• This record comes from PubMed

Current Aspects of the Role of Autoantibodies Directed Against Appetite-Regulating Hormones and the Gut Microbiome in Eating Disorders

. 2021 ; 12 () : 613983. [epub] 20210419

Language English Country Switzerland Media electronic-ecollection

Document type Journal Article, Research Support, Non-U.S. Gov't, Review

The equilibrium and reciprocal actions among appetite-stimulating (orexigenic) and appetite-suppressing (anorexigenic) signals synthesized in the gut, brain, microbiome and adipose tissue (AT), seems to play a pivotal role in the regulation of food intake and feeding behavior, anxiety, and depression. A dysregulation of mechanisms controlling the energy balance may result in eating disorders such as anorexia nervosa (AN) and bulimia nervosa (BN). AN is a psychiatric disease defined by chronic self-induced extreme dietary restriction leading to an extremely low body weight and adiposity. BN is defined as out-of-control binge eating, which is compensated by self-induced vomiting, fasting, or excessive exercise. Certain gut microbiota-related compounds, like bacterial chaperone protein Escherichia coli caseinolytic protease B (ClpB) and food-derived antigens were recently described to trigger the production of autoantibodies cross-reacting with appetite-regulating hormones and neurotransmitters. Gut microbiome may be a potential manipulator for AT and energy homeostasis. Thus, the regulation of appetite, emotion, mood, and nutritional status is also under the control of neuroimmunoendocrine mechanisms by secretion of autoantibodies directed against neuropeptides, neuroactive metabolites, and peptides. In AN and BN, altered cholinergic, dopaminergic, adrenergic, and serotonergic relays may lead to abnormal AT, gut, and brain hormone secretion. The present review summarizes updated knowledge regarding the gut dysbiosis, gut-barrier permeability, short-chain fatty acids (SCFA), fecal microbial transplantation (FMT), blood-brain barrier permeability, and autoantibodies within the ghrelin and melanocortin systems in eating disorders. We expect that the new knowledge may be used for the development of a novel preventive and therapeutic approach for treatment of AN and BN.

See more in PubMed

Hsu LK. Epidemiology of the eating disorders. Psychiatr Clin North Am (1996) 19:681–700c. 10.1016/S0193-953X(05)70375-0 PubMed DOI

Arcelus J, Mitchell AJ, Wales J, Nielsen S. Mortality rates in patients with anorexia nervosa and other eating disorders. A meta-analysis of 36 studies. Arch Gen Psychiatry (2011) 68:724–31. 10.1001/archgenpsychiatry.2011.74 PubMed DOI

American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders, 5th ed. (DSM-5R ). 5th ed. Washington, DC: American Psychiatric Association Publishing; (2013). 10.1176/appi.books.9780890425596 DOI

Fetissov SO, Hallman J, Oreland L, Af Klinteberg B, Grenbäck 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. 10.1073/pnas.222658699 PubMed DOI PMC

Raevuori A, Haukka J, Vaarala O, Suvisaari JM, Gissler M, Grainger M, et al. . The increased risk for autoimmune diseases in patients with eating disorders. PloS One (2014) 9(8):e104845. 10.1371/journal.pone.0104845 PubMed DOI PMC

Takii M, Uchigata Y, Kishimoto J, Morita C, Hata T, Nozaki T, et al. . The relationship between the age of onset of type 1 diabetes and the subsequent development of a severe eating disorder by female patients. Pediatr Diabetes (2011) 12:396–401. 10.1111/j.1399-5448.2010.00708.x PubMed DOI

Hedman A, Breithaupt L, Hübel C, Thornton LM, Tillander A, Norring C, et al. . Bidirectional relationship between eating disorders and autoimmune diseases. J Child Psychol Psychiatry (2019) 60:803–12. 10.1111/jcpp.12958 PubMed DOI

Zerwas S, Larsen JT, Petersen L, Thornton LM, Quaranta M, Koch SV, et al. . Eating Disorders, Autoimmune, and Autoinflammatory Disease. Pediatrics (2017) 140:e20162089. 10.1542/peds.2016-2089 PubMed DOI PMC

Hommer RE, Swedo SE. Anorexia and Autoimmunity: Challenging the Etiologic Constructs of Disordered Eating. Pediatrics (2017) 140:e20173060. 10.1542/peds.2017-3060 PubMed DOI PMC

Watson HJ, Yilmaz Z, Thornton LM, Hübel C, Coleman JRI, Gaspar HA, et al. . Genome-wide association study identifies eight risk loci and implicates metabo-psychiatric origins for anorexia nervosa. Nat Genet (2019) 51:1207–14. 10.1038/s41588-019-0439-2 PubMed DOI PMC

Periyasamy S, John S, Padmavati R, Rajendren P, Thirunavukkarasu P, Gratten J, et al. . Association of Schizophrenia Risk With Disordered Niacin Metabolism in an Indian Genome-wide Association Study. JAMA Psychiatry (2019) 76:1026–36. 10.1001/jamapsychiatry.2019.1335 PubMed DOI PMC

Portale S, Sculati M, Sanford FC, Cena H. Pellagra and anorexia nervosa: a case report. Eat Weight Disord (2020) 25:1493–96. 10.1007/s40519-019-00781-x PubMed DOI PMC

Haleem DJ. Improving therapeutics in anorexia nervosa with tryptophan. Life Sci (2017) 178:87–93. 10.1016/j.lfs.2017.04.015 PubMed DOI

Roubalová R, Procházková P, Papežová H, Smitka K, Bilej M, Tlaskalová-Hogenová H. Anorexia nervosa: Gut microbiota-immune-brain interactions. Clin Nutr (2020) 39:676–84. 10.1016/j.clnu.2019.03.023 PubMed DOI

