Relation between Inflammation, Oxidative Stress, and Macronutrient Intakes in Normal and Excessive Body Weight Adolescent Girls with Clinical Features of Polycystic Ovary Syndrome

Małgorzata Mizgier, Grażyna Jarząbek-Bielecka, Natalia Wendland, Elżbieta Jodłowska-Siewert, Marcin Nowicki, Alicja Brożek, Witold Kędzia, Dorota Formanowicz, Justyna Opydo-Szymaczek, Małgorzata Mizgier, Grażyna Jarząbek-Bielecka, Natalia Wendland, Elżbieta Jodłowska-Siewert, Marcin Nowicki, Alicja Brożek, Witold Kędzia, Dorota Formanowicz, Justyna Opydo-Szymaczek

Abstract

The impact of diet on inflammation and oxidative stress (OS) in girls with polycystic ovary syndrome (PCOS) is unknown. Therefore, our study aimed to investigate, in PCOS girls, whether certain macronutrient intakes can be associated with these disturbances. For this purpose, 59 PCOS participants (aged 14-18 years) were recruited to this study and divided into two subgroups: overweight/obese-Ov/Ob group (n = 22) and normal weight-N group (n = 37). Nutrition was assessed using a 3-day food record. The studied markers were total antioxidant capacity (TAC), malondialdehyde (MDA), C-reactive protein (CRP), tumor necrosis factor α (TNF-α), and interleukins 1 and 6 (IL-1 and IL-6). We found plant protein intake inversely correlated with IL-6 (p = 0.007; r = -0.557), TNF-α (p = 0.006; r = -0.564), MDA (p = 0.01; r = -0.539) in the Ov/Ob group and with TAC (p = 0.021; r = -0.38) in the N group. Inverse correlations in the Ov/Ob group were observed between protein intake and IL-6 (p = 0.031; r = -0.461), TNF- α (p = 0.043; r = -0.435); carbohydrates and IL-6 (p = 0.037; r = -0.448), MDA (p = 0.045; r = -0.431); fiber and IL-6 (p = 0.025; r = -0.475). A positive relationship between cholesterol intake and CRP concentration (p = 0.038; r = 0.342) was also found in the N group. These findings revealed that inflammation and OS are increased in Ov/Ob girls with decreased plant protein intake and low carbohydrates in the diet. Moreover, inflammation may be increased by cholesterol intake in slim PCOS girls. On the other hand, decreased intake of fiber and total protein intake increased inflammation. ClinicalTrials.gov Identifier: NCT04738409.

Keywords: adolescent girls; diet; food environments; hyperandrogenism; obesity; polycystic ovary syndrome.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Lai M.M., Li C.I., Kardia S.L., Liu C.S., Lin W.Y., Lee Y.D., Chang P.C., Lin C.C., Li T.C. Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population. BMC Public Health. 2010;10:429. doi: 10.1186/1471-2458-10-429.
    1. Ren Z., Zhao A., Wang Y., Meng L., Szeto I.M.Y., Li T., Gong H., Tian Z., Zhang Y., Wang P. Association between dietary inflammatory index, c-reactive protein and metabolic syndrome: A cross-sectional study. Nutrients. 2018;10:831. doi: 10.3390/nu10070831.
    1. Stringa N., Brahimaj A., Zaciragic A., Dehghan A., Ikram M.A., Hofman A., Muka T., Kiefte-de Jong J.C., Franco O.H. Relation of antioxidant capacity of diet and markers of oxidative status with C-reactive protein and adipocytokines: A prospective study. Metab. Clin. Exp. 2017;71:171–181. doi: 10.1016/j.metabol.2017.03.015.
    1. Christ A., Lauterbach M., Latz E. Western Diet and the Immune System: An Inflammatory Connection. Immunity. 2019;51:794–811. doi: 10.1016/j.immuni.2019.09.020.
    1. Ma K., Jin X., Zhao Q., Zhang X. Inflammatory mediators involved in the progression of the metabolic syndrome. Diabetes/Metab. Res. Rev. 2012;28:388–394. doi: 10.1002/dmrr.2291.
    1. Jarząbek-Bielecka G., Opydo-Szymaczek J., Mizgier M., Bojanowska K., Pisarska-Krawczyk M., Chuchracki M., Kędzia W., Wojtyła A. Zespół policystycznych jajników jako problem w ginekologii i medycynie rodzinnej, z uwzględnieniem pacjentek w wieku rozwojowym (Polycystic ovary syndrome as a problem in gynecology and family medicine, including patients in developmental age) Med. Rodz. 2018;21:335–338. doi: 10.25121/MR.2018.21.4.335.
