The potential of micronutrient support with omega-3 and omega-6 fatty acids in the prevention of human reproductive disorders

Abstract

Omega-3 and omega-6 polyunsaturated fatty acids are among the nutrients essential for the vital functions of the human body. Fundamental cellular functions of omega-3 and omega-6 polyunsaturated fatty acids affect both physical and reproductive health. Based on the principles of personalized medicine, early detection of polyunsaturated fatty acid deficiency is necessary for its prompt correction and prevention of further diseases. We present a literature review on the effects of polyunsaturated fatty acids on female and male fertility. The brief information on biochemical aspects, current data on diagnosis, and possible methods for correction of polyunsaturated fatty acid deficiency are described in this article.

Keywords

polyunsaturated fatty acids / omega-3 / omega-6 / omega-3 index / infertility

References

[1] Kodentsova VM, Beketova NA, Nikitjuk DB, Tutelyan VA. Characteristics of vitamin provision in the adult population of the Russian Federation. Profilakticheskaja medicina. 2018;21(4):32−37. DOI: 10.17116/profmed201821432

[2] Коденцова В.М., Бекетова Н.А., Никитюк Д.Б., Тутельян В.А. Характеристика обеспеченности витаминами взрослого населения Российской Федерации // Профилактическая медицина. 2018. Т. 21. № 4. С. 32−37. DOI: 10.17116/profmed201821432

[3] Sinclair H. Highlights in the study of omega-3 essential fatty acids. World Rev Nutr Diet. 1991;66:9−11. DOI: 10.1159/000419268

[4] Sinclair H. Highlights in the study of omega-3 essential fatty acids // World Rev. Nutr. Diet. 1991. Vol. 66. P. 9−11. DOI: 10.1159/000419268

[5] Berezov TT, Korovkin BF. Biologicheskaja himija. 3rd ed. Moscow: Medicina; 1998. (In Russ.)

[6] Березов Т.Т., Коровкин Б.Ф. Биологическая химия. 3-е изд. Москва: Медицина, 1998.

[7] Vorslov LO. Omega-3 polyunsaturated fatty acids as a source of longevity. Questions of dietetics. 2017;7(1):36−41. (In Russ.). DOI: 10.20953/2224-5448-2017-1-36-41

[8] Ворслов Л.О. Омега-3 полиненасыщенные жирные кислоты как источник долголетия // Вопросы диетологии. 2017. Т. 7. № 1. С. 36−41. DOI: 10.20953/2224-5448-2017-1-36-41

[9] Lopes-Otin Ñ. The hallmarks of aging. Cell. 2013;153(6):1194−217. DOI: 10.1016/j.cell.2013.05.03

[10] Lopes-Otin Ñ. The hallmarks of aging // Cell. 2013. Vol. 153. No. 6. P. 1194−217. DOI: 10.1016/j.cell.2013.05.03

[11] Serhan CN, Chiang N, Dalli J. The resolution code of acute inflammation: Novel proresolving lipid mediators in resolution. Semin Immunol. 2015:27(3):200−215. DOI: 10.1016/j.smim.2015.03.004

[12] Serhan C.N., Chiang N., Dalli J. The resolution code of acute inflammation: Novel proresolving lipid mediators in resolution // Semin. Immunol. 2015. Vol. 27. No. 3. P. 200−215. DOI: 10.1016/j.smim.2015.03.004

[13] von Schacky C. A review of omega-3 ethyl esters for cardiovascular prevention and treatment of increased blood triglyceride levels. Vasc Health Risk Manag. 2006;2(3):251−262. DOI: 10.2147/vhrm.2006.2.3.251

[14] von Schacky C. A review of omega-3 ethyl esters for cardiovascular prevention and treatment of increased blood triglyceride levels // Vasc. Health Risk Manag. 2006. Vol. 2. No. 3. P. 251−262. DOI: 10.2147/vhrm.2006.2.3.251

[15] Field CJ, Van Aerde JE, Robinson LE, Clandinin MT. Effect of providing a formula supplemented with long-chain polyunsaturated fatty acids on immunity in full-term neonates. Br J Nutr. 2008;99(1):91−99. DOI: 10.1017/S0007114507791845

[16] Field C., van Aerde J., Robinson L., Clandinin M.T. Effect of providing a formula supplemented with long-chain polyunsaturated fatty acids on immunity in full-term neonates. // Br. J. Nutrition. 2008. Vol. 99. No. 1. P. 91−99. DOI: 10.1017/S0007114507791845

[17] Pregravidarnaja podgotovka. Klinicheskij protokol Mezhdisciplinarnoj associacii specialistov reproduktivnoj mediciny (MARS). Versija 2.0. Moscow: Status Praesens; 2020 [cited 23 Aug 2021]. Available from: https://praesens.ru/files/2020/broshyury/Protokol_MARS.pdf. (In Russ.)