Cryan JF, O’Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, et al. . The Microbiota-Gut-Brain Axis. Physiol Rev (2019) 99:1877–2013. 10.1152/physrev.00018.2018 PubMed DOI

Lundgren P, Thaiss CA. The microbiome-adipose tissue axis in systemic metabolism. Am J Physiol Gastrointest Liver Physiol (2020) 318(4):G717–24. 10.1152/ajpgi.00304.2019 PubMed DOI PMC

Prince AC, Brooks SJ, Stahl D, Treasure J. Systematic review and meta-analysis of the baseline concentrations and physiologic responses of gut hormones to food in eating disorders. Am J Clin Nutr (2009) 89:755–65. 10.3945/ajcn.2008.27056 PubMed DOI

Fetissov SO. Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour. Nat Rev Endocrinol (2017) 13(1):11–25. 10.1038/nrendo.2016.150 PubMed DOI

Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, Lodinová-Zádníková R, et al. . Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett (2004) 93(2-3):97–108. 10.1016/j.imlet.2004.02.005 PubMed DOI

Oldstone MB. Molecular mimicry, microbial infection, and autoimmune disease: evolution of the concept. Curr Top Microbiol Immunol (2005) 296:1–17. 10.1007/3-540-30791-5_1 PubMed DOI PMC

Fetissov SO, Hökfelt T. On the origin of eating disorders: altered signaling between gut microbiota, adaptive immunity and the brain melanocortin system regulating feeding behavior. Curr Opin Pharmacol (2019) 48:82–91. 10.1016/j.coph.2019.07.004 PubMed DOI

Fetissov SO, Harro J, Jaanisk M, Järv A, Podar I, Allik J, et al. . Autoantibodies against neuropeptides are associated with psychological traits in eating disorders. Proc Natl Acad Sci U S A (2005) 102:14865–70. 10.1073/pnas.0507204102 PubMed DOI PMC

Lucas N, Legrand R, Bôle-Feysot C, Breton J, Coëffier M, Akkermann K, et al. . Immunoglobulin G modulation of the melanocortin 4 receptor signaling in obesity and eating disorders. Transl Psychiatry (2019) 9(1):87. 10.1038/s41398-019-0422-9 PubMed DOI PMC

Fetissov SO, Déchelotte P. The new link between gut-brain axis and neuropsychiatric disorders. Curr Opin Clin Nutr Metab Care (2011) 14:477–82. 10.1097/MCO.0b013e32834936e7 PubMed DOI

Fetissov SO, Sinno MH, Coëffier M, Bole-Feysot C, Ducrotte P, Hökfelt T, et al. . Autoantibodies against appetite-regulating peptide hormones and neuropeptides: Putative modulation by gut microflora. Nutrition (2008) 24:348–59. 10.1016/j.nut.2007.12.006 PubMed DOI PMC

Terashi M, Asakawa A, Harada T, Ushikai M, Coquerel Q, Sinno MH, et al. . Ghrelin reactive autoantibodies in restrictive anorexia nervosa. Nutrition (2011) 27:407–13. 10.1016/j.nut.2011.01.002 PubMed DOI

Takagi K, Legrand R, Asakawa A, Amitani H, François M, Tennoune N, et al. . Anti-ghrelin immunoglobulins modulate ghrelin stability and its orexigenic effect in obese mice and humans. Nat Commun (2013) 4:2685. 10.1038/ncomms3685 PubMed DOI PMC

Garcia FD, Coquerel Q, do Rego JC, Cravezic A, Bole-Feysot C, Kiive E, et al. . Anti-neuropeptide Y plasma immunoglobulins in relation to mood and appetite in depressive disorder. Psychoneuroendocrinology (2012) 37(9):1457–67. 10.1016/j.psyneuen.2012.01.015 PubMed DOI

Breton J, Jacquemot J, Yaker L, Leclerc C, Connil N, Feuilloley M, et al. . Host Starvation and Female Sex Influence Enterobacterial ClpB Production: A Possible Link to the Etiology of Eating Disorders. Microorganisms (2020) 8(4):530. 10.3390/microorganisms8040530 PubMed DOI PMC

Bouhajja H, Bougacha-Elleuch N, Lucas N, Legrand R, Marrakchi R, Kaveri SV, et al. . Affinity kinetics of leptin-reactive immunoglobulins are associated with plasma leptin and markers of obesity and diabetes. Nutr Diabetes (2018) 8(1):32. 10.1038/s41387-018-0044-y PubMed DOI PMC

Hu X, Chen F. Exogenous insulin antibody syndrome (EIAS): a clinical syndrome associated with insulin antibodies induced by exogenous insulin in diabetic patients. Endocr Connect (2018) 7(1):R47–R55. 10.1530/EC-17-0309 PubMed DOI PMC

Corcos M, Atger F, Lévy-Soussan P, Avrameas S, Guilbert B, Cayol V, et al. . Bulimia nervosa and autoimmunity. Psychiatry Res (1999) 87:77–82. 10.1016/S0165-1781(99)00048-7 PubMed DOI

Fetissov SO. Neuropeptide autoantibodies assay. Methods Mol Biol (2011) 789:295–302. 10.1007/978-1-61779-310-3_19 PubMed DOI

François M, Takagi K, Legrand R, Lucas N, Beutheu S, Bôle-Feysot C, et al. . Increased Ghrelin but Low Ghrelin-Reactive Immunoglobulins in a Rat Model of Methotrexate Chemotherapy-Induced Anorexia. Front Nutr (2016) 3:23. 10.3389/fnut.2016.00023 PubMed DOI PMC

