The family Enterobacteriaceae, often referred to as enterics, consists of a large number of diverse organisms. The Enterobacterieaceae have several key laboratory features in common, but as DNA studies on each of these organisms progress, classification of the members changes. Some are being added (like Plesiomonas), and some may eventually be removed from the family. At this time several characteristics are still used to place an organism in the family Enterobacteriaceae (Box 20-1). Common characteristics also subcategorize members of the Enterobacteriaceae into a number of tribes.


Microscopic and Colonial Morphology

Members of the family Enterobacteriaceae are gramnegative, nons pore-forming, facultatively anaerobic bacilli. On Gram-stained smears, they may appear as coccobacilli or as straight rods. Colonial morphology on nonselective media, such as sheep blood agar (SBA) or chocolate (CHOC)agar, is of little value in their initial identification. With the exception of certain members

(e.g., Klebsiella) that produce characteristically large and very mucoid colonies, all members of this family produce large, moist, gray colonies on nonselective media and are therefore indistinguishable. However, many isolates of E. coli are ~-hemolytic.

A wide variety of differential and selective media, such as MacConkey agar, and highly selective media, such as Hektoen enteric (HE) agar and xylose-lysine deoxycholate (XLD) agar, are available for the presumptive identification of enteric pathogens. These media contain one or more carbohydrates, such as lactose and sucrose, which show the ability of the species to ferment specific carbohydrates. Fermentation is indicated by a color change on the medium, which results from a drop in pH detected by a pH indicator incorporated into the medium. Nonfermenting species are differentiated by lack of color change, and colonies retain the original color of the medium.

Species that produce hydrogen sulfide (H2S)may be readily distinguished when placed on HE or XLDagar.

HE and XLD agars contain sodium thiosulfate and ferric ammonium citrate, which produce blackening of H2S-producing colonies. These features have been used initially to differentiate and characterize certain genera. Definitive identification depends on the biochemical reactions and serologic antigenic structures demonstrated by the particular species.



The use of tribes in classifying the members in this family was proposed by Ewing in 1963 and has since been continued and extended in subsequent editions of Edwards and Ewing’s Identification of Enterobacteriaceae.

In classifying species into tribes, Ewing grouped bacterial species with similar biochemical characteristics. Within the tribes, species are further classified into their respective genera.

Differentiation of each genus and definitive identification of species are based on biochemical characteristics.

Table 20-1 lists the bacterial species in the family Enterobacteriaceae and their respective tribes; Table 20-2 shows the biochemical features that differentiate the tribes. Although the concept of using tribes in the classification of bacteria has not been used in Bergey’s Manual of Systematic Bacteriology, this classification has been an effective way of placing species in groups based on similar biochemical features.


Virulence and Antigenic Factors

The virulence of the Enterobacteriaceae species is controlled by a number of factors, such as the ability to adhere, colonize, produce various toxins, and invade tissue. Some species harbor plasmids that can provide antimicrobial resistance genes. For example, an increasing number of E. coli, K pneumoniae, and Klebsiella oxytoca clinical strains produce plasmid-mediated extended-spectrum I3~-Iactamases (ESBLs), which can inactivate extended-spectrum cephalosporins (such as cefotaxime), penicillins, and aztreonam. Testing procedures for the detection of ESBLs are described in Chapter 13.

Many members of this family possess antigens that can be used in the identification of different serologic

groups. These antigens include the following:

·0 antigen, or somatic antigen-this is a heatstable antigen located on the cell wall.

· H antigen, or flagellar antigen-this is a heatlabile antigen found on the surface of flagella,

organelles responsible for motility.

·Kantigen, or capsular antigen-this is a heat-labile polysaccharide found only in certain encapsulated

species. Examples are the Kl antigen of E. coli, and the Vi antigen of Salmonella enterica subsp. enterica serotype Typhi.


Clinical Significance

Members of the family Enterobacteriaceae are ubiquitous in nature. Additionally, the Enterobacteriaceae, with few exceptions, share a common niche; they reside in the gastrointestinal (GOtract. Except for Salmonella, Shigella; and Yersinia, they can be resident flora if confined to their natural environment. Paradoxically they are often commensals, causing no harm, and yet can be responsible for a large number of opportunistic infections. Some species exist as free-living organisms in water, soil, and sewage, and some are plant pathogens.

Based on the clinical infections they produce, members of the Enterobacteriaceae may be divided into two broad categories: (1) opportunistic pathogens and (2) primary pathogens. The opportunistic pathogens are often a part of the usual intestinal flora of both humans and animals. Outside their normal body sites, however, these organisms may produce serious extraintestinal, opportunistic infections, many of which are described in this chapter. For example, E. coli, one of the best-studied members of the Enterobacteriaceae, is a member of the normal bowel flora but can cause urinary tract infections CUTis), septicemia, wound infections in healthy individuals, and meningitis in neonates. Other organisms can be equally devastating in immunocompromised hosts or when introduced towounds from contaminated soil or water.

The primary pathogens, which include Salmonella enterica, Shigella spp., and Yersinia spp., are considered true pathogens; that is, they are not present as commensal flora in the GI tract of humans. These organisms produce infections resulting from ingestion of contaminated food or water, or from other sources, which are discussed in this chapter. Table 20-3 lists some of the diseases associated with members of the family Enterobacteriaceae.

box 20-1 table 20-1

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