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01-05-2017 | Review

Restrictive Eating Disorders and Skeletal Health in Adolescent Girls and Young Women

Authors: Darcey Thornton, Catherine M. Gordon

Published in: Calcified Tissue International | Issue 5/2017

Abstract

This article reviews the effects of restrictive eating disorders on bone health. The relationship between eating disorders and amenorrhea is discussed in detail. The pathologic impact of malnutrition on bone is explored by examining the results of studies using various available imaging techniques. The multiple hormonal alterations seen in adolescents and young women with anorexia nervosa are reviewed, as well as how these alterations may influence bone turnover, density, structure, and strength. The diagnostic clinical evaluation for adolescents and young women with these disorders is also outlined. Available treatment options, including those that hold promise for efficacy, as well as those we deemed to be ineffective, are considered from both the clinical and mechanistic standpoints. Finally, future research opportunities are offered, including intriguing work in the area of fat and bone interactions.

Donaldson AA, Gordon CM (2015) Skeletal complications of eating disorders. Metabolism 64(9):943–951. doi:10.1016/j.metabol.2015.06.007 PubMedPubMedCentralCrossRef

American psychiatric association american psychiatric association DSM-5 task force (2013) Diagnostic and statistical manual of mental disorders: DSM-5, 5th edn. American Psychiatric Publishing, Washington, D.CCrossRef

Vestergaard P, Emborg C, Støving RK, Hagen C, Mosekilde L, Brixen K (2002) Fractures in patients with anorexia nervosa, bulimia nervosa, and other eating disorders—a nationwide register study. Int J Eat Disord 32(3):301–308. doi:10.1002/eat.10101 PubMedCrossRef

Faje AT, Fazeli PK, Miller KK, Katzman DK, Ebrahimi S, Lee H, Mendes N, Snelgrove D, Meenaghan E, Misra M, Klibanski A (2014) Fracture risk and areal bone mineral density in adolescent females with anorexia nervosa. Int J Eat Disord 47(5):458–466. doi:10.1002/eat.22248 PubMedPubMedCentralCrossRef

American psychiatric association (2000) Diagnostic criteria from DSM-IV-TR. The Association, Washington, D.C

Baker D, Roberts R, Towell T (2000) Factors predictive of bone mineral density in eating-disordered women: a longitudinal study. Int J Eat Disord 27(1):29–35PubMedCrossRef

Barrack MT, Van Loan MD, Rauh MJ, Nichols JF (2010) Physiologic and behavioral indicators of energy deficiency in female adolescent runners with elevated bone turnover. Am J Clin Nutr 92(3):652–659. doi:10.3945/ajcn.2009.28926 PubMedCrossRef

Wiksten-Almströmer M, Hirschberg AL, Hagenfeldt K (2009) Reduced bone mineral density in adult women diagnosed with menstrual disorders during adolescence. Acta Obstet Gynecol Scand 88(5):543–549. doi:10.1080/00016340902846080 PubMedCrossRef

Tolle V, Kadem M, Bluet-Pajot MT, Frere D, Foulon C, Bossu C, Dardennes R, Mounier C, Zizzari P, Lang F, Epelbaum J, Estour B (2003) Balance in ghrelin and leptin plasma levels in anorexia nervosa patients and constitutionally thin women. J Clin Endocrinol Metab 88(1):109–116. doi:10.1210/jc.2002-020645 PubMedCrossRef

10.

Gordon CM (2010) Clinical practice. Functional hypothalamic amenorrhea. N Engl J Med 363(4):365–371. doi:10.1056/NEJMcp0912024 PubMedCrossRef

11.

Roberto CA, Steinglass J, Mayer LE, Attia E, Walsh BT (2008) The clinical significance of amenorrhea as a diagnostic criterion for anorexia nervosa. Int J Eat Disord 41(6):559–563. doi:10.1002/eat.20534 PubMedCrossRef

12.

Shepherd JA, Schousboe JT, Broy SB, Engelke K, Leslie WD (2015) Executive Summary of the ISCD Position Development Conference on Advanced Measures from DXA and QCT: fracture prediction beyond BMD. J Clin Densitom 18(3):274–286. doi:10.1016/j.jocd.2015.06.013 PubMedCrossRef

13.

