The Intestinal Microbiota in Acute Anorexia Nervosa and during Renourishment: Relationship to Depression, Anxiety, and Eating Disorder Psychopathology

Psychosomatic Medicine

Volumn 77, Issue 9, 2015, Pages 969-981

  Kleiman, Susan C ^a   Watson, Hunna J ^a,b,c,d,e   Bulik Sullivan, Emily C ^a,b,g   Huh, Eun Young ^b   Tarantino, Lisa M ^b,d   Bulik, Cynthia M ^b,f,g   Carroll, Ian M ^b  

^a IL   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c Child and Adolescent Health Service   (Australia)

^d CURTIN UNIVERSITY   (Australia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f KENYON COLLEGE   (United States)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

anorexia nervosa; anxiety; depression; eating disorders; gut brain axis; intestinal microbiota

Indexed keywords

GENOMIC DNA; RNA 16S; BACTERIAL DNA;

ADOLESCENT; ADULT; ANOREXIA NERVOSA; ANXIETY DISORDER; ARTICLE; ASSESSMENT OF HUMANS; BACILLI; BECK DEPRESSION INVENTORY; CLINICAL ARTICLE; CLOSTRIDIA; CLOSTRIDIALES; COHORT ANALYSIS; CONTROLLED STUDY; CORIOBACTERIALES; DEPRESSION; DNA ISOLATION; EATING DISORDER EXAMINATION QUESTIONNAIRE; FAECALIBACTERIUM; FECES ANALYSIS; FEMALE; GENE SEQUENCE; HOSPITAL ADMISSION; HOSPITAL DISCHARGE; HUMAN; INTESTINE FLORA; MICROBIAL DIVERSITY; NONHUMAN; PARABACTEROIDES; PRIORITY JOURNAL; PYROSEQUENCING; RUMINOCOCCACEAE; TAXONOMY; WEIGHT CONTROL; AFFECT; ANXIETY; BACTEROIDETES; BODY COMPOSITION; CASE CONTROL STUDY; COMPARATIVE STUDY; CONVALESCENCE; FECES; FEEDING BEHAVIOR; FIRMICUTES; GENETICS; ISOLATION AND PURIFICATION; LACTOBACILLUS; METHANOBREVIBACTER; MICROBIOLOGY; PHYSIOLOGY; PSYCHOLOGY; QUESTIONNAIRE; RIBOTYPING; RUMINOCOCCUS; YOUNG ADULT;

ADOLESCENT; ADULT; AFFECT; ANOREXIA NERVOSA; ANXIETY; BACTEROIDETES; BODY COMPOSITION; CASE-CONTROL STUDIES; CONVALESCENCE; DEPRESSION; DNA, BACTERIAL; FECES; FEEDING BEHAVIOR; FEMALE; FIRMICUTES; GASTROINTESTINAL MICROBIOME; HUMANS; LACTOBACILLUS; METHANOBREVIBACTER; RIBOTYPING; RUMINOCOCCUS; SURVEYS AND QUESTIONNAIRES; YOUNG ADULT;

EID: 84947488777     PISSN: 00333174     EISSN: 15347796     Source Type: Journal    
DOI: 10.1097/PSY.0000000000000247     Document Type: Article

References (85)