    1. Małecka-Tendera E. Zespół policystycznych jajników u dziewcząt (Polycystic ovary syndrome in girls) Endokrynol. Ped. 2015;14:51. doi: 10.18544/EP-01.14.02.1573.
    1. Rojas J., Chávez M., Olivar L., Rojas M., Morillo J., Mejías J., Calvo M., Bermudez V. Polycystic Ovary Syndrome, Insulin Resistance, and Obesity: Navigating the patophysiologic labyrinth. Int. J. Reprod. Med. 2014:719050. doi: 10.1155/2014/719050.
    1. Turan V., Sezer E.D., Zeybek B., Sendag F. Infertility and the Presence of Insulin Resistance Are Associated with Increased Oxidative Stress in Young, Non-obese Turkish Women with Polycystic Ovary Syndrome. J. Pediatr. Adolesc. Gynecol. 2015;28:119–123. doi: 10.1016/j.jpag.2014.05.003.
    1. Murri M., Luque-Ramírez M., Insenser M., Ojeda-Ojeda M., Escobar-Morreale H.F. Circulating markers of oxidative stress and polycystic ovary syndrome (PCOS): A systemic review and meta-analysis. Hum. Reprod. Update. 2013;19:268–288. doi: 10.1093/humupd/dms059.
    1. Mancini A., Bruno C., Vergani E., D′abate C., Giacchi E., Silvestrini A. Oxidative Stress and Low-Grade Inflammation in Polycystic Ovary Syndrome: Controversies and New Insights. Int. J. Mol. Sci. 2021;22:1667. doi: 10.3390/ijms22041667.
    1. Tao T., Li S., Zhao A., Zhang Y., Liu W. Expression of the CD11c gene in subcutaneous adipose tissue is associated with cytokine level and insulin resistance in women with polycystic ovary syndrome. Eur. J. Endocrinol. 2012;167:705–713. doi: 10.1530/EJE-12-0340.
    1. Goodman N.F., Cobin R.H., Futterweit W., Glueck J.S., Legro R.S., Carmina E. American association of clinical endocrinologists, American college of endocrinology, and androgen excess and pcos society disease state clinical review: Guide to the best practices in the evaluation and treatment of polycystic ovary syndrome—Part 2. Endocr. Pract. 2015;21:1415–1426. doi: 10.4158/EP15748.DSCPT2.
    1. Khashchenko E., Vysokikh M., Uvarova E., Krechetova L., Vtorushina V., Ivanets T., Volodina M., Tarasova N., Sukhanova I., Sukhikh G. Activation of Systemic Inflammation and Oxidative Stress in Adolescent Girls with Polycystic Ovary Syndrome in Combination with Metabolic Disorders and Excessive Body Weight. J. Clin. Med. 2020;9:1399. doi: 10.3390/jcm9051399.
    1. Deans R. Medical sciences Review Polycystic Ovary Syndrome in Adolescence. Med. Sci. 2019;7:101. doi: 10.3390/medsci7100101.
    1. Milewicz A., Kudła M., Spaczyński R.Z., Dębski R., Męczekalski B., Wielgoś M., Ruchała M., Małecka-Tendera E., Kos-Kudła B., Jędrzejuk D., et al. The polycystic ovary syndrome: A position statement from the Polish Society of Endocrinology, the Polish Society of Gynaecologists and Obstetricians, and the Polish Society of Gynaecological Endocrinology. Endokrynol. Pol. 2018;68:328–344. doi: 10.5603/EP.2018.0046.
    1. Naz M.S.G., Tehrani F.R., Majd H.A., Ahmadi F., Ozgoli G., Fakari F.R., Ghasemi V. The prevalence of polycystic ovary syndrome in adolescents: A systematic review and meta-analysis. Int. J. Reprod. Biomed. 2019;17:533–542. doi: 10.18502/ijrm.v17i8.4818.
    1. Teede H.J., Misso M.L., Costello M.F., Dokras A., Laven J., Moran L., Piltonen T., Norman R.J., Andersen M., Azziz R., et al. Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Hum. Reprod. 2018;33:1602–1618. doi: 10.1093/humrep/dey256.
