Blood Circulating Levels of Adipokines in Polycystic Ovary Syndrome Patients: A Systematic Review and Meta-analysis.
Apelin
Chemerin
Meta-analysis
PCOS
Resistin
Vaspin
Journal
Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
06
11
2020
accepted:
30
07
2021
pubmed:
3
9
2021
medline:
5
3
2022
entrez:
2
9
2021
Statut:
ppublish
Résumé
A body of studies has examined the circulating concentration of adipokines including apelin, vapin, resistin, and chemerin in polycystic ovary syndrome (PCOS) patients. However, their findings have been inconclusive. Therefore, we systematically reviewed available studies to illuminate the overall circulating concentration of adipokines in PCOS subjects. Cochrane's Library, PubMed, Scopus, and ISI Web of Science databases were searched from the earliest available date up to April 2021 for relevant articles. The quality of each study was assessed by the Newcastle-Ottawa Quality Assessment Scale. The pooled effect size was estimated based on the random effects model, and the standard mean differences (SMD) with a 95% confidence interval (CI) were reported. A total of 88 studies met the inclusion criteria and were included in the current systematic review and meta-analysis. The results of the analysis showed that serum levels of vaspin (SMD 0.69; 95% CI, 0.22 to 1.17; P = 0.004; I
Identifiants
pubmed: 34472034
doi: 10.1007/s43032-021-00709-w
pii: 10.1007/s43032-021-00709-w
doi:
Substances chimiques
Adipokines
0
Biomarkers
0
Types de publication
Journal Article
Meta-Analysis
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
3032-3050Informations de copyright
© 2021. Society for Reproductive Investigation.
Références
Altinkaya SO, Nergiz S, Kucuk M, Yuksel H. Apelin levels in relation with hormonal and metabolic profile in patients with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2014;176:168–72.
pubmed: 24642195
doi: 10.1016/j.ejogrb.2014.02.022
Munir I, Yen HW, Baruth T, Tarkowski R, Azziz R, Magoffin DA, et al. Resistin stimulation of 17alpha-hydroxylase activity in ovarian theca cells in vitro: relevance to polycystic ovary syndrome. J Clin Endocrinol Metab. 2005;90(8):4852–7.
pubmed: 15886251
doi: 10.1210/jc.2004-2152
Arslanian SA, Lewy VD, Danadian K. Glucose intolerance in obese adolescents with polycystic ovary syndrome: roles of insulin resistance and beta-cell dysfunction and risk of cardiovascular disease. J Clin Endocrinol Metab. 2001;86(1):66–71.
pubmed: 11231980
Chang C-Y, Tsai Y-C, Lee C-H, Chan T-F, Wang S-H, Su J-H. Lower serum apelin levels in women with polycystic ovary syndrome. Fertil Steril. 2011;95(8):2520-3.e2.
pubmed: 21575945
doi: 10.1016/j.fertnstert.2011.04.044
Ashraf S, Nabi M, Rasool SuA, Rashid F, Amin S. Hyperandrogenism in polycystic ovarian syndrome and role of CYP gene variants: a review. Egypt J Med Hum Genet. 2019;20(1):25.
doi: 10.1186/s43042-019-0031-4
Sahin Y, Unluhizarci K, Yilmazsoy A, Yikilmaz A, Aygen E, Kelestimur F. The effects of metformin on metabolic and cardiovascular risk factors in nonobese women with polycystic ovary syndrome. Clin Endocrinol (Oxf). 2007;67(6):904–8.
doi: 10.1111/j.1365-2265.2007.02985.x
As A. The association between omentin and diabetes: a systematic review and meta-analysis of observational studies. Diabetes Metab Syndr Obes. 2019;12:1277.
doi: 10.2147/DMSO.S206981
Pellegrinelli V, Carobbio S, Vidal-Puig A. Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues. Diabetologia. 2016;59(6):1075–88.
pubmed: 27039901
pmcid: 4861754
doi: 10.1007/s00125-016-3933-4
Saedii AAF, Kamal AM, AbdelNaeem EA, Matta RA. Apelin-36 and Copeptin Levels in Polycystic Ovary Syndrome. J Infect Dis Treat. 2017;3(1):1–5.
Uyar GO, Sanlier N. Association of adipokines and insulin, which have a role in obesity, with colorectal cancer. Eurasian J Med. 2019;51(2):191.
pubmed: 31258362
pmcid: 6592445
Francisco V, Pino J, Gonzalez-Gay MA, Mera A, Lago F, Gómez R, et al. Adipokines and inflammation: is it a question of weight? Br J Pharmacol. 2018;175(10):1569–79.
pubmed: 29486050
pmcid: 5913397
doi: 10.1111/bph.14181
Kim WK, Bae K-H, Lee SC, Oh K-J. The Latest Insights into Adipokines in Diabetes. J Clin Med. 2019;8(11):1874.
pmcid: 6912383
doi: 10.3390/jcm8111874
Bongrani A, Mellouk N, Rame C, Cornuau M, Guérif F, Froment P, et al. Ovarian expression of adipokines in polycystic ovary syndrome: a role for chemerin, omentin, and apelin in follicular growth arrest and ovulatory dysfunction? Int J Mol Sci. 2019;20(15):3778.