1. Turnbaugh PJ, Gordon JI,. The core gut microbiome, energy balance and obesity. J Physiol 2009; 587 (pt 17): 4153-8.
2. Klump KL, Bulik CM, Kaye WH, Treasure J, Tyson E,. Academy for eating disorders position paper: eating disorders are serious mental illnesses. Int J Eat Disord 2009; 42: 97-103.
3. Milner MR, McAnarney ER, Klish WJ,. Metabolic abnormalities in adolescent patients with anorexia nervosa. J Adolesc Health Care 1985; 6: 191-5.
4. Mira M, Stewart PM, Vizzard J, Abraham S,. Biochemical abnormalities in anorexia nervosa and bulimia. Ann Clin Biochem 1987; 24 (pt 1): 29-35.
5. Mont L, Castro J, Herreros B, Paré C, Azqueta M, Magriña J, Puig J, Toro J, Brugada J,. Reversibility of cardiac abnormalities in adolescents with anorexia nervosa after weight recovery. J Am Acad Child Adolesc Psychiatry 2003; 42: 808-13.
6. Nova E, Gómez-Martínez S, Morandé G, Marcos A,. Cytokine production by blood mononuclear cells from in-patients with anorexia nervosa. Br J Nutr 2002; 88: 183-8.
7. Ulger Z, Gürses D, Ozyurek AR, Arikan C, Levent E, Aydoʇdu S,. Follow-up of cardiac abnormalities in female adolescents with anorexia nervosa after refeeding. Acta Cardiol 2006; 61: 43-9.
8. Umeki S,. Biochemical abnormalities of the serum in anorexia nervosa. J Nerv Ment Dis 1988; 176: 503-6.
9. Sullivan PF,. Mortality in anorexia nervosa. Am J Psychiatry 1995; 152: 1073-4.
10. Birmingham CL, Su J, Hlynsky JA, Goldner EM, Gao M,. The mortality rate from anorexia nervosa. Int J Eat Disord 2005; 38: 143-6.
11. Hudson JI, Hiripi E, Pope HG Jr, Kessler RC,. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry 2007; 61: 348-58.
12. Papadopoulos FC, Ekbom A, Brandt L, Ekselius L,. Excess mortality, causes of death and prognostic factors in anorexia nervosa. Br J Psychiatry 2009; 194: 10-7.
13. Hart LM, Granillo MT, Jorm AF, Paxton SJ,. Unmet need for treatment in the eating disorders: a systematic review of eating disorder specific treatment seeking among community cases. Clin Psychol Rev 2011; 31: 727-35.
14. NICE. Eating disorders: core interventions in the treatment and management of anorexia nervosa, bulimia nervosa and related eating disorders. National Institute for Health and Care Excellence. 2004. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23346610. Accessed on June 4, 2013.
15. HMP. Human Microbiome Project-Core Microbiome Sampling Protocol A. Available at: http://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/GetPdf.cgi?id=phd002854.2. Accessed on June 4, 2013.
16. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 2012; 486: 215-21.
17. Sartor RB,. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008; 134: 577-94.
18. Azad MB, Kozyrskyj AL,. Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol 2012; 2012: 932072.
19. Blaser MJ,. Equilibria of humans and our indigenous microbiota affecting asthma. Proc Am Thorac Soc 2012; 9: 69-71.
20. Brar T, Nagaraj S, Mohapatra S,. Microbes and asthma: the missing cellular and molecular links. Curr Opin Pulm Med 2012; 18: 14-22.
21. Couzin-Frankel J,. Bacteria and asthma: untangling the links. Science 2010; 330: 1168-9.
22. Han MK, Huang YJ, Lipuma JJ, Boushey HA, Boucher RC, Cookson WO, Curtis JL, Erb-Downward J, Lynch SV, Sethi S, Toews GB, Young VB, Wolfgang MC, Huffnagle GB, Martinez FJ,. Significance of the microbiome in obstructive lung disease. Thorax 2012; 67: 456-63.
23. Vael C, Vanheirstraeten L, Desager KN, Goossens H,. Denaturing gradient gel electrophoresis of neonatal intestinal microbiota in relation to the development of asthma. BMC Microbiol 2011; 11: 68.
24. 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: e7125.
25. Calvani R, Miccheli A, Capuani G, Tomassini Miccheli A, Puccetti C, Delfini M, Iaconelli A, Nanni G, Mingrone G,. Gut microbiome-derived metabolites characterize a peculiar obese urinary metabotype. Int J Obes (Lond) 2010; 34: 1095-8.
26. Kootte RS, Vrieze A, Holleman F, Dallinga-Thie GM, Zoetendal EG, de Vos WM, Groen AK, Hoekstra JB, Stroes ES, Nieuwdorp M,. The therapeutic potential of manipulating gut microbiota in obesity and type 2 diabetes mellitus. Diabetes Obes Metab 2012; 14: 112-20.
27. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI,. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005; 102: 11070-5.
28. Ley RE, Turnbaugh PJ, Klein S, Gordon JI,. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444: 1022-3.
29. 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: 1027-31.
30. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI,. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 1: 6ra14.
31. Cryan JF, O'Mahony SM,. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011; 23: 187-92.
32. Fernandez-Aranda F, Pinheiro AP, Tozzi F, Thornton LM, Fichter MM, Halmi KA, Kaplan AS, Klump KL, Strober M, Woodside DB, Crow S, Mitchell J, Rotondo A, Keel P, Plotnicov KH, Berrettini WH, Kaye WH, Crawford SF, Johnson C, Brandt H, La Via M, Bulik CM,. Symptom profile of major depressive disorder in women with eating disorders. Aust N Z J Psychiatry 2007; 41: 24-31.
33. Bulik CM, Sullivan PF, Fear J, Pickering A,. Predictors of the development of bulimia nervosa in women with anorexia nervosa. J Nerv Ment Dis 1997; 185: 704-7.
34. Godart NT, Flament MF, Perdereau F, Jeammet P,. Comorbidity between eating disorders and anxiety disorders: a review. Int J Eat Disord 2002; 32: 253-70.
35. Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K,. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry 2004; 161: 2215-21.
36. Samuel BS, Gordon JI,. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A 2006; 103: 10011-6.
37. Bulik CM, Berkman ND, Brownley KA, Sedway JA, Lohr KN,. Anorexia nervosa treatment: a systematic review of randomized controlled trials. Int J Eat Disord 2007; 40: 310-20.
38. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI,. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013; 341: 1241214.
39. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M,. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012; 143: 913-6. e7.
40. 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: 1471-81.
41. Tennoune N, Chan P, Breton J, Legrand R, Chabane YN, Akkermann K, Järv A, Ouelaa W, Takagi K, Ghouzali I, Francois M, Lucas N, Bole-Feysot C, Pestel-Caron M, do Rego JC, Vaudry D, Harro J, Dé E, Déchelotte P, Fetissov SO,. Bacterial ClpB heat-shock protein, an antigen-mimetic of the anorexigenic peptide <-MSH, at the origin of eating disorders. Transl Psychiatry 2014; 4: e458.
42. Pickard JM, Maurice CF, Kinnebrew MA, Abt MC, Schenten D, Golovkina TV, Bogatyrev SR, Ismagilov RF, Pamer EG, Turnbaugh PJ, Chervonsky AV,. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 2014; 514: 638-41.
43. Carroll IM, Ringel-Kulka T, Siddle JP, Ringel Y,. Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 2012; 24: 521-30,. e248.
44. Cooper Z, Fairburn C,. The eating disorders examination: a semi-structured interview for the assessment of the specific psychopathology of eating disorders. Int J Eat Disord 1987; 6: 1-8.
45. First M, Spitzer R, Gibbon M, Williams J,. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. New York: New York State Psychiatric Institute; 2002.
46. Steer RA, Rissmiller DJ, Ranieri WF, Beck AT,. Structure of the computer-assisted Beck Anxiety Inventory with psychiatric inpatients. J Pers Assess 1993; 60: 532-42.
47. Steer RA, Ball R, Ranieri WF, Beck AT,. Dimensions of the Beck Depression Inventory-II in clinically depressed outpatients. J Clin Psychol 1999; 55: 117-28.
48. Luce KH, Crowther JH,. The reliability of the Eating Disorder Examination-Self-Report Questionnaire Version (EDE-Q). Int J Eat Disord 1999; 25: 349-51.
49. Carroll IM, Ringel-Kulka T, Keku TO, Chang YH, Packey CD, Sartor RB, Ringel Y,. Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2011; 301: G799-807.
50. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R,. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335-6.
51. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R,. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 2008; 5: 235-7.
52. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P,. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012; 6: 610-8.
53. Lozupone C, Knight R,. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71: 8228-35.
54. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R,. UniFrac: an effective distance metric for microbial community comparison. ISME J 2011; 5: 169-72.
55. Lozupone CA, Hamady M, Kelley ST, Knight R,. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 2007; 73: 1576-85.
56. Chao A, Colwell RK, Lin CW, Gotelli NJ,. Sufficient sampling for asymptotic minimum species richness estimators. Ecology 2009; 90: 1125-33.
57. Preheim SP, Perrotta AR, Martin-Platero AM, Gupta A, Alm EJ,. Distribution-based clustering: using ecology to refine the operational taxonomic unit. Appl Environ Microbiol 2013; 79: 6593-603.
