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Blood Circulating Levels of Adipokines in Polycystic Ovary Syndrome Patients: A Systematic Review and Meta-analysis

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Abstract

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; I2 = 90.6%), chemerin (SMD 1.87; 95% CI, 1.35 to 2.40; P < 0.001; I2 = 94.4%), and resistin (SMD 0.66; 95% CI, 0.41 to 0.91; P < 0.001; I2 = 92.6%) were significantly higher in the PCOS group compared to controls. However, there was no significant difference between the PCOS and control groups in relation to apelin levels (SMD − 0.17; 95% CI, − 1.06 to 0.73; P = 0.714; I2 = 97.8%). We found that serum levels of vaspin, chemerin, and resistin were significantly higher in PCOS subjects compared with controls. It seems that these adipokines can be measured as a useful marker to predict the development of PCOS.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. 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.

    Article  CAS  PubMed  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    CAS  PubMed  Google Scholar 

  4. 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.

    Article  CAS  PubMed  Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. 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.

    Article  CAS  Google Scholar 

  7. As A. The association between omentin and diabetes: a systematic review and meta-analysis of observational studies. Diabetes Metab Syndr Obes. 2019;12:1277.

    Article  Google Scholar 

  8. Pellegrinelli V, Carobbio S, Vidal-Puig A. Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues. Diabetologia. 2016;59(6):1075–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 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.

    Google Scholar 

  10. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim WK, Bae K-H, Lee SC, Oh K-J. The Latest Insights into Adipokines in Diabetes. J Clin Med. 2019;8(11):1874.

    Article  CAS  PubMed Central  Google Scholar 

  13. 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.

    Article  CAS  PubMed Central  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. 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.

    Article  CAS  PubMed  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  CAS  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  CAS  PubMed  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Article  CAS  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. 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.

    Article  CAS  PubMed  Google Scholar 

  27. 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.

    Article  CAS  Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

    Article  CAS  PubMed  Google Scholar 

  31. 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.

    Article  PubMed  CAS  Google Scholar 

  32. 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.

    Article  CAS  Google Scholar 

  33. 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.

    Article  CAS  PubMed  Google Scholar 

  34. 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.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. 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.

    Article  CAS  Google Scholar 

  37. 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).

    Article  PubMed  Google Scholar 

  38. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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.

  40. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Green S, Higgins J. Cochrane handbook for systematic reviews of interventions. Version. 2005;5(0).

  42. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.

    Article  CAS  PubMed  Google Scholar 

  43. 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.

    Article  CAS  Google Scholar 

  44. 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.

    Article  CAS  PubMed  Google Scholar 

  45. 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.

    Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  CAS  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. 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.

    Article  Google Scholar 

  52. 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.

    Article  CAS  Google Scholar 

  53. 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.

    Article  CAS  PubMed  Google Scholar 

  54. 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.

    Article  CAS  PubMed  Google Scholar 

  55. 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  Google Scholar 

  56. 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.

  57. 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.

    Article  PubMed  Google Scholar 

  58. 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.

    Article  CAS  PubMed  Google Scholar 

  59. 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.

    Article  PubMed  CAS  Google Scholar 

  60. 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.

    Article  CAS  PubMed  Google Scholar 

  61. 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.

    Article  Google Scholar 

  62. 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.

    Article  PubMed Central  CAS  Google Scholar 

  63. 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.

    Article  CAS  Google Scholar 

  64. 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.

    Article  Google Scholar 

  65. 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.

    CAS  PubMed  Google Scholar 

  66. 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.

    Article  CAS  Google Scholar 

  67. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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.

    Article  CAS  Google Scholar 

  69. 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.

    CAS  Google Scholar 

  70. 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.

    Article  PubMed  Google Scholar 

  71. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  72. 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.

    Google Scholar 

  73. 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.

    CAS  PubMed  Google Scholar 

  74. 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.

    CAS  PubMed  Google Scholar 

  75. 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.

    Google Scholar 

  76. 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.

    Article  CAS  Google Scholar 

  77. 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.