    1. Messinis I.E., Messini C.I., Anifandis G., Dafopoulos K. Polycystic ovaries and obesity. Best Pract. Res. Clin. Obstet. Gynaecol. 2015;29:479–488. doi: 10.1016/j.bpobgyn.2014.11.001.
    1. Stepto N.K., Cassar S., Joham A.E., Hutchison S.K., Harrison C.L., Goldstein R.F., Teede H.J. Women with polycystic ovary syndrome have intrinsic insulin resistance on euglycaemic-hyperinsulaemic clamp. Hum. Reprod. 2013;28:777–784. doi: 10.1093/humrep/des463.
    1. Liou T.H., Yang J.H., Hsieh C.H., Lee C.Y., Hsu C., Hsu M.I.S. Clinical and biochemical presentations of polycystic ovary syndrome among obese and nonobese women. Fertil. Steril. 2009;93:e27. doi: 10.1016/j.fertnstert.2008.09.003.
    1. Mizgier M., Jarząbek-Bielecka G., Opydo-Szymaczek J., Wendland N., Więckowska B., Kędzia W. Risk Factors of Overweight and Obesity Related to Diet and Disordered Eating Attitudes in Adolescent Girls with Clinical Features of Polycystic Ovary Syndrome. J. Clin. Med. 2020;9:3041. doi: 10.3390/jcm9093041.
    1. Repaci A., Gambineri A., Pasquali R. The role of low-grade inflammation in the polycystic ovary syndrome. Mol. Cell. Endocrinol. 2011;335:30–41. doi: 10.1016/j.mce.2010.08.002.
    1. Sathyapalan T., Atkin S.L. Mediators of Inflammation in Polycystic Ovary Syndrome in Relation to Adiposity. Mediat. Inflamm. 2010 doi: 10.1155/2010/758656.
    1. Pfutzner A., Schöndorf T., Hanefeld M., Forst T. High-sensitivity C-reactive protein predicts cardiovascular risk in diabetic and nondiabetic patients: Effects of insulin-sensitizing treatment with pioglitazone. J. Diabetes Sci. Technol. 2010;4:706–716. doi: 10.1177/193229681000400326.
    1. Hotamisligil G.S., Peraldi P., Budavari A., Ellis R., White M.F., Spiegelman B.M. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science. 1996;271:665–668. doi: 10.1126/science.271.5249.665.
    1. Hirabara S.M., Gorjao R., Vinolo M.A., Rodrigues A.C., Nachbar R.T., Curi R. Molecular targets related to inflammation and insulin resistance and potential interventions. BioMed Res. Int. 2012 doi: 10.1155/2012/379024.
    1. Alberti K.G.M.M., Eckel R.H., Grundy S.M., Zimmet P.Z., Cleeman J.I., Donato K.A., Fruchart J.C., James W.P.T., Loria C.M., Smith S.C. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International atherosclerosis society; And international association for the study of obesity. Circulation. 2009 doi: 10.1161/CIRCULATIONAHA.109.192644.
    1. Mohammadi M., Gozashti M.H., Aghadavood M., Mehdizadeh M.R., Hayatbakhsh M.M. Clinical Significance of Serum IL-6 and TNF-α Levels in Patients with Metabolic Syndrome. Rep. Biochem. Mol. Biol. 2017;6:74–79.
    1. Savini I., Catani M.V., Evangelista D., Gasperi V., Avigliano L. Obesity-Associated Oxidative Stress: Strategies Finalized to Improve Redox State. Int. J. Mol. Sci. 2013;14:10497–10538. doi: 10.3390/ijms140510497.
    1. Bondia-Pons I., Ryan L., Martinez J.A. Oxidative stress and inflammation interactions in human obesity. J. Physiol. Biochem. 2012;68:701–711. doi: 10.1007/s13105-012-0154-2.
    1. Sies H. Oxidative stress: Impact in redox biology and medicine. Arch. Med. Biomed. Res. 2015;2:146–150. doi: 10.4314/ambr.v2i4.6.
    1. Swain J.H., Alekel D.L., Dent S.B., Peterson C., Reddy M.B. Iron indexes and total antioxidant status in response to soy protein intake in perimenopausal women. Am. J. Clin. Nutr. 2002;76:165–171. doi: 10.1093/ajcn/76.1.165.
    1. Halliwell B., Cross C.E. Oxygen-derived species: Their relation to human disease and environmental stress. Environ. Health Perspect. 1994;102(Suppl. S10):5–12. doi: 10.1289/ehp.94102s105.