pmcid: 6695651
doi: 10.3390/ijms20153778
Toulis KA, Goulis DG, Farmakiotis D, Georgopoulos NA, Katsikis I, Tarlatzis BC, et al. Adiponectin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Hum Reprod Update. 2009;15(3):297–307.
pubmed: 19261627
doi: 10.1093/humupd/dmp006
Wang Q, Kim JY, Xue K, Liu JY, Leader A, Tsang BK. Chemerin, a novel regulator of follicular steroidogenesis and its potential involvement in polycystic ovarian syndrome. Endocrinology. 2012;153(11):5600–11.
pubmed: 22948218
doi: 10.1210/en.2012-1424
Lima PDA, Nivet AL, Wang Q, Chen YA, Leader A, Cheung A, et al. Polycystic ovary syndrome: possible involvement of androgen-induced, chemerin-mediated ovarian recruitment of monocytes/macrophages. Biol Reprod. 2018;99(4):838–52.
pubmed: 29688269
pmcid: 6203875
doi: 10.1093/biolre/ioy096
Kort DH, Kostolias A, Sullivan C, Lobo RA. Chemerin as a marker of body fat and insulin resistance in women with polycystic ovary syndrome. Gynecol Endocrinol. 2015;31(2):152–5.
pubmed: 25295622
doi: 10.3109/09513590.2014.968547
Li X, Zhu Q, Wang W, Qi J, He Y, Wang Y, et al. Elevated chemerin induces insulin resistance in human granulosa-lutein cells from polycystic ovary syndrome patients. FASEB J. 2019;33(10):11303–13.
pubmed: 31311314
doi: 10.1096/fj.201802829R
Hosoya M, Kawamata Y, Fukusumi S, Fujii R, Habata Y, Hinuma S, et al. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem. 2000;275(28):21061–7.
pubmed: 10777510
doi: 10.1074/jbc.M908417199
Roche J, Ramé C, Reverchon M, Mellouk N, Cornuau M, Guerif F, et al. Apelin (APLN) and apelin receptor (APLNR) in human ovary: expression, signaling, and regulation of steroidogenesis in primary human luteinized granulosa cells. Biol Reprod. 2016;95(5):104.
pubmed: 27683264
doi: 10.1095/biolreprod.116.141754
Bongrani A, Mellouk N, Ramé C, Cornuau M, Guerif F, Froment P, et al. Vaspin, a novel adipokine in woman granulosa cells physiology and PCOS pathogenesis? J Endocrinol. 2021;249(1):57–70.
pubmed: 33608490
doi: 10.1530/JOE-20-0550
Dogan K, Ekin M, Helvacioğlu Ç, Yaşar L. Can serum vaspin levels predict clomiphene resistance in infertile women with PCOS? Eur J Obstet Gynecol Reprod Biol. 2017;217:6–11.
pubmed: 28826039
doi: 10.1016/j.ejogrb.2017.08.006
Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, et al. The hormone resistin links obesity to diabetes. Nature. 2001;409(6818):307–12.
pubmed: 11201732
doi: 10.1038/35053000
Seow KM, Juan CC, Wu LY, Hsu YP, Yang WM, Tsai YL, et al. Serum and adipocyte resistin in polycystic ovary syndrome with insulin resistance. Hum Reprod (Oxford, England). 2004;19(1):48–53.
doi: 10.1093/humrep/deh010
Chu Y, Cui Q, Feng G, Song Z, Jiang X. The expression of resistin in adipose tissues of patients with polycystic ovary syndrome and insulin resistance. J Huazhong Univ Sci Technol Med Sci Hua zhong ke ji da xue xue bao Yi xue Ying De wen ban Huazhong keji daxue xuebao Yixue Yingdewen ban. 2009;29(5):642–5.
doi: 10.1007/s11596-009-0521-6
Tang YL, Yu J, Zeng ZG, Liu Y, Liu JY, Xu JX. Circulating omentin-1 levels in women with polycystic ovary syndrome: a meta-analysis. Gynecol Endocrinol. 2017;33(3):244–9.
pubmed: 27908216
doi: 10.1080/09513590.2016.1254180
Zheng SH, Du DF, Li XL. Leptin levels in women with polycystic ovary syndrome: a systematic review and a meta-analysis. Reprod Sci (Thousand Oaks, Calif). 2017;24(5):656–70.
doi: 10.1177/1933719116670265
Li S, Huang X, Zhong H, Peng Q, Chen S, Xie Y, et al. Low circulating adiponectin levels in women with polycystic ovary syndrome: an updated meta-analysis. Tumour Biol. 2014;35(5):3961–73.
pubmed: 24414393
doi: 10.1007/s13277-013-1595-0
Sun Y, Wu Z, Wei L, Liu C, Zhu S, Tang S. High-visfatin levels in women with polycystic ovary syndrome: evidence from a meta-analysis. Gynecol Endocrinol. 2015;31(10):808–14.
pubmed: 26422683
doi: 10.3109/09513590.2015.1056140
Cai X, Qiu S, Li L, Zügel M, Steinacker JM, Schumann U. Circulating irisin in patients with polycystic ovary syndrome: a meta-analysis. Reprod Biomed Online. 2018;36(2):172–80.