[18] Прегравидарная подготовка. Клинический протокол Междисциплинарной ассоциации специалистов репродуктивной медицины (МАРС). Версия 2.0. Москва: Status Praesens, 2020 [дата обращения: 23.08.2021]. Доступ по ссылке: https://praesens.ru/files/2020/broshyury/Protokol_MARS.pdf

[19] Gromova OA, Torshin IJu. Vitaminy i mineraly: mezhdu Scilloj i Haribdoj: o miskoncepcijah i drugih chudovishhah. Moscow: MCNMO; 2013. (In Russ.)

[20] Громова О.А., Торшин И.Ю. Витамины и минералы: между Сциллой и Харибдой: о мисконцепциях и других чудовищах. Москва: МЦНМО, 2013.

[21] Wathes DC, Abayasekara DR, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod. 2007;77(2):190−201. DOI: 10.1095/biolreprod.107.060558

[22] Wathes D.C., Abayasekara D.R., Aitken R.J. Polyunsaturated fatty acids in male and female reproduction // Biol. Reprod. 2007. Vol. 77. No. 7. P. 190−201. DOI: 10.1095/biolreprod.107.060558

[23] Sturmey RG, Reis A, Leese HJ, McEvoy TG. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim. 2009;44(Suppl 3):50−58. DOI: 10.1111/j.1439-0531.2009.01402.x

[24] Sturmey R.G., Reis A., Leese H.J., McEvoy T.G. Role of fatty acids in energy provision during oocyte maturation and early embryo development // Reprod. Domest. Anim. 2009. Vol. 44. No. 3. Suppl. P. 50−58. DOI: 10.1111/j.1439-0531.2009.01402.x

[25] Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy. N Engl J Med. 2001;345:1400−1408. DOI: 10.1056/NEJMra000763

[26] Norwitz E.R., Schust D.J., Fisher S.J. Implantation and the survival of early pregnancy // N. Engl. J. Med. 2001. Vol. 345. P. 1400−1408. DOI: 10.1056/NEJMra000763

[27] Murakami K, Chan SY, Routtenberg A. Protein kinase C activation by cis-fatty acid in the absence of Ca2+ and phospholipids. J Biol Chem. 1986;261(33):15424−15429. DOI: 10.1016/s0021-9258(18)66728-6

[28] Murkami K., Chan S.Y., Routtenberg A. Protein kinase C activation by cis-fatty acid in the absence of Ca2+ and phospholipids // J. Biol. Chem. 1986. Vol. 261. No. 33. P. 15424−15429. DOI: 10.1016/s0021-9258(18)66728-6

[29] Ruzhilo OS, Divakova TS. Vlijanie polimorfnyh variantov genov receptorov, aktivirujushhih proliferaciju peroksisom PPARα i PPARGC1A, na razvitie sindroma polikistoznyh jaichnikov. Vestnik Vitebskogo gosudarstvennogo medicinskogo universiteta. 2013;12(3):78−83.

[30] Ружило О.С., Дивакова Т.С. Влияние полиморфных вариантов генов рецепторов, активирующих пролиферацию пероксисом PPARα и PPARGC1A, на развитие синдрома поликистозных яичников // Вестник Витебского государственного медицинского университета. 2013. Т. 12. № 3. С. 78−83.

[31] Berger J, Moller DE. The mechanisms of action of PPARs. Annu Rev Med. 2002;53:409−435. DOI: 10.1146/annurev.med.53.082901.104018

[32] Berger J., Moller D.E. The mechanisms of action of PPARs // Ann. Rev. Med. 2002. Vol. 53. P. 409−435. DOI: 10.1146/annurev.med.53.082901.104018

[33] International classification of diseases 10th revision (ICD 10) [cited 23 Aug 2021]. Available from: https://mosgorzdrav.ru/ru-RU/magic/default/download/4286.html. (In Russ.)

