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Licensed Unlicensed Requires Authentication Published by De Gruyter December 22, 2015

Sex-related differences in the association of ghrelin levels with obesity in adolescents

  • Leandro Soriano-Guillén , Lorena Ortega , Pilar Navarro , Pía Riestra , Teresa Gavela-Pérez and Carmen Garcés EMAIL logo

Abstract

Background: The utility of ghrelin as a biomarker may be different depending on gender. The aim of this study was to assess ghrelin levels in a population-based sample of adolescents, and to evaluate their association with obesity and obesity-related parameters depending on sex.

Methods: The studied population included 601 randomly selected 14-to 16-year-old children. Anthropometrical data were measured and body mass index (BMI) and waist to hip ratio calculated. Body composition was assessed using an impedance body composition analyzer. Total serum ghrelin levels were determined using a multiplexed bead immunoassay. Serum leptin and adiponectin levels were determined by ELISA and insulin by RIA.

Results: Ghrelin levels were significantly higher in girls than in boys. Serum ghrelin concentrations were significantly lower (p<0.01) in obese than in normal weight (NW) girls, but showed no differences by weight category in boys. Ghrelin showed a significant negative relationship with waist circumference (WC), waist to hip ratio and fat mass (p<0.05) in both genders, and with weight and BMI (p<0.01) in girls, and insulin (p<0.01) and HOMA (p<0.05) in boys. Ghrelin also correlated negatively with leptin levels in girls (p<0.01).

Conclusions: Our study describes serum ghrelin levels in adolescents, showing a sexual dimorphism in ghrelin levels in these 14-to 16-year-old children, and a different association of ghrelin levels with obesity by gender that suggests a different appetite and energy expenditure control depending on sex at this age.


Dedicated to the late Prof. Manuel de Oya, as the warmest homage to his memory.



Corresponding author: Carmen Garcés, Lipid Research Laboratory, IIS-Fundación Jiménez Díaz, UAM. Avda. Reyes Católicos 2, 28040 Madrid, Spain, Phone/Fax: +34-91-5432880, E-mail:

Acknowledgments

This article is dedicated to the late Prof. Manuel de Oya. Prof de Oya designed the Four Province Study and the ideas reflected in our work can be traced back to him. We thank Asha Jois for her revision of the original manuscript.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This study was supported by grants from the Fondo de Investigación Sanitaria (PI 11/00344, PI 14/00344) and Biobank grant FEDER RD09/0076/00101. The contract of Carmen Garcés is co-financed by the Fondo de Investigación Sanitaria.

  3. Employment or leadership: Lorena Ortega and Pilar Navarro are fellows of the Conchita Rábago Foundation.

  4. Honorarium: None declared.

  5. Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

References

1. Kojima M, Hosoda H, Date Y, Nakzato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999;402:656–60.10.1038/45230Search in Google Scholar

2. Klok MD, Jakobsdottir S, Drent ML. The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev 2007;8:21–34.10.1111/j.1467-789X.2006.00270.xSearch in Google Scholar

3. Sun Y, Asnicar M, Smith RG. Central and peripheral roles of ghrelin on glucose homeostasis. Neuroendocrinology 2007;86:215–28.10.1159/000109094Search in Google Scholar

4. Wang Y, Nishi M, Doi A, Shono T, Furukawa Y, Shimada T, et al. Ghrelin inhibits insulin secretion through the AMPK-UCP2 pathway in beta cells. FEBS Lett 2010;584:1503–8.10.1016/j.febslet.2010.02.069Search in Google Scholar

5. Tschöp M, Weyer C, Tataranni PA, Devanarayan V, Ravussin E, Heiman ML. Circulating ghrelin levels are decreased in human obesity. Diabetes 2001;50:707–9.10.2337/diabetes.50.4.707Search in Google Scholar

6. Shiiya T, Nakazato M, Mizuta M, Date Y, Mondal MS, Tanaka M, et al. Plasma ghrelin levels in lean and obese humans and the effect of glucose on ghrelin secretion. J Clin Endocrinol Metab 2002;87:240–4.10.1210/jcem.87.1.8129Search in Google Scholar