Ma NS, Gordon CM (2012) Pediatric osteoporosis: where are we now? J Pediatr 161(6):983–990PubMedCrossRef

14.

van Rijn RR, Van Kuijk C (2009) Of small bones and big mistakes; bone densitometry in children revisited. Eur J Radiol 71(3):432–439. doi:10.1016/j.ejrad.2008.08.017 PubMedCrossRef

15.

Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM, Densitometry ISfC (2014) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD pediatric official positions. J Clin Densitom 17(2):225–242. doi:10.1016/j.jocd.2014.01.003 PubMedCrossRef

16.

Högler W, Briody J, Woodhead HJ, Chan A, Cowell CT (2003) Importance of lean mass in the interpretation of total body densitometry in children and adolescents. J Pediatr 143(1):81–88. doi:10.1016/S0022-3476(03)00187-2 PubMedCrossRef

17.

Leonard MB, Shults J, Elliott DM, Stallings VA, Zemel BS (2004) Interpretation of whole body dual energy X-ray absorptiometry measures in children: comparison with peripheral quantitative computed tomography. Bone 34(6):1044–1052. doi:10.1016/j.bone.2003.12.003 PubMedCrossRef

18.

Gordon CM, Leonard MB, Zemel BS, DensitometryISfC (2014) 2013 Pediatric Position Development Conference: executive summary and reflections. J Clin Densitom 17(2):219–224. doi:10.1016/j.jocd.2014.01.007 PubMedCrossRef

19.

Pitts S, Blood E, Divasta A, Gordon CM (2014) Percentage body fat by dual-energy X-ray absorptiometry is associated with menstrual recovery in adolescents with anorexia nervosa. J Adolesc Health 54(6):739–741. doi:10.1016/j.jadohealth.2013.12.033 PubMedPubMedCentralCrossRef

20.

Engelke K, Adams JE, Armbrecht G, Augat P, Bogado CE, Bouxsein ML, Felsenberg D, Ito M, Prevrhal S, Hans DB, Lewiecki EM (2008) Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD official positions. J Clin Densitom 11(1):123–162. doi:10.1016/j.jocd.2007.12.010 PubMedCrossRef

21.

Milos G, Spindler A, Rüegsegger P, Seifert B, Mühlebach S, Uebelhart D, Häuselmann HJ (2005) Cortical and trabecular bone density and structure in anorexia nervosa. Osteoporos Int 16(7):783–790. doi:10.1007/s00198-004-1759-2 PubMedCrossRef

22.

Li X, Kuo D, Schafer AL, Porzig A, Link TM, Black D, Schwartz AV (2011) Quantification of vertebral bone marrow fat content using 3 tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging 33(4):974–979. doi:10.1002/jmri.22489 PubMedPubMedCentralCrossRef

23.

Shen W, Chen J, Punyanitya M, Shapses S, Heshka S, Heymsfield SB (2007) MRI-measured bone marrow adipose tissue is inversely related to DXA-measured bone mineral in caucasian women. Osteoporos Int 18(5):641–647. doi:10.1007/s00198-006-0285-9 PubMedCrossRef

24.

Bredella MA, Fazeli PK, Daley SM, Miller KK, Rosen CJ, Klibanski A, Torriani M (2014) Marrow fat composition in anorexia nervosa. Bone 66:199–204. doi:10.1016/j.bone.2014.06.014 PubMedPubMedCentralCrossRef

25.

Pansini V, Monnet A, Salleron J, Hardouin P, Cortet B, Cotten A (2014) 3 tesla (1) H MR spectroscopy of hip bone marrow in a healthy population, assessment of normal fat content values and influence of age and sex. J Magn Reson Imaging 39(2):369–376. doi:10.1002/jmri.24176 PubMedCrossRef

26.

Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N, Meenaghan E, Goldstein MA, Bouxsein ML, Misra M, Klibanski A (2013) Adolescent girls with anorexia nervosa have impaired cortical and trabecular microarchitecture and lower estimated bone strength at the distal radius. J Clin Endocrinol Metab 98(5):1923–1929. doi:10.1210/jc.2012-4153 PubMedPubMedCentralCrossRef

27.

