Divergences in insulin resistance between the different phenotypes of the polycystic ovary syndrome

Journal of Clinical Endocrinology and Metabolism

Volumn 98, Issue 4, 2013, Pages

  Moghetti, Paolo ^a   Tosi, Flavia ^a   Bonin, Cecilia ^b   Di Sarra, Daniela ^a   Fiers, Tom ^c   Kaufman, Jean Marc ^c   Giagulli, Vito Angelo ^d   Signori, Chiara ^b   Zambotti, Francesca ^a   Dall'Alda, Marlene ^a   Spiazzi, Giovanna ^a   Zanolin, Maria Elisabetta ^e   Bonora, Enzo ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY HOSPITAL OF VERONA   (Italy)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d ASL Bari   (Italy)

^e UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; TRIACYLGLYCEROL;

ADULT; ARTICLE; CAUCASIAN; CHRONIC OLIGOANOVULATION; CLASSIC PHENOTYPE; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; FEMALE; GLUCOSE CLAMP TECHNIQUE; HORMONE ACTION; HUMAN; HYPERANDROGENISM; INSULIN RESISTANCE; INSULIN SENSITIVITY; MAJOR CLINICAL STUDY; METABOLIC SYNDROME X; METABOLISM; NORMOANDROGENIC PHENOTYPE; OVARY INSUFFICIENCY; OVARY POLYCYSTIC DISEASE; OVULATORY PHENOTYPE; PHENOTYPIC VARIATION; PREDICTION; PRIORITY JOURNAL;

ADULT; ANOVULATION; BLOOD GLUCOSE; FEMALE; HUMANS; HYPERANDROGENISM; INDIVIDUALITY; INSULIN; INSULIN RESISTANCE; METABOLIC SYNDROME X; PHENOTYPE; POLYCYSTIC OVARY SYNDROME; TESTOSTERONE; YOUNG ADULT;

EID: 84876254180     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2012-3908     Document Type: Article

References (71)