pubmed: 29217128
doi: 10.1016/j.rbmo.2017.10.114
Ustun Y, Engin-Ustun Y, Ozkaya M, Kilinc M. Serum vaspin and C-reactive protein levels in women with polycystic ovaries and polycystic ovary syndrome. Gynecol Endocrinol. 2011;27(7):491–5.
pubmed: 20626239
doi: 10.3109/09513590.2010.501874
Allam NE, Mohamed Maarouf T, Mostafa H. The effect of metformin therapy on serum leptin and resistin levels in women with polycystic ovary syndrome. Evid Based Womenʼs Health J. 2014;4(3):135–40.
doi: 10.1097/01.EBX.0000440888.46582.8f
Baldani DP, Skrgatic L, Kasum M, Zlopasa G, Kralik Oguic S, Herman M. Altered leptin, adiponectin, resistin and ghrelin secretion may represent an intrinsic polycystic ovary syndrome abnormality. Gynecol Endocrinol. 2019;35(5):401–5.
pubmed: 30623695
doi: 10.1080/09513590.2018.1534096
Akbarzadeh S, Ghasemi S, Kalantarhormozi M, Nabipour I, Abbasi F, Aminfar A, et al. Relationship among plasma adipokines, insulin and androgens level as well as biochemical glycemic and lipidemic markers with incidence of PCOS in women with normal BMI. Gynecol Endocrinol. 2012;28(7):521–4.
pubmed: 22309615
doi: 10.3109/09513590.2011.650747
Arikan S, Bahceci M, Tuzcu A, Kale E, Gökalp D. Serum resistin and adiponectin levels in young non-obese women with polycystic ovary syndrome. Gynecol Endocrinol. 2010;26(3):161–6.
pubmed: 20148738
doi: 10.3109/09513590903247816
Baranova A, Tran TP, Afendy A, Wang L, Shamsaddini A, Mehta R, et al. Molecular signature of adipose tissue in patients with both non-alcoholic fatty liver disease (NAFLD) and polycystic ovarian syndrome (PCOS). J Transl Med. 2013;11(1):1–8.
doi: 10.1186/1479-5876-11-133
Escobar-Morreale HF, Luque-Ramírez M, San-Millán JL. Serum visceral adipose tissue–derived serine protease inhibitor concentrations in human obesity and polycystic ovary syndrome. Diabetes Care. 2009;32(1):e6 (e).
pubmed: 19114623
doi: 10.2337/dc08-1690
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
pubmed: 19621072
pmcid: 2707599
doi: 10.1371/journal.pmed.1000097
Wells G, Shea B, O’connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa: Ottawa Hospital Research Institute. oxford. asp; 2011.
Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5(1):13.
pubmed: 15840177
pmcid: 1097734
doi: 10.1186/1471-2288-5-13
Green S, Higgins J. Cochrane handbook for systematic reviews of interventions. Version. 2005;5(0).
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.
pubmed: 3802833
doi: 10.1016/0197-2456(86)90046-2
Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed). 1997;315(7109):629–34.
doi: 10.1136/bmj.315.7109.629
Seow KM, Juan CC, Ho LT, Hsu YP, Lin YH, Huang LW, et al. Adipocyte resistin mRNA levels are down-regulated by laparoscopic ovarian electrocautery in both obese and lean women with polycystic ovary syndrome. Hum Reprod. 2007;22(4):1100–6.
pubmed: 17208941
doi: 10.1093/humrep/del489
Ahmed H, Ghamry N. Serum Resistin and Plasma Visfatin: Relation to Insulin Resistance and Hyperandrogenism in Women with Polycystic Ovary Syndrome. Bull Egypt Soc Physiol Sci. 2007;27(2):157–76.
Yilmaz M, Bukan N, Demirc H, Öztürk Ç, Kan E, Ayvaz G, et al. Serum resistin and adiponectin levels in women with polycystic ovary syndrome. Gynecol Endocrinol. 2009;25(4):246–52.
pubmed: 19408174
doi: 10.1080/09513590802653833
Wang Y, Xie X, Zhu W. Serum adiponectin and resistin levels in patients with polycystic ovarian syndrome and their clinical implications. J Huazhong Univ Sci Technol - Med Sci. 2010;30(5):638–42.
doi: 10.1007/s11596-010-0556-8
Olszanecka-Glinianowicz M, Kuglin D, Dbkowska-Huć A, Skałba P. Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2011;154(1):51–6.
pubmed: 20889251
doi: 10.1016/j.ejogrb.2010.08.022
Pangaribuan B, Yusuf I, Mansyur M, Wijaya A. Serum adiponectin and resistin in relation to insulin resistance and markers of hyperandrogenism in lean and obese women with polycystic ovary syndrome. Ther Adv Endocrinol Metab. 2011;2(6):235–45.
pubmed: 23148188
pmcid: 3474644
doi: 10.1177/2042018811423770
Svendsen PF, Christiansen M, Hedley PL, Nilas L, Pedersen SB, Madsbad S. Adipose expression of adipocytokines in women with polycystic ovary syndrome. Fertil Steril. 2012;98(1):235–41.