58. Benjamini Y, Hochberg Y,. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995; 57: 289-300.
59. Chi YY, Gribbin M, Lamers Y, Gregory JF 3rd, Muller KE,. Global hypothesis testing for high-dimensional repeated measures outcomes. Stat Med 2012; 31: 724-42.
60. Beck JG, Stanley MA, Zebb BJ,. Characteristics of generalized anxiety disorder in older adults: a descriptive study. Behav Res Ther 1996; 34: 225-34.
61. Aardoom JJ, Dingemans AE, Slof Op't Landt MC, Van Furth EF,. Norms and discriminative validity of the Eating Disorder Examination Questionnaire (EDE-Q). Eat Behav 2012; 13: 305-9.
62. Welch E, Birgegård A, Parling T, Ghaderi A,. Eating disorder examination questionnaire and clinical impairment assessment questionnaire: general population and clinical norms for young adult women in Sweden. Behav Res Ther 2011; 49: 85-91.
63. Berry D, Reinisch W,. Intestinal microbiota: a source of novel biomarkers in inflammatory bowel diseases? Best Pract Res Clin Gastroenterol 2013; 27: 47-58.
64. Rajilić-Stojanović M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, Tims S, de Vos WM,. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 2011; 141: 1792-801.
65. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, Marmon S, Neimann A, Brusca S, Patel T, Manasson J, Pamer EG, Littman DR, Abramson SB,. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015; 67: 128-39.
66. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, Liu J, Houpt E, Li JV, Holmes E, Nicholson J, Knights D, Ursell LK, Knight R, Gordon JI,. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013; 339: 548-54.
67. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD, Barratt MJ, VanArendonk LG, Zhang Q, Province MA, Petri WA Jr, Ahmed T, Gordon JI,. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 2014; 510: 417-21.
68. Ahmed T, Auble D, Berkley JA, Black R, Ahern PP, Hossain M, Hsieh A, Ireen S, Arabi M, Gordon JI,. An evolving perspective about the origins of childhood undernutrition and nutritional interventions that includes the gut microbiome. Ann N Y Acad Sci 2014; 1332: 22-38.
69. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S,. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108: 3047-52.
70. Neufeld KM, Kang N, Bienenstock J, Foster JA,. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2011; 23: 255-64,. e119.
71. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF,. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2013; 18: 666-73.
72. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J, McCoy KD, Verdu EF, Collins SM,. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011; 141: 599-609,. e1-3.
73. Barden N,. Implication of the hypothalamic-pituitary-adrenal axis in the physiopathology of depression. J Psychiatry Neurosci 2004; 29: 185-93.
74. Heuser IJ, Schweiger U, Gotthardt U, Schmider J, Lammers CH, Dettling M, Yassouridis A, Holsboer F,. Pituitary-adrenal-system regulation and psychopathology during amitriptyline treatment in elderly depressed patients and normal comparison subjects. Am J Psychiatry 1996; 153: 93-9.
75. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y,. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558 (pt 1): 263-75.
76. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF,. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108: 16050-5.
77. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG,. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-88.
78. Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, Rudi K,. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil 2014; 26: 1155-62.
79. Foster JA, McVey Neufeld KA,. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 2013; 36: 305-12.
80. Rees JC,. Obsessive-compulsive disorder and gut microbiota dysregulation. Med Hypotheses 2014; 82: 163-6.
81. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD,. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-8.
82. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P,. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010; 107: 14691-6.
83. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ,. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559-63.
84. Hoek HW,. Incidence, prevalence and mortality of anorexia nervosa and other eating disorders. Curr Opin Psychiatry 2006; 19: 389-94.
85. Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, Valero R, Vialettes B, Raoult D,. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes (Lond) 2013; 37: 1460-6.