    1. Zalata A., Yahia S., El-Bakary A., Elsheikha H.M. Increased DNAdam-age in children caused by passive smoking as assessed by comet assay and oxidative stress. Mutat. Res. 2007;629:140–147. doi: 10.1016/j.mrgentox.2007.02.001.
    1. Kato T., Inoue T., Morooka T., Yoshimoto N., Node K. Short-term passive smoking causes endothelial dysfunction via oxidative stress in nonsmok-ers. Can. J. Physiol. Pharmacol. 2006;84:523–529. doi: 10.1139/y06-030.
    1. Dludla P., Nkambule B.B., Jack B., Mkandla Z., Mutize T., Silvestri S., Orlando P., Tiano L., Louw J., Mazibuko-Mbeje S.E. Inflammation and Oxidative Stress in an Obese State and the Protective Effects of Gallic Acid. Nutrients. 2019;11:23. doi: 10.3390/nu11010023.
    1. Rupérez A.I., Mesa M.D., Anguita-Ruiz A., González-Gil E.M., Vázquez-Cobela R., Moreno L.A., Gil Á., Gil-Campos M., Leis R., Bueno G., et al. Antioxidants and Oxidative Stress in Children: Influence of Puberty and Metabolically Unhealthy Status. Antioxidants. 2020;9:618. doi: 10.3390/antiox9070618.
    1. Kilic E., Özer Ö.F., Toprak A.E., Erman H., Torun E., Ayhan S.K., Caglar H.G., Selek S., Kocyigit A., Erek A.T. Oxidative Stress Status in Childhood Obesity: A Potential Risk Predictor. Med Sci. Monit. 2016;22:3673–3679. doi: 10.12659/MSM.897965.
    1. Groner J.A., Huang H., Eastman N., Lewis L., Joshi M.S., Schanbacher B.L., Nicholson L., Bauer J.A. Oxidative stress in youth and adolescents with elevated body mass index exposed to secondhand smoke. Nicotine Tob. Res. 2016;18:1622–1627. doi: 10.1093/ntr/ntw025.
    1. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007;39:44–84. doi: 10.1016/j.biocel.2006.07.001.
    1. Zorov D.B., Juhaszova M., Sollott S.J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 2014;94:909–950. doi: 10.1152/physrev.00026.2013.
    1. Amato M.C., Guarnotta V., Forti D., Donatelli M., Dolcimascolo S., Giordano C. Metabolically healthypolycystic ovary syndrome (MH-PCOS) and metabolically unhealthy polycystic ovary syndrome (MU-PCOS): A comparative analysis of four simple methods useful for metabolic assessment. Hum. Reprod. 2013;28:1919–1928. doi: 10.1093/humrep/det105.
    1. Barbaresko J., Koch M., Schulze M.B., Nöthlings U. Dietary pattern analysis and biomarkers of low-grade inflammation: A systematic literature review. Nutr. Rev. 2013;71:511–527. doi: 10.1111/nure.12035.
    1. Basu A., Devaraj S., Jialal I. Dietary factors that promote or retard inflammation. Arterioscler. Thromb. Vasc. Biol. 2006;26:995–1001. doi: 10.1161/01.ATV.0000214295.86079.d1.
    1. Hezaveha Z.S., Sikaroudia M.K., Vafaa M., Claytonb Z.S., Soltanicd S. Effect of egg consumption on inflammatory markers: A systematic review and meta-analysis of randomized controlled clinical trials. J. Sci. Food Agric. 2019;99:6663–6670. doi: 10.1002/jsfa.9903.
    1. Wirth M.D., Burch J., Shivappa N., Violanti J.M., Burchfiel C.M., Fekedulegn D., Andrew M.E., Hartley T.A., Miller D.B., Mnatsakanova A. Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J. Occup. Environ. Med. 2014;56:986–989. doi: 10.1097/JOM.0000000000000213.
    1. Sokol A., Wirth M.D., Manczuk M., Shivappa N., Zatonska K., Hurley T.G., Hébert J.R. Association between the dietary inflammatory index, waist-to-hip ratio and metabolic syndrome. Nutr. Res. 2016;36:1298–1303. doi: 10.1016/j.nutres.2016.04.004.
