Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of the Efficacy of Sex Hormone–Binding Globulin in Insulin Resistance Assessment Based on HOMA-IR in Patients with PCOS

  • Reproductive Endocrinology: Original Article
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

This study aimed to evaluate the efficacy of SHBG in predicting insulin resistance (IR) in newly diagnosed, untreated patients with polycystic ovary syndrome (PCOS). Hundred newly diagnosed, untreated patients with PCOS and 61 subjects without PCOS (41 healthy volunteers with normal BMI and 20 subjects with overweight/obese) were included in the study. Receiver-operating characteristic (ROC) analysis was used to assess the effectiveness of SHBG in predicting IR in overweight/obese and non-overweight PCOS patients and the optimal cut-off values of SHBG. The results showed negative correlations between log-SHBG and log-I0 (r = − 0.372, P < 0.001) and log-SHBG and log-Homeostatic Model Assessment of Insulin Resistance (HOMA-IR) (r = − 0.393, P < 0.001) after adjusting for blood pressure, serum lipid, age, and body mass index (BMI) in all of the PCOS patients. In patients with IR (defined as HOMA-IR ≥2.29), the area under the ROC curves (AUCs) of the SHBG for ROC analysis in the non-overweight group, overweight/obese group, and all PCOS patients were 0.774 (P = 0.0001), 0.922 (P = 0.0001), and 0.885 (P = 0.0001), respectively. The optimal cut-off value of SHBG was 37 nmol/L with a sensitivity of 97.62% and specificity of 80.85% in the overweight group. In patients with IR (HOMA-IR ≥2.5), the AUCs of SHBG for ROC analysis in the non-overweight group, overweight/obese group, and all PCOS patients were 0.741 (P = 0.0003), 0.928 (P = 0.0001), and 0.880 (P = 0.0001), respectively. The optimal cut-off value of SHBG was 30.2 nmol/L with a sensitivity of 97.44% and specificity of 82.69% in the overweight/obese group. In conclusion, this study observed a negative correlation between SHBG and HOMA-IR in PCOS patients after adjustment of confounding factors. SHBG was an independent influential factor of HOMA-IR and can be used as a positive predictive marker for IR in PCOS patients, especially in those who are overweight/obese.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of Data and Materials

The data used to support the findings of the current study are available from the corresponding author on request.

Abbreviations

AUC:

area under curve

BMI:

body mass index

CVs:

coefficients of variability

DBP:

diastolic blood pressure

E2 :

estrogen

FSH:

follicle-stimulating hormone

G0 :

glucose level at fasting status

G60 :

glucose level after 60 min

G120 :

glucose level after 120 min

HDL-C:

high-density lipoprotein cholesterol

HOMA-IR:

homeostasis model assessment for insulin resistance

I0 :

insulin level at fasting status

I60 :

insulin level after 60 min

I120 :

insulin level after 120 min

LDL-C:

low-density lipoprotein cholesterol

LH:

luteinizing hormone

OGTT:

oral glucose tolerance test

PCOS:

polycystic ovary syndrome

ROC:

receiver-operating characteristic

SBP:

systolic blood pressure

SHBG:

sex hormone–binding globulin

TC:

total cholesterol

TG:

triglycerides

TT:

total testosterone

References

  1. Escobar-Morreale HF. Polycystic ovary syndrome: definition, aetiology, diagnosis and treatment. Nat Rev Endocrinol. 2018;14(5):270–84.

    Article  Google Scholar 

  2. Skiba MA, Islam RM, Bell RJ, Davis SR. Understanding variation in prevalence estimates of polycystic ovary syndrome: a systematic review and meta-analysis. Hum Reprod Update. 2018;24(6):694–709.

    Article  Google Scholar 

  3. Chen C, Jing G, Li Z, Juan S, Bin C, Jie H. Insulin resistance and polycystic ovary syndrome in a Chinese population. Endocr Pract. 2017.

  4. Alebić MŠ, Bulum T, Stojanović N, Duvnjak L. Definition of insulin resistance using the homeostasis model assessment (HOMA-IR) in IVF patients diagnosed with polycystic ovary syndrome (PCOS) according to the Rotterdam criteria. Endocrine. 2014;47(2):625–30.