[34] Международная классификация болезней 10-го пересмотра (МКБ 10) [дата обращения: 23.08.2021]. Доступ по ссылке: https://mosgorzdrav.ru/ru-RU/magic/default/download/4286.html

[35] Lass A, Belluzzi A. Omega-3 polyunsaturated fatty acids and in-vitro fertilization treatment. Reproductive BioMedicine. 2008;38(1):95−99. DOI: 10.1016/j.rbmo.2018.10.008

[36] Lass A., Belluzzi A. Omega-3 polyunsaturated fatty acids and in-vitro fertilization treatment // Reproductive BioMedicine. 2008. Vol. 38. No. 1. P. 95−99. DOI: 10.1016/j.rbmo.2018.10.008

[37] Salleh N. Diverse roles of prostaglandins in blastocyst implantation. ScientificWorldJournal. 2014;2014:968141. DOI: 10.1155/2014/968141

[38] Salleh N. Diverse roles of prostaglandins in blastocyst implantation // ScientificWorldJournal. 2014. Vol. 2014. P. 968141. DOI: 10.1155/2014/968141

[39] Nehra D, Le HD, Fallon EM, et al. Prolonging the female reproductive lifespan and improving egg quality with dietary omega-3 fatty acids. Aging Cell. 2012;11(6):1046−1054. DOI: 10.1111/acel.12006

[40] Nehra D., Le H.D., Fallon E.M. et al. Prolonging the female reproductive lifespan and improving egg quality with dietary omega-3 fatty acids // Aging. Cell. 2012. Vol. 11. No. 6. P. 1046−1054. DOI: 10.1111/acel.12006

[41] Gaskins AJ, Chavarro JE. Diet and fertility: A review. Am J Obstet Gynecol. 2018;218:379−389. DOI: 10.1016/j.ajog.2017.08.010

[42] Gaskins A.J., Chavarro J.E. Diet and fertility: A review // Am. J. Obstet. Gynecol. 2018. Vol. 218. P. 379−389. DOI: 10.1016/j.ajog.2017.08.010

[43] Wakefield SL, Lane M, Schulz SJ, et al. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am J Physiol Endocrinol Metab. 2008;294:E425−E434. DOI: 10.1152/ajpendo.00409.2007

[44] Wakefield S.L., Lane M., Schulz S.J. et al. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse // Am. J. Physiol. Endocrinol. Metab. 2008. Vol. 294. P. E425−E434. DOI: 10.1152/ajpendo.00409.2007

[45] Chavarro JE, Rich-Edwards JW, Rosner BA, Willett WC. Dietary fatty acid intakes and the risk of ovulatory infertility. Am J Clin Nutr. 2007;85:231−237. DOI: 10.1093/ajcn/85.1.231

[46] Chavarro J.E., Rich-Edwards J.W., Rosner B.A., Willett W.C. Dietary fatty acid intakes and the risk of ovulatory infertility // Am. J. Clin. Nutr. 2007. Vol. 85. P. 231−237. DOI: 10.1093/ajcn/85.1.231

[47] Mumford SL, Chavarro JE, Zhang C, et al. Dietary fat intake and reproductive hormone concentrations and ovulation in regularly menstruating women. Am J Clin Nutr. 2016;103(3):868−877. DOI: 10.3945/ajcn.115.119321

[48] Mumford S.L., Chavarro J.E., Zhang C. et al. Dietary fat intake and reproductive hormone concentrations and ovulation in regularly menstruating women // Am. J. Clin. Nutr. 2016. Vol. 103. No. 3. P. 868−877. DOI: 10.3945/ajcn.115.119321

[49] Missmer SA, Chavarro JE, Malspeis S, et al. A prospective study of dietary fat consumption and endometriosis risk. Hum Reprod. 2010;25:1528−1535. DOI: 10.1093/humrep/deq044

[50] Missmer S.A., Chavarro J.E., Malspeis S. et al. A prospective study of dietary fat consumption and endometriosis risk // Hum. Reprod. 2010. Vol. 25. P. 1528−1535. DOI: 10.1093/humrep/deq044

[51] Hopeman MM, Riley JK, Frolova AI, et al. Serumpolyunsaturated fatty acids and endometriosis. Reprod Sci. 2015;22:1083−1087. DOI: 10.1177/1933719114565030

[52] Hopeman M.M., Riley J.K., Frolova A.I. et al. Serumpolyunsaturated fatty acids and endometriosis // Reprod. Sci. 2015. Vol. 22. P. 1083−1087. DOI: 10.1177/1933719114565030

[53] Hammiche F, Vujkovic M, Wijburg W, et al. Increased preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology. Fertil Steril. 2011;95:1820−1823. DOI: 10.1016/j.fertnstert.2010.11.021

[54] Hammiche F., Vujkovic M., Wijburg W. et al. Increased preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology // Fertil. Steril. 2011. Vol. 95. P. 1820−1823. DOI: 10.1016/j.fertnstert.2010.11.021

