Horm Metab Res 2016; 48(03): 174-177
DOI: 10.1055/s-0035-1559632
Endocrine Care
© Georg Thieme Verlag KG Stuttgart · New York

Is Serum Serotonin Involved in the Bone Loss of Young Females with Anorexia Nervosa?

L. Maïmoun
1   Département de Médecine Nucléaire, Hôpital Lapeyronie, Centre Hospitalier Régional Universitaire (CHRU) Montpellier, Montpellier, France
2   PhyMedExp, University of Montpellier, INSERM U1046, CNRS UMR 9214. 34295 Montpellier cedex 5, France
,
S. Guillaume
3   Département d’Urgence et Post-Urgence Psychiatrique, Hôpital Lapeyronie, CHRU Montpellier, UMI, INSERM, Montpellier, France
,
P. Lefebvre
4   Departement d’Endocrinologie, Diabète, Nutrition, Hôpital Lapeyronie, CHRU Montpellier, Montpellier, France
,
P. Philibert
5   Departement de Biochimie et d’Hormonologie, Hôpital Lapeyronie, CHRU Montpellier, Montpellier, France
,
H. Bertet
6   Unité de Recherche Clinique et Epidémiologie, Hôpital Lapeyronie, CHRU Montpellier, Montpellier, France
,
M.-C. Picot
6   Unité de Recherche Clinique et Epidémiologie, Hôpital Lapeyronie, CHRU Montpellier, Montpellier, France
7   CIC INSERM, Hôpital Gui de Chauliac, CHRU Montpellier, Montpellier, France
,
P. Courtet
3   Département d’Urgence et Post-Urgence Psychiatrique, Hôpital Lapeyronie, CHRU Montpellier, UMI, INSERM, Montpellier, France
,
D. Mariano-Goulart
1   Département de Médecine Nucléaire, Hôpital Lapeyronie, Centre Hospitalier Régional Universitaire (CHRU) Montpellier, Montpellier, France
2   PhyMedExp, University of Montpellier, INSERM U1046, CNRS UMR 9214. 34295 Montpellier cedex 5, France
,
E. Renard
4   Departement d’Endocrinologie, Diabète, Nutrition, Hôpital Lapeyronie, CHRU Montpellier, Montpellier, France
7   CIC INSERM, Hôpital Gui de Chauliac, CHRU Montpellier, Montpellier, France
8   Institut de Génomique Fonctionnelle, CNRS UMR 5203/INSERM U661/Université Montpellier 1 et 2, Montpellier, France
,
C. Sultan
9   Unité d’Endocrinologie et Gynécologie Pédiatrique, Département de Pédiatrie, Hôpital Arnaud de Villeneuve, CHRU Montpellier et UMI, Montpellier, France
› Author Affiliations
Further Information

Publication History

received 27 March 2015

accepted 08 July 2015

Publication Date:
29 September 2015 (online)

Abstract

Recent experimental data suggest that circulating serotonin interacts with bone metabolism, although this is less clear in humans. This study investigated whether serum serotonin interferes with bone metabolism in young women with anorexia nervosa (AN), a clinical model of energy deprivation. Serum serotonin, markers of bone turnover [osteocalcin (OC), procollagen type I N-terminal propeptide (PINP), type I-C telopeptide breakdown products (CTX)], leptin, soluble leptin receptor (sOB-R), and insulin-like growth factor-1 (IGF-1) and its binding protein (IGFBP-3) were assessed. Whole body, spine, hip, and radius areal bone mineral density BMD (aBMD) were assessed by dual-energy X-ray absorptiometry in 21 patients with AN and 19 age-matched controls. Serum serotonin, leptin, IGF-1, IGFBP-3, OC, PINP, and aBMD at all sites, radius excepted, were significantly reduced in AN whereas CTX and sOB-R were increased compared with controls. Serum serotonin levels were positively correlated with weight, body mass index, whole body fat mass, leptin, and IGF-1, and negatively with CTX for the entire population. Low serum serotonin levels are observed in patients with AN. Although no direct link between low serum serotonin levels and bone mass was identified in these patients, the negative relationship between serotonin and markers of bone resorption found in all population nevertheless suggests the implication of serotonin in bone metabolism. Impact of low serum serotonin on bone in AN warrants further studies.