Wheatland R. Chronic ACTH autoantibodies are a significant pathological factor in the disruption of the hypothalamic-pituitary-adrenal axis in chronic fatigue syndrome, anorexia nervosa and major depression. Med Hypotheses (2005) 65(2):287–95. 10.1016/j.mehy.2005.02.031 PubMed DOI

Smitka K, Papezova H, Vondra K, Hill M, Hainer V, Nedvidkova J. A higher response of plasma neuropeptide Y, growth hormone, leptin levels and extracellular glycerol levels in subcutaneous abdominal adipose tissue to Acipimox during exercise in patients with bulimia nervosa: single-blind, randomized, microdialysis study. Nutr Metab (2011) 8:81. 10.1186/1743-7075-8-81 PubMed DOI PMC

Holden RJ, Pakula IS. Tumor necrosis factor-alpha: is there a continuum of liability between stress, anxiety states and anorexia nervosa? Med Hypotheses (1999) 52(2):155–62. 10.1054/mehy.1997.0641 PubMed DOI

Patsalos O, Dalton B, Leppanen J, Ibrahim MAA, Himmerich H. Impact of TNF-α Inhibitors on Body Weight and BMI: A Systematic Review and Meta-Analysis. Front Pharmacol (2020) 11:481. 10.3389/fphar.2020.00481 PubMed DOI PMC

Patsalos O, Dalton B, Himmerich H. Effects of IL-6 Signaling Pathway Inhibition on Weight and BMI: A Systematic Review and Meta-Analysis. Int J Mol Sci (2020) 21(17):6290. 10.3390/ijms21176290 PubMed DOI PMC

Solmi M, Santonastaso P, Caccaro R, Favaro A. A case of anorexia nervosa with comorbid Crohn’s disease: beneficial effects of anti-TNF-α therapy? Int J Eat Disord (2013) 46(6):639–41. 10.1002/eat.22153 PubMed DOI

Barber J, Sheeran T, Mulherin D. Anti-tumour necrosis factor treatment in a patient with anorexia nervosa and juvenile idiopathic arthritis. Ann Rheum Dis (2003) 62(5):490–1. 10.1136/ard.62.5.490 PubMed DOI PMC

Smitka K, Nedvidkova J, Vondra K, Hill M, Papezova H, Hainer V. Acipimox Administration With Exercise Induces a Co-feedback Action of the GH, PP, and PYY on Ghrelin Associated With a Reduction of Peripheral Lipolysis in Bulimic and Healthy-Weight Czech Women: A Randomized Study. Front Endocrinol (Lausanne) (2019) 10:108. 10.3389/fendo.2019.00108 PubMed DOI PMC

Nedvidkova J, Dostalova I, Bartak V, Papezova H, Pacak K. Increased subcutaneous abdominal tissue norepinephrine levels in patients with anorexia nervosa: an in vivo microdialysis study. Physiol Res (2004) 53:409–13. PubMed

Bi S, Kim YJ, Zheng F. Dorsomedial hypothalamic NPY and energy balance control. Neuropeptides (2012) 46(6):309–14. 10.1016/j.npep.2012.09.002 PubMed DOI PMC

Lancaster E, Dalmau J. Neuronal autoantigens–pathogenesis, associated disorders and antibody testing. Nat Rev Neurol (2012) 8(7):380–90. 10.1038/nrneurol.2012.99 PubMed DOI PMC

Najjar S, Pearlman DM, Alper K, Najjar A, Devinsky O. Neuroinflammation and psychiatric illness. J Neuroinflamm (2013) 10:43. 10.1186/1742-2094-10-43 PubMed DOI PMC

Margutti P, Delunardo F, Ortona E. Autoantibodies associated with psychiatric disorders. Curr Neurovasc Res (2006) 2:149–57. 10.2174/156720206776875894 PubMed DOI

Caspani G, Swann J. Small talk: microbial metabolites involved in the signaling from microbiota to brain. Curr Opin Pharmacol (2019) 48:99–106. 10.1016/j.coph.2019.08.001 PubMed DOI

Parker A, Fonseca S, Carding SR. Gut microbes and metabolites as modulators of blood-brain barrier integrity and brain health. Gut Microbes (2020) 11(2):135–57. 10.1080/19490976.2019.1638722 PubMed DOI PMC

Fasano A. All disease begins in the (leaky) gut: role of zonulin-mediated gut permeability in the pathogenesis of some chronic inflammatory diseases. F1000Res (2020) 9:F1000 Faculty Rev–69. 10.12688/f1000research.20510.1 PubMed DOI PMC

Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, et al. . The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med (2014) 6(263):263ra158. 10.1126/scitranslmed.3009759 PubMed DOI PMC

Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, et al. . The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun (2014) 5:3611. 10.1038/ncomms4611 PubMed DOI PMC

Chambers ES, Morrison DJ, Frost G. Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms? Proc Nutr Soc (2015) 74(3):328–36. 10.1017/S0029665114001657 PubMed DOI

Monteleone P, Carratu R, Carteni M, Generoso M, Lamberti M, De Magistris L, et al. . Intestinal permeability is decreased in anorexia nervosa. Mol Psychiatry (2004) 9:76–80. 10.1038/sj.mp.4001374 PubMed DOI

Naisberg Y, Modai I, Weizman A. Metabolic bioenergy homeostatic disruption: a cause of anorexia nervosa. Med Hypotheses (2001) 56:454–61. 10.1054/mehy.2000.1199 PubMed DOI

Morris AA. Cerebral ketone body metabolism. J Inherit Metab Dis (2005) 28(2):109–21. 10.1007/s10545-005-5518-0 PubMed DOI

Puxley F, Midtsund M, Iosif A, Lask B. PANDAS anorexia nervosa–endangered, extinct or nonexistent? Int J Eat Disord (2008) 41:15–21. 10.1002/eat.20462 PubMed DOI

