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Published in: Osteoporosis International 6/2016

01-06-2016 | Review

A systematic review and meta-analysis of the association between eating disorders and bone density

Authors: L. Robinson, V. Aldridge, E. M. Clark, M. Misra, N. Micali

Published in: Osteoporosis International | Issue 6/2016

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Abstract

This meta-analysis investigates the effect of an eating disorder on bone mineral density in two eating disorder subtypes. Following conflicting findings in previous literature, this study finds that not only anorexia nervosa, but also bulimia nervosa has a detrimental effect on BMD. Key predictors of this relationship are discussed. This systematic review and meta-analysis investigates bone mineral density (BMD) in individuals with anorexia nervosa (AN) and bulimia nervosa (BN) in comparison to healthy controls (HCs). AN has been associated with low BMD and a risk of fractures and mixed results have been obtained for the relationship between BN and BMD. Deciphering the effect these two ED subtypes on BMD will determine the effect of low body weight (a characteristic of AN) versus the effects of periods of restrictive eating and malnutrition which are common to both AN and BN. We conducted a systematic search through the electronic databases MedLine, EMBASE and PsychInfo and the Cochrane Library to investigate and quantify this relationship. We screened 544 articles and included 27 studies in a random-effect meta-analysis and calculated the standardised mean difference (SMD) in BMD between women with a current diagnosis of AN (n = 785) vs HCs (n = 979) and a current diagnosis of BN (n = 187) vs HCs (n = 350). The outcome measures investigated were spinal, hip, femoral neck and whole body BMD measured by DXA or DPA scanning. A meta-regression investigated the effect of factors including age, duration since diagnosis, duration of amenorrhea and BMI on BMD. The mean BMI of participants was 16.65 kg/m2 (AN), 21.16 kg/m2 (BN) and 22.06 kg/m2 (HC). Spine BMD was lowest in AN subjects (SMD, −3.681; 95 % CI, −4.738, −2.625; p < 0.0001), but also lower in BN subjects compared with HCs (SMD, −0.472; 95 % CI, −0.688, −0.255; p < 0.0001). Hip, whole body and femoral neck BMD were reduced to a statistically significant level in AN but not BN groups. The meta-regression was limited by the number of included studies and did not find any significant predictors. This meta-analysis confirms the association between low BMD and AN and presents a strong argument for assessing BMD not only in patients with AN, but also in patients with BN.
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Literature
1.
go back to reference Gehlbach SH, Avrunin JS, Puleo E (2007) Trends in hospital care for hip fractures. Osteoporos Int 18(5):585–91CrossRefPubMed Gehlbach SH, Avrunin JS, Puleo E (2007) Trends in hospital care for hip fractures. Osteoporos Int 18(5):585–91CrossRefPubMed
2.
go back to reference Seeman E, Szmukler GI, Formica C, Tsalamandris C, Mestrovic R (1992) Osteoporosis in anorexia nervosa: the influence of peak bone density, bone loss, oral contraceptive use, and exercise. J Bone Miner Res 7(12):1467–74CrossRefPubMed Seeman E, Szmukler GI, Formica C, Tsalamandris C, Mestrovic R (1992) Osteoporosis in anorexia nervosa: the influence of peak bone density, bone loss, oral contraceptive use, and exercise. J Bone Miner Res 7(12):1467–74CrossRefPubMed
3.
go back to reference Rigotti NA, Nussbaum SR, Herzog DB, Neer RM (1984) Osteoporosis in women with anorexia nervosa. N Engl J Med 311(25):1601–6CrossRefPubMed Rigotti NA, Nussbaum SR, Herzog DB, Neer RM (1984) Osteoporosis in women with anorexia nervosa. N Engl J Med 311(25):1601–6CrossRefPubMed
5.
go back to reference AP A. Diagnostic and statistical manual of mental disorders: DSM-5. ManMag, 2003 AP A. Diagnostic and statistical manual of mental disorders: DSM-5. ManMag, 2003
6.
go back to reference Johnson JG, Cohen P, Kasen S, Brook JS (2002) Eating disorders during adolescence and the risk for physical and mental disorders during early adulthood. Arch Gen Psychiatry 59(6):545–52CrossRefPubMed Johnson JG, Cohen P, Kasen S, Brook JS (2002) Eating disorders during adolescence and the risk for physical and mental disorders during early adulthood. Arch Gen Psychiatry 59(6):545–52CrossRefPubMed
7.
