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Current Osteoporosis Reports

Published in:

01-02-2018 | Secondary Causes of Osteoporosis (S Warden, Section Editor)

Linking the Gut Microbiota to Bone Health in Anorexia Nervosa

Authors: Nicole C. Aurigemma, Kristen J. Koltun, Hannah VanEvery, Connie J. Rogers, Mary Jane De Souza

Published in: Current Osteoporosis Reports | Issue 1/2018

Abstract

Purpose of Review

The purpose of this review is to examine the anorexia nervosa-microbiota-bone relationship, offering a compilation of the relevant human and animal studies that may contribute to a more comprehensive understanding of potential mechanisms involved.

Recent Findings

Recent studies have implicated fermentation by-products of the gut microbiota in bone metabolism.

Summary

Compromised bone health often accompanies anorexia nervosa due to energy deficiency and hypoestrogenism. The gut microbiome has been implicated as a link between these conditions and impaired bone growth phenotypes. Current research supports decrements in Firmicutes and short-chain fatty acids with increases in Methanobrevibacter smithii and Proteobacteria in anorexia nervosa. A potential mechanism for microbiome-regulated bone growth is through modulation of insulin-like growth factor-1. Future research should aim to examine short-chain fatty acids, probiotics, and prebiotics as alternative therapies to treat low bone density in anorexia nervosa.

van de Wouw M, Schellekens H, Dinan TG, Cryan JF. Microbiota-gut-brain axis: modulator of host metabolism and appetite. J Nutr. 2017;147(5):727–45. https://doi.org/10.3945/jn.116.240481.CrossRefPubMed

Carr J, Kleiman SC, Bulik CM, Bulik-Sullivan EC, Carroll IM. Can attention to the intestinal microbiota improve understanding and treatment of anorexia nervosa? Expert Rev Gastroenterol Hepatol. 2016;10(5):565–9. https://doi.org/10.1586/17474124.2016.1166953.CrossRefPubMedPubMedCentral

Herpertz-Dahlmann B, Seitz J, Baines J. Food matters: how the microbiome and gut-brain interaction might impact the development and course of anorexia nervosa. Eur Child Adolesc Psychiatry. 2017;26(9):1031–41. https://doi.org/10.1007/s00787-017-0945-7.CrossRefPubMedPubMedCentral

Legroux-Gerot I, Vignau J, D'Herbomez M, Collier F, Marchandise X, Duquesnoy B, et al. Evaluation of bone loss and its mechanisms in anorexia nervosa. Calcif Tissue Int. 2007;81(3):174–82. https://doi.org/10.1007/s00223-007-9038-9.CrossRefPubMed

Klibanski A, Biller BM, 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(3):898–904. https://doi.org/10.1210/jcem.80.3.7883849.PubMed

Herzog W, Minne H, Deter C, Leidig G, Schellberg D, Wuster C, et al. Outcome of bone mineral density in anorexia nervosa patients 11.7 years after first admission. J Bone Miner Res. 1993;8(5):597–605. https://doi.org/10.1002/jbmr.5650080511.CrossRefPubMed

Herzog W, Deter HC, Fiehn W, Petzold E. Medical findings and predictors of long-term physical outcome in anorexia nervosa: a prospective, 12-year follow-up study. Psychol Med. 1997;27(2):269–79. https://doi.org/10.1017/S0033291796004394.CrossRefPubMed

Bachrach LK, Katzman DK, Litt IF, Guido D, Marcus R. Recovery from osteopenia in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab. 1991;72(3):602–6. https://doi.org/10.1210/jcem-72-3-602.CrossRefPubMed

Grinspoon S, Thomas E, Pitts S, Gross E, Mickley D, Miller K, et al. Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med. 2000;133(10):790–4. https://doi.org/10.7326/0003-4819-133-10-200011210-00011.CrossRefPubMedPubMedCentral

10.