pubmed: 22607892
doi: 10.1016/j.fertnstert.2012.03.056
Wang YX, Zhu WJ. Evaluation of adiponectin, resistin, IL-6, TNF-α in obese and non-obese women with polycystic ovary syndrome. J Reprod Contracept. 2012;23(4):237–44.
doi: 10.1016/S1001-7844(12)60032-7
Cassar S, Teede HJ, Harrison CL, Joham AE, Moran LJ, Stepto NK. Biomarkers and insulin sensitivity in women with polycystic ovary syndrome: characteristics and predictive capacity. Clin Endocrinol. 2015;83(1):50–8.
doi: 10.1111/cen.12619
Gul OO, Cander S, Gul B, Açıkgoz E, Sarandol E, Ersoy C. Evaluation of insulin resistance and plasma levels for visfatin and resistin in obese and non-obese patients with polycystic ovary syndrome. Eur Cytokine Netw. 2015;26(4):73–8.
pubmed: 26967765
doi: 10.1684/ecn.2015.0370
Nambiar V, Vijesh VV, Lakshmanan P, Sukumaran S, Suganthi R. Association of adiponectin and resistin gene polymorphisms in South Indian women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2016;200:82–8.
pubmed: 26995146
doi: 10.1016/j.ejogrb.2016.02.031
Zwirska-Korczala K, Sodowski K, Konturek SJ, Kuka D, Kukla M, Brzozowski T, et al. Postprandial response of ghrelin and PYY and indices of low-grade chronic inflammation in lean young women with polycystic ovary syndrome. J Physiol Pharmacol. 2008;59(Suppl 2):161–78.
pubmed: 18812636
Waheed Huda J, Saifallah PH, Salman IN. Study of Some Cytokines and Hormones in a Sample of Iraqi women with Polycystic ovarian syndrome and Their Relation to Obesity. Al-Mustansiriyah J Pharma Sci (AJPS). 2013;13(2):58-64.
Franik G, Plinta R, Madej P, Owczarek A, Bozentowicz-Wikarek M, Chudek J, Skrzypulec-Plinta V, Olszanecka-Glinianowicz M. Circulating vaspin levels and nutritional status and insulin resistance in polycystic ovary syndrome. Ginekologia Polska. 2020;91(5):251–5.
pubmed: 32495930
doi: 10.5603/GP.2020.0056
Guzel EC, Celik C, Abali R, Kucukyalcin V, Celik E, Guzel M, et al. Omentin and chemerin and their association with obesity in women with polycystic ovary syndrome. Gynecol Endocrinol. 2014;30(6):419–22.
pubmed: 24524360
doi: 10.3109/09513590.2014.888412
Wang LQ, Zhong Y, Ding YL, Shi XB, Huang J, Zhu FF. Elevated serum chemerin in Chinese women with hyperandrogenic PCOS. Gynecol Endocrinol. 2014;30(10):746–50.
pubmed: 24927079
doi: 10.3109/09513590.2014.928687
Yang SY, Wang QY, Huang W, Song Y, Feng GM, Zhou L, et al. Are serum chemerin levels different between obese and non-obese polycystic ovary syndrome women? Gynecol Endocrinol. 2016;32(1):38–41.
pubmed: 26291816
doi: 10.3109/09513590.2015.1075501
Foda AA, Foda EA, El-Negeri MA, El-Said ZH. Serum chemerin levels in polycystic ovary syndrome after metformin therapy. Diabetes Metab Syndr Clin Res Rev. 2019;13(2):1309–15.
doi: 10.1016/j.dsx.2019.01.050
Martínez-García M, Moncayo S, Insenser M, Álvarez-Blasco F, Luque-Ramírez M, Escobar-Morreale HF. Metabolic cytokines at fasting and during macronutrient challenges: influence of obesity, female androgen excess and sex. Nutrients. 2019;11(11):2566.
pmcid: 6893420
doi: 10.3390/nu11112566
Reda AM, Soud AA, El Sawaf AH, Ezzat OI, Salman TM, Sawaf HA. Association of altered serum levels of Chemerin, Paraoxonase-1 (PON1), Asymmetric Dimethyl arginine (ADMA) and obesitin the development of Polycystic Ovarian Syndrome (PCOS) in Egyptian women. Indian J Pharm Biol Res. 2015;3(03):35–43.
doi: 10.30750/ijpbr.3.3.6
El-Omda FA, Emara IA, Abdel-Latef DM, Zayan RH. Level of chemerin and anti-Müllerian hormone in Egyptian obese women with polycystic ovarian syndrome. Egypt J Hosp Med. 2018;70(7):1097–110.
doi: 10.12816/0044533
Ademoglu E, Berberoglu Z, Carlioglu A, Dellal FD, Gorar S, Alphan Z, et al. Higher levels of circulating chemerin in both lean and obese patients with polycystic ovary syndrome. Minerva Ginecol. 2014;66(6):535–42.