1. Azziz R, Carmina E, Dewailly D, et al. The Androgen Excess and PCOS Society criteria for the polycystic ovary syndrome: the complete task force report. Fertil Steril. 2009;91:456-488.
2. Randeva HS, Tan BK, Weickert MO, et al. Cardiometabolic aspects of the polycystic ovary syndrome. Endocr Rev. 2012;33:812-841.
3. 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. Fertil Steril. 2004;81:19-25.
4. Zawadzki JK, Dunaif A. Diagnostic criteria for polycystic ovary syndrome: towards a rational approach. In: Dunaif A, Givens JR, Haseltine FP, Merriam GR, eds. Polycystic Ovary Syndrome. Cambridge, MA: Blackwell Scientific Publications; 1992:377-384.
5. March WA, Moore VM, Willson KJ, Phillips DI, Norman RJ, Davies MJ. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod. 2010;25:544-551.
6. Yildiz BO, Bozdag G, Yapici Z, Esinler I, Yarali H. Prevalence, phenotype and cardiometabolic risk of polycystic ovary syndrome under different diagnostic criteria. Hum Reprod. 2012;27:3067-3073.
7. Moran L, Teede H. Metabolic features of the reproductive phenotypes of polycystic ovary syndrome. Hum Reprod Update. 2009; 15:477-488.
8. Moran C, Arriaga M, Rodriguez G, Moran S. Obesity differentially affects phenotypes of polycystic ovary syndrome. Int J Endocrinol. 2012;2012:317241.
9. Reaven GM. The insulin resistance syndrome: definition and dietary approaches to treatment. Annu Rev Nutr. 2005;25:391-406.
10. Diamanti-Kandarakis E, Dunaif A. Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications. Endocr Rev. 2012;33:981-1030.
11. Carmina E, Lobo RA. Use of fasting blood to assess the prevalence of insulin resistance in women with polycystic ovary syndrome. Fertil Steril. 2004;82:661-665.
12. DeUgarte CM, Bartolucci AA, Azziz R. Prevalence of insulin resistance in the polycystic ovary syndrome using the homeostasis model assessment. Fertil Steril. 2005;83:1454-1460.
13. Ferrannini E, Mari A. How to measure insulin sensitivity. J Hypertens. 1998;16:895-906.
14. Muniyappa R, Lee S, Chen H, Quon MJ. Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am J Physiol Endocrinol Metab. 2008;294:E15-E26.
15. Quon MJ. Limitations of the fasting glucose to insulin ratio as an index of insulin sensitivity. J Clin Endocrinol Metab. 2001;86: 4615-4617.
16. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004;27:1487-1495.
17. Hücking K, Watanabe RM, Stefanovski D, Bergman RN. OGTT-derived measures of insulin sensitivity are confounded by factors other than insulin sensitivity itself. Obesity (Silver Spring). 2008; 16:1938-1945.
18. Buchanan TA, Watanabe RM, Xiang AH. Limitations in surrogate measures of insulin resistance. J Clin Endocrinol Metab. 2010;95: 4874-4876.
19. Bhasin S, Zhanga A, Coviello A, et al. The impact of assay quality and reference ranges on clinical decision making in the diagnosis of and rogen disorders. Steroids. 2008;73:1311-1317.
20. Rosner W, Vesper H, The Endocrine Society and the Endorsing Organizations. Toward excellence in testosterone testing: a consensus statement. J Clin Endocrinol Metab. 2010;95:4542-4548.
21. Escobar-Morreale HF, Carmina E, Dewailly D, et al. Epidemiology, diagnosis and management of hirsutism: a consensus statement by the Androgen Excess and Polycystic Ovary Syndrome Society. Hum Reprod Update. 2012;18:146-170.
22. Moghetti P, Tosi F, Castello R, et al. The insulin resistance in women with hyperandrogenism is partially reversed by antiandrogen treatment: evidence that and rogens impairs insulin action in women. J Clin Endocrinol Metab. 1996;81:952-960.
23. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol. 1979;237:E214-E223.
24. DeFronzo RA. The triumvirate: β-cell, muscle, liver: a collusion responsible for NIDDM. Diabetes. 1988;37:667-687.
25. Gray DS, Bray GA, Gemayel N, Kaplan K. Effect of obesity on bioelectrical impedance. Am J Clin Nutr. 1989;50:255-260.
26. Alberti KG, Eckel RH, Grundy SM, et al. 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;120:1640-1645.
27. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III): final report. Circulation. 2002;106: 3143-3421.
28. Vermeulen A, Stoica T, Verdonck L. The apparent free testosterone concentration, an index of and rogenicity. J Clin Endocrinol. 1971; 33:759-767.
29. Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999;84:3666-3672.
30. World Health Organization. Definition, Diagnosis and Classification of Diabetes Mellitus and Its Complications. Report of a Who Consultation. Part 1: Diagnosis and Classification of Diabetes Mellitus. Geneva, Switzerland: World Health Organization; 1999.
31. Balkau B, Charles MA, Drivsholm T, et al. Frequency of the WHO metabolic syndrome in European cohorts, and an alternative definition of an insulin resistance syndrome. Diabetes Metab. 2002;28: 364-376.
32. Ferrannini E, Vichi S, Beck-Nielsen H, Laakso M, Paolisso G, Smith U. Insulin action and age. European Group for the Study of Insulin Resistance (EGIR). Diabetes. 1996;45:947-953.
33. Reaven GM. Insulin resistance: the link between obesity and cardiovascular disease. Med Clin North Am. 2011;95:875-892.
34. Diamanti-Kandarakis E, Katsikis I, Piperi C, et al. Increased serum advanced glycation end-products is a distinct finding in lean women with polycystic ovary syndrome (PCOS). Clin Endocrinol (Oxf). 2008;69:634-641.
35. Broekmans FJ, Knauff EAH, Valkenburg O, Laven JS, Eijkemans MJ, Fauser BCJM. PCOS according to the Rotterdam consensus criteria: change in prevalence among WHO-II anovulation and association with metabolic factors. BJOG. 2006;113:1210-1217.
36. Park HR, Choi Y, LeeH-J, OH J-Y, Hong YS, Sung Y-A. Phenotypic characteristics according to insulin sensitivity in non-obese Korean women with polycystic ovary syndrome. Diabetes Res Clin Pract. 2007;77:S233-S237.
37. Goverde AJ, van Koert AJB, Eijkemans MJ, et al. Indicators for metabolic disturbances in anovulatory womenwith polycystic ovary syndrome diagnosed according to the Rotterdam consensus criteria. Hum Reprod. 2009;24:710-717.
38. Svendsen PF, Madsbad S, Nilas L. The insulin-resistant phenotype of polycystic ovary syndrome. Fertil Steril. 2010;94:1052-1058.
39. Norman RJ, Hague WM, Masters SC, Wang XJ. Subjects with polycystic ovaries without hyperandrogenaemia exhibit similar disturbances in insulin and lipid profiles as those with polycystic ovary syndrome. Hum Reprod. 1995;10:2258-2261.
40. Legro RS, Chiu P, Kunselman AR, et al. Polycystic ovaries are common in women with hyperandrogenic chronic anovulation but do not predict metabolic or reproductive phenotype. J Clin Endocrinol Metab. 2005;90:2571-2579.
41. Dewailly D, Catteau-Jonard S, Reyss A-C, Leroy M, Pigny P. Oligoanovulation with polycystic ovaries but not overt hyperandrogenism. J Clin Endocrinol Metab. 2006;91:3922-3927.
42. Hahn S, Bering van Halteren W, Roesler S, et al. The combination of increased ovarian volume and follicle number is associated with more severe hyperandrogenism in German women with polycystic ovary syndrome. Exp Clin Endocrinol Diabetes. 2006;114:175-181.
43. Guastella E, Longo RA, Carmina E. Clinical and endocrine characteristics of the main polycystic ovary syndrome phenotypes. Fertil Steril. 2010;94:2197-2201.
44. Johnstone EB, Rosen MP, Neril R, et al. The polycystic ovary postRotterdam: a common, age-dependent finding in ovulatory women without metabolic significance. J Clin Endocrinol Metab. 2010;95: 4965-4972.
45. Adams JM, Taylor AE, Crowley WF, Hall JE. Polycystic ovarian morphology with regular ovulatory cycles: insights into the pathophysiology of polycystic ovarian syndrome. J Clin Endocrinol Metab. 2004;89:4343-4350.
46. Michelmore K, Ong K, Mason S, et al. Clinical features in women with polycystic ovaries: relationships to insulin sensitivity, insulin gene VNTR and birth weight. Clin Endocrinol (Oxf). 2001;55:439-446.
47. Mehrabian F, Khani B, Kelishadi R, Kermani N. The prevalence of metabolic syndrome and insulin resistance according to the phenotypic subgroups of polycystic ovary syndrome in a representative sample of Iranian females. J Res Med Sci. 2011;16:763-769.
48. Carmina E, Chu MC, Longo RA, Rini GB, Lobo RA. Phenotypic variation in hyperandrogenic women influences the findings of abnormal metabolic and cardiovascular risk parameters. J Clin Endocrinol Metab. 2005;90:2545-2549.
49. Welt CK, Gudmundsson JA, Arason G, et al. Characterizing discrete subsets of polycystic ovary syndrome as defined by the Rotterdam criteria: the impact of weight on phenotype and metabolic features. J Clin Endocrinol Metab. 2006;91:4842-4848.