    Google Scholar 

  78. 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.

    Article  CAS  PubMed  Google Scholar 

  79. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. 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.

    Article  CAS  PubMed  Google Scholar 

  81. 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.

    Article  CAS  PubMed  Google Scholar 

  82. 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.

    Article  Google Scholar 

  83. 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.

    Article  PubMed  Google Scholar 

  84. 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  Google Scholar 

  85. 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.

    Article  CAS  Google Scholar 

  86. 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.

    Article  PubMed  CAS  Google Scholar 

  87. 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.

    Article  CAS  Google Scholar 

  88. 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.

    Article  CAS  PubMed  Google Scholar 

  89. 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.

    Article  PubMed  Google Scholar 

  90. 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.

    Article  CAS  PubMed  Google Scholar 

  91. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. 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.

    Article  CAS  PubMed  Google Scholar 

  93. 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.

    Article  CAS  PubMed  Google Scholar 

  94. 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  PubMed Central  Google Scholar 

  95. 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.

  96. 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.

    Article  PubMed  CAS  Google Scholar 

  97. 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.

    Article  Google Scholar 

  98. Zia Karira KA, Rani M, Zuberi NA. Serum status of resistin and insulin in polycystic ovary syndrome. Med Channel. 2011;17:11–5.

    Google Scholar 

  99. 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.

    Article  CAS  PubMed  Google Scholar 

  100. 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.

    Article  CAS  Google Scholar 

  101. 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.

    Article  Google Scholar 

  102. 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.

    Article  CAS  PubMed  Google Scholar 

  103. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. 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.

    Google Scholar 

  105. 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.

    Article  CAS  PubMed  Google Scholar 

  106. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. 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.

    Article  CAS  PubMed  Google Scholar 

  108. Pepene CE. Evidence for visfatin as an independent predictor of endothelial dysfunction in polycystic ovary syndrome. Clin Endocrinol. 2012;76(1):119–25.

    Article  CAS  Google Scholar 

  109. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. 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.

    Article  CAS  PubMed  Google Scholar 

  111. 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.

    Article  Google Scholar 

  112. Steppan CM, Lazar MA. Resistin and obesity-associated insulin resistance. Trends Endocrinol Metab. 2002;13(1):18–23.

    Article  CAS  PubMed  Google Scholar 

  113. 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.

    Article  CAS  PubMed  Google Scholar 

  114. 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.

    Article  CAS  PubMed  Google Scholar 

  115. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  117. 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.

    Article  CAS  PubMed  Google Scholar 

  118. 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.

    Article  CAS  PubMed  Google Scholar 

  119. 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.

    Article  CAS  PubMed  Google Scholar 

  120. 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.

    Article  CAS  PubMed  Google Scholar 

  121. 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.

    Article  CAS  PubMed  Google Scholar 

  122. 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.

    Article  PubMed  Google Scholar 

  123. 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.

    Article  CAS  PubMed  Google Scholar 

  124. 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.

    Article  CAS  PubMed  Google Scholar 

  125. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  127. 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.

    Article  CAS  PubMed  Google Scholar 

  128. 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.

    Article  CAS  PubMed  Google Scholar 

  129. 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.

    Article  CAS  PubMed  Google Scholar 

  130. 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.

    Article  CAS  PubMed  Google Scholar 

  131. Xu S, Tsao PS, Yue P. Apelin and insulin resistance: another arrow for the quiver? J Diabetes. 2011;3(3):225–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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A.A, S.M, and M.M contributed to the conception of research. A.A, S.M, M.N, M.M, and E.K searched databases, screened articles, and extracted data. A.A and M.M performed statistical analysis; and all authors contributed to the writing and revision of the manuscript.

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Correspondence to Marjan Mansourian.

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Mehrabani, S., Arab, A., Karimi, E. et al. Blood Circulating Levels of Adipokines in Polycystic Ovary Syndrome Patients: A Systematic Review and Meta-analysis. Reprod. Sci. 28, 3032–3050 (2021). https://doi.org/10.1007/s43032-021-00709-w

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