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Gut Microbiota and Bipolar Disorder: an Overview on a Novel Biomarker for Diagnosis and Treatment

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Gut Microbiota and Bipolar Disorder: an Overview on a Novel Biomarker for Diagnosis and Treatment International Journal of Molecular Sciences Review Gut Microbiota and Bipolar Disorder: An Overview on a Novel Biomarker for Diagnosis and Treatment Lorenza Lucidi 1, Mauro Pettorruso 1, Federica Vellante 1 , Francesco Di Carlo 1 , Franca Ceci 1 , Maria Chiara Santovito 1, Ilenia Di Muzio 1 , Michele Fornaro 2 , Antonio Ventriglio 3 , Carmine Tomasetti 4, Alessandro Valchera 5, Alessandro Gentile 6, Yong-Ku Kim 7 , Giovanni Martinotti 1 , Silvia Fraticelli 1, Massimo Di Giannantonio 1 and Domenico De Berardis 8,*,† 1 Department of Neurosciences and Imaging, Chair of Psychiatry, University “G. D’Annunzio”, 66100 Chieti, Italy; [email protected] (L.L.); [email protected] (M.P.); [email protected] (F.V.); [email protected] (F.D.C.); [email protected] (F.C.); [email protected] (M.C.S.); [email protected] (I.D.M.); [email protected] (G.M.); [email protected] (S.F.); [email protected] (M.D.G.) 2 Department of Psychiatry, Federico II University, 80131 Naples, Italy; [email protected] 3 Department of Psychiatry, University of Foggia, 71121 Foggia, Italy; [email protected] 4 NHS, Department of Mental Health, Psychiatric Service for Diagnosis and Treatment, Hospital “Maria SS. dello Splendore” ASL 4, 64021 Giulianova, Italy; [email protected] 5 Villa “S. Giuseppe” Clinic, Hermanas Hospitalarias, 63100 Ascoli Piceno, Italy; [email protected] 6 Department of Mental Health, ASREM, 86039 Termoli, Italy; [email protected] 7 College of Medicine, Department of Psychiatry, Korea University, Seoul 02841, Korea; [email protected] 8 NHS, Department of Mental Health, Psychiatric Service for Diagnosis and Treatment, Citation: Lucidi, L.; Pettorruso, M.; Hospital “G. Mazzini”, ASL 4, 64100 Teramo, Italy * Correspondence: [email protected] Vellante, F.; Di Carlo, F.; Ceci, F.; † Current address: Dipartimento di Salute Mentale, Servizio Psichiatrico Diagnosi e Cura, Santovito, M.C.; Di Muzio, I.; Fornaro, Ospedale Civile “G. Mazzini”, ASL 4 Teramo, p.zza Italia 1, 64100 Teramo, Italy. M.; Ventriglio, A.; Tomasetti, C.; et al. Gut Microbiota and Bipolar Disorder: Abstract: The gut microbiota is the set of microorganisms that colonize the gastrointestinal tract of An Overview on a Novel Biomarker living creatures, establishing a bidirectional symbiotic relationship that is essential for maintaining for Diagnosis and Treatment. Int. J. homeostasis, for their growth and digestive processes. Growing evidence supports its involvement Mol. Sci. 2021, 22, 3723. https:// doi.org/10.3390/ijms22073723 in the intercommunication system between the gut and the brain, so that it is called the gut–brain– microbiota axis. It is involved in the regulation of the functions of the Central Nervous System (CNS), Academic Editors: Claudia Vuotto behavior, mood and anxiety and, therefore, its implication in the pathogenesis of neuropsychiatric and Rustam I. Aminov disorders. In this paper, we focused on the possible correlations between the gut microbiota and Bipolar Disorder (BD), in order to determine its role in the pathogenesis and in the clinical manage- Received: 5 February 2021 ment of BD. Current literature supports a possible relationship between the compositional alterations Accepted: 31 March 2021 of the intestinal microbiota and BD. Moreover, due to its impact on psychopharmacological treatment Published: 2 April 2021 absorption, by acting on the composition of the microbiota beneficial effects can be obtained on BD symptoms. Finally, we discussed the potential of correcting gut microbiota alteration as a novel Publisher’s Note: MDPI stays neutral augmentation strategy in BD. Future studies are necessary to better clarify the relevance of gut with regard to jurisdictional claims in microbiota alterations as state and disease biomarkers of BD. published maps and institutional affil- iations. Keywords: gut microbiota; bipolar disorder; mood; anxiety; mania; depression Copyright: © 2021 by the authors. 1. Introduction Licensee MDPI, Basel, Switzerland. 