sissan MA, Menon VP, Leelamma S. Effects of low-dose oral contraceptive oestrogen and progestin on lipid peroxidation in rats. J Int Med Res 1995;23:272-278.
Souci, Fechmann, Kraut. La composition des aliments, tableaux des valeurs nutritives. 6th edn. Medpharm Scientific Publishers, London, England, 2000.
Sturup S, Hayes RB, Peters U. Development and application of a simple routine method for the determination of selenium in serum by octopole reaction with ICPMS. Anal Bioanal Chem 2005;381:686-694.
Subakir SB, Abdul Madjid O, Sabariah S, Affandi B. Oxidative stress, vitamin E and progestin breakthrough bleeding. Hum Reprod 2000; S3: 18-23.
Sugioka K, Shimosegawa Y, Nakano M. Estrogen as natural antioxidant of membrane phospholipid peroxidation. FEBS Letters 1987;210 37-39.
Telci A, Cakatay U, Akhan SE, Bilgin ME, Turfanda A, Sivas A. Posmenopausal hormone replacement hormone therapy use decreases oxidative protein damage. Gynecol Obstet Invest 2002;54 88-93.
Thibodeau PA, Kachadourian R, Lemay R, Bisson M, Day BJ, Paquette B. In vitro pro- and antioxidant properties of estrogens. J Steroid Biochem Mol Biol 2002;81:227-236.
Wakatsuki A, Okatani Y, Ikenoue N, Shinohara K, Watanabe K, Fukaya T. Effect of lower dose of oral conjugated equine estrogen on size and oxidative susceptibility of low-density lipoprotein particles in postmenopausal women. Circulation 2003;108:808-813.
Wagner KH, Kamal - Eldin A, Elmadfa I. Gamma - tocopherol - an underestimated vitamin? Am Nutr Metab 2004;48:169-188.
Wen Y, Doyle MC, Cooke T, Feely J. Effect of menopause on low-density lipoprotein oxidation: Is oestrogen an important determinant? Maturitas 2000;34:233-238.
Wu T, Sempos CT, Freudenheim JL, Muti P, Smit E. Serum iron, copper and zinc concentrations and risk of cancer mortality in US adults. Ann Epidemiol 2004;14:195-201.
Wynn V, Adams PW, Godsland I, Melrose J, Niththyananthan R, Oakley NW, Seed M. Comparison of effects of different combined oral-contraceptives on carbohydrate and lipid metabolism. Lancet 1979;1 1045-1049.
Yen CH, Hsieh CC, Chou SY, Lau YT. 17 β-estradiol inhibits oxidized low density lipoprotein-induced generation of reactive oxygen species in endothelial cells. Life Sci 2001;70:403-413.
Yeung DL. Relationships between cigarette smoking, oral contraceptives, and plasma vitamins A, E, C, and plasma triglycerides and cholesterol. Am J Clin Nutr 1976;29:1216-1221.
Zhao B, Tham SY, Lai MH, Lee LK, Moochhala SM. Simultaneous determination of vitamins C, E and beta-carotene in human plasma by high-performance liquid chromatography with photodiode-array detection J Pharm Pharm Sci 2004;30:200-204.