    1. Alkerwi A.A., Shivappa N., Crichton G., Hébert J.R. No significant independent relationships with cardiometabolic biomarkers were detected in the Observation of Cardiovascular Risk Factors in Luxembourg study population. Nutr. Res. 2014;34:1058–1065. doi: 10.1016/j.nutres.2014.07.017.
    1. Neufcourt L., Assmann K.E., Fezeu L.K., Touvier M., Graffouillère L., Shivappa N., Hébert J.R., Wirth M.D., Hercberg S., Galan P. Prospective association between the dietary inflammatory index and metabolic syndrome: Findings from the SU.VI.MAX study. Nutr. Metab. Cardiovasc. Dis. 2015;25:988–996. doi: 10.1016/j.numecd.2015.09.002.
    1. Shivappa N., Hébert J.R., Rietzschel E.R., De Buyzere M.L., Langlois M., Debruyne E., Marcos A., Huybrechts I. Associations between dietary inflammatory index and inflammatory markers in the Asklepios Study. Br. J. Nutr. 2015;113:665–671. doi: 10.1017/S000711451400395X.
    1. Correa-Rodríguez M., González-Jiménez E., Rueda-Medina B., Tovar-Gálvez M.I., Ramírez-Vélez R., Correa-Bautista J.E., Schmidt-RioValle J. Dietary inflammatory index and cardiovascular risk factors in Spanish children and adolescents. Res. Nurs. Health. 2018:448–458. doi: 10.1002/nur.21904.
    1. Willcox J.K., Ash S.L., Catignani G.L. Antioxidants and prevention of chronic disease. Crit. Rev. Food Sci. Nutr. 2004;44:275–295. doi: 10.1080/10408690490468489.
    1. Stahl W., Sies H. Antioxidant activity of carotenoids. Mol. Asp. Med. 2003;24 doi: 10.1016/S0098-2997(03)00030-X.
    1. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006;160:1–40. doi: 10.1016/j.cbi.2005.12.009.
    1. Friedman A., Moe S. Review of the effects of omega-3 supplementation in dialysis patients. Clin. J. Am. Soc. Nephrol. 2006;1:182–192. doi: 10.2215/CJN.00740805.
    1. Van Beelen V.A., Aarts J.M., Reus A., Mooibroek H., Sijtsma L., Bosch D., Rietjens I.M.C.M., Alink G.M. Differential induction of electrophile-responsive element-regulated genes byn-3 and n-6 polyunsaturated fatty acids. FEBS Lett. 2006;580:4587–4590. doi: 10.1016/j.febslet.2006.07.028.
    1. Calder P.C. N-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006;83:1505S–1519S. doi: 10.1093/ajcn/83.6.1505S.
    1. Lakkur S., Judd J., Goodman M. Oxidative Stress, Inflammation, and Markers of Cardiovascular Health. Atherosclerosis. 2015;243:38–43. doi: 10.1016/j.atherosclerosis.2015.08.032.
    1. The Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS) The Rotterdam ESHRE/ASRM-sponsored PCOS consensus workshop group. Hum. Reprod. 2004;19:41–47. doi: 10.1093/humrep/deh098.
    1. Sirmans S.M., Pate K.A. Epidemiology, diagnosis, and management of polycystic ovary syndrome. Clin. Epidemiol. 2014;6:1–13. doi: 10.2147/CLEP.S37559.
    1. Sultan C. Pediatric and Adolescent Gynecology: Evidence-based Clinical Practice. Volume 12. Karger Medical and Scientific Publishers; Basel, Switzerland: 2012. pp. 9–22.
    1. World Health Organization Growth Reference 5-19. BMI-for-Age for Girls. [(accessed on 21 July 2020)];2007 Available online: .
    1. Mizgier M., Jarzabek-Bielecka G., Jakubek E., Kedzia W. The relationship between body mass index, body composition and premenstrual syndrome prevalence in girls. Ginekol. Pol. 2019;90:256–261. doi: 10.5603/GP.2019.0048.
    1. Wan C.S., Ward L.C., Halim J., Gow M.L., Ho M., Briody J.N., Leung K., Cowell C.T., Garnett S.P. Bioelectrical impedance analysis to estimate body composition, and change in adiposity, in overweight and obese adolescents: Comparison with dual-energy x-ray absorptiometry. BMC Pediatr. 2014;14:249. doi: 10.1186/1471-2431-14-249.
    1. Gronowska-Senger A. Przewodnik Metodyczny Badań Sposobu Żywienia. Komitet Nauki o Żywieniu Człowieka Polskiej Akademii Nauk; Warszawa, Poland: 2013.
