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New insights on diabetes in Turner syndrome: results from an observational study in adulthood

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Abstract

Objective

To explore the characteristics of diabetes mellitus in adults with Turner syndrome.

Design

Observational study consisting of a prospective phase after the access of adults with Turner syndrome to the Endocrinology Unit (median period of follow-up 15.6, interquartile range: 12.0–24.5 months) and a retrospective collection of data from the diagnosis of Turner syndrome until the time of access to the Endocrinology Unit. A total of 113 Italian Turner syndrome patients were included in the study. During the prospective phase of the study, each patient underwent physical examination, fasting blood sampling, and an oral glucose tolerance test on a yearly basis. Oral glucose tolerance test was used to perform the diagnosis of diabetes mellitus.

Results

Before access to the Endocrinology Unit, diabetes mellitus was diagnosed in two Turner syndrome patients. Another five cases of diabetes mellitus were diagnosed at the first access to the Endocrinology Unit, whereas seven new cases of diabetes mellitus were diagnosed during the prospective phase of the study. At the diagnosis of diabetes mellitus, only one patient had fasting glucose above 126 mg/dL, and only two had an HbA1c value >6.5% (48 mmol/mol). When compared to normo-glucose tolerant patients, the diabetic patients had a significantly lower insulin-to-glucose ratio at 30 and 60 min of the oral glucose tolerance test. In the regression analyses, only age was associated with the development of diabetes mellitus.

Conclusions

This study confirms that diabetes mellitus is frequent in Turner syndrome and suggests that it is specific to the syndrome. In addition, this study demonstrates that oral glucose tolerance test is a more sensitive test than HbA1c for the diagnosis of diabetes mellitus in Turner syndrome.

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References

  1. M. Elsheikh, D.B. Dunger, G.S. Conway et al., Turner’s syndrome in adulthood. Endocr. Rev. 23, 120–140 (2002)

    CAS  PubMed  Google Scholar 

  2. B.E. Hjerrild, K. Mortensen, C.H. Gravholt, Turner syndrome and clinical treatment. Br. Med. Bull. 86, 77–93 (2008)

    Article  Google Scholar 

  3. Bondy CA for the Turner Syndrome Consensus Study Group, Care of girls and women with Turner syndrome: a guideline of the turner syndrome study group. J. Clin. Endocrinol. Metab. 92, 10–25 (2007)

    Article  Google Scholar 

  4. K. Stochholm, S. Juul, K. Juel et al., Prevalence, incidence, diagnostic delay, and mortality in Turner syndrome. J. Clin. Endocrinol. Metab. 91, 3897–3902 (2006)

    Article  CAS  Google Scholar 

  5. M.J. Schoemaker, A.J. Swerdlow, C.D. Higgins et al., Mortality in women with Turner syndrome in Great Britain: a national cohort study. J. Clin. Endocrinol. Metab. 93, 4735–4742 (2008)

    Article  CAS  Google Scholar 

  6. M.J. Schoemaker, A.J. Swerdlow, C.D. Higgins et al.; UK Clinical Cytogenetics Group., Cancer incidence in women with Turner syndrome in Great Britain: a national cohort study. Lancet Oncol. 9, 239–246 (2008)

    Article  Google Scholar 

  7. M.H. Viuff, C. Trolle, J. Wen et al., Coronary artery anomalies in Turner syndrome. J. Cardiovasc. Comput. Tomogr. 10, 480–484 (2016)

    Article  Google Scholar 

  8. A. Gawlik, E. Malecka-Tendera, Treatment of Turner’s syndrome during transition. Eur. J. Endocrinol. 170, R57–R74 (2014)

    Article  CAS  Google Scholar 

  9. A. Hokken-Koelega, A.-J. van der Lely, B. Hauffa et al. Bridging the gap: metabolic and endocrine care of patients during transition. Endocr. Connect. 5, R44–R54 (2016)

    Article  Google Scholar 

  10. C.H. Gravholt, R.W. Naeraa, B. Nyholm et al., Glucose metabolism, lipid metabolism, and cardiovascular risk factors in adult Turner’s syndrome. The impact of sex hormone replacement. Diabetes Care 21, 1062–1070 (1998)

    Article  CAS  Google Scholar 

  11. V.K. Bakalov, M.M. Cooley, M.J. Quon et al., Impaired insulin secretion in the Turner metabolic syndrome. J. Clin. Endocrinol. Metab. 89, 3516–3520 (2004)

    Article  CAS  Google Scholar 

  12. V.K. Bakalov, C. Cheng, J. Zhou et al., X-chromosome gene dosage and the risk of diabetes in Turner syndrome. J. Clin. Endocrinol. Metab. 94, 3289–3296 (2009)

    Article  CAS  Google Scholar 

  13. S. Caprio, S. Boulware, M. Diamond et al., Insulin resistance: an early metabolic defect of Turner’s syndrome. J. Clin. Endocrinol. Metab. 72, 832–836 (1991)

    Article  CAS  Google Scholar 

  14. World Health Organization, Preventing and managing the global epidemic: report of a WHO Consultation on Obesity. World Health Org, Geneva. [WHO/NUT/NCD/98.1] (1997)

  15. American Diabetes Association, Classification and diagnosis of diabetes. Diabetes Care 39, S13–S22 (2016)

    Article  Google Scholar 

  16. Italian Institute of Statistics-ISTAT www.istat.it. Table 4.16: 148 (2015)

  17. B.E. Hjerrild, J.J. Holst, C.B. Juhl et al., Delayed beat-cell response and glucose intolerance in young women with Turner syndrome. BMC Endocr. Disord. 11, 6 (2011)