Soyka LA, Grinspoon S, Levitsky LL, Herzog DB, Klibanski A. The effects of anorexia nervosa on bone metabolism in female adolescents. J Clin Endocrinol Metab. 1999;84(12):4489–96. https://doi.org/10.1210/jcem.84.12.6207.PubMed

11.

Grinspoon S, Thomas L, Miller K, Herzog D, Klibanski A. Effects of recombinant human IGF-I and oral contraceptive administration on bone density in anorexia nervosa. J Clin Endocrinol Metab. 2002;87(6):2883–91. https://doi.org/10.1210/jcem.87.6.8574.CrossRefPubMed

12.

Rigotti NA, Neer RM, Skates SJ, Herzog DB, Nussbaum SR. The clinical course of osteoporosis in anorexia nervosa. A longitudinal study of cortical bone mass. JAMA. 1991;265(9):1133–8. https://doi.org/10.1001/jama.1991.03460090081037.CrossRefPubMed

13.

Lucas AR, Melton LJ 3rd, Crowson CS, O’Fallon WM. Long-term fracture risk among women with anorexia nervosa: a population-based cohort study. Mayo Clin Proc. 1999;74(10):972–7. https://doi.org/10.1016/S0025-6196(11)63994-3.CrossRefPubMed

14.

Scheid JL, De Souza MJ. Menstrual irregularities and energy deficiency in physically active women: the role of ghrelin, PYY and adipocytokines. Med Sport Sci. 2010;55:82–102. https://doi.org/10.1159/000321974.CrossRefPubMed

15.

Fourman LT, Fazeli PK. Neuroendocrine causes of amenorrhea—an update. J Clin Endocrinol Metab. 2015;100(3):812–24. https://doi.org/10.1210/jc.2014-3344.CrossRefPubMedPubMedCentral

16.

Association AP. Diagnostic and statistical manual of mental disorders. Fifth ed. Arlington: American Psychiatric Association; 2013. https://doi.org/10.1176/appi.books.9780890425596.

17.

Baker JH, Sisk CL, Thornton LM, Brandt H, Crawford S, Fichter MM, et al. Primary amenorrhea in anorexia nervosa: impact on characteristic masculine and feminine traits. Eur Eat Disord Rev. 2014;22(1):32–8. https://doi.org/10.1002/erv.2263.CrossRefPubMed

18.

Poyastro Pinheiro A, Thornton LM, Plotonicov KH, Tozzi F, Klump KL, Berrettini WH, et al. Patterns of menstrual disturbance in eating disorders. Int J Eat Disord. 2007;40(5):424–34. https://doi.org/10.1002/eat.20388.CrossRefPubMed

19.

Nakamura T, Imai Y, Matsumoto T, Sato S, Takeuchi K, Igarashi K, et al. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell. 2007;130(5):811–23. https://doi.org/10.1016/j.cell.2007.07.025.CrossRefPubMed

20.

VanHouten JN, Wysolmerski JJ. Low estrogen and high parathyroid hormone-related peptide levels contribute to accelerated bone resorption and bone loss in lactating mice. Endocrinology. 2003;144(12):5521–9. https://doi.org/10.1210/en.2003-0892.CrossRefPubMed

21.

Brennan O, Kuliwaba JS, Lee TC, Parkinson IH, Fazzalari NL, McNamara LM, et al. Temporal changes in bone composition, architecture, and strength following estrogen deficiency in osteoporosis. Calcif Tissue Int. 2012;91(6):440–9. https://doi.org/10.1007/s00223-012-9657-7.CrossRefPubMed

22.

De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone. 2008;43(1):140–8. https://doi.org/10.1016/j.bone.2008.03.013.CrossRefPubMed

23.

Olson LE, Ohlsson C, Mohan S. The role of GH/IGF-I-mediated mechanisms in sex differences in cortical bone size in mice. Calcif Tissue Int. 2011;88(1):1–8.CrossRefPubMed

24.

Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO. Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell. 2008;7(5):681–7. https://doi.org/10.1111/j.1474-9726.2008.00417.x.CrossRefPubMedPubMedCentral

25.

Grinspoon S, Baum H, Lee K, Anderson E, Herzog D, Klibanski A. Effects of short-term recombinant human insulin-like growth factor I administration on bone turnover in osteopenic women with anorexia nervosa. J Clin Endocrinol Metab. 1996;81(11):3864–70. https://doi.org/10.1210/jcem.81.11.8923830.PubMed

26.

Yakar S, Canalis E, Sun H, Mejia W, Kawashima Y, Nasser P, et al. Serum IGF-1 determines skeletal strength by regulating subperiosteal expansion and trait interactions. J Bone Miner Res. 2009;24(8):1481–92. https://doi.org/10.1359/jbmr.090226.CrossRefPubMedPubMedCentral

27.

Sjögren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, et al. The gut microbiota regulates bone mass in mice. J Bone Miner Res. 2012;27(6):1357–67. https://doi.org/10.1002/jbmr.1588.CrossRefPubMedPubMedCentral

28.

Li JY, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, et al. Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest. 2016;126(6):2049–63. https://doi.org/10.1172/JCI86062.CrossRefPubMedPubMedCentral

29.

Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–21. https://doi.org/10.1038/nature13421.CrossRefPubMedPubMedCentral

30.

Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351(6275):aad3311. https://doi.org/10.1126/science.aad3311.CrossRefPubMed

31.

Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339(6119):548–54. https://doi.org/10.1126/science.1229000.CrossRefPubMedPubMedCentral

32.

Inui A, Chen CY, Meguid M. Microbiome, peptide autoantibodies, and eating disorders: a missing link between gut and brain. Nutrition. 2015;31(3):544–5. https://doi.org/10.1016/j.nut.2015.01.007.CrossRefPubMed

33.

Kleiman SC, Carroll IM, Tarantino LM, Bulik CM. Gut feelings: a role for the intestinal microbiota in anorexia nervosa? Int J Eat Disord. 2015;48(5):449–51. https://doi.org/10.1002/eat.22394.CrossRefPubMedPubMedCentral

34.

D'Argenio V, Salvatore F. The role of the gut microbiome in the healthy adult status. Clin Chim Acta. 2015;451(Pt A):97–102.CrossRefPubMed

35.

Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–41. https://doi.org/10.1016/j.cell.2014.03.011.CrossRefPubMedPubMedCentral

36.

Barlow GM, Yu A, Mathur R. Role of the gut microbiome in obesity and diabetes mellitus. Nutr Clin Pract. 2015;30(6):787–97. https://doi.org/10.1177/0884533615609896.CrossRefPubMed

37.

Garrett WS. Cancer and the microbiota. Science. 2015;348(6230):80–6.CrossRefPubMedPubMedCentral

38.

Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–8. https://doi.org/10.1126/science.1110591.CrossRefPubMedPubMedCentral

39.

Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab. 2015;26(9):493–501.CrossRefPubMedPubMedCentral

40.

Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–5. https://doi.org/10.1073/pnas.0504978102.CrossRefPubMedPubMedCentral

41.

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31. https://doi.org/10.1038/nature05414.CrossRefPubMed

42.

Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One. 2009;4(9):e7125. https://doi.org/10.1371/journal.pone.0007125.CrossRefPubMedPubMedCentral

43.

Mack I, Cuntz U, Gramer C, Niedermaier S, Pohl C, Schwiertz A, et al. Weight gain in anorexia nervosa does not ameliorate the faecal microbiota, branched chain fatty acid profiles, and gastrointestinal complaints. Sci Rep. 2016;6(26752) https://doi.org/10.1038/srep26752.

44.

Zhu Y, Niu Q, Shi C, Wang J, Zhu W. The role of microbiota in compensatory growth of protein-restricted rats. Microb Biotechnol. 2017;10(2):480–91. https://doi.org/10.1111/1751-7915.12451.CrossRefPubMed

45.