go back to reference Bredella MA, Fazeli PK, Freedman LM, Calder G, Lee H, Rosen CJ et al (2012) Young women with cold-activated brown adipose tissue have higher bone mineral density and lower Pref-1 than women without brown adipose tissue: a study in women with anorexia nervosa, women recovered from anorexia nervosa, and normal-weight women. J Clin Endocrinol Metab 97(4):E584–E90CrossRefPubMedPubMedCentral Bredella MA, Fazeli PK, Freedman LM, Calder G, Lee H, Rosen CJ et al (2012) Young women with cold-activated brown adipose tissue have higher bone mineral density and lower Pref-1 than women without brown adipose tissue: a study in women with anorexia nervosa, women recovered from anorexia nervosa, and normal-weight women. J Clin Endocrinol Metab 97(4):E584–E90CrossRefPubMedPubMedCentral
8.
go back to reference Bredella MA, Fazeli PK, Miller KK, Misra M, Torriani M, Thomas BJ et al (2009) Increased bone marrow fat in anorexia nervosa. J Clin Endocrinol Metab 94(6):2129–36CrossRefPubMedPubMedCentral Bredella MA, Fazeli PK, Miller KK, Misra M, Torriani M, Thomas BJ et al (2009) Increased bone marrow fat in anorexia nervosa. J Clin Endocrinol Metab 94(6):2129–36CrossRefPubMedPubMedCentral
9.
go back to reference Bredella MA, Misra M, Miller KK, Klibanski A, Gupta R (2008) Trabecular structure analysis of the distal radius in adolescent patients with anorexia nervosa using ultra high resolution flat panel based volume CT. J Musculoskelet Neuronal Interact 8(4):315PubMed Bredella MA, Misra M, Miller KK, Klibanski A, Gupta R (2008) Trabecular structure analysis of the distal radius in adolescent patients with anorexia nervosa using ultra high resolution flat panel based volume CT. J Musculoskelet Neuronal Interact 8(4):315PubMed
10.
go back to reference Davies KM, Pearson PH, Huseman CA, Greger NG, Kimmel DK, Recker RR (1990) Reduced bone mineral in patients with eating disorders. Bone 11(3):143–7CrossRefPubMed Davies KM, Pearson PH, Huseman CA, Greger NG, Kimmel DK, Recker RR (1990) Reduced bone mineral in patients with eating disorders. Bone 11(3):143–7CrossRefPubMed
11.
go back to reference Milos G, Spindler A, Ruegsegger P, Hasler G, Schnyder U, Laib A et al (2007) Does weight gain induce cortical and trabecular bone regain in anorexia nervosa? A two-year prospective study. Bone 41(5):869–74CrossRefPubMed Milos G, Spindler A, Ruegsegger P, Hasler G, Schnyder U, Laib A et al (2007) Does weight gain induce cortical and trabecular bone regain in anorexia nervosa? A two-year prospective study. Bone 41(5):869–74CrossRefPubMed
12.
go back to reference Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N et al (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):1923–9CrossRefPubMedPubMedCentral Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N et al (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):1923–9CrossRefPubMedPubMedCentral
13.
go back to reference Misra M, Klibanski A (2011) Bone metabolism in adolescents with anorexia nervosa. J Endocrinol Investig 34(4):324–32CrossRef Misra M, Klibanski A (2011) Bone metabolism in adolescents with anorexia nervosa. J Endocrinol Investig 34(4):324–32CrossRef
14.
go back to reference Heaney R, Abrams S, Dawson-Hughes B, Looker A, Looker A, Marcus R et al (2000) Peak bone mass. Osteoporos Int 11(12):985–1009CrossRefPubMed Heaney R, Abrams S, Dawson-Hughes B, Looker A, Looker A, Marcus R et al (2000) Peak bone mass. Osteoporos Int 11(12):985–1009CrossRefPubMed
15.
go back to reference 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):548–54CrossRefPubMed 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):548–54CrossRefPubMed
16.
go back to reference Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR (1991) The clinical course of osteoporosis in anorexia nervosa: a longitudinal study of cortical bone mass. Jama 265(9):1133–8CrossRefPubMed Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR (1991) The clinical course of osteoporosis in anorexia nervosa: a longitudinal study of cortical bone mass. Jama 265(9):1133–8CrossRefPubMed
17.
go back to reference Grinspoon S, Thomas E, Pitts S, Gross E, Mickley D, Miller K et al (2000) Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med 133(10):790–4CrossRefPubMedPubMedCentral Grinspoon S, Thomas E, Pitts S, Gross E, Mickley D, Miller K et al (2000) Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med 133(10):790–4CrossRefPubMedPubMedCentral
18.