    Article  Google Scholar 

  5. Lim SS, Norman RJ, Davies MJ, Moran LJ. The effect of obesity on polycystic ovary syndrome: a systematic review and meta-analysis. Obes Rev. 2013;14(2):95–109.

    Article  CAS  Google Scholar 

  6. Plymate SR, Matej LA, Jones RE, Friedl KE. Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. J Clin Endocrinol Metab. 1988;67(3):460–4.

    Article  CAS  Google Scholar 

  7. Zhu JL, Chen Z, Feng WJ, Long SL, Mo ZC. Sex hormone-binding globulin and polycystic ovary syndrome. Clin Chim Acta. 2019.

  8. Jayagopal V, Kilpatrick ES, Jennings PE, Hepburn DA, Atkin SL. The biological variation of testosterone and sex hormone-binding globulin (SHBG) in polycystic ovarian syndrome: implications for SHBG as a surrogate marker of insulin resistance. J Clin Endocrinol Metab. 2003;88(4):1528–33.

    Article  CAS  Google Scholar 

  9. Dahan MH, Goldstein J. Serum sex hormone-binding globulin levels show too much variability to be used effectively as a screening marker for insulin resistance in women with polycystic ovary syndrome. Fertil Steril. 2006;86(4):934–41.

    Article  CAS  Google Scholar 

  10. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004;19(1):41-7.

  11. Zhou BF. Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults--study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Biomed Environ Sci. 2002;15(1):83–96.

    PubMed  Google Scholar 

  12. Radikova Z, Koska J, Huckova M, Ksinantova L, Imrich R, Vigas M, et al. Insulin sensitivity indices: a proposal of cut-off points for simple identification of insulin-resistant subjects. Exp Clin Endocrinol Diabetes. 2006;114(5):249–56.

    Article  CAS  Google Scholar 

  13. Münzker J, Hofer D, Trummer C, Ulbing M, Harger A, Pieber T, et al. Testosterone to dihydrotestosterone ratio as a new biomarker for an adverse metabolic phenotype in the polycystic ovary syndrome. J Clin Endocrinol Metab. 2015;100(2):653–60.

    Article  Google Scholar 

  14. Daka B, Rosen T, Jansson PA, Råstam L, Larsson CA, Lindblad U. Inverse association between serum insulin and sex hormone-binding globulin in a population survey in Sweden. Endocr Connect. 2013;2(1):18–22.

    Article  CAS  Google Scholar 

  15. Hamilton-Fairley D, White D, Griffiths M, et al. Diurnal variation of sex hormone binding globulin and insulin-like growth factor binding protein-1 in women with polycystic ovary syndrome. Clin Endocrinol. 1995;43(2):159–65.

    Article  CAS  Google Scholar 

  16. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Phys. 1979;237(3):E214–23.

    CAS  Google Scholar 

  17. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.

    Article  CAS  Google Scholar 

  18. Singh B, Saxena A. Surrogate markers of insulin resistance: a review. World J Diabetes. 2010;1(2):36–47.

    Article  Google Scholar 

  19. Patlolla S, Vaikkakara S, Sachan A, Venkatanarasu A, Bachimanchi B, Bitla A, et al. Heterogenous origins of hyperandrogenism in the polycystic ovary syndrome in relation to body mass index and insulin resistance. Gynecol Endocrinol. 2018;34(3):238–42.

    Article  CAS  Google Scholar 

  20. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70.

    Article  CAS  Google Scholar 

  21. Fulghesu AM, Angioni S, Portoghese E, Milano F, Batetta B, Paoletti AM, et al. Failure of the homeostatic model assessment calculation score for detecting metabolic deterioration in young patients with polycystic ovary syndrome. Fertil Steril. 2006;86(2):398–404.

    Article  Google Scholar 

  22. Kajaia N, Binder H, Dittrich R, Oppelt PG, Flor B, Cupisti S, et al. Low sex hormone-binding globulin as a predictive marker for insulin resistance in women with hyperandrogenic syndrome. Eur J Endocrinol. 2007;157(4):499–507.