Vincenzi B, O’Toole J, Lask B. PANDAS and anorexia nervosa–a spotters’ guide: suggestions for medical assessment. Eur Eat Disord Rev (2010) 8(2):116–23. 10.1002/erv.977 PubMed DOI

Kılıç F, Işık Ü, Demirdaş A, Doğuç DK, Bozkurt M. Serum zonulin and claudin-5 levels in patients with bipolar disorder. J Affect Disord (2020) 266:37–42. 10.1016/j.jad.2020.01.117 PubMed DOI

Fu A, Hui EK, Lu JZ, Boado RJ, Pardridge WM. Neuroprotection in stroke in the mouse with intravenous erythropoietin-Trojan horse fusion protein. Brain Res (2011) 1369:203–7. 10.1016/j.brainres.2010.10.097 PubMed DOI

Fetissov SO, Lucas N, Legrand R. Ghrelin-Reactive Immunoglobulins in Conditions of Altered Appetite and Energy Balance. Front Endocrinol (Lausanne) (2017) 8:10. 10.3389/fendo.2017.00010 PubMed DOI PMC

Jésus P, Ouelaa W, François M, Riachy L, Guérin C, Aziz M, et al. . Alteration of intestinal barrier function during activity-based anorexia in mice. Clin Nutr (2014) 33(6):1046–53. 10.1016/j.clnu.2013.11.006 PubMed DOI

Sinno MH, Coquerel Q, Boukhettala N, Coëffier M, Gallas S, Terashi M, et al. . Chemotherapy-induced anorexia is accompanied by activation of brain pathways signaling dehydration. Physiol Behav (2010) 101(5):639–48. 10.1016/j.physbeh.2010.09.016 PubMed DOI

Coquerel Q, Sinno MH, Boukhettala N, Coëffier M, Terashi M, Bole-Feysot C, et al. . Intestinal inflammation influences α-MSH reactive autoantibodies: relevance to food intake and body weight. Psychoneuroendocrinology (2012) 37(1):94–106. 10.1016/j.psyneuen.2011.05.008 PubMed DOI

Wiercinska-Drapalo A, Jaroszewicz J, Siwak E, Pogorzelska J, Prokopowicz D. Intestinal fatty acid binding protein (I-FABP) as a possible biomarker of ileitis in patients with ulcerative colitis. Regul Pept (2008) 147(1-3):25–8. 10.1016/j.regpep.2007.12.002 PubMed DOI

Henderson AL, Brand MW, Darling RJ, Maas KJ, Detzel CJ, Hostetter J, et al. . Attenuation of Colitis by Serum-Derived Bovine Immunoglobulin/Protein Isolate in a Defined Microbiota Mouse Model. Dig Dis Sci (2015) 60(11):3293–303. 10.1007/s10620-015-3726-5 PubMed DOI PMC

Bass N. The cellular fatty acid binding proteins: aspects of structure, regulation, and function. Int Rev Cytol (1988) 111:143–84. 10.1016/S0074-7696(08)61733-7 PubMed DOI

Prochazkova P, Roubalova R, Dvorak J, Tlaskalova-Hogenova H, Cermakova M, Tomasova P, et al. . Microbiota, Microbial Metabolites, and Barrier Function in A Patient with Anorexia Nervosa after Fecal Microbiota Transplantation. Microorganisms (2019) 7(9):338. 10.3390/microorganisms7090338 PubMed DOI PMC

Monteiro MP, Batterham RL. The Importance of the Gastrointestinal Tract in Controlling Food Intake and Regulating Energy Balance. Gastroenterology (2017) 152:1707–17.e2. 10.1053/j.gastro.2017.01.053 PubMed DOI

Sakata N, Yoshimatsu G, Kodama S. Development and Characteristics of Pancreatic Epsilon Cells. Int J Mol Sci (2019) 20(8):1867. 10.3390/ijms20081867 PubMed DOI PMC

Smitka K, Papezova H, Vondra K, Hill M, Hainer V, Nedvidkova J. The role of “mixed” orexigenic and anorexigenic signals and autoantibodies reacting with appetite-regulating neuropeptides and peptides of the adipose tissue-gut-brain axis: relevance to food intake and nutritional status in patients with anorexia nervosa and bulimia nervosa. Int J Endocrinol (2013) 2013:483145. 10.1155/2013/483145 PubMed DOI PMC

Mani BK, Zigman JM. Ghrelin as a Survival Hormone. Trends Endocrinol Metab (2017) 8(12):843–54. 10.1016/j.tem.2017.10.001 PubMed DOI PMC

Müller TD, Nogueiras R, Andermann ML, Andrews ZB, Anker SD, Argente J, et al. . Ghrelin. Mol Metab (2015) 4:437–60. 10.1016/j.molmet.2015.03.005 PubMed DOI PMC

Asakawa A, Inui A, Fujimiya M, Sakamaki R, Shinfuku N, Ueta Y, et al. . Stomach regulates energy balance via acylated ghrelin and desacyl ghrelin. Gut (2005) 54(1):18–24. 10.1136/gut.2004.038737 PubMed DOI PMC

Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes (2001) 50(8):1714–9. 10.2337/diabetes.50.8.1714 PubMed DOI

Hassouna R, Labarthe A, Tolle V. Hypothalamic regulation of body growth and appetite by ghrelin-derived peptides during balanced nutrition or undernutrition. Mol Cell Endocrinol (2016) 438:42–51. 10.1016/j.mce.2016.09.027 PubMed DOI