• Queipo-Ortuno MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One. 2013;8(5):e65465. This is the first study to examine the microbial changes associated with a model of activity-based anorexia.CrossRefPubMedPubMedCentral

46.

Morita C, Tsuji H, Hata T, Gondo M, Takakura S, Kawai K, et al. Gut dysbiosis in patients with anorexia nervosa. PLoS One. 2015;10(12):e0145274. https://doi.org/10.1371/journal.pone.0145274.CrossRefPubMedPubMedCentral

47.

Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, Valero R, et al. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes. 2013;37(11):1460–6. https://doi.org/10.1038/ijo.2013.20.CrossRef

48.

Borgo F, Riva A, Benetti A, Casiraghi MC, Bertelli S, Garbossa S, et al. Microbiota in anorexia nervosa: the triangle between bacterial species, metabolites and psychological tests. PLoS One. 2017;12(6):e0179739. https://doi.org/10.1371/journal.pone.0179739.CrossRefPubMedPubMedCentral

49.

Kleiman SC, Watson HJ, Bulik-Sullivan EC, Huh EY, Tarantino LM, Bulik CM, et al. The intestinal microbiota in acute anorexia nervosa and during renourishment: relationship to depression, anxiety, and eating disorder psychopathology. Psychosom Med. 2015;77(9):969–81. https://doi.org/10.1097/PSY.0000000000000247.CrossRefPubMedPubMedCentral

50.

Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62(1):67–72. https://doi.org/10.1079/PNS2002207.CrossRefPubMed

51.

Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91–119. https://doi.org/10.1016/B978-0-12-800100-4.00003-9.CrossRefPubMed

52.

Suzuki T, Yoshida S, Hara H. Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr. 2008;100(2):297–305.CrossRefPubMed

53.

Sahakian AB, Jee SR, Pimentel M. Methane and the gastrointestinal tract. Dig Dis Sci. 2010;55(8):2135–43. https://doi.org/10.1007/s10620-009-1012-0.CrossRefPubMed

54.

Flourie B, Etanchaud F, Florent C, Pellier P, Bouhnik Y, Rambaud JC. Comparative study of hydrogen and methane production in the human colon using caecal and faecal homogenates. Gut. 1990;31(6):684–5. https://doi.org/10.1136/gut.31.6.684.CrossRefPubMedPubMedCentral

55.

Million M, Maraninchi M, Henry M, Armougom F, Richet H, Carrieri P, et al. Obesity-associated gut microbiota is enriched in lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes. 2012;36(6):817–25. https://doi.org/10.1038/ijo.2011.153.CrossRef

56.

• Tennoune N, Chan P, Breton J, Legrand R, Chabane YN, Akkermann K, et al. Bacterial ClpB heat-shock protein, an antigen-mimetic of the anorexigenic peptide alpha-MSH, at the origin of eating disorders. Transl Psychiatry. 2014;4:e458. This is the first study implicating the E. coli by-product, ClpB, as a suppressor of appetite.CrossRefPubMedPubMedCentral

57.

Breton J, Legrand R, Akkermann K, Jarv A, Harro J, Dechelotte P, et al. Elevated plasma concentrations of bacterial ClpB protein in patients with eating disorders. Int J Eat Disord. 2016;49(8):805–8. https://doi.org/10.1002/eat.22531.CrossRefPubMed

58.

Cone RD. Anatomy and regulation of the central melanocortin system. Nat Neurosci. 2005;8(5):571–8. https://doi.org/10.1038/nn1455.CrossRefPubMed

59.

Fetissov SO, Hallman J, Oreland L, Af Klinteberg B, Grenback E, Hulting AL, et al. Autoantibodies against alpha -MSH, ACTH, and LHRH in anorexia and bulimia nervosa patients. Proc Natl Acad Sci U S A. 2002;99(26):17155–60. https://doi.org/10.1073/pnas.222658699.CrossRefPubMedPubMedCentral

60.