[55] Jungheim ES, Macones GA, Odem RR, et al. Elevated serum alpha-linolenic acid levels are associated with decreased chance of pregnancyafter in vitro fertilization. Fertil Steril. 2011;96:880−883. DOI: 10.1016/j.fertnstert.2011.07.1115

[56] Jungheim E.S., Macones G.A., Odem R.R. et al. Elevated serum alpha-linolenic acid levels are associated with decreased chance of pregnancy after in vitro fertilization // Fertil. Steril. 2011. Vol. 96. P. 880−883. DOI: DOI: 10.1016/j.fertnstert.2011.07.1115

[57] Jungheim ES, Frolova AI, Jiang H, Riley JK. Relationship between serum polyunsaturated fatty acids and pregnancy in women undergoing in vitrofertilization. J Clin Endocrinol Metab. 2013;98:E1364–E1368. DOI: 10.1210/jc.2012-4115

[58] Jungheim E.S., Frolova A.I., Jiang H., Riley J.K. Relationship between serum polyunsaturated fatty acids and pregnancy in women undergoing in vitrofertilization // J. Clin. Endocrinol. Metab. 2013. Vol. 98. P. E1364–E1368. DOI: 10.1210/jc.2012-4115

[59] Eskew AM, Wormer KC, Matthews ML, et al. The association between fatty acid index and in vitro fertilization outcomes. J Assist Reprod Genet. 2017;34(12):1627−1632. DOI: 10.1007/s10815-017-1032-1

[60] Eskew A.M., Wormer K.C., Matthews M.L. et al. The association between fatty acid index and in vitro fertilization outcomes // J. Assist. Reprod. Genet. 2017. Vol. 34. No. 12. P. 1627−1632. DOI: 10.1007/s10815-017-1032-1

[61] Mirabi P, Chaichi MJ, Esmaeilzadeh S, et al. The role of fatty acids on ICSI outcomes: A prospective cohortstudy. Lipids Health Dis. 2017;16:18. DOI: 10.1186/s12944-016-0396-z

[62] Mirabi P., Chaichi M.J., Esmaeilzadeh S. et al. The role of fatty acids on ICSI outcomes: A prospective cohortstudy // Lipids Health Dis. 2017. Vol. 16. P. 18. DOI: 10.1186/s12944-016-0396-z

[63] Chiu YH, Karmon AE, Gaskins AJ, et al. Serum omega-3 fatty acids and treatment outcomes among women undergoing assisted reproduction. Hum Reprod. 2018;33:156−165. DOI: 10.1093/humrep/dex335

[64] Chiu Y.H., Karmon A.E., Gaskins A.J. et al. Serum omega-3 fatty acids and treatment outcomes among women undergoing assisted reproduction // Hum. Reprod. 2018. Vol. 33. P. 156−165. DOI: 10.1093/humrep/dex335

[65] Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992;305(6854):609−613. DOI: 10.1136/bmj.305.6854.609

[66] Carlsen E., Giwercman A., Keiding N., Skakkebaek N.E. Evidence for decreasing quality of semen during past 50 years // BMJ. 1992. Vol. 305 (6854). P. 609−613. DOI: 10.1136/bmj.305.6854.609

[67] Davidyan OV, Tyuzikov IA, Tazhetdinov OKh, et al. Omega-3 polyunsaturated fatty acids in andrological practice. Questions of urology and andrology. 2018;6(2):28−39. DOI: 10.20953/2307-6631-2018-2-28-39

[68] Давидян О.В., Тюзиков И.А., Тажетдинов О.Х. и др. Омега-3 полиненасыщенные жирные кислоты в андрологической практике // Вопросы урологии и андрологии. 2018. Т. 6. № 2. С. 28−39. DOI: 10.20953/2307-6631-2018-2-28-39

[69] Safarinejad MR, Hosseini SY, Dadkha HF, Asgari MA. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and antioxidant status of seminal plasma: a comparison between fertile and infertile men. Clin Nutr. 2010;29(1):100−105. DOI: 10.1016/j.clnu.2009.07.008

[70] Safarinejad M.R., Hosseini S.Y., Dadkha H.F., Asgari M.A. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and antioxidant status of seminal plasma: a comparison between fertile and infertile men // Clin. Nutr. 2010. Vol. 29. № 1. P. 100−105. DOI: 10.1016/j.clnu.2009.07.008

[71] Aksoy Y, Aksoy H, Altinkaynak K, Aydin HR, Ozkan A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot Essent Fatty Acids. 2006;75(2):75−79. DOI: 10.1016/j.plefa.2006.06.002