Milos G, Häuselmann HJ, Krieg MA, Rüegsegger P, Gallo LM (2014) Are patterns of bone loss in anorexic and postmenopausal women similar? Preliminary results using high resolution peripheral computed tomography. Bone 58:146–150. doi:10.1016/j.bone.2013.09.016 PubMedCrossRef

28.

Fazeli PK, Faje AT, Cross EJ, Lee H, Rosen CJ, Bouxsein ML, Klibanski A (2015) Serum FGF-21 levels are associated with worsened radial trabecular bone microarchitecture and decreased radial bone strength in women with anorexia nervosa. Bone 77:6–11. doi:10.1016/j.bone.2015.04.001 PubMedPubMedCentralCrossRef

29.

Oftadeh R, Perez-Viloria M, Villa-Camacho JC, Vaziri A, Nazarian A (2015) Biomechanics and mechanobiology of trabecular bone: a review. J Biomech Eng. doi:10.1115/1.4029176 PubMedCentral

30.

Boskey AL, Coleman R (2010) Aging and bone. J Dent Res 89(12):1333–1348. doi:10.1177/0022034510377791 PubMedPubMedCentralCrossRef

31.

Lawson EA, Miller KK, Bredella MA, Phan C, Misra M, Meenaghan E, Rosenblum L, Donoho D, Gupta R, Klibanski A (2010) Hormone predictors of abnormal bone microarchitecture in women with anorexia nervosa. Bone 46(2):458–463. doi:10.1016/j.bone.2009.09.005 PubMedCrossRef

32.

Walsh CJ, Phan CM, Misra M, Bredella MA, Miller KK, Fazeli PK, Bayraktar HH, Klibanski A, Gupta R (2010) Women with anorexia nervosa: finite element and trabecular structure analysis by using flat-panel volume CT. Radiology 257(1):167–174. doi:10.1148/radiol.10100222 PubMedPubMedCentralCrossRef

33.

Devlin MJ, Rosen CJ (2015) The bone-fat interface: basic and clinical implications of marrow adiposity. Lancet Diabetes Endocrinol 3(2):141–147

34.

Hardouin P, Pansini V, Cortet B (2014) Bone marrow fat. Jt Bone Spine 81(4):313–319. doi:10.1016/j.jbspin.2014.02.013 CrossRef

35.

Abella E, Feliu E, Granada I, Millá F, Oriol A, Ribera JM, Sánchez-Planell L, Berga LI, Reverter JC, Rozman C (2002) Bone marrow changes in anorexia nervosa are correlated with the amount of weight loss and not with other clinical findings. Am J Clin Pathol 118(4):582–588. doi:10.1309/2Y7X-YDXK-006B-XLT2 PubMedCrossRef

36.

DiVasta AD, Mulkern RV, Gordon CM, Ecklund K (2015) MR imaging in a case of severe anorexia nervosa: the ‘flip-flop’ effect. Pediatr Radiol 45(4):617–620. doi:10.1007/s00247-014-3145-3 PubMedCrossRef

37.

Hiramatsu R, Ubara Y, Suwabe T, Hoshino J, Sumida K, Hasegawa E, Yamanouchi M, Hayami N, Sawa N, Takaichi K (2013) Bone histomorphometric analysis in a patient with anorexia nervosa. Bone 56(1):77–82. doi:10.1016/j.bone.2013.05.001 PubMedCrossRef

38.

Devlin MJ (2011) Why does starvation make bones fat? Am J Hum Biol 23(5):577–585. doi:10.1002/ajhb.21202 PubMedPubMedCentralCrossRef

39.

Rosen CJ, Klibanski A (2009) Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 122(5):409–414. doi:10.1016/j.amjmed.2008.11.027 PubMedCrossRef

40.

Ecklund K, Vajapeyam S, Feldman HA, Buzney CD, Mulkern RV, Kleinman PK, Rosen CJ, Gordon CM (2010) Bone marrow changes in adolescent girls with anorexia nervosa. J Bone Miner Res 25(2):298–304. doi:10.1359/jbmr.090805 PubMedCrossRef

41.

Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM (2009) Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr 19(2):109–124PubMedPubMedCentralCrossRef

42.

Manolagas SC, O’Brien CA, Almeida M (2013) The role of estrogen and androgen receptors in bone health and disease. Nat Rev Endocrinol 9(12):699–712. doi:10.1038/nrendo.2013.179 PubMedPubMedCentralCrossRef

43.

Della Torre S, Rando G, Meda C, Stell A, Chambon P, Krust A, Ibarra C, Magni P, Ciana P, Maggi A (2011) Amino acid-dependent activation of liver estrogen receptor alpha integrates metabolic and reproductive functions via IGF-1. Cell Metab 13(2):205–214. doi:10.1016/j.cmet.2011.01.002 PubMedCrossRef

44.

dos Santos E, dos Santos JE, Ribeiro RP, Rosa E Silva AC, Moreira AC, Silva de Sá MF (2007) Absence of circadian salivary cortisol rhythm in women with anorexia nervosa. J Pediatr Adolesc Gynecol 20(1):13–18. doi:10.1016/j.jpag.2006.10.011 PubMedCrossRef

45.

Miller KK, Grinspoon S, Gleysteen S, Grieco KA, Ciampa J, Breu J, Herzog DB, Klibanski A (2004) Preservation of neuroendocrine control of reproductive function despite severe undernutrition. J Clin Endocrinol Metab 89(9):4434–4438. doi:10.1210/jc.2004-0720 PubMedCrossRef

46.

Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, Herzog DB, Klibanski A (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114(6):1574–1583. doi:10.1542/peds.2004-0540 PubMedCrossRef

47.

Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M, Katzman DK, Klibanski A (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92(6):2046–2052. doi:10.1210/jc.2006-2855 PubMedCrossRef

48.

Soyka LA, Grinspoon S, Levitsky LL, Herzog DB, Klibanski A (1999) The effects of anorexia nervosa on bone metabolism in female adolescents. J Clin Endocrinol Metab 84(12):4489–4496. doi:10.1210/jcem.84.12.6207 PubMed

49.

Ohlsson C, Bengtsson BA, Isaksson OG, Andreassen TT, Slootweg MC (1998) Growth hormone and bone. Endocr Rev 19(1):55–79. doi:10.1210/edrv.19.1.0324 PubMed

50.

Brick DJ, Gerweck AV, Meenaghan E, Lawson EA, Misra M, Fazeli P, Johnson W, Klibanski A, Miller KK (2010) Determinants of IGF1 and GH across the weight spectrum: from anorexia nervosa to obesity. Eur J Endocrinol 163(2):185–191. doi:10.1530/EJE-10-0365 PubMedPubMedCentralCrossRef

51.

Bex M, Bouillon R (2003) Growth hormone and bone health. Horm Res 60(Suppl 3):80–86PubMed

52.

Prado TM, Wettemann RP, Spicer LJ, Vizcarra JA, Morgan GL (2002) Influence of exogenous gonadotropin-releasing hormone on ovarian function in beef cows after short- and long-term nutritionally induced anovulation. J Anim Sci 80(12):3268–3276PubMedCrossRef

53.

Canalis E, Mazziotti G, Giustina A, Bilezikian JP (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18(10):1319–1328. doi:10.1007/s00198-007-0394-0 PubMedCrossRef

54.

Mazziotti G, Chiavistelli S, Giustina A (2015) Pituitary diseases and bone. Endocrinol Metab Clin North Am 44(1):171–180. doi:10.1016/j.ecl.2014.10.014 PubMedCrossRef

55.

Mayer L, Walsh BT, Pierson RN, Heymsfield SB, Gallagher D, Wang J, Parides MK, Leibel RL, Warren MP, Killory E, Glasofer D (2005) Body fat redistribution after weight gain in women with anorexia nervosa. Am J Clin Nutr 81(6):1286–1291PubMed

56.

Clarke BL, Khosla S (2009) Androgens and bone. Steroids 74(3):296–305. doi:10.1016/j.steroids.2008.10.003 PubMedCrossRef

57.

Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C (2004) Androgens and bone. Endocr Rev 25(3):389–425. doi:10.1210/er.2003-0003 PubMedCrossRef

58.

Miller KK, Lawson EA, Mathur V, Wexler TL, Meenaghan E, Misra M, Herzog DB, Klibanski A (2007) Androgens in women with anorexia nervosa and normal-weight women with hypothalamic amenorrhea. J Clin Endocrinol Metab 92(4):1334–1339. doi:10.1210/jc.2006-2501 PubMedPubMedCentralCrossRef

59.

Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ (2014) Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 15(2):154–168. doi:10.1016/j.stem.2014.06.008 PubMedPubMedCentralCrossRef

60.

Zheng B, Jiang J, Luo K, Liu L, Lin M, Chen Y, Yan F (2015) Increased osteogenesis in osteoporotic bone marrow stromal cells by overexpression of leptin. Cell Tissue Res 361(3):845–856. doi:10.1007/s00441-015-2167-y PubMedCrossRef

61.

Laharrague P, Truel N, Fontanilles AM, Corberand JX, Pénicaud L, Casteilla L (2000) Regulation by cytokines of leptin expression in human bone marrow adipocytes. Horm Metab Res 32(10):381–385. doi:10.1055/s-2007-978658 PubMedCrossRef

62.

Liu K, Liu P, Liu R, Wu X, Cai M (2015) Relationship between serum leptin levels and bone mineral density: a systematic review and meta-analysis. Clin Chim Acta 444:260–263. doi:10.1016/j.cca.2015.02.040 PubMedCrossRef

63.

Vilà R, Adán C, Grasa MM, Masanés RM, Esteve M, Cabot C, Fernández-López JA, Remesar X, Alemany M (1999) Effect of food deprivation on rat plasma estrone fatty acid esters. Diabetes Obes Metab 1(6):353–356PubMedCrossRef

64.

Holtkamp K, Mika C, Grzella I, Heer M, Pak H, Hebebrand J, Herpertz-Dahlmann B (2003) Reproductive function during weight gain in anorexia nervosa. Leptin represents a metabolic gate to gonadotropin secretion. J Neural Transm (Vienna). doi:10.1007/s00702-002-0800-x

65.

Misra M, Miller KK, Kuo K, Griffin K, Stewart V, Hunter E, Herzog DB, Klibanski A (2005) Secretory dynamics of leptin in adolescent girls with anorexia nervosa and healthy adolescents. Am J Physiol Endocrinol Metab 289(3):E373–E381. doi:10.1152/ajpendo.00041.2005 PubMedCrossRef

66.

Legroux-Gérot I, Vignau J, Biver E, Pigny P, Collier F, Marchandise X, Duquesnoy B, Cortet B (2010) Anorexia nervosa, osteoporosis and circulating leptin: the missing link. Osteoporos Int 21(10):1715–1722. doi:10.1007/s00198-009-1120-x PubMedCrossRef

67.

Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402(6762):656–660. doi:10.1038/45230 PubMedCrossRef

68.

Misra M, Klibanski A (2016) Anorexia nervosa and its associated endocrinopathy in young people. Horm Res Paediatr 85(3):147–157. doi:10.1159/000443735 PubMedPubMedCentralCrossRef

69.

Misra M, Miller KK, Kuo K, Griffin K, Stewart V, Hunter E, Herzog DB, Klibanski A (2005) Secretory dynamics of ghrelin in adolescent girls with anorexia nervosa and healthy adolescents. Am J Physiol Endocrinol Metab 289(2):E347–E356. doi:10.1152/ajpendo.00615.2004 PubMedCrossRef

70.

Misra M, Miller KK, Stewart V, Hunter E, Kuo K, Herzog DB, Klibanski A (2005) Ghrelin and bone metabolism in adolescent girls with anorexia nervosa and healthy adolescents. J Clin Endocrinol Metab 90(9):5082–5087. doi:10.1210/jc.2005-0512 PubMedCrossRef

71.