Koyama KI, Yasuhara D, Nakahara T, Harada T, Uehara M, Ushikai M, et al. . Changes in acyl ghrelin, des-acyl ghrelin, and ratio of acyl ghrelin to total ghrelin with short-term refeeding in female inpatients with restricting-type anorexia nervosa. Horm Metab Res (2010) 42(8):595–8. 10.1055/s-0030-1252017 PubMed DOI

Igudesman D, Sweeney M, Carroll IM, Mayer-Davis EJ, Bulik CM. Gut-Brain Interactions: Implications for a Role of the Gut Microbiota in the Treatment and Prognosis of Anorexia Nervosa and Comparison to Type I Diabetes. Gastroenterol Clin North Am (2019) 48:343–56. 10.1016/j.gtc.2019.04.003 PubMed DOI PMC

Hotta M, Ohwada R, Katakami H, Shibasaki T, Hizuka N, Takano K. Plasma levels of intact and degraded ghrelin and their responses to glucose infusion in anorexia nervosa. J Clin Endocrinol Metab (2004) 89(11):5707–12. 10.1210/jc.2004-0353 PubMed DOI

Fazeli PK, Lawson EA, Faje AT, Eddy KT, Lee H, Fiedorek FT, et al. . Treatment With a Ghrelin Agonist in Outpatient Women With Anorexia Nervosa: A Randomized Clinical Trial. J Clin Psychiatry (2018) 79(1):17m11585. 10.4088/JCP.17m11585 PubMed DOI PMC

Gorwood P, Blanchet-Collet C, Chartrel N, Duclos J, Dechelotte P, Hanachi M, et al. . New Insights in Anorexia Nervosa. Front Neurosci (2016) 10:256. 10.3389/fnins.2016.00256 PubMed DOI PMC

Dostalova I, Smitka K, Papezova H, Kvasnickova H, Nedvidkova J. Increased insulin sensitivity in patients with anorexia nervosa: the role of adipocytokines. Physiol Res (2007) 56:587–94. PubMed

Prioletta A, Muscogiuri G, Sorice GP, Lassandro AP, Mezza T, Policola C, et al. . In anorexia nervosa, even a small increase in abdominal fat is responsible for the appearance of insulin resistance. Clin Endocrinol (2011) 75:202–6. 10.1111/j.1365-2265.2011.04046.x PubMed DOI

Yahya AS, Khawaja S, Chukwuma J, Chukwuma C. Early Diagnosis and Management of Bulimia Nervosa in Type 1 Diabetes. Prim Care Companion CNS Disord (2020) 22(6):20nr02707. 10.4088/PCC.20nr02707 PubMed DOI

Martínez-Ansó E, Pérez M, Martínez JA. Induction of hypothermia, hypoglycemia and hyperinsulinemia after acute leptin immunoneutralization in overnight fasted mice. Int J Mol Med (1998) 2(6):681–3. 10.3892/ijmm.2.6.681 PubMed DOI

Zhang JV, Ren PG, Avsian-Kretchmer O, Luo CW, Rauch R, Klein C, et al. . Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin’s effects on food intake. Science (2005) 310(5750):996–9. 10.1126/science.1117255 PubMed DOI

Garg A. The ongoing saga of obestatin: is it a hormone? J Clin Endocrinol Metab (2007) 92(9):3396–8. 10.1210/jc.2007-0999 PubMed DOI

Monteleone P, Serritella C, Martiadis V, Scognamiglio P, Maj M. Plasma obestatin, ghrelin, and ghrelin/obestatin ratio are increased in underweight patients with anorexia nervosa but not in symptomatic patients with bulimia nervosa. J Clin Endocrinol Metab (2008) 93(11):4418–21. 10.1210/jc.2008-1138 PubMed DOI

Matafome P, Eickhoff H, Letra L, Seiça R. Neuroendocrinology of Adipose Tissue and Gut-Brain Axis. Adv Neurobiol (2017) 19:49–70. 10.1007/978-3-319-63260-5_3 PubMed DOI

Manning S, Batterham RL. The role of gut hormone peptide YY in energy and glucose homeostasis: twelve years on. Annu Rev Physiol (2014) 76:585–608. 10.1146/annurev-physiol-021113-170404 PubMed DOI

Rudenko O, Shang J, Munk A, Ekberg JP, Petersen N, Engelstoft MS, et al. . The aromatic amino acid sensor GPR142 controls metabolism through balanced regulation of pancreatic and gut hormones. Mol Metab (2019) 19:49–64. 10.1016/j.molmet.2018.10.012 PubMed DOI PMC

Engelstoft MS, Schwartz TW. Opposite Regulation of Ghrelin and Glucagon-like Peptide-1 by Metabolite G-Protein-Coupled Receptors. Trends Endocrinol Metab (2016) 27(9):665–75. 10.1016/j.tem.2016.07.001 PubMed DOI

Engelstoft MS, Park WM, Sakata I, Kristensen LV, Husted AS, Osborne-Lawrence S, et al. . Seven transmembrane G protein coupled receptor repertoire of gastric ghrelin cells. Mol Metab (2013) 2:376–92. 10.1016/j.molmet.2013.08.006 PubMed DOI PMC

Lund ML, Egerod KL, Engelstoft MS, Dmytriyeva O, Theodorsson E, Patel BA, et al. . Enterochromaffin 5-HT cells - A major target for GLP-1 and gut microbial metabolites. Mol Metab (2018) 11:70–83. 10.1016/j.molmet.2018.03.004 PubMed DOI PMC

Zaibi MS, Stocker CJ, O’Dowd J, Davies A, Bellahcene M, Cawthorne MA, et al. . Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett (2010) 584(11):2381–6. 10.1016/j.febslet.2010.04.027 PubMed DOI

Al-Lahham SH, Roelofsen H, Priebe M, Weening D, Dijkstra M, Hoek A, et al. . Regulation of adipokine production in human adipose tissue by propionic acid. Eur J Clin Invest (2010) 40(5):401–7. 10.1111/j.1365-2362.2010.02278.x PubMed DOI