50. Barber TM, Wass JAH, McCarthy MI, Franks S. Metabolic characteristics of women with polycystic ovaries and oligo-amenorrhoea but normal and rogen levels: implications for the management of polycystic ovary syndrome. Clin Endocrinol. 2007;66:513-517.
51. Rizzo M, Berneis K, Hersberger M, et al. Milder forms of atherogenic dyslipidemia in ovulatory versus anovulatory polycystic ovary syndrome phenotype. Hum Reprod. 2009;24:2286-2292.
52. Yilmaz M, Isaoglu U, Delibas IB, Kadanali S. Anthropometric, clinical and laboratory comparison of four phenotypes of polycystic ovary syndrome based on Rotterdam criteria. J Obstet Gynaecol Res. 2011;37:1020-1026.
53. Melo AS, Vieira CS, Maltoni Romano LG, Ferriani RA, Navarro PA. The frequency of metabolic syndrome is higher among PCOS Brazilian women with menstrual irregularity plus hyperandrogenism. Reprod Sci. 2011;18:1230-1236.
54. Amato MC, Verghi M, Galluzzo A, Giordano C. The oligomenorrheic phenotypes of polycystic ovary syndrome are characterized by a high visceral adiposity index: alikely condition ofcardiometabolic risk. Hum Reprod. 2011;26:1486-1494.
55. Shroff R, Syrop CH, Davis W, Van Voorhis BJ, Dokras A. Risk of metabolic complications in the new PCOS phenotypes based on the Rotterdam criteria. Fertil Steril. 2007;88:1389-1395.
56. Chae SJ, Kim JJ, Choi YM, et al. Clinical and biochemical characteristics of polycystic ovary syndrome in Korean women. Hum Reprod. 2008;23:1924-1931.
57. Kauffman RP, Baker TE, Baker VM, DiMarino P, Castracane VD. Endocrine and metabolic differences among phenotypic expressions of polycystic ovary syndrome according to the 2003 Rotterdam consensus criteria. Am J Obstet Gynecol. 2008;198:670.e1-670.e10.
58. Wang Y, Qu JW, Wu XK, Hou LH, Erkkola R, Wang Y. Different phenotypes of polycystic ovary syndrome by Rotterdam criteria are differently steroidogenic but similarly insulin resistant. Fertil Steril. 2010;93:1362-1365.
59. Moran LJ, Cameron JD, Strauss BJ, Teede HJ. Vascular function in the diagnostic categories of polycystic ovary syndrome. Hum Reprod. 2011;26:2192-2199.
60. Dilbaz B, Ozkaya E, Cinar M, Cakir E, Dilbaz S. Cardiovascular disease risk characteristics of the main polycystic ovary syndrome phenotypes. Endocrinology 2011;39:272-277.
61. Panidis D, Tziomalos K, Misichronis G, et al. Insulin resistance and endocrine characteristics of the different phenotypes of polycystic ovary syndrome: a prospective study. Hum Reprod. 2012;27:541-549.
62. Gluszak O, Stopinska-Gluszak U, Glinicki P, et al. Phenotype and metabolic disorders in polycystic ovary syndrome. ISRN Endocrinol. 2012;2012:569862.
63. 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.
64. Diamanti-Kandarakis E, Panidis D. Unravelling the phenotypic map of polycystic ovary syndrome (PCOS): a prospective study of 634 women with PCOS. Clin Endocrinol. 2007;67:735-742.
65. Diamanti-Kandarakis E, Kouli C, Alexandraki K, Spina G. Failure of mathematical indices to accurately assess insulin resistance in lean, overweight, or obese women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2004;89:1273-1276.
66. Jackson JA, Hawa MI, Roshania RD, Sim BM, DiSilvio L, Jaspan JB. Influence of aging on hepatic and peripheral glucose metabolism in humans. Diabetes. 1988;36:119-129.
67. Elting MW, Korsen TJ, Rekers-Mombarg LT, Schoemaker J. Women with polycystic ovary syndrome gain regular menstrual cycles when aging. Hum Reprod. 2000;15:24-28.
68. Bili H, Laven J, Imani B, Eijkemans MJ, Fauser BC. Age-related differences in features associated with polycystic ovary syndrome in normogonadotrophic oligo-amenorrhoeic infertile women of reproductive years. Eur J Endocrinol. 2001;145:749-755.
69. Alsamarai S, Adams JM, Murphy MK, et al. Criteria for polycystic ovarian morphology in polycystic ovary syndrome as a function of age. J Clin Endocrinol Metab. 2009;94:4961-4970.
70. Brown ZA, Louwers YV, Fong SL, et al. Thephenotype of polycystic ovary syndrome ameliorates with aging. Fertil Steril. 2011;96: 1259-1265.
71. Panidis D, Tziomalos K, Macut D, et al. Cross-sectional analysis of the effects of age on the hormonal, metabolic, and ultrasonographic features and the prevalence of the different phenotypes of polycystic ovary syndrome. Fertil Steril. 2012;97:494-500.