[72] Aksoy Y., Aksoy H. Altinkaynak K. et al. Sperm fatty acid composition in subfertile men // Prostaglandins Leukot. Essent. Fatty Acids. 2006. Vol. 75. No. 2. P. 75−79. DOI: 10.1016/j.plefa.2006.06.002

[73] Safarinejad MR. Effect of omega-3 polyunsaturated fatty acid supplementation on semen profile and enzymatic antioxidant capacity of seminal plasma in infertile men with idiopathic oligoasthenoteratospermia: a double-blind, placebo-controlled, randomised study. Andrologia. 2011;43(1):38−47. DOI: 10.1111/j.1439-0272.2009.01013.x

[74] Safarinejad M.R. Effect of omega-3 polyunsaturated fatty acid supplementation on semen profile and enzymatic antioxidant capacity of seminal plasma in infertile men with idiopathic oligoasthenoteratospermia: a double-blind, placebo-controlled, randomised study // Andrologia. 2011. Vol. 43. No. 1. P. 38−47. DOI: 10.1111/ j.1439-0272.2009.01013.x

[75] Attaman JA, Toth TL, Furtado J, et al. Dietary fat and semen quality among men attending a fertility clinic. Hum Reprod. 2012;27(5):1466. DOI: 10.1093/humrep/des065

[76] Attaman J.A., Toth T.L., Furtado J. et al. Dietary fat and semen quality among men attending a fertility clinic // Hum. Reprod. 2012. Vol. 27. No. 5. P. 1466. DOI: 10.1093/humrep/des065

[77] Roqueta-Rivera M, Abbott TL, Sivaguru M, et al. Deficiency in the omega-3 fatty acid pathway results in failure of acrosome biogenesis in mice. Biol Reprod. 2011;85(4):721−732. DOI: 10.1095/biolreprod.110.089524

[78] Roqueta-Rivera M., Abbott T.L., Sivaguru M. et al. Deficiency in the omega-3 fatty acid pathway results in failure of acrosome biogenesis in mice // Biol. Reprod. 2011. Vol. 85. No. 4. P. 721−732. DOI: 10.1095/biolreprod.110.089524

[79] Aitken RJ. The Amoroso Lecture. The human spermatozoon – a cell in crisis? J Reprod Fertil. 1999;115(1):1−7. DOI: 10.1530/jrf.0.1150001

[80] Aitken R.J. The Amoroso Lecture. The human spermatozoon – a cell in crisis? // J. Reprod. Fertil. 1999. Vol. 115. No. 1. P. 1−7. DOI: 10.1530/jrf.0.1150001

[81] Fraczek M, Kurpisz M. The redox system in human semen and peroxidative damage of spermatozoa. Postepy Hig Med Dosw (Online). 2005;59:523−534. DOI: 10.2164/jandrol.106.001149

[82] Fraczek M., Kurpisz M. The redox system in human semen and peroxidative damage of spermatozoa // Postepy Hig. Med. Dosw. (Online). 2005. Vol. 59. P. 523−534. DOI: 10.2164/jandrol.106.001149

[83] Aziz N, Saleh RA, Sharma RK. Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil Steril. 2004;81(2):349−354. DOI: 10.1016/j. fertnstert.2003.06.026

[84] Aziz N., Saleh R.A., Sharma R.K. Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index // Fertil. Steril. 2004. Vol. 81. No. 2. P. 349−354. DOI: 10.1016/j. fertnstert.2003.06.026

[85] Shang Y, Liu C, Cui D, et al. The effect of chronic bacterial prostatitis on semen quality in adult men: a metaanalysis of case-control studies. Sci Rep. 2014;4:7233. DOI: 10.1038/srep07233

[86] Shang Y., Liu C., Cui D. et al. The effect of chronic bacterial prostatitis on semen quality in adult men: a metaanalysis of case-control studies // Sci. Rep. 2014. Vol. 4. P. 7233. DOI: 10.1038/srep07233

[87] Hosseini B, Nourmohamadi M, Hajipour S, et al. The effect of omega-3 fatty acids, EPA, and/or DHA on male infertility: A systematic review and meta-analysis. J Diet Suppl. 2019;16(2):245−256. DOI: 10.1080/19390211.2018.1431753

[88] Hosseini B., Nourmohamadi M., Hajipour S. et al. The effect of omega-3 fatty acids, EPA, and/or DHA on male infertility: A systematic review and meta-analysis // J. Diet. Suppl. 2019. Vol. 16. No. 2. P. 245−256. DOI: 10.1080/19390211.2018.1431753