Hoyles L, Snelling T, Umlai UK, Nicholson JK, Carding SR, Glen RC, et al. . Microbiome-host systems interactions: protective effects of propionate upon the blood-brain barrier. Microbiome (2018) 6(1):55. 10.1186/s40168-018-0439-y PubMed DOI PMC

Friedrichs P, Saremi B, Winand S, Rehage J, Dänicke S, Sauerwein H, et al. . Energy and metabolic sensing G protein-coupled receptors during lactation-induced changes in energy balance. Domest Anim Endocrinol (2014) 48:33–41. 10.1016/j.domaniend.2014.01.005 PubMed DOI

Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S, et al. . Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun (2015) 6:6734. 10.1038/ncomms7734 PubMed DOI

Schorr M, Miller KK. The endocrine manifestations of anorexia nervosa: mechanisms and management. Nat Rev Endocrinol (2017) 13(3):174–86. 10.1038/nrendo.2016.175 PubMed DOI PMC

Lawson EA, Eddy KT, Donoho D, Misra M, Miller KK, Meenaghan E, et al. . Appetite-regulating hormones cortisol and peptide YY are associated with disordered eating psychopathology, independent of body mass index. Eur J Endocrinol (2011) 164(2):253–61. 10.1530/EJE-10-0523 PubMed DOI PMC

Nakahara T, Kojima S, Tanaka M, Yasuhara D, Harada T, Sagiyama K, et al. . Incomplete restoration of the secretion of ghrelin and PYY compared to insulin after food ingestion following weight gain in anorexia nervosa. J Psychiatr Res (2007) 41(10):814–20. 10.1016/j.jpsychires.2006.07.021 PubMed DOI

Otto B, Cuntz U, Fruehauf E, Wawarta R, Folwaczny C, Riepl RL, et al. . Weight gain decreases elevated plasma ghrelin concentrations of patients with anorexia nervosa. Eur J Endocrinol (2001) 145(5):669–73. 10.1530/EJE-1450669 PubMed DOI

Tong J, D’Alessio D. Eating disorders and gastrointestinal peptides. Curr Opin Endocrinol Diabetes Obes (2011) 18(1):42–9. 10.1097/MED.0b013e328341e12b PubMed DOI

Kojima S, Nakahara T, Nagai N, Muranaga T, Tanaka M, Yasuhara D, et al. . Altered ghrelin and peptide YY responses to meals in bulimia nervosa. Clin Endocrinol (Oxf) (2005) 62(1):74–8. 10.1111/j.1365-2265.2004.02176.x PubMed DOI

Monteleone P, Martiadis V, Rigamonti AE, Fabrazzo M, Giordani C, Muller EE, et al. . Investigation of peptide YY and ghrelin responses to a test meal in bulimia nervosa. Biol Psychiatry (2005) 57(8):926–31. 10.1016/j.biopsych.2005.01.004 PubMed DOI

Feltrin KL, Little TJ, Meyer JH, Horowitz M, Rades T, Wishart J, et al. . Comparative effects of intraduodenal infusions of lauric and oleic acids on antropyloroduodenal motility, plasma cholecystokinin and peptide YY, appetite, and energy intake in healthy men. Am J Clin Nutr (2008) 87(5):1181–7. 10.1093/ajcn/87.5.1181 PubMed DOI

Hannon-Engel SL, Filin EE, Wolfe BE. CCK response in bulimia nervosa and following remission. Physiol Behav (2013) 122:56–61. 10.1016/j.physbeh.2013.08.014 PubMed DOI PMC

Cone RD. Anatomy and regulation of the central melanocortin system. Nat Neurosci (2005) 8:571–8. 10.1038/nn1455 PubMed DOI

Sinno MH, Do Rego JC, Coëffier M, Bole-Feysot C, Ducrotté P, Gilbert D, et al. . Regulation of feeding and anxiety by alpha-MSH reactive autoantibodies. Psychoneuroendocrinology (2009) 34(1):140–9. 10.1016/j.psyneuen.2008.08.021 PubMed DOI

Schaefer JM, Fetissov SO, Legrand R, Claeyssens S, Hoekstra PJ, Verhulst FC, et al. . Corticotropin (ACTH)-reactive immunoglobulins in adolescents in relation to antisocial behavior and stress-induced cortisol response. The TRAILS study. Psychoneuroendocrinology (2013) 38(12):3039–47. 10.1016/j.psyneuen.2013.08.015 PubMed DOI

Galmiche M, Lucas N, Déchelotte P, Deroissart C, Solliec ML, Rondeaux J, et al. . Plasma Peptide Concentrations and Peptide-Reactive Immunoglobulins in Patients with Eating Disorders at Inclusion in the French EDILS Cohort (Eating Disorders Inventory and Longitudinal Survey). Nutrients (2020) 12(2):522. 10.3390/nu12020522 PubMed DOI PMC

Dominique M, Legrand R, Galmiche M, Azhar S, Deroissart C, Guérin C, et al. . Changes in Microbiota and Bacterial Protein Caseinolytic Peptidase B During Food Restriction in Mice: Relevance for the Onset and Perpetuation of Anorexia Nervosa. Nutrients (2019) 11(10):2514. 10.3390/nu11102514 PubMed DOI PMC

Panaro BL, Tough IR, Engelstoft MS, Matthews RT, Digby GJ, Møller CL, et al. . The melanocortin-4 receptor is expressed in enteroendocrine L cells and regulates the release of peptide YY and glucagon-like peptide 1in vivo. Cell Metab (2014) 20(6):1018–29. 10.1016/j.cmet.2014.10.004 PubMed DOI PMC