7. Purnell JQ, Weigle DS, Breen P, Cummings DE. Ghrelin levels correlate with insulin levels, insulin resistance, and high-density lipoprotein cholesterol, but not with gender, menopausal status, or cortisol levels in humans. J Clin Endocrinol Metab 2003;88:5747–52.10.1210/jc.2003-030513Search in Google Scholar

8. Bennett NR, Boyne MS, Cooper RS, Royal-Thomas TY, Bennett FI, Luke A, et al. Impact of adiponectin and ghrelin on incident glucose intolerance and on weight change. Clin Endocrinol (Oxf) 2009;70:408–14.10.1111/j.1365-2265.2008.03344.xSearch in Google Scholar

9. Fagerberg B, Hulten LM, Hulthe J. Plasma ghrelin, body fat, insulin resistance, and smoking in clinically healthy men: the atherosclerosis and insulin resistance study. Metabolism 2003;52:1460–3.10.1016/S0026-0495(03)00274-9Search in Google Scholar

10. Pöykkö SM, Kellokoski E, Hörkkö S, Kauma H, Kesäniemi YA, Ukkola O. Low plasma ghrelin is associated with insulin resistance, hypertension, and the prevalence of type 2 diabetes. Diabetes 2003;52:2546–53.10.2337/diabetes.52.10.2546Search in Google Scholar PubMed

11. Katsuki A, Urakawa H, Gabazza EC, Murashima S, Nakatni K, Togashi K, et al. Circulating levels of active ghrelin is associated with abdominal adiposity, hyperinsulinemia and insulin resistance in patients with type 2 diabetes mellitus. Eur J Endocrinol 2004;151:573–7.10.1530/eje.0.1510573Search in Google Scholar PubMed

12. Amini P, Wadden D, Cahill F, Randell E, Vasdev S, Chen X, et al. Serum acylated ghrelin is negatively correlated with the insulin resistance in the CODING study. Plos One 2012;7:e45657.10.1371/journal.pone.0045657Search in Google Scholar PubMed PubMed Central

13. Reinehr T, de Sousa G, Roth CL. Obestatin and ghrelin levels in obese children and adolescents before and after reduction of overweight. Clin Endocrinol (Oxf) 2008;68:304–10.10.1111/j.1365-2265.2007.03042.xSearch in Google Scholar PubMed

14. Zhang N, Yuan C, Li Z, Li J, Li X, Li C, et al. Meta-analysis of the relationship between obestatin and ghrelin levels and the ghrelin/obestatin ratio with respect to obesity. Am J Med Sci 2011;341:48–55.10.1097/MAJ.0b013e3181ec41edSearch in Google Scholar PubMed

15. Whatmore AJ, Hall CM, Jones J, Westwood M, Clayton PE. Ghrelin concentrations in healthy children and adolescents. Clin Endocrinol (Oxf) 2003;59;649–54.10.1046/j.1365-2265.2003.01903.xSearch in Google Scholar PubMed

16. Bunt JC, Salbe AD, Tschöp MH, Del Parigi A, Daychild P, Tatarnni PA. Cross-sectional and prospective relationships of fasting plasma ghrelin concentrations with anthropometric measures in Pima Indian children. J Clin Endocrinol Metab 2003;88:3756–61.10.1210/jc.2003-030227Search in Google Scholar PubMed

17. Soriano-Guillén L, Barrios V, Chowen JA, Sánchez I, Vila S, Quero J, et al. Ghrelin levels from fetal life through early adulthood: relationship with endocrine and metabolic and anthropometric measures. J Pediatr 2004;144:30–5.10.1016/j.jpeds.2003.08.050Search in Google Scholar PubMed

18. Baldelli R, Bellone S, Castellino N, Petri A, Rapa A, Vivenza D, et al. Oral glucose load inhibits circulating ghrelin levels to the same extent in normal and obese children. Clin Endocrinol (Oxf) 2006;64:255–9.10.1111/j.1365-2265.2006.02441.xSearch in Google Scholar PubMed