    1. Szponar L., Wolnicka K., Rychlik E. Album Fotografii Produktów i Potraw. Wydawnictwo IżiŻ; Warszawa, Poland: 2000.
    1. Jarosz M. Normy Żywienia dla Populacji Polski. Instytut Żywności i Żywienia; Warszawa, Poland: 2017.
    1. Gayoso-Diz P., Otero-González A., Rodriguez-Alvarez M.X., Gude F., García F., De Francisco A., Quintela A.G. Insulin resistance (HOMA-IR) cut-off values and the metabolic syndrome in a general adult population: Effect of gender and age: EPIRCE cross-sectional study. BMC Endocr. Disord. 2013;13:47. doi: 10.1186/1472-6823-13-47.
    1. Wendland N., Opydo-Szymaczek J., Mizgier M., Jarząbek-Bielecka G. Subgingival microflora in adolescent females with polycystic ovary syndrome and its association with oral hygiene, gingivitis, and selected metabolic and hormonal parameters. Clin. Oral Investig. 2020 doi: 10.1007/s00784-020-03456-5.
    1. Ilie I.R. Advances in PCOS Pathogenesis and Progression-Mitochondrial Mutations and Dysfunction. Adv. Clin. Chem. 2018;86:127–155. doi: 10.1016/bs.acc.2018.05.003.
    1. Zhang J., Fan P., Liu H., Bai H., Wang Y., Zhang F. Apolipoprotein A-I and B levels, dyslipidemia and metabolic syndrome in south-west Chinese women with PCOS. Hum. Reprod. 2012;27:2484–2493. doi: 10.1093/humrep/des191.
    1. Lim S.S., Davies M.J., Norman R.J., Moran L.J. Overweight, obesity and central obesity in women with polycystic ovary syndrome: A systematic review and meta-analysis. Hum. Reprod. Update. 2012;18:618–637. doi: 10.1093/humupd/dms030.
    1. De Groot P.C.M., Dekkers O.M., Romijn J.A., Dieben S.W.M., Helmerhorst F.M. PCOS, coronary heart disease, stroke and the influence of obesity: A systematic review and meta-analysis. Hum. Reprod. Update. 2011;17:495–500. doi: 10.1093/humupd/dmr001.
    1. Moran L.J., Misso M.L., Wild R.A., Norman R.J. Impaired glucose tolerance, type 2 diabetes and metabolic syndrome in polycystic ovary syndrome: A systematic review and meta-analysis. Hum. Reprod. Update. 2010;16:347–363. doi: 10.1093/humupd/dmq001.
    1. Kałużna M., Człapka-Matyasik M., Wachowiak-Ochmańska K., Moczko J., Kaczmarek J., Janicki A., Piątek K., Ruchała M., Ziemnicka K. Effect of Central Obesity and Hyperandrogenism on Selected Inflammatory Markers in Patients with PCOS: A WHtR-Matched Case-Control Study. J. Clin. Med. 2020;9:3024. doi: 10.3390/jcm9093024.
    1. Nasiri N., Moini A., Eftekhari-Yazdi P., Kariman L., Salman-Yazdi R., Zolfaghari Z., Arabipoor A. Abdominal obesity can induce both systemic and follicular fluid oxidative stress independent from polycystic ovary syndrome. Eur. J. Obstet. Gynecol. Reprod. Biol. 2015;184:112–116. doi: 10.1016/j.ejogrb.2014.11.008.
    1. Savic-Radojevic A., Bozic Antic I., Coric V., Bjekic-Macut J., Radic T., Zarkovic M., Djukic T., Pljesa-Ercegovac M., Panidis D., Katsikis I., et al. Effect of hyperglycemia and hyperinsulinemia on glutathione peroxidase activity in non-obese women with polycystic ovary syndrome. Horm. (Athens) 2015;14:101–108. doi: 10.14310/horm.2002.1525.
    1. Gonzalez F., Nair K.S., Daniels J.K., Basal E., Schimke J.M. Hyperandrogenism sensitizes mononuclear cells to promote glucose-induced inflammation in lean reproductive-age women. Am. J. Physiol. Endocrinol. Metab. 2012;302:E297–E306. doi: 10.1152/ajpendo.00416.2011.