    Article  CAS  Google Scholar 

  23. Li C, Ford ES, Li B, Giles WH, Liu S. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care. 2010;33(7):1618–24.

    Article  CAS  Google Scholar 

  24. Akin F, Bastemir M, Alkiş E, Kaptanoglu B. SHBG levels correlate with insulin resistance in postmenopausal women. Eur J Intern Med. 2009;20(2):162–7.

    Article  CAS  Google Scholar 

  25. Ottarsdottir K, Hellgren M, Bock D, Nilsson AG, Daka B. Longitudinal associations between sex hormone-binding globulin and insulin resistance. Endocr Connect. 2020;9(5):418–25.

    Article  CAS  Google Scholar 

  26. Cibula D, Fanta M, Vrbikova J, Stanicka S, Dvorakova K, Hill M, et al. The effect of combination therapy with metformin and combined oral contraceptives (COC) versus COC alone on insulin sensitivity, hyperandrogenaemia, SHBG and lipids in PCOS patients. Hum Reprod. 2005;20(1):180–4.

    Article  CAS  Google Scholar 

  27. Sepilian V, Nagamani M. Effects of rosiglitazone in obese women with polycystic ovary syndrome and severe insulin resistance. J Clin Endocrinol Metab. 2005;90(1):60–5.

    Article  CAS  Google Scholar 

  28. Penna IA, Canella PR, Reis RM, de Sá MFS, Ferriani RA. Acarbose in obese patients with polycystic ovarian syndrome: a double-blind, randomized, placebo-controlled study. Hum Reprod. 2005;20(9):2396–401.

    Article  CAS  Google Scholar 

  29. Li S, Chu Q, Ma J, Sun Y, Tao T, Huang R, et al. Discovery of Novel Lipid Profiles in PCOS: Do Insulin and Androgen Oppositely Regulate Bioactive Lipid Production. J Clin Endocrinol Metab. 2017;102(3):810–21.

    PubMed  Google Scholar 

Download references

Acknowledgements

The author would like to thank Editage for technical language editing of the manuscript.

Funding

This study was supported by grants from the National Natural Science Foundation of China (grant number: 81200619) and the Medical Scientific Research Foundation of Guangdong Province, China (grant number: A2020390).

Author information

Author notes

  1. Fu Chen and Yingyang Liao contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Nutrition, The First Affiliated Hospital of Shantou University Medical College, Shantou, 515041, Guangdong Province, China

    Fu Chen

  2. Department of Nutrition, The Affiliated Tumor Hospital of Guangxi Medical University, Nanning, 530021, Guangxi Province, China

    Yingyang Liao

  3. Department of Endocrinology, The First Affiliated Hospital of Shantou University Medical College, Shantou, 515041, Guangdong Province, China

    Minjie Chen, Huihuang Yin, Guishan Chen, Qingxia Huang, Lan Chen, Xiaoping Yang, Weichun Zhang & Guoshu Yin

  4. Laboratory of Molecular Cardiology and Laboratory of Molecular Imaging, The First Affiliated Hospital of Shantou University Medical College, Shantou, 515041, Guangdong Province, China

    Minjie Chen, Huihuang Yin & Weichun Zhang

  5. Department of Endocrinology, The First Affiliated Hospital of Hainan Medical University, Haikou, 570102, Hainan Province, China

    Ping Wang

Authors
  1. Fu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yingyang Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Minjie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huihuang Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guishan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qingxia Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaoping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Weichun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Guoshu Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guoshu Yin.

Ethics declarations

Ethics Approval and Consent to Participate

The study was approved by the Ethics Committee of the First Affiliated Hospital Shantou University Medical College according to the Council for International Organizations of Medical Sciences. Written informed consent was obtained from all participants.

Conflict of Interest

The authors declare that there is no conflict of interest regarding the publication of this article.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, F., Liao, Y., Chen, M. et al. Evaluation of the Efficacy of Sex Hormone–Binding Globulin in Insulin Resistance Assessment Based on HOMA-IR in Patients with PCOS. Reprod. Sci. 28, 2504–2513 (2021). https://doi.org/10.1007/s43032-021-00535-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43032-021-00535-0

Keywords

Search

Navigation