pubmed: 25373013
Olszanecka-Glinianowicz M, Madej P, Owczarek A, Chudek J, Skałba P. Circulating anti-Müllerian hormone levels in relation to nutritional status and selected adipokines levels in polycystic ovary syndrome. Clin Endocrinol. 2015;83(1):98–104.
doi: 10.1111/cen.12687
Sun X, Wu X, Zhou Y, Yu X, Zhang W. Evaluation of apelin and insulin resistance in patients with PCOS and therapeutic effect of drospirenone-ethinylestradiol plus metformin. Med Sci Monit. 2015;21:2547–52.
pubmed: 26314870
pmcid: 4556163
doi: 10.12659/MSM.894926
Escobar-Morreale HF, Villuendas G, Botella-Carretero JI, Alvarez-Blasco F, Sanchón R, Luque-Ramírez M, et al. Adiponectin and resistin in PCOS: a clinical, biochemical and molecular genetic study. Hum Reprod (Oxford, England). 2006;21(9):2257–65.
doi: 10.1093/humrep/del146
Dikmen E, Tarkun I, Öztürk F, Arslan B, Cantürk Z. Plasma adiponectin and resistin levels in women with polycystic ovary syndrome: relation to body mass index and insulin resistance. Turk J Med Sci. 2011;41(1):45–52.
Dogan K, Helvacioglu C, Baghaki S, Ekin M. Comparison of body mass index and metabolic parameters with serum vaspin levels in women with polycystic ovary syndrome. Diabetes Metab Syndr. 2020;14(2):137–9.
pubmed: 32087564
doi: 10.1016/j.dsx.2020.01.008
Guvenc Y, Var A, Goker A, Kuscu NK. Assessment of serum chemerin, vaspin and omentin-1 levels in patients with polycystic ovary syndrome. J Int Med Res. 2016;44(4):796–805.
pubmed: 27225862
pmcid: 5536625
doi: 10.1177/0300060516645421
Çapoǧlu I, Erdem F, UyanIk A, Turhan H. Serum levels of resistin and hsCRP in women with PCOS. Cent Eur J Med. 2009;4(4):428–32.
Tarkun I, Dikmen E, Cetinarslan B, Canturk Z. Impact of treatment with metformin on adipokines in patients with polycystic ovary syndrome. Eur Cytokine Netw. 2010;21(4):272–7.
pubmed: 21126943
Erkan M, Albayrak M, Karatas A, Keskin F, Aydin Y, Ak HY, et al. Are insulin resistance and serum resistin levels increased in women with idiopathic hirsutism? Eur Rev Med Pharmacol Sci. 2014;18(13):1889–95.
pubmed: 25010619
Silfeler D, Gokce C, Kurt R, Yılmaz N, Ozturk O, Turhan E, et al. Does polycystic ovary syndrome itself have additional effect on apelin levels? Obstet Gynecol Int. 2014;2014:536896.
Caglayan EK, Engin-Ustun Y, Sari N, Gocmen AY, Seckin L, Kara M, et al. Is there association between vitamin D levels, apelin 36, and visfatin in PCOS? Gynecol Endocrinol. 2016;32(5):386–9.
doi: 10.3109/09513590.2015.1124260
Goren K, Sagsoz N, Noyan V, Yucel A, Caglayan O, Bostanci MS. Plasma apelin levels in patients with polycystic ovary syndrome. J Turk German Gynecol Assoc. 2012;13(1):27–31.
Cakal E, Ustun Y, Engin-Ustun Y, Ozkaya M, Kilinç M. Serum vaspin and C-reactive protein levels in women with polycystic ovaries and polycystic ovary syndrome. Gynecol Endocrinol. 2011;27(7):491–5.
pubmed: 20626239
doi: 10.3109/09513590.2010.501874
Lu XE, Huang HF, Li MG, Zhu YM, Qiang YL, Dong MY. Resistin levels of serum and follicular fluid in non-obese patients with polycystic ovary syndrome during IVF cycles. J Zhejiang Univ Sci B. 2005;6(9):897–902.
pubmed: 16130192
pmcid: 1389908
doi: 10.1631/jzus.2005.B0897
Huang R, Yue J, Sun Y, Zheng J, Tao T, Li S, et al. Increased serum chemerin concentrations in patients with polycystic ovary syndrome: relationship between insulin resistance and ovarian volume. Clin Chim Acta. 2015;450:366–9.
pubmed: 26387454
doi: 10.1016/j.cca.2015.09.015
Zhang J, Zhou L, Tang L, Xu L. The plasma level and gene expression of resistin in polycystic ovary syndrome. Gynecol Endocrinol. 2011;27(12):982–7.
pubmed: 21557697
doi: 10.3109/09513590.2011.569794
Ibrahim MKS, Mostafa MI, Abdella RM, Marzouk SA, El-attar S. Relation of serum apelin levels to ultrasound images and Doppler indices in diagnosed polycystic ovary syndrome in overweight and obese women. Middle East Fertil Soc J. 2018;23(4):377–83.
doi: 10.1016/j.mefs.2018.05.007
Foda AA, Foda EA, El-Negeri MA, El-Said ZH. Serum chemerin levels in polycystic ovary syndrome after metformin therapy. Diabetes Metab Syndr. 2019;13(2):1309–15.