 
  • References

  • 1 Klibanski ABB, Schoenfeld DA, Herzog DB, Saxe VC. The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab 1995; 80: 898-904
  • 2 Maïmoun L, Guillaume S, Lefebvre P, Philibert P, Bertet H, Picot MC, Gaspari L, Paris F, Courtet P, Thomas E, Mariano-Goulart D, Bringer J, Renard E, Sultan C. Role of sclerostin and Dickkopf-1 in the dramatic alteration in bone mass acquisition in adolescents and young women with recent anorexia nervosa. J Clin Endocrinol Metab 2014; 99: 4037-4050
  • 3 Hudson JI, Hiripi E, Pope Jr HG, Kessler RC. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry 2007; 61: 348-358
  • 4 Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC, Bonjour JP. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 1992; 75: 1060-1065
  • 5 Maïmoun L, Coste O, Mura T, Philibert P, Galtier F, Mariano-Goulart D, Paris F, Sultan C. Specific bone mass acquisition in elite female athletes. J Clin Endocrinol Metab 2013; 98: 2844-2853
  • 6 Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int 2003; 14: 843-847
  • 7 Faje AT, Fazeli PK, Miller KK, Katzman DK, Ebrahimi S, Lee H, Mendes N, Snelgrove D, Meenaghan E, Misra M, Klibanski A. Fracture risk and areal bone mineral density in adolescent females with anorexia nervosa. Int J Eat Disord 2014; 47: 458-466
  • 8 Miller KK. Endocrine dysregulation in anorexia nervosa update. J Clin Endocrinol Metab 2011; 96: 2939-2949
  • 9 Ducy P, Karsenty G. The two faces of serotonin in bone biology. J Cell Biol 2010; 191: 7-13
  • 10 Yadav VK, Oury F, Suda N, Liu ZW, Gao XB, Confavreux C, Klemenhagen KC, Tanaka KF, Gingrich JA, Guo XE, Tecott LH, Mann JJ, Hen R, Horvath TL, Karsenty G. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 2009; 138: 976-989
  • 11 Sibilia V, Pagani F, Dieci E, Mrak E, Marchese M, Zarattini G, Guidobono F. Dietary tryptophan manipulation reveals a central role for serotonin in the anabolic response of appendicular skeleton to physical activity in rats. Endocrine 2013; 44: 790-802
  • 12 Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, Fink H, Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003; 299: 76
  • 13 Sibilia V, Pagani F, Lattuada N, Greco A, Guidobono F. Linking chronic tryptophan deficiency with impaired bone metabolism and reduced bone accrual in growing rats. J Cell Biochem 2009; 107: 890-898
  • 14 Gustafsson BI, Westbroek I, Waarsing JH, Waldum H, Solligard E, Brunsvik A, Dimmen S, van Leeuwen JP, Weinans H, Syversen U. Long-term serotonin administration leads to higher bone mineral density, affects bone architecture, and leads to higher femoral bone stiffness in rats. J Cell Biochem 2006; 97: 1283-1291
  • 15 Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schutz G, Glorieux FH, Chiang CY, Zajac JD, Insogna KL, Mann JJ, Hen R, Ducy P, Karsenty G. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 2008; 135: 825-837
  • 16 Modder UI, Achenbach SJ, Amin S, Riggs BL, Melton 3rd LJ, Khosla S. Relation of serum serotonin levels to bone density and structural parameters in women. J Bone Miner Res 2010; 25: 415-422
  • 17 Wang Q, Chen D, Nicholson P, Cheng S, Alen M, Mao L. The associations of serum serotonin with bone traits are age- and gender-specific. PLoS One 2014; 9: e109028
  • 18 Eskandari F, Martinez PE, Torvik S, Phillips TM, Sternberg EM, Mistry S, Ronsaville D, Wesley R, Toomey C, Sebring NG, Reynolds JC, Blackman MR, Calis KA, Gold PW, Cizza G. Low bone mass in premenopausal women with depression. Arch Intern Med 2007; 167: 2329-2336
  • 19 Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, Herzog DB, Klibanski A. Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 2004; 114: 1574-1583
  • 20 Misra M, Le Clair M, Mendes N, Miller KK, Lawson E, Meenaghan E, Weigel T, Ebrahimi S, Herzog DB, Klibanski A. Use of SSRIs may Impact Bone Density in Adolescent and Young Women with Anorexia Nervosa. CNS Spectr 2010; 15: 579-586
  • 21 Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000; 100: 197-207
  • 22 Lechin F, van der Dijs B, Pardey-Maldonado B, Rivera JE, Baez S, Lechin ME. Anorexia nervosa depends on adrenal sympathetic hyperactivity: opposite neuroautonomic profile of hyperinsulinism syndrome. Diabetes Metab Syndr Obes 2010; 3: 311-317
  • 23 Farr JN, Charkoudian N, Barnes JN, Monroe DG, McCready LK, Atkinson EJ, Amin S, Melton 3rd LJ, Joyner MJ, Khosla S. Relationship of sympathetic activity to bone microstructure, turnover, and plasma osteopontin levels in women. J Clin Endocrinol Metab 2012; 97: 4219-4227
  • 24 Elefteriou F. Regulation of bone remodeling by the central and peripheral nervous system. Arch Biochem Biophys 2008; 473: 231-236