go back to reference Newton JR, Freeman CP, Hannan WJ, Cowen S (1993) Osteoporosis and normal weight bulimia nervosa—which patients are at risk? J Psychosom Res 37(3):239–47CrossRefPubMed Newton JR, Freeman CP, Hannan WJ, Cowen S (1993) Osteoporosis and normal weight bulimia nervosa—which patients are at risk? J Psychosom Res 37(3):239–47CrossRefPubMed
19.
go back to reference Gordon CM, Goodman E, Emans SJ, Grace E, Becker KA, Rosen CJ et al (2002) Physiologic regulators of bone turnover in young women with anorexia nervosa. J Pediatr 141(1):64–70CrossRefPubMed Gordon CM, Goodman E, Emans SJ, Grace E, Becker KA, Rosen CJ et al (2002) Physiologic regulators of bone turnover in young women with anorexia nervosa. J Pediatr 141(1):64–70CrossRefPubMed
20.
go back to reference Iketani T, Kiriike N, Nakanishi S, Nakasuji T (1995) Effects of weight gain and resumption of menses on reduced bone density in patients with anorexia nervosa. Biol Psychiatry 37(8):521–7CrossRefPubMed Iketani T, Kiriike N, Nakanishi S, Nakasuji T (1995) Effects of weight gain and resumption of menses on reduced bone density in patients with anorexia nervosa. Biol Psychiatry 37(8):521–7CrossRefPubMed
21.
go back to reference Sundgot-Borgen J, Bahr R, Falch JA, Schneider LS (1998) Normal bone mass in bulimic women. J Clin Endocrinol Metab 83(9):3144–9CrossRefPubMed Sundgot-Borgen J, Bahr R, Falch JA, Schneider LS (1998) Normal bone mass in bulimic women. J Clin Endocrinol Metab 83(9):3144–9CrossRefPubMed
22.
go back to reference Goebel G, Schweiger U, Kruger R, Fichter MM (1999) Predictors of bone mineral density in patients with eating disorders. Int J Eat Disord 25(2):143–50CrossRefPubMed Goebel G, Schweiger U, Kruger R, Fichter MM (1999) Predictors of bone mineral density in patients with eating disorders. Int J Eat Disord 25(2):143–50CrossRefPubMed
23.
go back to reference Newman MM, Halmi KA (1989) Relationship of bone density to estradiol and cortisol in anorexia nervosa and bulimia. Psychiatry Res 29(1):105–12CrossRefPubMed Newman MM, Halmi KA (1989) Relationship of bone density to estradiol and cortisol in anorexia nervosa and bulimia. Psychiatry Res 29(1):105–12CrossRefPubMed
24.
go back to reference Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA et al (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114(6):1574–83CrossRefPubMed Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA et al (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114(6):1574–83CrossRefPubMed
26.
go back to reference Klibanski A, Biller BMK, Schoenfeld DA, Herzog DB, Saxe VC (1995) The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab 80(3):898–904PubMed Klibanski A, Biller BMK, Schoenfeld DA, Herzog DB, Saxe VC (1995) The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab 80(3):898–904PubMed
27.
go back to reference Strokosch GR, Friedman AJ, Wu S-C, 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):819–27CrossRefPubMed Strokosch GR, Friedman AJ, Wu S-C, 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):819–27CrossRefPubMed
28.
go back to reference Zipfel S, Seibel MJ, Lowe B, Beumont PJ, Kasperk C, Herzog W (2001) Osteoporosis in eating disorders: a follow-up study of patients with anorexia and bulimia nervosa. J Clin Endocrinol Metab 86(11):5227–33CrossRefPubMed Zipfel S, Seibel MJ, Lowe B, Beumont PJ, Kasperk C, Herzog W (2001) Osteoporosis in eating disorders: a follow-up study of patients with anorexia and bulimia nervosa. J Clin Endocrinol Metab 86(11):5227–33CrossRefPubMed
29.
go back to reference Guo LJ, Jiang TJ, Liao L, Liu H, He HB (2013) Relationship between serum omentin-1 level and bone mineral density in girls with anorexia nervosa. J Endocrinol Investig 36(3):190–4 Guo LJ, Jiang TJ, Liao L, Liu H, He HB (2013) Relationship between serum omentin-1 level and bone mineral density in girls with anorexia nervosa. J Endocrinol Investig 36(3):190–4
30.