pubmed: 31336483
doi: 10.1016/j.dsx.2019.01.050
Zwirska-Korczala K, Sodowski K, Konturek S, Kuka D, Kukla M, Brzozowski T, et al. Postprandial response of ghrelin and PYY and indices of low-grade chronic inflammation in lean young women with polycystic ovary syndrome. J Physiol Pharmacol. 2008;59(Suppl 2):161–78.
pubmed: 18812636
Olszanecka-Glinianowicz M, Madej P, Owczarek A, Chudek J, Skalba P. Circulating anti-Mullerian hormone levels in relation to nutritional status and selected adipokines levels in polycystic ovary syndrome. Clin Endocrinol (Oxf). 2015;83(1):98–104.
doi: 10.1111/cen.12687
Ożegowska K, Bartkowiak-Wieczorek J, Bogacz A, Seremak-Mrozikiewicz A, Duleba AJ, Pawelczyk L. Relationship between adipocytokines and angiotensin converting enzyme gene insertion/deletion polymorphism in lean women with and without polycystic ovary syndrome. Gynecol Endocrinol. 2020;36(6):496–500.
pubmed: 31814467
doi: 10.1080/09513590.2019.1695248
Olszanecka-Glinianowicz M, Madej P, Nylec M, Owczarek A, Szanecki W, Skalba P, et al. Circulating apelin level in relation to nutritional status in polycystic ovary syndrome and its association with metabolic and hormonal disturbances. Clin Endocrinol (Oxf). 2013;79(2):238–42.
doi: 10.1111/cen.12120
Seow KM, Juan CC, Wu LY, Hsu YP, Yang WM, Tsai YL, et al. Serum and adipocyte resistin in polycystic ovary syndrome with insulin resistance. Hum Reprod. 2004;19(1):48–53.
pubmed: 14688155
doi: 10.1093/humrep/deh010
Seow KM, Juan CC, Hsu YP, Ho LT, Wang YY, Hwang JL. Serum and follicular resistin levels in women with polycystic ovarian syndrome during IVF-stimulated cycles. Hum Reprod. 2005;20(1):117–21.
pubmed: 15513972
doi: 10.1093/humrep/deh589
Chen YC, Tsai EM, Chen HS, Liu YH, Lee CH, Chou FH, et al. Serum resistin level is a predictor of ovarian response in in vitro fertilisation cycle. Acta Obstet Gynecol Scand. 2007;86(8):963–7.
pubmed: 17653882
doi: 10.1080/00016340701434492
Koiou E, Dinas K, Tziomalos K, Toulis K, Kandaraki EA, Kalaitzakis E, et al. The phenotypes of polycystic ovary syndrome defined by the 1990 diagnostic criteria are associated with higher serum vaspin levels than the phenotypes introduced by the 2003 criteria. Obes Facts. 2011;4(2):145–50.
pubmed: 21577021
pmcid: 6450045
doi: 10.1159/000327935
Koiou E, Tziomalos K, Dinas K, Katsikis I, Kalaitzakis E, Delkos D, et al. The effect of weight loss and treatment with metformin on serum vaspin levels in women with polycystic ovary syndrome. Endocr J. 2011;58(4):237–46.
pubmed: 21325745
doi: 10.1507/endocrj.K10E-330
Spanos N, Tziomalos K, Macut D, Koiou E, Kandaraki EA, Delkos D, et al. Adipokines, insulin resistance and hyperandrogenemia in obese patients with polycystic ovary syndrome: cross-sectional correlations and the effects of weight loss. Obes Facts. 2012;5(4):495–504.
pubmed: 22854419
doi: 10.1159/000341579
Mahde A, Shaker M, Al-Mashhadani Z. Study of omentin1 and other adipokines and hormones in PCOS patients. Oman Med J. 2009;24(2):108–18.
pubmed: 22334855
pmcid: 3273948
Ibrahim NA, Mohammad WJ, Abdawahab ST. Levels of Apelin, Endoglin, and Transforming Growth Factor Beta 1 in Iraqi Women with Polycystic Ovary Syndrome. Cihan Univ.-Erbil Sci J. 2020;4(1):21–5.
Martínez-García M, Montes-Nieto R, Fernández-Durán E, Insenser M, Luque-Ramírez M, Escobar-Morreale HF. Evidence for masculinization of adipokine gene expression in visceral and subcutaneous adipose tissue of obese women with polycystic ovary syndrome (PCOS). J Clin Endocrinol Metab. 2013;98(2):E388–96.
pubmed: 23337724
doi: 10.1210/jc.2012-3414
Nawaz Y, Ghazanvi S, Rasheed N, Jahan S, Ullah MI. Association of Serum Resistin Level and Resistin (RETN) Gene (-420 C> G) Polymorphism in Pakistani Women with Polycystic Ovarian Syndrome. Turk J Endocrinol Metab. 2020;24(1):16–22.
doi: 10.25179/tjem.2019-66784
Zia Karira KA, Rani M, Zuberi NA. Serum status of resistin and insulin in polycystic ovary syndrome. Med Channel. 2011;17:11–5.