[89] Shim JS, Kim DH, Bae JH, Moon du G. Effects of omega-3 fatty acids on erectile dysfunction in a rat model of atherosclerosis-induced chronic pelvic ischemia. J Korean Med Sci. 2016;31(4):585−589. DOI: 10.3346/jkms.2016.31.4.585

[90] Shim J.S., Kim D.H., Bae J.H., Moon du G. Effects of omega-3 fatty acids on erectile dysfunction in a rat model of atherosclerosis-induced chronic pelvic ischemia // J. Korean Med. Sci. 2016. Vol. 31. No. 4. P. 585−589. DOI: 10.3346/jkms.2016.31.4.585

[91] Liao CH, Wu YN, Chen BH, et al. Neuroprotective effect of docosahexaenoic acid nanoemulsion on erectile function in a rat model of bilateral cavernous nerve injury. Sci Rep. 2016;6:33040. DOI: 10.1038/srep33040

[92] Liao C.H., Wu Y.N., Chen B.H. et al. Neuroprotective effect of docosahexaenoic acid nanoemulsion on erectile function in a rat model of bilateral cavernous nerve injury // Sci. Rep. 2016. Vol. 6. P. 33040. DOI: 10.1038/srep33040

[93] Ehehalt R, Fiillekrug J, Pohl J, et al. Translocation of long chain fatty acids across the plasma membrane – lipid rafts and fatty acid transport proteins. Mol Cell Biochem. 2006;284(1−2):135−140.

[94] Ehehalt R., Fiillekrug J., Pohl J. et al. Translocation of long chain fatty acids across the plasma membrane – lipid rafts and fatty acid transport proteins // Mol. Cell. Biochem. 2006. Vol. 284. No. 1−2. P. 135−140.

[95] Gromova OA, Torshin IYu, Limanova OA. Omega-3 polyunsaturated fatty acids and active folates: perspectives of complex application for nutritional support of pregnancy and prevention of malformations. Obstetrics and gynecology. 2018;(1):21−28. (In Russ.). DOI: 10.18565/aig.2018.1.21-28

[96] Громова О.А., Торшин И.Ю., Лиманова О.А. Омега-3 полиненасыщенные жирные кислоты и активные фолаты: перспективы комплексного применения для нутрициальной поддержки беременности и профилактики пороков развития // Акушерство и гинекология. 2018. № 1. С. 21−28. DOI: 10.18565/aig.2018.1.21-28

[97] Gromova OA, Torshin IYu, Yurgel IS. Systematic analysis of the biochemical effects of eicosapentaenoic and docosahexaenoic omega 3 PUFAs on the physiology of pregnant women and fetal development. Difficult patient. 2009;1−2.

[98] Громова О.А., Торшин И.Ю., Юргель И.С. Систематический анализ биохимических эффектов эйкозапентаеновой и докозагексаеновой омега 3 ПНЖК на физиологию беременной и развитие плода // Трудный пациент. 2009. Т. 1−2. С. 10−16.

[99] Makrides M, Best K. Docosahexaenoic acid and preterm birth. Ann Nutr Metab. 2016;69:30−34. DOI: 10.1159/000448263

[100] Makrides M., Best K. Docosahexaenoic acid and preterm birth // Ann. Nutr. Metab. 2016. Vol. 69. P. 30−34. DOI: 10.1159/000448263

[101] Middleton P, Gomersall JC, Gould JF, et al. Omega-3 fatty acid addition during pregnancy. Cochrane Database Syst Rev. 2018;11(11):CD003402. DOI: 10.1002/14651858.CD003402.pub3

[102] Middleton P., Gomersall J.C., Gould J.F. et al. Omega-3 fatty acid addition during pregnancy // Cochrane Database Syst. Rev. 2018. Vol. 11. No. 11. P. CD003402. DOI: 10.1002/14651858.CD003402.pub3

[103] Makrides M, Duley L, Olsen SF. Marine oil, and other prostaglandin precursor, supplementation for pregnancy uncomplicated by pre-eclampsia or intrauterine growth restriction. Cochrane Database Syst Rev. 2006;(3):CD003402. DOI: 10.1002/14651858.CD003402.pub2

[104] Makrides M., Duley L., Olsen S.F. Marine oil, and other prostaglandin precursor, supplementation for pregnancy uncomplicated by pre-eclampsia or intrauterine growth restriction // Cochrane Database Syst. Rev. 2006. Vol. 3. P. CD003402. DOI: 10.1002/14651858.CD003402.pub2