go back to reference Karlsson MK, Weigall SJ, Duan Y, Seeman E (2000) Bone size and volumetric density in women with anorexia nervosa receiving estrogen replacement therapy and in women recovered from anorexia nervosa. J Clin Endocrinol Metab 85(9):3177–82CrossRefPubMed Karlsson MK, Weigall SJ, Duan Y, Seeman E (2000) Bone size and volumetric density in women with anorexia nervosa receiving estrogen replacement therapy and in women recovered from anorexia nervosa. J Clin Endocrinol Metab 85(9):3177–82CrossRefPubMed
31.
go back to reference Maimoun L, Guillaume S, Lefebvre P, Philibert P, Bertet H, Picot MC et al (2014) 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 99(4):E582–E90CrossRefPubMed Maimoun L, Guillaume S, Lefebvre P, Philibert P, Bertet H, Picot MC et al (2014) 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 99(4):E582–E90CrossRefPubMed
32.
go back to reference Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M et al (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92(6):2046–52CrossRefPubMed Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M et al (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92(6):2046–52CrossRefPubMed
33.
go back to reference Wojcik MH, Meenaghan E, Lawson EA, Misra M, Klibanski A, Miller KK (2010) Reduced amylin levels are associated with low bone mineral density in women with anorexia nervosa. Bone 46(3):796–800CrossRefPubMedPubMedCentral Wojcik MH, Meenaghan E, Lawson EA, Misra M, Klibanski A, Miller KK (2010) Reduced amylin levels are associated with low bone mineral density in women with anorexia nervosa. Bone 46(3):796–800CrossRefPubMedPubMedCentral
34.
go back to reference Flynn J, Foley S, Jones G (2007) Can BMD assessed by DXA at age 8 predict fracture risk in boys and girls during puberty?: an eight-year prospective study. J Bone Miner Res 22(9):1463–7CrossRefPubMed Flynn J, Foley S, Jones G (2007) Can BMD assessed by DXA at age 8 predict fracture risk in boys and girls during puberty?: an eight-year prospective study. J Bone Miner Res 22(9):1463–7CrossRefPubMed
35.
go back to reference Ackerman KE, Sokoloff NC, De Nardo MG, Clarke H, Lee H, Misra M. Fractures in relation to menstrual status and bone parameters in young athletes. Medicine and science in sports and exercise. 2014 Ackerman KE, Sokoloff NC, De Nardo MG, Clarke H, Lee H, Misra M. Fractures in relation to menstrual status and bone parameters in young athletes. Medicine and science in sports and exercise. 2014
36.
go back to reference Hedges LV, Vevea JL (1998) Fixed-and random-effects models in meta-analysis. Psychol Methods 3(4):486CrossRef Hedges LV, Vevea JL (1998) Fixed-and random-effects models in meta-analysis. Psychol Methods 3(4):486CrossRef
37.
go back to reference Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions: Wiley Online Library; 2008 Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions: Wiley Online Library; 2008
38.
go back to reference Duval S, Tweedie R (2000) A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. J Am Stat Assoc 95(449):89–98 Duval S, Tweedie R (2000) A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. J Am Stat Assoc 95(449):89–98
40.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(4):264–9CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(4):264–9CrossRefPubMed
41.
go back to reference Mazess R, Barden H, editors. Measurement of bone by dual-photon absorptiometry (DPA) and dual-energy X-ray absorptiometry (DEXA). Annales chirurgiae et gynaecologiae; 1987. Mazess R, Barden H, editors. Measurement of bone by dual-photon absorptiometry (DPA) and dual-energy X-ray absorptiometry (DEXA). Annales chirurgiae et gynaecologiae; 1987.
42.
go back to reference Masala S, Jacoangeli F, Fiori R, Mezzasalma FS, Marinetti A, Simonetti G et al (2003) Densitometric evaluation in women with anorexia nervosa. Acta Diabetol 40(1):S177–S9CrossRefPubMed Masala S, Jacoangeli F, Fiori R, Mezzasalma FS, Marinetti A, Simonetti G et al (2003) Densitometric evaluation in women with anorexia nervosa. Acta Diabetol 40(1):S177–S9CrossRefPubMed
43.
go back to reference Resch H, Newrkla S, Grampp S, Resch A, Zapf S, Piringer S et al (2000) Ultrasound and X-ray-based bone densitometry in patients with anorexia nervosa. Calcif Tissue Int 66(5):338–41CrossRefPubMed Resch H, Newrkla S, Grampp S, Resch A, Zapf S, Piringer S et al (2000) Ultrasound and X-ray-based bone densitometry in patients with anorexia nervosa. Calcif Tissue Int 66(5):338–41CrossRefPubMed
44.