Breton J, Tennoune N, Lucas N, Francois M, Legrand R, Jacquemot J, et al. Gut commensal E. coli proteins activate host satiety pathways following nutrient-induced bacterial growth. Cell Metab. 2016;23(2):324–34. https://doi.org/10.1016/j.cmet.2015.10.017.CrossRefPubMed

61.

Ohlsson C, Sjögren K. Effects of the gut microbiota on bone mass. Trends Endocrinol Metab. 2015;26(2):69–74. https://doi.org/10.1016/j.tem.2014.11.004.CrossRefPubMed

62.

Jones RM, Mulle JG, Pacifici R. Osteomicrobiology: the influence of gut microbiota on bone in health and disease. Bone. 2017; https://doi.org/10.1016/j.bone.2017.04.009.

63.

•• Yan J, Herzog JW, Tsang K, Brennan CA, Bower MA, Garrett WS, et al. Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci U S A. 2016;113(47):E7554–E63. This is the first study to link the gut microbiota to IGF-1, through SCFAs. Additionally, this study demonstrates the differences in short-term versus long-term colonization of GF mice with regard to microbiota-mediated bone remodeling.CrossRefPubMedPubMedCentral

64.

Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science. 2016;351(6275):854–7. https://doi.org/10.1126/science.aad8588.CrossRefPubMed

65.

Allaway HC, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Horm Mol Biol Clin Investig. 2016;25(2):91–119. https://doi.org/10.1515/hmbci-2015-0053.PubMed

66.

De Souza MJ, Toombs RJ, Scheid JL, O’Donnell E, West SL, Williams NI. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod. 2010;25(2):491–503. https://doi.org/10.1093/humrep/dep411.CrossRefPubMed

67.

Melville KM, Kelly NH, Khan SA, Schimenti JC, Ross FP, Main RP, et al. Female mice lacking estrogen receptor-alpha in osteoblasts have compromised bone mass and strength. J Bone Miner Res. 2014;29(2):370–9. https://doi.org/10.1002/jbmr.2082.CrossRefPubMed

68.

Tivesten A, Moverare-Skrtic S, Chagin A, Venken K, Salmon P, Vanderschueren D, et al. Additive protective effects of estrogen and androgen treatment on trabecular bone in ovariectomized rats. J Bone Miner Res. 2004;19(11):1833–9. https://doi.org/10.1359/JBMR.040819.CrossRefPubMed

69.

Mohan S, Bhat CG, Wergedal JE, Kesavan C. In vivo evidence of IGF-I-estrogen crosstalk in mediating the cortical bone response to mechanical strain. Bone Res. 2014;2:14007. https://doi.org/10.1038/boneres.2014.7.CrossRefPubMedPubMedCentral

70.

Pacifici R. Estrogen deficiency, T cells and bone loss. Cell Immunol. 2008;252(1–2):68–80. https://doi.org/10.1016/j.cellimm.2007.06.008.CrossRefPubMed

71.

Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, et al. Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One. 2014;9(3):e92368. https://doi.org/10.1371/journal.pone.0092368.CrossRefPubMedPubMedCentral

72.

Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, et al. Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol. 2014;229(11):1822–30. https://doi.org/10.1002/jcp.24636.CrossRefPubMedPubMedCentral

73.

• Jafarnejad S, Djafarian K, Fazeli MR, Yekaninejad MS, Rostamian A, Keshavarz SA. Effects of a multispecies probiotic supplement on bone health in osteopenic postmenopausal women: a randomized, double-blind, controlled trial. J Am Coll Nutr. 2017;36(7):497–506. This is the first clinical trial to examine the effects of probiotics on bone markers and BMD. https://doi.org/10.1080/07315724.2017.1318724.CrossRefPubMed

74.

