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Gut Microbiota and Probiotics/Synbiotics for Modulation of Immunity in Critically Ill Patients

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Gut Microbiota and Probiotics/Synbiotics for Modulation of Immunity in Critically Ill Patients nutrients Review Gut Microbiota and Probiotics/Synbiotics for Modulation of Immunity in Critically Ill Patients Kentaro Shimizu * , Masahiro Ojima and Hiroshi Ogura Department of Traumatology and Acute Critical Medicine, Osaka University Graduate School of Medicine, Osaka 565-0871, Japan; [email protected] (M.O.); [email protected] (H.O.) * Correspondence: [email protected] Abstract: Patients suffering from critical illness have host inflammatory responses against injuries, such as infection and trauma, that can lead to tissue damage, organ failure, and death. Modulation of host immune response as well as infection and damage control are detrimental factors in the management of systemic inflammation. The gut is the motor of multiple organ failure following injury, and it is recognized that gut dysfunction is one of the causative factors of disease progression. The gut microbiota has a role in maintaining host immunity, and disruption of the gut microbiota might induce an immunosuppressive condition in critically ill patients. Treatment with probiotics and synbiotics has been reported to attenuate systemic inflammation by maintaining gut microbiota and to reduce postoperative infectious complications and ventilator-associated pneumonia. The administration of prophylactic probiotics/synbiotics could be an important treatment option for preventing infectious complications and modulating immunity. Further basic and clinical research is needed to promote intestinal therapies for critically ill patients. Citation: Shimizu, K.; Ojima, M.; Keywords: microbiota; gut; ICU; immune; ventilator; inflammation; probiotics; prebiotics; Ogura, H. Gut Microbiota and synbiotics; critically Probiotics/Synbiotics for Modulation of Immunity in Critically Ill Patients. Nutrients 2021, 13, 2439. https:// doi.org/10.3390/nu13072439 1. Introduction Patients suffering from critical illness can have a life-threatening host response to injuries, Academic Editor: such as infection, trauma, burn, and cardiac arrest, that can lead to tissue damage, organ Katarzyna Sli´ zewska˙ failure, and death. Sepsis management is a major challenge for healthcare systems through- out the world. About 50 million patients with sepsis were reported, with about 20% of all Received: 14 May 2021 global deaths [1]. Trauma is the leading cause of death of children, adolescents, and younger Accepted: 10 July 2021 Published: 16 July 2021 adults [2]. These responses to injury affect cells and mediators of the innate and adaptive immune systems against pathogen-associated pattern molecules or damage-associated pattern Publisher’s Note: MDPI stays neutral molecules and have been referred to as systemic inflammatory response syndrome (SIRS) with regard to jurisdictional claims in and compensatory anti-inflammatory response syndrome [3]. In contrast, prolonged SIRS published maps and institutional affil- suppresses Th1-type immune reactivity, and it also increases Th2-type cytokine production iations. and activity of regulatory T cells. These conditions can easily progress to persistent inflam- mation, immunosuppression, and catabolism syndrome (PICS), which results in multiple immunologic and physiologic defects that are difficult to survive [4]. Modulation of host response against injury has been an important topic in this field (Figure1). Gut dysfunction, including the intestinal epithelium, intestinal immune system, and Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. intestinal microbiota, is one of the causative factors of disease progression [5]. A loss This article is an open access article of beneficial microbes, expansion of pathobionts, and loss of diversity are defined as distributed under the terms and “dysbiosis”, which can change host immunity [6]. Especially, the gut microbiota and conditions of the Creative Commons microbial metabolites, such as short-chain fatty acids (SCFAs) and trimethylamine N- Attribution (CC BY) license (https:// oxide, are associated with human diseases, such as allergic and immune disorders, cancer, creativecommons.org/licenses/by/ cardiovascular disease, and neurological disorders [7]. This review summarizes how gut 4.0/). microbiota leads to systemic inflammation and intestinal therapy in the critically ill setting. Nutrients 2021, 13, 2439. https://doi.org/10.3390/nu13072439 https://www.mdpi.com/journal/nutrients Nutrients 2021, 13, x FOR PEER REVIEW 2 of 12 are associated with human diseases, such as allergic and immune disorders, cancer, car- diovascular disease, and neurological disorders [7]. This review summarizes how gut mi- Nutrients 2021, 13, 2439 crobiota leads to