go back to reference Morris J, Tothill P, Gard M, McPhail K, Hannan J, Cowen S et al (2004) Reduced bone mineral density in bulimia as well as anorexia nervosa. Eur Eat Disord Rev 12(2):71–8CrossRef Morris J, Tothill P, Gard M, McPhail K, Hannan J, Cowen S et al (2004) Reduced bone mineral density in bulimia as well as anorexia nervosa. Eur Eat Disord Rev 12(2):71–8CrossRef
45.
go back to reference Walsh CJ, Phan CM, Misra M, Bredella MA, Miller KK, Fazeli PK et al (2010) Women with anorexia nervosa: finite element and trabecular structure analysis by using flat-panel volume CT. Radiology 257(1):167–74CrossRefPubMedPubMedCentral Walsh CJ, Phan CM, Misra M, Bredella MA, Miller KK, Fazeli PK et al (2010) Women with anorexia nervosa: finite element and trabecular structure analysis by using flat-panel volume CT. Radiology 257(1):167–74CrossRefPubMedPubMedCentral
46.
go back to reference Misra M, Miller KK, Stewart V, Hunter E, Kuo K, Herzog DB et al (2005) Ghrelin and bone metabolism in adolescent girls with anorexia nervosa and healthy adolescents. J Clin Endocrinol Metab 90(9):5082–7CrossRefPubMed Misra M, Miller KK, Stewart V, Hunter E, Kuo K, Herzog DB et al (2005) Ghrelin and bone metabolism in adolescent girls with anorexia nervosa and healthy adolescents. J Clin Endocrinol Metab 90(9):5082–7CrossRefPubMed
47.
go back to reference Fernández-Soto ML, González-Jiménez A, Chamorro-Fernández M, Leyva-Martínez S (2013) Clinical and hormonal variables related to bone mass loss in anorexia nervosa patients. Vitam Horm 92:259–69CrossRefPubMed Fernández-Soto ML, González-Jiménez A, Chamorro-Fernández M, Leyva-Martínez S (2013) Clinical and hormonal variables related to bone mass loss in anorexia nervosa patients. Vitam Horm 92:259–69CrossRefPubMed
48.
go back to reference Misra M, Katzman D, Miller KK, Mendes N, Snelgrove D, Russell M et al (2011) Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. J Bone Miner Res 26(10):2430–8CrossRefPubMedPubMedCentral Misra M, Katzman D, Miller KK, Mendes N, Snelgrove D, Russell M et al (2011) Physiologic estrogen replacement increases bone density in adolescent girls with anorexia nervosa. J Bone Miner Res 26(10):2430–8CrossRefPubMedPubMedCentral
49.
go back to reference Organization WH. The ICD-10 classification of mental and behavioural disorders: clinical descriptions and diagnostic guidelines: Geneva: World Health Organization; 1992 Organization WH. The ICD-10 classification of mental and behavioural disorders: clinical descriptions and diagnostic guidelines: Geneva: World Health Organization; 1992
50.
go back to reference First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for DSM-IV® axis I disorders (SCID-I), Clinician Version, Administration Booklet: American Psychiatric Pub; 2012 First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for DSM-IV® axis I disorders (SCID-I), Clinician Version, Administration Booklet: American Psychiatric Pub; 2012
51.
go back to reference Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M et al (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J ClinEndocrinol Metab 92(6):2046–52CrossRef Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M et al (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J ClinEndocrinol Metab 92(6):2046–52CrossRef
52.
go back to reference Kooh SW, Noriega E, Leslie K, Muller C, Harrison JE (1996) Bone mass and soft tissue composition in adolescents with anorexia nervosa. Bone 19(2):181–8CrossRefPubMed Kooh SW, Noriega E, Leslie K, Muller C, Harrison JE (1996) Bone mass and soft tissue composition in adolescents with anorexia nervosa. Bone 19(2):181–8CrossRefPubMed
53.
go back to reference 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):4489–96PubMed 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):4489–96PubMed
54.
go back to reference Naessen S, Carlstrom K, Glant R, Jacobsson H, Hirschberg AL (2006) Bone mineral density in bulimic women—influence of endocrine factors and previous anorexia. Eur J Endocrinol 155(2):245–51CrossRefPubMed Naessen S, Carlstrom K, Glant R, Jacobsson H, Hirschberg AL (2006) Bone mineral density in bulimic women—influence of endocrine factors and previous anorexia. Eur J Endocrinol 155(2):245–51CrossRefPubMed
55.