Weaver CM. Diet, gut microbiome, and bone health. Curr Osteoporos Rep. 2015;13(2):125–30. https://doi.org/10.1007/s11914-015-0257-0.CrossRefPubMedPubMedCentral

75.

Weitkunat K, Schumann S, Petzke KJ, Blaut M, Loh G, Klaus S. Effects of dietary inulin on bacterial growth, short-chain fatty acid production and hepatic lipid metabolism in gnotobiotic mice. J Nutr Biochem. 2015;26(9):929–37. https://doi.org/10.1016/j.jnutbio.2015.03.010.CrossRefPubMed

76.

Weaver CM, Martin BR, Nakatsu CH, Armstrong AP, Clavijo A, McCabe LD, et al. Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J Agric Food Chem. 2011;59(12):6501–10. https://doi.org/10.1021/jf2009777.CrossRefPubMed

77.

Whisner CM, Martin BR, Schoterman MH, Nakatsu CH, McCabe LD, McCabe GP, et al. Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr. 2013;110(7):1292–303. https://doi.org/10.1017/S000711451300055X.CrossRefPubMed

78.

Whisner CM, Martin BR, Nakatsu CH, McCabe GP, McCabe LD, Peacock M, et al. Soluble maize fibre affects short-term calcium absorption in adolescent boys and girls: a randomised controlled trial using dual stable isotopic tracers. Br J Nutr. 2014;112(3):446–56. https://doi.org/10.1017/S0007114514000981.CrossRefPubMed

79.

Whisner CM, Martin BR, Nakatsu CH, Story JA, MacDonald-Clarke CJ, McCabe LD, et al. Soluble corn fiber increases calcium absorption associated with shifts in the gut microbiome: arandomized dose-response trial in free-living pubertal females. J Nutr. 2016;146(7):1298–306. https://doi.org/10.3945/jn.115.227256.CrossRefPubMed

80.

Weaver CM, Martin BR, Story JA, Hutchinson I, Sanders L. Novel fibers increase bone calcium content and strength beyond efficiency of large intestine fermentation. J Agric Food Chem. 2010;58(16):8952–7. https://doi.org/10.1021/jf904086d.CrossRefPubMed

81.

Chen J, Toyomasu Y, Hayashi Y, Linden DR, Szurszewski JH, Nelson H, et al. Altered gut microbiota in female mice with persistent low body weights following removal of post-weaning chronic dietary restriction. Genome Med. 2016;8(1):103. https://doi.org/10.1186/s13073-016-0357-1.CrossRefPubMedPubMedCentral

82.

Gouba N, Raoult D, Drancourt M. Gut microeukaryotes during anorexia nervosa: a case report. BMC Res Notes. 2014;7(1):33. https://doi.org/10.1186/1756-0500-7-33.CrossRefPubMedPubMedCentral

83.

Pfleiderer A, Lagier JC, Armougom F, Robert C, Vialettes B, Raoult D. Culturomics identified 11 new bacterial species from a single anorexia nervosa stool sample. Eur J Clin Microbiol Infect Dis. 2013;32(11):1471–81. https://doi.org/10.1007/s10096-013-1900-2.CrossRefPubMed

84.

Kleiman SC, Glenny EM, Bulik-Sullivan EC, Huh EY, Tsilimigras MCB, Fodor AA, et al. Daily changes in composition and diversity of the intestinal microbiota in patients with anorexia nervosa: a series of three cases. Eur Eat Disord Rev. 2017;25(5):423–7. https://doi.org/10.1002/erv.2524.CrossRefPubMed

85.

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63. https://doi.org/10.1038/nature12820.CrossRefPubMed

86.

Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–8. https://doi.org/10.1126/science.1208344.CrossRefPubMedPubMedCentral

87.

Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun. 2014;5(4500) https://doi.org/10.1038/ncomms5500.

88.