[105] Harris MA, Reece MS, McGregor JA, et al. The effect of omega-3 docosahexaenoic acid supplementation on gestational length: randomized trial of supplementation compared to nutrition education for increasing n-3 intake from Foods. Biomed Res Int. 2015;2015:123078. DOI: 10.1155/2015/123078

[106] Harris M.A., Reece M.S., McGregor J.A. et al. The effect of omega-3 docosahexaenoic acid supplementation on gestational length: randomized trial of supplementation compared to nutrition education for increasing n-3 intake from Foods // Biomed. Res. Int. 2015. Vol. 2015. P. 123078. DOI: 10.1155/2015/123078

[107] Carvajal JA. Docosahexaenoic acid supplementation early in pregnancy may prevent deep placentation disorders. Biomed Res Int. 2014:526895. DOI: 10.1155/2014/526895

[108] Carvajal J.A. Docosahexaenoic acid supplementation early in pregnancy may prevent deep placentation disorders // Biomed. Res. Int. 2014. Vol. 2014. P. 526895. DOI: 10.1155/2014/526895

[109] Pietrantoni E, Del Chierico F, Rigon G, et al. Docosahexaenoic acid supplementation during pregnancy: a potential tool to prevent membrane rupture and preterm labor. Int J Mol Sci. 2014;15(5):8024−8036. DOI: 10.3390/ijms15058024

[110] Pietrantoni E., Del Chierico F., Rigon G. et al. Docosahexaenoic acid supplementation during pregnancy: a potential tool to prevent membrane rupture and preterm labor // Int. J. Mol. Sci. 2014. Vol. 15. No. 5. P. 8024−8036. DOI: 10.3390/ijms15058024

[111] Ismail AM, Ramadan MF, Ali MK, et al. A randomized controlled study of the efficacy of 4 weeks of supplementation with ω-3 poly-unsaturated fatty acids in cases of unexplained oligohydramnios. J Perinatol. 2016;36(11):944−947. DOI: 10.1038/jp.2016.134

[112] Ismail A.M., Ramadan M.F., Ali M.K. et al. A randomized controlled study of the efficacy of 4 weeks of supplementation with ω-3 poly-unsaturated fatty acids in cases of unexplained oligohydramnios // J. Perinatol. 2016. Vol. 36. No. 11. P. 944−947. DOI: 10.1038/jp.2016.134

[113] Qawasmi A, Landeros-Weisenberger A, Bloch MH. Meta-analysis of LCPUFA supplementation of infant formula and visual acuity. Pediatrics. 2013;131(1):262−272. DOI: 10.1542/peds.2012-0517

[114] Qawasmi A., Landeros-Weisenberger A., Bloch M.H. Meta-analysis of LCPUFA supplementation of infant formula and visual acuity // Pediatrics. 2013. Vol. 131. No. 1. P. 262−272. DOI: 10.1542/peds.2012-0517

[115] Torshin IYu, Gusev EI, Gromova OA, et al. World experience in studying the effects of omega-3 polyunsaturated fatty acids: influence on cognitive potential and some mental disorders. Journal of Neurology and Psychiatry by SS Korsakov. 2011;111(11):79−86. (In Russ.)

[116] Торшин И.Ю., Гусев Е.И., Громова О.А. и др. Мировой опыт изучения эффектов омега-3 полиненасыщенных жирных кислот: влияние на когнитивный потенциал и некоторые психические расстройства // Журнал неврологии и психиатрии им. С.С. Корсакова. 2011. Т. 111. № 11. С. 79−86.

[117] Golding J, Steer C, Emmett P. et al. High levels of depressive symptoms in pregnancy with low omega-3 fatty acid intake from fish. Epidemiology. 2009;20(4):598−603. DOI: 10.1097/EDE.0b013e31819d6a57

[118] Golding J., Steer C., Emmett P. et al. High levels of depressive symptoms in pregnancy with low omega-3 fatty acid intake from fish // Epidemiology. 2009. Vol. 20. No. 4. P. 598−603. DOI: 10.1097/EDE.0b013e31819d6a57

[119] Pinto TJ, Vilela AA, Farias DR, et al. Serum n-3 polyunsaturated fatty acids are inversely associated with longitudinal changes in depressive symptoms during pregnancy. Epidemiol Psychiatr Sci. 2017;26(2):157−168. DOI: 10.1017/S204579601500116X