1.1. Bipolar Disorder This article is an open access article distributed under the terms and Bipolar Disorder (BD) is a severe and chronic mood disorder defined by alternating conditions of the Creative Commons episodes of mania, hypomania, and depression. It is widely diffused with a prevalence of Attribution (CC BY) license (https:// more than 1% [1]. creativecommons.org/licenses/by/ Manic or hypomanic episodes are characterized by elevated mood and increased 4.0/). activity; they differ in severity and length, with manic episodes being more severe than Int. J. Mol. Sci. 2021, 22, 3723. https://doi.org/10.3390/ijms22073723 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 19 Int. J. Mol. Sci. 2021, 22, 3723 2 of 19 Manic or hypomanic episodes are characterized by elevated mood and increased ac- tivity; they differ in severity and length, with manic episodes being more severe than hy- pomanic ones. At the onset of the disorder, most patients with BD present a depressive episode,hypomanic subtly ones. differing At the onsetfrom unipolar of the disorder, depressive most ones patients [2]. with BD present a depressive episode,As to subtly pathogenesis, differing BD from is unipolara highly depressiveheritable disorder ones [2]. and a multifactorial model of gene andAs to environment pathogenesis, interaction BD is a highly has been heritable proposed disorder [3]. An and imbalance a multifactorial in monoaminer- model of gene and environment interaction has been proposed [3]. An imbalance in monoaminergic gic systems, as the serotonergic, dopaminergic, and noradrenergic neurotransmitter sys- systems, as the serotonergic, dopaminergic, and noradrenergic neurotransmitter systems, tems, plays a key role in the disorder [4]. Neural plasticity seems also to be important in plays a key role in the disorder [4]. Neural plasticity seems also to be important in the circuitry regulating affective functions, with neurotrophic molecules, such as brain- the circuitry regulating affective functions, with neurotrophic molecules, such as brain- derived neurotrophic factor (BDNF), having a vital role in dendritic sprouting and synap- derived neurotrophic factor (BDNF), having a vital role in dendritic sprouting and synaptic tic plasticity [5]. plasticity [5]. Apart from this evidence, several studies conducted over the last few years have Apart from this evidence, several studies conducted over the last few years have evaluated the possible implications of the gut microbiota in the pathogenesis of BD [6,7]. evaluated the possible implications of the gut microbiota in the pathogenesis of BD [6,7]. 1.2.1.2. Composition Composition and and Development Development of of the the Gut Gut Microbiota Microbiota TheThe microbiota microbiota represents represents the the set set of of microor microorganismsganisms present present in in an an environment environment [8,9], [8,9], withwith the the intestinal intestinal one one including including at atleast least 1000 1000 different different species. species. These These microorganisms microorganisms ex- pressexpress more more than than 3 million 3 million genes genes that take that th takee name the of name the microbiome of the microbiome and which, and accord- which, ingaccording to some to researchers, some researchers, represent represent our second our secondgenome genome [10–12]. [10 –12]. BacteriaBacteria (especially (especially the the obligate obligate anaerobes), anaerobes), as as well well as as viruses, viruses, protozoa, protozoa, archaea archaea and and fungi,fungi, participate participate in in the the constitution constitution of of the the microbiota microbiota [10,13]. [10,13]. The The bacteria bacteria mainly mainly belong belong toto two two phyla, phyla, Bacteroidetes Bacteroidetes and and Firmicutes Firmicutes [14] [14 and,] and, even even if to if a to lesser a lesser extent, extent, the theProteo- Pro- bacteria,teobacteria, Actinobacteria, Actinobacteria, Fuso Fusobacteriabacteria and and Verrucomicrobia Verrucomicrobia phyla phyla are arealso also present present [15]. [15 ]. AccordingAccording to to most most of of the the current current evidence evidence,, microbial microbial colonization colonization of the of thegastrointes- gastroin- tinaltestinal tract tract begins begins at birth, at birth, so sothe the way way in inwh whichich delivery delivery is is carried carried out out might might affect affect the the compositioncomposition of of the the microbiota. microbiota. Specifically, Specifically, in in the the case case of of vaginal vaginal birth, birth, the the new-born new-born is is exposedexposed to to the the mother’s mother’s vaginal vaginal microbiota, microbiota, while while in in the the case case of of a a caesarean caesarean section section it it is is exposedexposed to to the the mother’s mother’s skin skin microbiota microbiota [16,17 [16,17].]. However, However, there there is is more more recent recent evidence evidence thatthat new-borns new-borns begin begin to to acquire acquire their their microbiota microbiota in in utero utero through through the the microbes microbes which, which, crossingcrossing the the maternal maternal digestive digestive tract, tract, are are thou thoughtght to colonize to colonize the thedigestive digestive tract tract of the of em- the bryo.embryo. Regardless Regardless of what of what the exact the exact timing timing of colonization of colonization
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