    1. Federico A., Morgillo F., Tuccillo C., Ciardiello F., Loguercio C. Chronic inflammation and oxidative stress in human carcinogenesis. Int. J. Cancer. 2007;121:2381–2386. doi: 10.1002/ijc.23192.
    1. Montero D., Walther G., Perez-Martin A., Roche E., Vinet A. Endothelial dysfunction, inflammation, and oxidative stress in obese children and adolescents: Markers and effect of lifestyle intervention. Obes. Rev. 2012;13:441–455. doi: 10.1111/j.1467-789X.2011.00956.x.
    1. Codoner-Franch P., Valls-Belles V., Arilla-Codoner A., Alonso-Iglesias E. Oxidant mechanisms in childhood obesity: The link between inflammation and oxidative stress. Trans. Res. 2011;158:369–384. doi: 10.1016/j.trsl.2011.08.004.
    1. Yoost J., Savage A. Screening and Management of the Hyperandrogenic Adolescent: ACOG Committee Opinion, Number 789. Obstet. Gynecol. 2019;134:E106–E114. doi: 10.1097/AOG.0000000000003475.
    1. Block G., Dietrich M., Norkus E.P. Factors associated with oxidative stress in human populations. Am. J. Epidemiol. 2002;156:274–285. doi: 10.1093/aje/kwf029.
    1. Zuo T., Zhu M., Xu W. Roles of Oxidative Stress in Polycystic Ovary Syndrome and Cancers. Oxid. Med. Cell. Longev. 2016 doi: 10.1155/2016/8589318.
    1. Escobar-Morreale H.F., Luque-Ramírez M., González F. Circulating inflammatory markers in polycystic ovary syndrome: A systematic review and meta-analysis. Fertil. Steril. 2011;95:1048–1058. doi: 10.1016/j.fertnstert.2010.11.036.
    1. Lee H., Oh J.Y., Sung Y.A. Adipokines, insulin-like growth factor binding protein-3 levels, and insulin sensitivity in women with polycystic ovary syndrome. Korean J. Intern. Med. 2013;28:456–463. doi: 10.3904/kjim.2013.28.4.456.
    1. Khashchenko E.P., Sukhanova Y.A., Pyataeva S.V., Volodina M.A., Tarasova N.V., Tsvirkun D.V., Uvarova E.V., Vysokikh M.Y. Indicators of mitochondrial functioning in adolescent girls with polycystic ovary syndrome with regard to the presence of metabolic disorders and overweight. Akusherstvo i Ginekologiya (Russian Federation) 2017;7:104–113. doi: 10.18565/aig.2017.7.104-13.
    1. Möhlig M., Spranger J., Osterhoff M., Ristow M., Pfeiffer A.F., Schill T., Schlösser H.W., Brabant G., Schöfl C. The polycystic ovary syndrome per se is not associated with increased chronic inflammation. Eur. J. Endocrinol. 2004;150:525–532. doi: 10.1530/eje.0.1500525.
    1. Toscani M.K., Mario F.M., Radavelli-Bagatini S., Wiltgen D., Cristina Matos M., Spritzer P.M. Effect of high-protein or normal-protein diet on weight loss, body composition, hormone, and metabolic profile in southern Brazilian women with polycystic ovary syndrome: A randomized study. Gynecol. Endocrinol. 2011;27:925–930. doi: 10.3109/09513590.2011.564686.
    1. Garcia-Arellano A., Ramallal R., Ruiz-Canela M., Salas-Salvadó J., Corella D., Shivappa N., Schröder H., Hébert J.R., Ros E., Gómez-Garcia E., et al. Dietary inflammatory index and incidence of cardiovascular disease in the PREDIMED study. Nutrients. 2015;7:4124–4138. doi: 10.3390/nu7064124.
    1. Hruby A., Jacques P.F. Dietary Protein and Changes in Biomarkers of Inflammation and Oxidative Stress in the Framingham Heart Study Offspring Cohort. Curr. Dev. Nutr. 2019;3:nzz019. doi: 10.1093/cdn/nzz019.
    1. Vallianou N.G., Bountziouka V.P., Georgousopoulou E., Evangelopoulos A.A., Bonou M.S., Vogiatzakis E.D., Barbetseas J.D., Avgerinos P.C., Panagiotakos D.B. Influence of protein intake from haem and non-haem animals and plant origin on inflammatory biomarkers among apparently-healthy adults in Greece. J. Health Popul. Nutr. 2013;31:446–454. doi: 10.3329/jhpn.v31i4.19992.