Carmina E, Orio F, Palomba S, Cascella T, Longo RA, Colao AM, et al. Evidence for altered adipocyte function in polycystic ovary syndrome. Eur J Endocrinol. 2005;152(3):389–94.
pubmed: 15757855
doi: 10.1530/eje.1.01868
Carmina E, Orio F, Palomba S, Longo RA, Cascella T, Colao A, et al. Endothelial dysfunction in PCOS: role of obesity and adipose hormones. Am J Med. 2006;119(4):356.e1-6.
doi: 10.1016/j.amjmed.2005.10.059
Ganie MA, Sahar T, Rashid A, Wani IA, Nisar S, Sathyapalan T, et al. Comparative evaluation of biomarkers of inflammation among Indian women with polycystic ovary syndrome (PCOS) consuming vegetarian vs. non-vegetarian diet. Front Endocrinol (Lausanne). 2019;10:699.
doi: 10.3389/fendo.2019.00699
Tan BK, Heutling D, Chen J, Farhatullah S, Adya R, Keay SD, et al. Metformin decreases the adipokine vaspin in overweight women with polycystic ovary syndrome concomitant with improvement in insulin sensitivity and a decrease in insulin resistance. Diabetes. 2008;57(6):1501–7.
pubmed: 18375437
doi: 10.2337/db08-0127
Tan BK, Chen J, Farhatullah S, Adya R, Kaur J, Heutling D, et al. Insulin and metformin regulate circulating and adipose tissue chemerin. Diabetes. 2009;58(9):1971–7.
pubmed: 19502420
pmcid: 2731540
doi: 10.2337/db08-1528
Koleva D, Orbetzova M, Nyagolova P, Mitkov M. Adipokines, metabolic and atherogenic parameters in insulin resistant and non-insulin resistant women with polycystic ovary syndrome. G Ital Ostetricia Ginecol. 2016;38:114–8.
Sarray S, Madan S, Saleh LR, Mahmoud N, Almawi WY. Validity of adiponectin-to-leptin and adiponectin-to-resistin ratios as predictors of polycystic ovary syndrome. Fertil Steril. 2015;104(2):460–6.
pubmed: 26051098
doi: 10.1016/j.fertnstert.2015.05.007
Daan NM, Koster MP, de Wilde MA, Dalmeijer GW, Evelein AM, Fauser BC, et al. Biomarker profiles in women with PCOS and PCOS offspring; a pilot study. PLoS One. 2016;11(11):e0165033.
pubmed: 27806063
pmcid: 5091782
doi: 10.1371/journal.pone.0165033
Abruzzese GA, Gamez J, Belli SH, Levalle OA, Mormandi E, Otero P, Graffigna MN, Cerrone GE, Motta AB. Increased chemerin serum levels in hyperandrogenic and normoandrogenic women from Argentina with polycystic ovary syndrome. Gynecol Endocrinol. 2020;36(12):1057–61.
pubmed: 32496833
doi: 10.1080/09513590.2020.1769061
Pepene CE. Evidence for visfatin as an independent predictor of endothelial dysfunction in polycystic ovary syndrome. Clin Endocrinol. 2012;76(1):119–25.
doi: 10.1111/j.1365-2265.2011.04171.x
Obirikorang C, Owiredu WKBA, Adu-Afram S, Acheampong E, Asamoah EA, Antwi-Boasiakoh EK, et al. Assessing the variability and predictability of adipokines (adiponectin, leptin, resistin and their ratios) in non-obese and obese women with anovulatory polycystic ovary syndrome. BMC Res Notes. 2019;12(1):513.
pubmed: 31416473
pmcid: 6696689
doi: 10.1186/s13104-019-4546-z
Choi YS, Yang HI, Cho S, Jung JA, Jeon YE, Kim HY, et al. Serum asymmetric dimethylarginine, apelin, and tumor necrosis factor-α levels in non-obese women with polycystic ovary syndrome. Steroids. 2012;77(13):1352–8.
pubmed: 22944040
doi: 10.1016/j.steroids.2012.08.005
Moustafa SR, Al-Hakeim HK. The impact of serum visfatin, and resistin levels on insulin resistance in patients with polycystic ovary syndrome. Zanco J Med Sci. 2020;24(1):80–8.
doi: 10.15218/zjms.2020.011
Steppan CM, Lazar MA. Resistin and obesity-associated insulin resistance. Trends Endocrinol Metab. 2002;13(1):18–23.
pubmed: 11750858
doi: 10.1016/S1043-2760(01)00522-7
Wang H, Chu WS, Hemphill C, Elbein SC. Human resistin gene: molecular scanning and evaluation of association with insulin sensitivity and type 2 diabetes in Caucasians. J Clin Endocrinol Metab. 2002;87(6):2520–4.
pubmed: 12050208
doi: 10.1210/jcem.87.6.8528
Levy JR, Davenport B, Clore JN, Stevens W. Lipid metabolism and resistin gene expression in insulin-resistant Fischer 344 rats. Am J Physiol-Endocrinol Metab. 2002;282(3):E626–33.
pubmed: 11832366
doi: 10.1152/ajpendo.00346.2001
Fontana A, Spadaro S, Copetti M, Spoto B, Salvemini L, Pizzini P, et al. Association between resistin levels and all-cause and cardiovascular mortality: a new study and a systematic review and meta-analysis. PloS one. 2015;10(3):e0120419.