Tennoune N, Legrand R, Ouelaa W, Breton J, Lucas N, Bole-Feysot C, et al. Sex-related effects of nutritional supplementation of Escherichia coli: relevance to eating disorders. Nutrition. 2015;31(3):498–507. https://doi.org/10.1016/j.nut.2014.11.003.CrossRefPubMed

89.

Lucas AR, Beard CM, O'Fallon WM, Kurland LT. 50-year trends in the incidence of anorexia nervosa in Rochester, Minn.: a population-based study. Am J Psychiatry. 1991;148(7):917–22. https://doi.org/10.1176/ajp.148.7.917.CrossRefPubMed

90.

Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe. 2011;10(4):324–35. https://doi.org/10.1016/j.chom.2011.10.003.CrossRefPubMedPubMedCentral

91.

Jarvenpaa P, Kosunen T, Fotsis T, Adlercreutz H. In vitro metabolism of estrogens by isolated intestinal micro-organisms and by human faecal microflora. J Steroid Biochem. 1980;13(3):345–9. https://doi.org/10.1016/0022-4731(80)90014-X.CrossRefPubMed

92.

Cole CB, Fuller R, Mallet AK, Rowland IR. The influence of the host on expression of intestinal microbial enzyme activities involved in metabolism of foreign compounds. J Appl Bacteriol. 1985;59(6):549–53. https://doi.org/10.1111/j.1365-2672.1985.tb03359.x.CrossRefPubMed

93.

Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas. 2017;103:45–53. https://doi.org/10.1016/j.maturitas.2017.06.025.CrossRefPubMed

94.

Hebebrand J, Exner C, Hebebrand K, Holtkamp C, Casper RC, Remschmidt H, et al. Hyperactivity in patients with anorexia nervosa and in semistarved rats: evidence for a pivotal role of hypoleptinemia. Physiol Behav. 2003;79(1):25–37. https://doi.org/10.1016/S0031-9384(03)00102-1.CrossRefPubMed

95.

Zipfel S, Mack I, Baur LA, Hebebrand J, Touyz S, Herzog W, et al. Impact of exercise on energy metabolism in anorexia nervosa. J Eat Disord. 2013;1(1):37. https://doi.org/10.1186/2050-2974-1-37.CrossRefPubMedPubMedCentral

96.

Dalle Grave R, Calugi S, Marchesini G. Compulsive exercise to control shape or weight in eating disorders: prevalence, associated features, and treatment outcome. Compr Psychiatry. 2008;49(4):346–52. https://doi.org/10.1016/j.comppsych.2007.12.007.CrossRefPubMed

97.

Kang SS, Jeraldo PR, Kurti A, Miller ME, Cook MD, Whitlock K, et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Mol Neurodegener. 2014;9(1):36. https://doi.org/10.1186/1750-1326-9-36.CrossRefPubMedPubMedCentral

98.

Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63(12):1913–20. https://doi.org/10.1136/gutjnl-2013-306541.CrossRefPubMed

99.

Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, Matsubara N, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008;72(2):572–6. https://doi.org/10.1271/bbb.70474.CrossRefPubMed

100.

Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–6. https://doi.org/10.1038/nature12506.CrossRefPubMed

101.

Klenotich SJ, Dulawa SC. The activity-based anorexia mouse model: Humana Press; 2012.

Title: Linking the Gut Microbiota to Bone Health in Anorexia Nervosa
Authors: Nicole C. Aurigemma
Kristen J. Koltun
Hannah VanEvery
Connie J. Rogers
Mary Jane De Souza
Publication date: 01-02-2018
Publisher: Springer US
Published in: Current Osteoporosis Reports / Issue 1/2018
Print ISSN: 1544-1873
Electronic ISSN: 1544-2241
DOI: https://doi.org/10.1007/s11914-018-0420-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Linking the Gut Microbiota to Bone Health in Anorexia Nervosa

Abstract

Purpose of Review

Recent Findings

Summary

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose of Review

Recent Findings

Summary

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