[120] Pinto T.J., Vilela A.A., Farias D.R. et al. Serum n-3 polyunsaturated fatty acids are inversely associated with longitudinal changes in depressive symptoms during pregnancy // Epidemiol. Psychiatr. Sci. 2017. Vol. 26. No. 2. P. 157−168. DOI: 10.1017/S204579601500116X

[121] Gunaratne AW, Makrides M, Collins CT. Maternal prenatal and/or postnatal n-3 long chain polyunsaturated fatty acids (LCPUFA) supplementation for preventing allergies in early childhood. Cochrane Database Syst Rev. 2015;7:CD010085. DOI: 10.1002/14651858.CD010085.pub2

[122] Gunaratne A.W., Makrides M., Collins C.T. Maternal prenatal and/or postnatal n-3 long chain polyunsaturated fatty acids (LCPUFA) supplementation for preventing allergies in early childhood // Cochrane Database Syst. Rev. 2015. Vol. 7. P. CD010085. DOI: 10.1002/14651858.CD010085.pub2

[123] FDA mercury levels in fish and shellfish [cited 23 Aug 2021]. Available from: https://www.fda.gov/food/metals-and-yourfood/mercury-levels-commercial-fish-and-shellfish-1990-2012

[124] FDA mercury levels in fish and shellfish [дата обращения: 23.08.2021]. Доступ по ссылке: https://www.fda.gov/food/metals-and-yourfood/mercury-levels-commercial-fish-and-shellfish-1990-2012

[125] Sakodynsky KI, Brazhnikov VV, Volkov SA, et al. Analytical chromatography. Moscow: Himija; 1993. (In Russ.)

[126] Сакодынский К.И., Бражников В.В., Волков С.А. и др. Аналитическая хроматография. Москва: Химия, 1993.

[127] Rinaldo P, Matern D, Bennett MJ. Fatty acid oxidation disorders. Ann Rev Physiol. 2002;64:477−502. DOI: 10.1146/annurev.physiol.64.082201.154705

[128] Rinaldo P., Matern D., Bennett M.J. Fatty acid oxidation disorders // Ann. Rev. Physiol. 2002. Vol. 64. P. 477−502. DOI: 10.1146/annurev.physiol.64.082201.154705

[129] Jeppesen PB, Chistensen MS, Hoy CE, Mortersen PB. Essential fatty acid deficiency in patients with severe fat malabsorption. Am J Clin Nutr. 1997;65:837−843. DOI: 10.1093/ajcn/65.3.837

[130] Jeppesen P.B., Chistensen M.S., Hoy C.E., Mortersen P.B. Essential fatty acid deficiency in patients with severe fat malabsorption // Am. J. Clin. Nutr. 1997. Vol. 65. P. 837−843. DOI: 10.1093/ajcn/65.3.837

[131] McCowen KC, Bistrian BR. Essential fatty acids and their derivatives. Curr Opin Gastroenterol. 2005;21(2):207−215. DOI: 10.1097/01.mog.0000153361.90653.cb

[132] McCowen K.C., Bistrian B.R. Essential fatty acids and their derivatives // Curr. Opin. Gastroenterol. 2005. Vol. 21. No. 2. P. 207−215. DOI: 10.1097/01.mog.0000153361.90653.cb

[133] Mayo Medical Laboratories [cited 23 Aug 2021]. Available from: https://www.mayocliniclabs.com/test-catalog/Clinical+and+Interpretive/81939

[134] Mayo Medical Laboratories [дата обращения: 23.08.2021]. Доступ по ссылке: https://www.mayocliniclabs.com/test-catalog/Clinical+and+Interpretive/81939

[135] Stark KD, Van Elswyk ME, Higgins MR, et al. Global survey of the omega-3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the bloodstream of healthy adults. Progr Lipid Res. 2016;63:132−152. DOI: 10.1016/j.plipres.2016.05.001

[136] Stark K.D., Van Elswyk M.E., Higgins M.R. et al. Global survey of the omega-3 fatty acids, docosahexaenoic acid and eicosapentaenoic acid in the bloodstream of healthy adults // Progr. Lipid Res. 2016. Vol. 63. P. 132−152. DOI: 10.1016/j.plipres.2016.05.001

[137] Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomedicine Pharmacotherapy. 2002;56(8):365−379. DOI: 10.1016/S0753-3322(02)00253-6

[138] Simopoulos A.P. The importance of the ratio of omega-6/omega-3 essential fatty acids // Biomedicine Pharmacotherapy. 2002. Vol. 56. No. 8. P. 365−379. DOI: 10.1016/S0753-3322(02)00253-6

RIGHTS & PERMISSIONS

Eсо-Vector