pubmed: 25793385
pmcid: 4368155
doi: 10.1371/journal.pone.0120419
Zhang Y, Li Y, Yu L, Zhou L. Association between serum resistin concentration and hypertension: A systematic review and meta-analysis. Oncotarget. 2017;8(25):41529.
pubmed: 28525369
pmcid: 5522312
doi: 10.18632/oncotarget.17561
Lobo TF, Torloni MR, Gueuvoghlanian-Silva BY, Mattar R, Daher S. Resistin concentration and gestational diabetes: a systematic review of the literature. J Reprod Immunol. 2013;97(1):120–7.
pubmed: 23432878
doi: 10.1016/j.jri.2012.10.004
Behboudi-Gandevani S, Ramezani Tehrani F, Bidhendi Yarandi R, Noroozzadeh M, Hedayati M, Azizi F. The association between polycystic ovary syndrome, obesity, and the serum concentration of adipokines. J Endocrinol Invest. 2017;40(8):859–66.
pubmed: 28332170
doi: 10.1007/s40618-017-0650-x
Lewandowski KC, Szosland K, O’Callaghan C, Tan BK, Randeva HS, Lewinski A. Adiponectin and resistin serum levels in women with polycystic ovary syndrome during oral glucose tolerance test: a significant reciprocal correlation between adiponectin and resistin independent of insulin resistance indices. Mol Genet Metab. 2005;85(1):61–9.
pubmed: 15862282
doi: 10.1016/j.ymgme.2004.12.014
Cakal E, Ustun Y, Engin-Ustun Y, Ozkaya M, Kilinç M. Serum vaspin and C-reactive protein levels in women with polycystic ovaries and polycystic ovary syndrome. Gynecol Endocrinol. 2011;27(7):491–5.
pubmed: 20626239
doi: 10.3109/09513590.2010.501874
Feng R, Li Y, Wang C, Luo C, Liu L, Chuo F, et al. Higher vaspin levels in subjects with obesity and type 2 diabetes mellitus: a meta-analysis. Diabetes Res Clin Pract. 2014;106(1):88–94.
pubmed: 25151227
doi: 10.1016/j.diabres.2014.07.026
Franik G, Plinta R, Madej P, Owczarek A, Bozentowicz-Wikarek M, Chudek J, et al. Circulating vaspin levels and nutritional status and insulin resistance in polycystic ovary syndrome. Ginekol Pol. 2020;91(5):251–5.
pubmed: 32495930
doi: 10.5603/GP.2020.0056
Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, Parlee SD, et al. Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem. 2007;282(38):28175–88.
pubmed: 17635925
doi: 10.1074/jbc.M700793200
Wang Y, Huang R, Li X, Zhu Q, Liao Y, Tao T, et al. High concentration of chemerin caused by ovarian hyperandrogenism may lead to poor IVF outcome in polycystic ovary syndrome: a pilot study. Gynecol Endocrinol. 2019;35(12):1072–7.
pubmed: 31155988
doi: 10.1080/09513590.2019.1622087
Li Y, Shi B, Li S. Association between serum chemerin concentrations and clinical indices in obesity or metabolic syndrome: a meta-analysis. PloS one. 2014;9(12):e113915.
pubmed: 25469985
pmcid: 4254750
doi: 10.1371/journal.pone.0113915
Zhou Z, Chen H, Ju H, Sun M. Circulating chemerin levels and gestational diabetes mellitus: a systematic review and meta-analysis. Lipids Health Dis. 2018;17(1):169.
pubmed: 30041634
pmcid: 6058359
doi: 10.1186/s12944-018-0826-1
Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology. 2007;148(10):4687–94.
pubmed: 17640997
doi: 10.1210/en.2007-0175
Chakaroun R, Raschpichler M, Klöting N, Oberbach A, Flehmig G, Kern M, et al. Effects of weight loss and exercise on chemerin serum concentrations and adipose tissue expression in human obesity. Metabolism. 2012;61(5):706–14.
pubmed: 22136911
doi: 10.1016/j.metabol.2011.10.008
Karimi E, Moini A, Yaseri M, Shirzad N, Sepidarkish M, Hossein-Boroujerdi M, et al. Effects of synbiotic supplementation on metabolic parameters and apelin in women with polycystic ovary syndrome: a randomised double-blind placebo-controlled trial. Br J Nutr. 2018;119(4):398–406.
pubmed: 29498342
doi: 10.1017/S0007114517003920
Ma W-Y, Yu T-Y, Wei J-N, Hung C-S, Lin M-S, Liao Y-J, et al. Plasma apelin: a novel biomarker for predicting diabetes. Clin Chim Acta. 2014;435:18–23.
pubmed: 24721640
doi: 10.1016/j.cca.2014.03.030
Xu S, Tsao PS, Yue P. Apelin and insulin resistance: another arrow for the quiver? J Diabetes. 2011;3(3):225–31.
pubmed: 21631898
pmcid: 3156858
doi: 10.1111/j.1753-0407.2011.00132.x