19. Zou CC, Liang L, Zhao ZY. Factors associated with fasting plasma ghrelin levels in children and adolescents. World J Gastroenterol 2008;14:790–4.10.3748/wjg.14.790Search in Google Scholar PubMed PubMed Central

20. Carrascosa A, Fernandez JM, Fernandez C, Fernandez A, López-Siguero JP, Sánchez E, et al. [Spanish cross-sectional growth study 2008. Part II. Height, weight and body mass index values from birth to adulthood]. An Pediatr (Barc) 2008;68:552–69.Search in Google Scholar

21. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide international survey. Br Med J 2000;320:1240–3.10.1136/bmj.320.7244.1240Search in Google Scholar PubMed PubMed Central

22. Vilarrasa N, Vendrell J, Maravall J, Broch M, Estepa A, Megia A, et al. Distribution and determinants of adiponectin, resistin and ghrelin in a randomly selected healthy population. Clin Endocrinol (Oxf) 2005;63:329–35.10.1111/j.1365-2265.2005.02346.xSearch in Google Scholar PubMed

23. Greenman Y, Golani N, Gilad S, Yaron M, Limor R, Stern N. Ghrelin secretion is modulated in a nutrient- and gender-specific manner. Clin Endocrinol (Oxf) 2004;60:382–8.10.1111/j.1365-2265.2004.01993.xSearch in Google Scholar PubMed

24. Makovey J, Naganathan V, Seibel M, Sambrook P. Gender differences in plasma ghrelin and its relations to body composition and bone-an opposite-sex twin study. Clin Endocrinol (Oxf) 2007;66:530–7.10.1111/j.1365-2265.2007.02768.xSearch in Google Scholar PubMed

25. Ingelsson E, Larson MG, Yin X, Wang TJ, Meigs JB, Lipinska I, et al. Circulating ghrelin, leptin, and soluble leptin receptor concentrations and cardiometabolic risk factors in a community-based sample. J Clin Endocrinol Metab 2008;93:3149–57.10.1210/jc.2008-0207Search in Google Scholar PubMed PubMed Central

26. Kelishadi R, Hashemipour M, Mohammadifard N, Alikhassy H, Adeli K. Short- and long-term relationships of serum ghrelin with changes in body composition and the metabolic syndrome in prepubescent obese children following two different weight loss programmes. Clin Endocrinol (Oxf) 2008;69:721–9.10.1111/j.1365-2265.2008.03220.xSearch in Google Scholar PubMed

27. Pacifico L, Poggiogalle E, Costantino F, Anania C, Ferraro F, Chiarelli F, et al. Acylated and nonacylated ghrelin levels and their associations with insulin resistance in obese and NW children with metabolic syndrome. Eur J Endocrinol 2009;161:861–70.10.1530/EJE-09-0375Search in Google Scholar PubMed

28. Stylianou C, Galli-Tsinopoulou A, Farmakiotis D, Rousso I, Karamouzis M, Koliakos G, et al. Ghrelin and leptin levels in obese adolescents. Relationship with body fat and insulin resistance. Hormones (Athens) 2007;6:295–303.10.14310/horm.2002.1111025Search in Google Scholar PubMed

29. Schoppen S, Riestra P, García-Anguita A, López-Simón L, Cano B, de Oya I, et al. Leptin and adiponectin levels in pubertal children: relationship with anthropometric variables and body composition. Clin Chem Lab Med 2010;48:707–11.10.1515/CCLM.2010.142Search in Google Scholar PubMed

30. Delhanty PJ, Neggers SJ, van der Lely AJ. Should we consider des-acyl ghrelin as a separate hormone and if so, what does it do? Front Horm Res 2014;42:163–74.10.1159/000358345Search in Google Scholar PubMed

Received: 2015-6-12
Accepted: 2015-11-12
Published Online: 2015-12-22
Published in Print: 2016-8-1

©2016 by De Gruyter

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