Microbial biofilms and gastrointestinal diseases

Pathogens and Disease ISSN 2049-632X MINIREVIEW Microbial biofilms and gastrointestinal diseases Erik C. von Rosenvinge1,2, Graeme A. O’May3, Sandra Macfarlane4, George T. Macfarlane4 & Mark E. Shirtliff3 1 2 3 4 Department of Gastroenterology and Hepatology, University of Maryland School of Medicine, Baltimore, MD, USA Department of Veterans Affairs, VA Maryland Health Care System, Baltimore, MD, USA Department of Microbial Pathogenesis, University of Maryland School of Dentistry, Baltimore, MD, USA Microbiology and Gut Biology Group, University of Dundee, Ninewells Hospital Medical School, Dundee, UK This timely review on the significance of microbial biofilms and gastrointestinal disease will stimulate research in this field. Correspondence Mark E. Shirtliff, Department of Microbial Pathogenesis, University of Maryland School of Dentistry, Baltimore, MD 21201, USA. Tel.: +1 410 706 2263 fax: 1 410 706 0193 e-mail: Received: 9 September 2012; revised 12 December 2012; accepted 12 December 2012. Final version published online 29 January 2013. Abstract The majority of bacteria live not planktonically, but as residents of sessile biofilm communities. Such populations have been defined as ‘matrix-enclosed microbial accretions, which adhere to both biological and nonbiological surfaces’. Bacterial formation of biofilm is implicated in many chronic disease states. Growth in this mode promotes survival by increasing community recalcitrance to clearance by host immune effectors and therapeutic antimicrobials. The human gastrointestinal (GI) tract encompasses a plethora of nutritional and physicochemical environments, many of which are ideal for biofilm formation and survival. However, little is known of the nature, function, and clinical relevance of these communities. This review summarizes current knowledge of the composition and association with health and disease of biofilm communities in the GI tract. doi:10.1111/2049-632X.12020 Editor: Ake Forsberg Introduction The human gastrointestinal (GI) tract extends from the esophagus through the stomach, small intestine, and large intestine (colon) and terminates in the rectum (Fig. 1). The small intestine is divided proximally-to-distally into the duodenum, jejunum, and ileum. This collection of interconnected organs harbors a diversity of microhabitats that are colonized by microorganisms to varying degrees, depending on local environmental conditions. For the purposes of this article, the oral and nasal cavities will not be regarded as being part of the GI tract, although these anatomical spaces also contain great microbiological complexity (Ledder et al., 2007). There exists in the GI tract a gradient of colonization, from the relatively sparsely populated esophagus and stomach to the much more heavily colonized colon, which can contain up to 1012 culturable bacteria per gram luminal contents (Hopkins et al., 2002). Evolution has dictated that the GI tract possess a large surface area to facilitate efficient nutrient uptake, its primary physiological role in the body. This coupled to high nutrient availability and a constant influx of microorganisms, together with stable autochthonous populations, makes the GI tract an ideal site for the development of sessile microbial biofilm communities. The microbiome of the gut has recently been determined in 124 subjects, and the microbial diversity indicates that the entire cohort harbors only between 1000 and 1150 prevalent bacterial species and each individual at least 160 such species (Qin et al., 2010). In addition, there were common microbial flora in subjects tested with 75 species common to > 50% of individuals and 57 species common to > 90%. Those microorganisms in closest proximity to host tissues have the most opportunity for interaction with host physiology, immunity, and metabolism; thus, mucosal populations are arguably the most important component of any host–microbiota interaction, whether beneficial or detrimental. The GI tract microbiota has been implicated in disease states such as inflammatory bowel disease (IBD; Macpherson et al., 1996), colon cancer (Horie et al., €rkholm et al., 2003), and 1999a, b), gastric cancer (Bjo irritable bowel syndrome (IBS; Swidsinski et al., 2005). In Pathogens and Disease (2013), 67, 25–38, © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved 25 Keywords biofilm; microbiota; gastrointestinal disease; gastrointestinal tract. Biofilms and GI diseases E.C. von Rosenvinge et al. are mainly Gram-positive facultatively anaerobic species such as lactobacilli and streptococci. These are thought to originate primarily in the oral cavity (Macfarlane & Dillon, 2007). While traditionally the stomach has been considered inhospitable for bacteria due to its acidity, using sensitive molecular techniques Bik et al. (2006) identified a surprisingly diverse bacterial population in gastric mucosal biopsies. Barrett’s esophagus addition, recent microbiome studies have uncovered a relationship between diet, microbiota, and health status, particularly in older subjects (Claesson et al., 2012). The GI tract is anatomically divided into ‘upper’ and ‘lower’ sections by the ligament of Treitz; however, from a microbial perspective, this division applies to the GI tract poorly. The colonization gradient in the GI tract, and particularly the large and rapid (relative to the length of the GI tract) increase in microbial population density from the terminal ileum to the cecum, renders possible a convenient – if somewhat artificial given their connectedness – microbial distinction between the ‘upper’ and ‘lower’ GI tracts at the level of the ileocecal valve. We will consider first the nature and influence of microbial biofilms in the upper GI tract, that is to say the esophagus, stomach and small intestine. Following this, we shall venture forth into the lower GI tract. The upper GI tract In quantitative terms, the esophagus and stomach carry the lightest bacterial load in the entire digestive system. In comparison with the lower GI tract, comparatively few microbiological investigations have been made on this part of the gut; this is due in part to difficulties in obtaining representative samples. In contradistinction, fecal effluent provides a ready supply of material for investigations of lower gut microbiology. Studies of the upper GI tract that have been carried out indicate that it is sparsely colonized in terms of microbial population density, but exhibits considerable diversity. Culturable bacteria in the healthy esophagus 26 Pathogens and Disease (2013), 67, 25–38, © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved Fig. 1 The human gastrointestinal tract. Barrett’s esophagus (BE) arises in individuals suffering from long-term gastroesophageal reflux disease. In this condition, squamous epithelial cells (...truncated)