    1. Schwedhelm C., Pischon T., Rohrmann S., Himmerich H., Linseisen J., Nimptsch K. Plasma inflammation markers of the tumor necrosis factor pathway but not C-reactive protein are associated with processed meat and unprocessed red meat consumption in Bavarian adults. J. Nutr. 2017;147:78–85. doi: 10.3945/jn.116.237180.
    1. Kim Y., Keogh J.B., Clifton P.M. Effects of two different dietary patterns on inflammatory markers, advanced glycation end products and lipids in subjects without type 2 diabetes: A randomised crossover study. Nutrients. 2017;9:336. doi: 10.3390/nu9040336.
    1. Montonen J., Boeing H., Fritsche A., Schleicher E., Joost H.-G., Schulze M.B., Steffen A., Pischon T. Consumption of red meat and whole-grain bread in relation to biomarkers of obesity, inflammation, glucose metabolism and oxidative stress. Eur. J. Nutr. 2013;52:337–345. doi: 10.1007/s00394-012-0340-6.
    1. Khayyatzadeh S.S., Kazemi-Bajestani S.M.R., Bagherniya M., Mehramiz M., Tayefi M., Ebrahimi M., Ferns G.A., Safarian M., Ghayour-Mobarhan M. Serum high C reactive protein concentrations are related to the intake of dietary macronutrients and fiber: Findings from a large representative Persian population sample. Clin. Biochem. 2017;50:750–755. doi: 10.1016/j.clinbiochem.2017.03.016.
    1. Björck I., Elmståhl H.L. The glycaemic index: Importance of dietary fibre and other food properties. Proc. Nutr. Soc. 2003;62:201–206. doi: 10.1079/PNS2002239.
    1. Buyken A.E., Goletzke J., Joslowski G., Felbick A., Cheng G., Herder C., Brand-Miller J.D. Association between carbohydrate quality and inflammatory markers: Systematic review of observational and interventional studies. Am. J. Clin. Nutr. 2014;99:813–833. doi: 10.3945/ajcn.113.074252.
    1. Szczuko M., Zapalowska-Chwyć M., Drozd R.A. Low Glycemic Index Decreases Inflammation by Increasing the Concentration of Uric Acid and the Activity of Glutathione Peroxidase (GPx3) in Patients with Polycystic Ovary Syndrome (PCOS) Molecules. 2019;24:1508. doi: 10.3390/molecules24081508.
    1. Barrea L., Marzullo P., Muscogiuri G., Di Somma C., Scacchi M., Orio F., Gianluca A., Aimaretti G., Colao A., Savastano S. Source and amount of carbohydrate in the diet and inflammation in women with polycystic ovary syndrome. Nutr. Res. Rev. 2018;31:291–301. doi: 10.1017/S0954422418000136.
    1. Kellner-Weibel G., Luke S.J., Rothblat G.H. Cytotoxic cellular cholesterol is selectively removed by apoA-I via ABCA1. Atherosclerosis. 2003;171:235–243. doi: 10.1016/j.atherosclerosis.2003.08.024.
    1. Surls J., Nazarov-Stoica C., Kehl M., Olsen C., Casares S., Brumeanu T.-D. Increased membrane cholesterol in lymphocytes diverts T-cells toward an inflammatory response. PLoS ONE. 2012;7:e38733. doi: 10.1371/journal.pone.0038733.
    1. Barbosa K.B.F., Pinheiro Volp A.C., Marques-Rocha J.L., Rocha Ribeiro S.M., Navarro-Blasco I., Zulet M.A., Martinez A., Bressan J. Low energy and carbohydrate intake associated with higher total antioxidant capacity in apparently healthy adults. Nutrition. 2014;30:1349–1354. doi: 10.1016/j.nut.2014.03.031.
    1. Aponte A., Agarwal A. Oxidative Stress Impact on the Fertility of Women with Polycystic Ovary Syndrome. In: Agarwal A., Aziz N., Rizk B., editors. Studies on Women’s Health. Humana Press; Totowa, NJ, USA: 2013. Oxidative Stress in Applied Basic Research and Clinical Practice.
    1. Drosdzol-Cop A., Sidło-Stawowy A., Sajdak D., Skrzypulec-Plinta V. Diagnosing polycystic ovary syndrome in adolescent girls. Ginekol. Pol. 2014;85:145–148. doi: 10.17772/gp/1705.

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