systemic inflammation and intestinal therapy in the critically ill setting.2 of 12 Figure 1. Figure 1. TheThe concept concept of ofinjury injury-induced-induced imbalances imbalances of ofthe the immune immune system. system. Once an insult occurs, it causes significant phenotypic changes in the immune sys- Once an insult occurs, it causes significant phenotypic changes in the immune sys- tem. The injured host develops inflammation following severe injury, which is called tem. The injured host develops inflammation following severe injury, which is called sys- systemic inflammatory response syndrome (SIRS). If the SIRS state is prolonged, it pro- temic inflammatory response syndrome (SIRS). If the SIRS state is prolonged, it progresses gresses to the multiple organ dysfunction syndrome (MODS) stage. Inflammation and to the multiple organ dysfunction syndrome (MODS) stage. Inflammation and immuno- immunosuppression coincidentally begin at the onset of sepsis, and persistent inflamma- suppressiontion, immunosuppression, coincidentally begin and catabolismat the onset syndrome of sepsis, and (PICS) persistent develops inflammation, in this concept im- [8]. munosuppression,This pro-inflammatory and catabolism state has syndrome been shown (PICS) to be develops mainly drivenin this concept by macrophages, [8]. This pro with- inflammatoryregulatory T state cells has being been the shown mediators to be of mainly this compensatory driven by macrophages, response following with regulatory injury. T cells being the mediators of this compensatory response following injury. 2. Gut Origin of Sepsis and Systemic Inflammation 2. Gut InjuryOrigin to of the Sepsis gut has and been Systemic known Inflammation to affect systemic organs and the gut itself. The gut is theInjury motor to of the multiple gut has organ been failure known [9 to], andaffect gut systemic dysfunction organs is and known the asgut a itself. causative The factorgut is inthe the motor progression of multiple of diseases organ suchfailure as [ sepsis,9], and infection, gut dysfunction shock, trauma, is known burn, as anda causative bleeding. factorIn 1994, in the Moore progression et al. reported of diseases that such in a as rat sepsis, intestinal infection, reperfusion shock, model,trauma, withburn 45-min, and bleeding.occlusion In of1994, the Moore supramesenteric et al. reported artery that following in a rat intestinal intraperitoneal reperfusion injection model of lipopolysac-, with 45- mincharide, occlusion white of bloodthe supramesenteric cells accumulated artery and following permeability intraperitoneal in the lung increased,injection of as lipopol- did lung ysaccharide,weight [10 ].white This blood result cells suggested accumulated that injury and permeability to the gut caused in the lung increased, inflammation as did and lungsystemic weight inflammation. [10]. This result One suggested of the mechanisms that injury is a to bacterial the gut translocation. caused lung Ininflammation a mouse burn andmodel, systemicEscherichia inflammation. coli was One identified of the mechanisms in the spleen is and a bacterial liver, five translocation. minutes after In injurya mouse [11 ]. burnThe model, mechanism Escherichia has not coli been was elucidated identified completely,in the spleen but and gut-derived liver, five factorsminutes were after carried injuryin [11]the. The mesenteric mechanism lymph has rather not been than theelucidated portal circulation completely, by but intestinal gut-derived lymphatic factors division were in carrieda rat shockin the modelmesenteric [12]. Inlymph the intestinal rather than epithelium, the portal burn circulation increases by gut intestinal epithelial lymphatic cell death divisionby apoptosis in a rat and shock permeability model [12] [13. In]. the The intestinal inhibition epithelium, of apoptosis burn could increases attenuate gut survival epithe- in lialP. cell aeruginosa death byinfection apoptosis mouse and permeability models [14]. [ In13] addition,. The inhibition intestinal of apoptosis tight junction could proteins, atten- uatesuch survival as claudin-5 in P. aeruginosa and occludin, infection decreased mouse and mode couldls change[14]. In gutaddition, permeability intestinal following tight junctioninjury inproteins a cecal, ligationsuch as punctureclaudin-5 model and occludin [15]. These, dec reportsreased indicated and could that change direct orgut indirect per- meabilityinjury to following the gut could injury cause in a cecal intestinal ligation damages puncture and model bacterial [15] translocation,. These reports which indicated lead to thatan direct inflammatory or indirect response injury to in the multiple gut could organs. cause intestinal damages and bacterial trans- location,In which clinical lead research, to an bacterialinflammatory translocation response was in multiple present in
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