Milošević V, Ajdžanović V, Nešić D, Starčević V, Filipović B, Rakočević R, Stevanović D (2013) Central ghrelin treatment stimulates ACTH cells in normal-fed, food-restricted and high-fed rats: an immunohistomorphometric and hormonal study. Acta Histochem 115(8):858–864. doi:10.1016/j.acthis.2013.04.003 PubMedCrossRef

72.

Fukushima N, Hanada R, Teranishi H, Fukue Y, Tachibana T, Ishikawa H, Takeda S, Takeuchi Y, Fukumoto S, Kangawa K, Nagata K, Kojima M (2005) Ghrelin directly regulates bone formation. J Bone Miner Res 20(5):790–798. doi:10.1359/JBMR.041237 PubMedCrossRef

73.

Grudell AB, Camilleri M (2007) The role of peptide YY in integrative gut physiology and potential role in obesity. Curr Opin Endocrinol Diabetes Obes 14(1):52–57. doi:10.1097/MED.0b013e3280123119 PubMedCrossRef

74.

Wortley KE, Garcia K, Okamoto H, Thabet K, Anderson KD, Shen V, Herman JP, Valenzuela D, Yancopoulos GD, Tschöp MH, Murphy A, Sleeman MW (2007) Peptide YY regulates bone turnover in rodents. Gastroenterology 133(5):1534–1543. doi:10.1053/j.gastro.2007.08.024 PubMedCrossRef

75.

Misra M, Miller KK, Tsai P, Gallagher K, Lin A, Lee N, Herzog DB, Klibanski A (2006) Elevated peptide YY levels in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 91(3):1027–1033. doi:10.1210/jc.2005-1878 PubMedCrossRef

76.

Utz AL, Lawson EA, Misra M, Mickley D, Gleysteen S, Herzog DB, Klibanski A, Miller KK (2008) Peptide YY (PYY) levels and bone mineral density (BMD) in women with anorexia nervosa. Bone 43(1):135–139. doi:10.1016/j.bone.2008.03.007 PubMedPubMedCentralCrossRef

77.

Williams GA, Wang Y, Callon KE, Watson M, Lin JM, Lam JB, Costa JL, Orpe A, Broom N, Naot D, Reid IR, Cornish J (2009) In vitro and in vivo effects of adiponectin on bone. Endocrinology 150(8):3603–3610. doi:10.1210/en.2008-1639 PubMedCrossRef

78.

Rhie YJ, Lee KH, Chung SC, Kim HS, Kim DH (2010) Effects of body composition, leptin, and adiponectin on bone mineral density in prepubertal girls. J Korean Med Sci 25(8):1187–1190. doi:10.3346/jkms.2010.25.8.1187 PubMedPubMedCentralCrossRef

79.

Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, Cortet B (2011) Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. J Clin Endocrinol Metab 96(9):2703–2713. doi:10.1210/jc.2011-0047 PubMedCrossRef

80.

Misra M, Golden NH, Katzman DK (2015) State of the art systematic review of bone disease in anorexia nervosa. Int J Eat Disord. doi:10.1002/eat.22451

81.

Golden NH, Katzman DK, Sawyer SM, Ornstein RM, Rome ES, Garber AK, Kohn M, Kreipe RE, SfAHa Medicine (2015) Position Paper of the Society for Adolescent Health and Medicine: medical management of restrictive eating disorders in adolescents and young adults. J Adolesc Health 56(1):121–125. doi:10.1016/j.jadohealth.2014.10.259 PubMedCrossRef

82.

Chou SH, Chamberland JP, Liu X, Matarese G, Gao C, Stefanakis R, Brinkoetter MT, Gong H, Arampatzi K, Mantzoros CS (2011) Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci U S A 108(16):6585–6590. doi:10.1073/pnas.1015674108 PubMedPubMedCentralCrossRef

83.

Sienkiewicz E, Magkos F, Aronis KN, Brinkoetter M, Chamberland JP, Chou S, Arampatzi KM, Gao C, Koniaris A, Mantzoros CS (2011) Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women. Metabolism 60(9):1211–1221. doi:10.1016/j.metabol.2011.05.016 PubMedCrossRef

84.