    Article  CAS  Google Scholar 

  18. F. Baronio, L. Mazzanti, Y. Girtler et al., The influence of GH treatment on glucose homeostasis in girls with Turner syndrome: a 7 years study. J. Clin. Endocrinol. Metab. 102, jc20163179 (2016). [Epub ahead of print]

    Article  Google Scholar 

  19. N. Wooten, V.K. Bakalov, S. Hill et al., Reduced abdominal adiposity and improved glucose tolerance in growth hormone-treated girls with Turner syndrome. J. Clin. Endocrinol. Metab. 93, 2109–2114 (2008)

    Article  CAS  Google Scholar 

  20. C. Le May, K. Chu, M. Hu et al., Estrogens protect pancreatic beta-cells from apoptosis and prevent insulin-deficient diabetes mellitus in mice. Proc. Natl Acad. Sci. USA 103, 9232–9237 (2006)

    Article  Google Scholar 

  21. R.P. Barros, U.F. Machado, M. Warner et al., Muscle GLUT4 regulation by estrogen receptors ERbeta and ERalpha. Proc. Natl Acad. Sci. USA. 103, 1605–1608 (2006)

    Article  CAS  Google Scholar 

  22. I.F. Godsland, Oestrogens and insulin secretion. Diabetologia 48, 2213–2220 (2005)

    Article  CAS  Google Scholar 

  23. T. Muthusamy, P. Murugesan, K. Balasubramanian, Sex steroids deficiency impairs glucose transporter 4 expression and its translocation through defective Akt phosphorylation in target tissues of adult male rat. Metabolism 58, 1581–1592 (2009)

    Article  CAS  Google Scholar 

  24. A.M. Kanaya, D. Herrington, E. Vittinghoff et al.; Heart and estrogen/progestin replacement Study, Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/Progestin Replacement Study. Ann. Intern. Med. 138, 1–9 (2003)

    Article  CAS  Google Scholar 

  25. K.L. Margolis, D.E. Bonds, R.J. Rodabough et al.; Women’s Health Initiative Investigators, Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the women’s health initiative hormone trial. Diabetologia 47, 1175–1187 (2004)

    Article  CAS  Google Scholar 

  26. L. Lucaccioni, S.C. Wong, A. Smyth et al., Turner syndrome-issues to consider for transition to adulthood. Br. Med. Bull. 113, 45–58 (2015)

    Article  CAS  Google Scholar 

  27. S.T. Alves, C.T. Gallichio, M.M. Guimarães, Insulin resistance and body composition in Turner syndrome: effect of sequential change in the route of estrogen administration. Gynecol. Endocrinol. 22, 590–594 (2006)

    Article  CAS  Google Scholar 

  28. C.H. Gravholt, B.E. Hjerrild, R.W. Naeraa et al., Effect of growth hormone and 17beta-oestradiol treatment on metabolism and body composition in girls with Turner syndrome. Clin. Endocrinol. 62, 616–622 (2005)

    Article  CAS  Google Scholar 

  29. N. Mauras, D. Shulman, H.Y. Hsiang et al., Metabolic effects of oral versus transdermal estrogen in growth hormone-treated girls with Turner syndrome. J. Clin. Endocrinol. Metab. 92, 4154–4160 (2007)

    Article  CAS  Google Scholar 

  30. B. Salgin, R. Amin, K. Yuen et al., Insulin resistance is an intrinsic defect independent of fat mass in women with Turner’s syndrome. Horm. Res. 65, 69–75 (2006)

    CAS  PubMed  Google Scholar 

  31. S.N. Rajpathak, S.K. Vellarikkal, A. Patowary et al., Human 45,X fibroblast transcriptome reveals distinct differentially expressed genes including long noncoding RNAs potentially associated with the pathophysiology of Turner syndrome. PLoS One 9, e100076 (2014)

    Article  Google Scholar 

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Acknowledgements

Dr. A. Gambineri is the guarantor of this work, had full access to all the data, and takes full responsibility for the integrity of data and accuracy of data analysis. We thank Susan West for assistance with the language revision of the manuscript.

Author contributions

D.I.-G. contributed to data acquisition, revision and interpretation, drafted and critically revised the article, and wrote and approved the final version of the manuscript. P.A., E.S., A.P., U.P., L.M., and R.P. contributed to data acquisition, critically revised the article for intellectual content and approved the final version of the manuscript. A.M.M.L. performed statistical analysis of data, drafted and critically revised the article, and approved the final version of the manuscript. A.G. contributed to data revision and interpretation, drafted and critically revised the article, and wrote and approved the final version of the manuscript.

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Authors and Affiliations

  1. Division of Endocrinology, Department of Medical & Surgical Sciences, University Alma Mater Studiorum, S. Orsola-Malpighi Hospital, Bologna, Italy

    Daniela Ibarra-Gasparini, Paola Altieri, Antonio M. Morselli-Labate, Uberto Pagotto, Renato Pasquali & Alessandra Gambineri

  2. Pediatric Endocrinology and Rare Disease Unit, Department of Medical & Surgical Sciences, University Alma Mater Studiorum, S. Orsola-Malpighi Hospital, Bologna, Italy

    Emanuela Scarano, Annamaria Perri & Laura Mazzanti

Authors
  1. Daniela Ibarra-Gasparini
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  2. Paola Altieri
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  9. Alessandra Gambineri
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Correspondence to Alessandra Gambineri.

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The authors declare that they have no competing interests.

Ethical approval

All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Ibarra-Gasparini, D., Altieri, P., Scarano, E. et al. New insights on diabetes in Turner syndrome: results from an observational study in adulthood. Endocrine 59, 651–660 (2018). https://doi.org/10.1007/s12020-017-1336-z

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  • DOI: https://doi.org/10.1007/s12020-017-1336-z

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