Galusca B, Prévost G, Germain N, Dubuc I, Ling Y, Anouar Y, et al. . Neuropeptide Y and α-MSH circadian levels in two populations with low body weight: anorexia nervosa and constitutional thinness. PloS One (2015) 10(3):e0122040. 10.1371/journal.pone.0122040 PubMed DOI PMC

Budzyński J, Kłopocka M. Brain-gut axis in the pathogenesis of Helicobacter pylori infection. World J Gastroenterol (2014) 20:5212–25. 10.3748/wjg.v20.i18.5212 PubMed DOI PMC

Yanagi H, Tsuda A, Matsushima M, Takahashi S, Ozawa G, Koga Y, et al. . Changes in the gut microbiota composition and the plasma ghrelin level in patients with Helicobacter pylori-infected patients with eradication therapy. BMJ Open Gastroenterol (2017) 4(1):e000182. 10.1136/bmjgast-2017-000182 PubMed DOI PMC

Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun (2011) 25(3):397–407. 10.1016/j.bbi.2010.10.023 PubMed DOI PMC

Queipo-Ortuño 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. 10.1371/journal.pone.0065465 PubMed DOI PMC

Breton J, Tirelle P, Hasanat S, Pernot A, L’Huillier C, do Rego JC, et al. . Gut microbiota alteration in a mouse model of Anorexia Nervosa. Clin Nutr (2021) 40(1):181–9. 10.1016/j.clnu.2020.05.002 PubMed DOI

Schalla MA, Stengel A. Effects of microbiome changes on endocrine ghrelin signaling - A systematic review. Peptides (2020) 133:170388. 10.1016/j.peptides.2020.170388 PubMed DOI

Dinan TG, Cryan JF. Microbes, Immunity and Behaviour: Psychoneuroimmunology Meets the Microbiome. Neuropsychopharmacology (2016) 42(1):178–92. 10.1038/npp.2016.103 PubMed DOI PMC

Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol (2012) 10(11):735–42. 10.1038/nrmicro2876 PubMed DOI

Tlaskalová-Hogenová H, Stěpánková R, Kozáková H, Hudcovic T, Vannucci L, Tučková L, et al. . The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol (2011) 8(2):110–20. 10.1038/cmi.2010.67 PubMed DOI PMC

Kostovcikova K, Coufal S, Galanova N, Fajstova A, Hudcovic T, Kostovcik M, et al. . Diet Rich in Animal Protein Promotes Pro-inflammatory Macrophage Response and Exacerbates Colitis in Mice. Front Immunol (2019) 10:919. 10.3389/fimmu.2019.00919 PubMed DOI PMC

Prochazkova P, Roubalova R, Dvorak J, Kreisinger J, Hill M, Tlaskalova-Hogenova H, et al. . The intestinal microbiota and metabolites in patients with anorexia nervosa. Gut Microbes (2021) 13(1):1–25. 10.1080/19490976.2021.1902771 PubMed PMC

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. 10.1002/eat.22394 PubMed DOI PMC

Breton J, Dechelotte P, Ribet D. Intestinal microbiota and anorexia nervosa. Clin Nutr Exp (2019) 28:11–21. 10.1016/j.yclnex.2019.05.001 DOI

Levy M, Kolodziejczyk AA, Thaiss CA, Elinav E. Dysbiosis and the immune system. Nat Rev Immunol (2017) 17(4):219–32. 10.1038/nri.2017.7 PubMed DOI

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. 10.1371/journal.pone.0007125 PubMed DOI PMC

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 (Lond) (2013) 37(11):1460–6. 10.1038/ijo.2013.20 PubMed DOI PMC

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. 10.1371/journal.pone.0145274 PubMed DOI PMC

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. 10.1097/PSY.0000000000000247 PubMed DOI PMC

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) 6:1–16. 10.1038/srep26752 PubMed DOI PMC

Mörkl S, Lackner S, Müller W, Gorkiewicz G, Kashofer K, Oberascher A, et al. . Gut microbiota and body composition in anorexia nervosa inpatients in comparison to athletes, overweight, obese, and normal weight controls. Int J Eat Disord (2017) 50(12):1421–31. 10.1002/eat.22801 PubMed DOI

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. 10.1371/journal.pone.0179739 PubMed DOI PMC

Hanachi M, Manichanh C, Schoenenberger A, Pascal V, Levenez F, Cournède N, et al. . Altered host-gut microbes symbiosis in severely malnourished anorexia nervosa (AN) patients undergoing enteral nutrition: An explicative factor of functional intestinal disorders? Clin Nutr (2019) 38(5):2304–10. 10.1016/j.clnu.2018.10.004 PubMed DOI

Monteleone AM, Troisi J, Fasano A, Dalle Grave R, Marciello F, Serena G, et al. . Multi-omics data integration in anorexia nervosa patients before and after weight regain: A microbiome-metabolomics investigation. Clin Nutr (2021) 40(3):1137–46. 10.1016/j.clnu.2020.07.021 PubMed DOI

Di Lodovico L, Mondot S, Doré J, Mack I, Hanachi M, Gorwood P. Anorexia nervosa and gut microbiota: A systematic review and quantitative synthesis of pooled microbiological data. Prog Neuropsychopharmacol Biol Psychiatry (2021) 22:110114. 10.1016/j.pnpbp.2020.110114 PubMed DOI

Mörkl S, Lackner S, Meinitzer A, Gorkiewicz G, Kashofer K, Painold A, et al. . [Pilot study: Gut microbiome and intestinal barrier in anorexia nervosa]. Fortschr Neurol Psychiatr (2019) 87:39–45. 10.1055/s-0043-123826 PubMed DOI

Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. . Human genetics shape the gut microbiome. Cell (2014) 159(4):789–99. 10.1016/j.cell.2014.09.053 PubMed DOI PMC

Ruaud A, Esquivel-Elizondo S, de la Cuesta-Zuluaga J, Waters JL, Angenent LT, Youngblut ND, et al. . Syntrophy via Interspecies H2 Transfer between Christensenella and Methanobrevibacter Underlies Their Global Cooccurrence in the Human Gut. mBio (2020) 11(1):e03235–19. 10.1128/mBio.03235-19 PubMed DOI PMC

Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, et al. . Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology (2012) 143(4):913–6.e7. 10.1053/j.gastro.2012.06.031 PubMed DOI

Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature (2006) 444(7122):1022–3. 10.1038/4441022a PubMed DOI

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. 10.1038/nature05414 PubMed DOI

Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. . Ingestion of Lactobacillus strain regulates emotional behaviour and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA (2011) 108:16050–55. 10.1073/pnas.1102999108 PubMed DOI PMC

Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res (2008) 43:164. 10.1016/j.jpsychires.2008.03.009 PubMed DOI

Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, et al. . The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol (2019) 4):623–32. 10.1038/s41564-018-0337-x PubMed DOI

Liu WH, Chuang HL, Huang YT, Wu CC, Chou GT, Wang S, et al. . Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice. Behav Brain Res (2016) 298(Pt B):202–9. 10.1016/j.bbr.2015.10.046 PubMed DOI

Shishov VA, Kirovskaia TA, Kudrin VS, Oleskin AV. Amine neuromediators, their precursors, and oxidation products in the culture of Escherichia coli K-12. Appl Biochem Mikrobiol (2009) 45:494–7. 10.1134/S0003683809050068 PubMed DOI

Asano Y, Hiramoto T, Nishino R, Aiba Y, Kimura T, Yoshihara K, et al. . Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol (2012) 303(11):G1288–95. 10.1152/ajpgi.00341.2012 PubMed DOI

Tsavkelova EA, Botvinko IV, Kudrin VS, Oleskin AV. Detection of neurotransmitter amines in microorganisms with the use of high-performance liquid chromatography. Dokl Biochem (2000) 372(1-6):115–7. PubMed

Stanaszek PM, Snell JF, O’Neill JJ. Isolation, extraction, and measurement of acetylcholine from Lactobacillus plantarum. Appl Environ Microbiol (1977) 34(2):237–9. 10.1128/AEM.34.2.237-239.1977 PubMed DOI PMC

Strandwitz P, Kim KH, Terekhova D, Liu JK, Sharma A, Levering J, et al. . GABA-modulating bacteria of the human gut microbiota. Nat Microbiol (2019) 4(3):396–403. 10.1038/s41564-018-0307-3 PubMed DOI PMC

Kunze WA, Mao YK, Wang B, Huizinga JD, Ma X, Forsythe P, et al. . Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med (2009) 13(8B):2261–70. 10.1111/j.1582-4934.2009.00686.x PubMed DOI PMC

De Vadder F, Grasset E, Mannerås Holm L, Karsenty G, Macpherson AJ, Olofsson LE, et al. . Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. Proc Natl Acad Sci U S A (2018) 115(25):6458–63. 10.1073/pnas.1720017115 PubMed DOI PMC

Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C. gamma-Aminobutyric acid production by culturable bacteria from the human intestine. Appl Microbiol (2012) 113(2):411–7. 10.1111/j.1365-2672.2012.05344.x PubMed DOI

Siragusa S, De Angelis M, Di Cagno R, Rizzello CG, Coda R, Gobbetti M. Synthesis of gamma-aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol (2007) 73(22):7283–90. 10.1128/AEM.01064-07 PubMed DOI PMC

Hata T, Miyata N, Takakura S, Yoshihara K, Asano Y, Kimura-Todani T, et al. . The Gut Microbiome Derived From Anorexia Nervosa Patients Impairs Weight Gain and Behavioral Performance in Female Mice. Endocrinology (2019) 160(10):2441–52. 10.1210/en.2019-00408 PubMed DOI

Monteleone P, Monteleone AM, Troisi J, Dalle Grave R, Corrivetti G, Calugi S, et al. . Metabolomics signatures of acutely ill and short-term weight recovered women with anorexia nervosa. Mol Psychiatry (2019). 10.1038/s41380-019-0573-3 PubMed DOI

Cammarota G, Masucci L, Ianiro G, Bibbò S, Dinoi G, Costamagna G, et al. . Randomised clinical trial: faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection. Aliment Pharmacol Ther (2015) 41(9):835–43. 10.1111/apt.13144 PubMed DOI

Zenzeri L, Tambucci R, Quitadamo P, Giorgio V, De Giorgio R, Di Nardo G. Update on chronic intestinal pseudo-obstruction. Curr Opin Gastroenterol (2020) 36(3):230–7. 10.1097/MOG.0000000000000630 PubMed DOI

Quigley EMM. The Spectrum of Small Intestinal Bacterial Overgrowth (SIBO). Curr Gastroenterol Rep (2019) 21(1):3. 10.1007/s11894-019-0671-z PubMed DOI

Santonicola A, Gagliardi M, Guarino MPL, Siniscalchi M, Ciacci C, Iovino P. Eating Disorders and Gastrointestinal Diseases. Nutrients (2019) 11(12):3038. 10.3390/nu11123038 PubMed DOI PMC

Vendrik KEW, Ooijevaar RE, de Jong PRC, Laman JD, van Oosten BW, van Hilten JJ, et al. . Fecal Microbiota Transplantation in Neurological Disorders. Front Cell Infect Microbiol (2020) 10:98. 10.3389/fcimb.2020.00098 PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...