Welt CK, Chan JL, Bullen J, Murphy R, Smith P, DePaoli AM, Karalis A, Mantzoros CS (2004) Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med 351(10):987–997. doi:10.1056/NEJMoa040388 PubMedCrossRef

85.

Divasta AD, Feldman HA, Giancaterino C, Rosen CJ, Leboff MS, Gordon CM (2012) The effect of gonadal and adrenal steroid therapy on skeletal health in adolescents and young women with anorexia nervosa. Metabolism 61(7):1010–1020. doi:10.1016/j.metabol.2011.11.016 PubMedPubMedCentralCrossRef

86.

DiVasta AD, Feldman HA, Beck TJ, LeBoff MS, Gordon CM (2014) Does hormone replacement normalize bone geometry in adolescents with anorexia nervosa? J Bone Miner Res 29(1):151–157. doi:10.1002/jbmr.2005 PubMedCrossRef

87.

Misra M, Katzman D, Miller KK, Mendes N, Snelgrove D, Russell M, Goldstein MA, Ebrahimi S, Clauss L, Weigel T, Mickley D, Schoenfeld DA, Herzog DB, Klibanski A (2011) Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. J Bone Miner Res 26(10):2430–2438. doi:10.1002/jbmr.447 PubMedPubMedCentralCrossRef

88.

Grinspoon S, Thomas L, Miller K, Herzog D, Klibanski A (2002) Effects of recombinant human IGF-I and oral contraceptive administration on bone density in anorexia nervosa. J Clin Endocrinol Metab 87(6):2883–2891. doi:10.1210/jcem.87.6.8574 PubMedCrossRef

89.

Fazeli PK, Wang IS, Miller KK, Herzog DB, Misra M, Lee H, Finkelstein JS, Bouxsein ML, Klibanski A (2014) Teriparatide increases bone formation and bone mineral density in adult women with anorexia nervosa. J Clin Endocrinol Metab 99(4):1322–1329. doi:10.1210/jc.2013-4105 PubMedPubMedCentralCrossRef

90.

Andrews EB, Gilsenan AW, Midkiff K, Sherrill B, Wu Y, Mann BH, Masica D (2012) The US postmarketing surveillance study of adult osteosarcoma and teriparatide: study design and findings from the first 7 years. J Bone Miner Res 27(12):2429–2437. doi:10.1002/jbmr.1768 PubMedPubMedCentralCrossRef

91.

Vahle JL, Long GG, Sandusky G, Westmore M, Ma YL, Sato M (2004) Bone neoplasms in F344 rats given teriparatide [rhPTH(1–34)] are dependent on duration of treatment and dose. Toxicol Pathol 32(4):426–438. doi:10.1080/01926230490462138 PubMedCrossRef

92.

Vahle JL, Sato M, Long GG, Young JK, Francis PC, Engelhardt JA, Westmore MS, Linda Y, Nold JB (2002) Skeletal changes in rats given daily subcutaneous injections of recombinant human parathyroid hormone (1–34) for 2 years and relevance to human safety. Toxicol Pathol 30(3):312–321PubMedCrossRef

93.

Vahle JL, Zuehlke U, Schmidt A, Westmore M, Chen P, Sato M (2008) Lack of bone neoplasms and persistence of bone efficacy in cynomolgus macaques after long-term treatment with teriparatide [rhPTH(1–34)]. J Bone Miner Res 23(12):2033–2039. doi:10.1359/jbmr.080807 PubMedCrossRef

94.

Miller KK, Grieco KA, Mulder J, Grinspoon S, Mickley D, Yehezkel R, Herzog DB, Klibanski A (2004) Effects of risedronate on bone density in anorexia nervosa. J Clin Endocrinol Metab 89(8):3903–3906. doi:10.1210/jc.2003-031885 PubMedCrossRef

95.

Miller KK, Meenaghan E, Lawson EA, Misra M, Gleysteen S, Schoenfeld D, Herzog D, Klibanski A (2011) Effects of risedronate and low-dose transdermal testosterone on bone mineral density in women with anorexia nervosa: a randomized, placebo-controlled study. J Clin Endocrinol Metab 96(7):2081–2088. doi:10.1210/jc.2011-0380 PubMedPubMedCentralCrossRef

96.