go back to reference Clark EM, Ness AR, Bishop NJ, Tobias JH (2006) Association between bone mass and fractures in children: a prospective cohort study. J Bone Miner Res 21(9):1489–95CrossRefPubMedPubMedCentral Clark EM, Ness AR, Bishop NJ, Tobias JH (2006) Association between bone mass and fractures in children: a prospective cohort study. J Bone Miner Res 21(9):1489–95CrossRefPubMedPubMedCentral
56.
go back to reference DiVasta AD, Beck TJ, Petit MA, Feldman HA, LeBoff MS, Gordon CM (2007) Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int 18(6):797–804CrossRefPubMedPubMedCentral DiVasta AD, Beck TJ, Petit MA, Feldman HA, LeBoff MS, Gordon CM (2007) Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int 18(6):797–804CrossRefPubMedPubMedCentral
57.
go back to reference Misra M, Miller KK, Almazan C, Ramaswamy K, Lapcharoensap W, Worley M et al (2004) Alterations in cortisol secretory dynamics in adolescent girls with anorexia nervosa and effects on bone metabolism. J Clin Endocrinol Metab 89(10):4972–80CrossRefPubMed Misra M, Miller KK, Almazan C, Ramaswamy K, Lapcharoensap W, Worley M et al (2004) Alterations in cortisol secretory dynamics in adolescent girls with anorexia nervosa and effects on bone metabolism. J Clin Endocrinol Metab 89(10):4972–80CrossRefPubMed
58.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–41CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–41CrossRefPubMed
59.
go back to reference Olmos JM, Valero C, Del Barrio AG, Amado JA, Hernandez JL, Menendez-Arango J et al (2010) Time course of bone loss in patients with anorexia nervosa. Int J Eat Disord 43(6):537–42CrossRefPubMed Olmos JM, Valero C, Del Barrio AG, Amado JA, Hernandez JL, Menendez-Arango J et al (2010) Time course of bone loss in patients with anorexia nervosa. Int J Eat Disord 43(6):537–42CrossRefPubMed
60.
go back to reference Dominguez J, Goodman L, Gupta SS, Mayer L, Etu SF, Walsh BT et al (2007) Treatment of anorexia nervosa is associated with increases in bone mineral density, and recovery is a biphasic process involving both nutrition and return of menses. Am J Clin Nutr 86(1):92–9PubMed Dominguez J, Goodman L, Gupta SS, Mayer L, Etu SF, Walsh BT et al (2007) Treatment of anorexia nervosa is associated with increases in bone mineral density, and recovery is a biphasic process involving both nutrition and return of menses. Am J Clin Nutr 86(1):92–9PubMed
61.
go back to reference 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):602–6CrossRefPubMed 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):602–6CrossRefPubMed
62.
go back to reference Valla Å, Groenning I, Syversen U, Hoeiseth A (2000) Anorexia nervosa: slow regain of bone mass. Osteoporos Int 11(2):141–5CrossRefPubMed Valla Å, Groenning I, Syversen U, Hoeiseth A (2000) Anorexia nervosa: slow regain of bone mass. Osteoporos Int 11(2):141–5CrossRefPubMed
63.
64.
go back to reference Van Marken Lichtenbelt WD, Heidendal GAK, Westerterp KR (1997) Energy expenditure and physical activity in relation to bone mineral density in women with anorexia nervosa. Eur J Clin Nutr 51(12):826–30CrossRefPubMed Van Marken Lichtenbelt WD, Heidendal GAK, Westerterp KR (1997) Energy expenditure and physical activity in relation to bone mineral density in women with anorexia nervosa. Eur J Clin Nutr 51(12):826–30CrossRefPubMed
65.
go back to reference First MB. Structured clinical interview for the DSM (SCID). The Encyclopedia of Clinical Psychology. 1995 First MB. Structured clinical interview for the DSM (SCID). The Encyclopedia of Clinical Psychology. 1995
Metadata
Title
A systematic review and meta-analysis of the association between eating disorders and bone density
Authors
L. Robinson
V. Aldridge
E. M. Clark
M. Misra
N. Micali
Publication date
01-06-2016
Publisher
Springer London
Published in
Osteoporosis International / Issue 6/2016
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-015-3468-4

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