Golden NH, Iglesias EA, Jacobson MS, Carey D, Meyer W, Schebendach J, Hertz S, Shenker IR (2005) Alendronate for the treatment of osteopenia in anorexia nervosa: a randomized, double-blind, placebo-controlled trial. J Clin Endocrinol Metab 90(6):3179–3185. doi:10.1210/jc.2004-1659 PubMedCrossRef

97.

DiVasta AD, Feldman HA, Quach AE, Balestrino M, Gordon CM (2009) The effect of bed rest on bone turnover in young women hospitalized for anorexia nervosa: a pilot study. J Clin Endocrinol Metab 94(5):1650–1655. doi:10.1210/jc.2008-1654 PubMedPubMedCentralCrossRef

98.

Golden NH, Jacobson MS, Schebendach J, Solanto MV, Hertz SM, Shenker IR (1997) Resumption of menses in anorexia nervosa. Arch Pediatr Adolesc Med 151(1):16–21PubMedCrossRef

99.

Milos G, Spindler A, Rüegsegger P, Hasler G, Schnyder U, Laib A, Gallo LM, Uebelhart D, Häuselmann H (2007) Does weight gain induce cortical and trabecular bone regain in anorexia nervosa?. A 2-year prospective study. Bone 41(5):869–874. doi:10.1016/j.bone.2007.07.017 PubMedCrossRef

100.

Bachrach LK, Katzman DK, Litt IF, Guido D, Marcus R (1991) Recovery from osteopenia in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 72(3):602–606. doi:10.1210/jcem-72-3-602 PubMedCrossRef

101.

Hartman D, Crisp A, Rooney B, Rackow C, Atkinson R, Patel S (2000) Bone density of women who have recovered from anorexia nervosa. Int J Eat Disord 28(1):107–112PubMedCrossRef

102.

Biller BM, Saxe V, Herzog DB, Rosenthal DI, Holzman S, Klibanski A (1989) Mechanisms of osteoporosis in adult and adolescent women with anorexia nervosa. J Clin Endocrinol Metab 68(3):548–554. doi:10.1210/jcem-68-3-548 PubMedCrossRef

103.

Misra M (2008) Long-term skeletal effects of eating disorders with onset in adolescence. Ann N Y Acad Sci 1135:212–218. doi:10.1196/annals.1429.002 PubMedCrossRef

104.

Golden NH, Lanzkowsky L, Schebendach J, Palestro CJ, Jacobson MS, Shenker IR (2002) The effect of estrogen-progestin treatment on bone mineral density in anorexia nervosa. J Pediatr Adolesc Gynecol 15(3):135–143PubMedCrossRef

105.

Strokosch GR, Friedman AJ, Wu SC, Kamin M (2006) Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in adolescent females with anorexia nervosa: a double-blind, placebo-controlled study. J Adolesc Health 39(6):819–827. doi:10.1016/j.jadohealth.2006.09.010 PubMedCrossRef

106.

Gordon CM, Grace E, Emans SJ, Feldman HA, Goodman E, Becker KA, Rosen CJ, Gundberg CM, LeBoff MS (2002) Effects of oral dehydroepiandrosterone on bone density in young women with anorexia nervosa: a randomized trial. J Clin Endocrinol Metab 87(11):4935–4941. doi:10.1210/jc.2002-020545 PubMedCrossRef

107.

Fazeli PK, Lawson EA, Prabhakaran R, Miller KK, Donoho DA, Clemmons DR, Herzog DB, Misra M, Klibanski A (2010) Effects of recombinant human growth hormone in anorexia nervosa: a randomized, placebo-controlled study. J Clin Endocrinol Metab 95(11):4889–4897. doi:10.1210/jc.2010-0493 PubMedPubMedCentralCrossRef

Title: Restrictive Eating Disorders and Skeletal Health in Adolescent Girls and Young Women
Authors: Darcey Thornton
Catherine M. Gordon
Publication date: 01-05-2017
Publisher: Springer US
Published in: Calcified Tissue International / Issue 5/2017
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI: https://doi.org/10.1007/s00223-016-0164-0

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